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Benign paroxysmal positional vertigo in Parkinson's disease
Parkinsonism and Related Disorders 19 (2013) 1110e1112
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Benign paroxysmal positional vertigo in Parkinson’s disease E. van Wensen a, *, R.B. van Leeuwen a, H.J. van der Zaag-Loonen a, S. Masius-Olthof a, B.R. Bloem b a b
Gelre Hospitals, Apeldoorn, A. Schweitzerlaan 31, 7334 DZ Apeldoorn, The Netherlands Radboud University Nijmegen Medical Centre, Donders Institute for Brain, Cognition and Behavior, Department of Neurology, Nijmegen, The Netherlands
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 February 2013 Received in revised form 16 July 2013 Accepted 23 July 2013
Background: Dizziness is a frequent complaint of patients with Parkinson’s disease (PD), and orthostatic hypotension (OH) is often thought to be the cause. We studied whether benign paroxysmal positional vertigo (BPPV) could also be an explanation. Aim: To assess the prevalence of benign paroxysmal positional vertigo in patients with Parkinson’s disease, with and without dizziness. Methods: 305 consecutive outpatients with PD completed the Movement Disorders Society-sponsored revision of the Unified Parkinsons’ Disease Rating Scale-motor score, the Dizziness Handicap Inventory, the DixeHallpike maneuver and a test for orthostatic hypotension. When positive for benign paroxysmal positional vertigo, a repositioning maneuver was performed. Patients were followed for three months to determine the clinical response. Results: 305 patients responded (186 men (61%), mean age 70.5 years (Standard Deviation 9.5 years)), of whom 151 (49%) complained of dizziness. 57 (38%) of the dizzy patients appeared to have orthostatic hypotension; 12 patients (8%) had a classical but previously unrecognized benign paroxysmal positional vertigo. A further four patients (3%) had a more atypical presentation of benign paroxysmal positional vertigo. Three months after treatment, 11 (92%) of patients with classical benign paroxysmal positional vertigo were almost or completely without complaints. We found no ‘hidden’ benign paroxysmal positional vertigo among patients without dizziness. The prevalence of benign paroxysmal positional vertigo among all patients with PD was 5.3%. Conclusion: Among Parkinson patients with symptoms of dizziness, up to 11% may have benign paroxysmal positional vertigo, which can be treated easily and successfully. Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.
Keywords: Parkinson’s disease Dizziness BPPV Orthostatic hypotension DixeHallpike maneuver
1. Introduction Balance disorders and falls are common in patients with Parkinson’s disease (PD). The pathophysiology is complex and multifactorial. Contributing factors that are reported frequently include freezing of gait, abnormal postural reflexes, frontal executive dysfunction and environmental factors [1e7]. Much less attention has focused on the possible role of periods of dizziness preceding a fall. Many patients with PD complain of dizziness, and in most cases this is attributed to orthostatic hypotension. Benign Paroxysmal Positional Vertigo (BPPV) is another cause of episodic dizziness, but it has rarely been associated with falls in PD. BPPV is a common condition, especially in the elderly [8e10]. It causes marked
* Corresponding author. Tel.: þ31 641290005; fax: þ31 555818234. E-mail addresses: [email protected], [email protected] (E. van Wensen).
disability, and has a great impact on the quality of life (QoL) [11,12]. BPPV can be diagnosed easily, and it is readily treatable. However, many affected patients remain undiagnosed, and both patients and caregivers are commonly unaware of the presence of BPPV [10]. It would be interesting to compare our present findings in Parkinson patients to baseline population rates for BPPV in a similar elderly cohort, but no prior study has reported this. The study of Ogholai et al. [10] comes closest to our approach, and the percentage of unrecognized benign paroxysmal positional vertigo in their hands ranged from 9% in an inner-city geriatric population up to 39% among patients aged 70 years or older in a dizziness clinic. We hypothesize that BPPV is often not recognized in patients with PD, and that its presence contributes to falls and poor QoL in this patient group. It is conceivable that PD patients are prone to develop BPPV, because their global hypokinesia and bradykinesia (leading to slower head movements) might facilitate earlier development of canalolithiasis or cupulolithiasis, causing BPPV. Indeed, reduced mobility e as occurs in patients with prolonged
1353-8020/$ e see front matter Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.parkreldis.2013.07.024
E. van Wensen et al. / Parkinsonism and Related Disorders 19 (2013) 1110e1112
bed rest e is associated with more frequent development of BPPV [13], but whether this applies to PD patients remains speculative. Another hypothesis is that BPPD in PD patients could result from head trauma secondary to the frequent falls that are common in PD patients. We therefore aimed to examine how many patients with PD have BPPV (classical and atypical [14e16]), how often this had remained undetected, and what factors would predict the presence of BPPV in PD patients. 2. Methods In an observational study we investigated the prevalence of BPPV in an unselected cohort of consecutive outpatients with PD who visited a large Dutch community hospital between 2004 and 2010. Inclusion criteria were a diagnosis of PD according to the UK Brain Bank criteria, and being able to visit the outpatient clinic. Exclusion criterion was a diagnosis of BPPV in the last year. All outpatients with a known diagnosis of PD from the registry of two regional hospitals received a standardized questionnaire. This questionnaire included demographic details and disease characteristics (including disease duration, frequency of falls and medication use). Patients also completed the Dizziness Handicap Inventory (DHI), which is a validated questionnaire to assess the impact of dizziness on daily life [17]. The DHI has a score range of 0e100, with higher scores representing more severe impairments by dizziness. During a hospital visit, patients were examined by a neurologist with experience in movement disorders. Examinations included the UPDRS- MDS motor-score [18] and orthostatic hypotension (blood pressure assessment both in the supine position and in the upright position every minute for a total of 3 min). An experienced vestibular technician performed the DixeHallpike maneuver [19] and diagnosed the patient according to the following combination of symptoms and signs: no dizziness or nystagmus: no BPPV; dizziness and classical nystagmus: classical BPPV; dizziness but no nystagmus: atypical BPPV; no dizziness but positive nystagmus: atypical BPPV; no dizziness and no nystagmus, but a classical history for BPPV: historical BPPV. Patients with classical or atypical BPPV were treated with a canalith-reposition maneuver [20] and clinically re-examined after three months. At this time, the effect of treatment was evaluated by asking patients whether they had experienced any improvement or deterioration, and if so, they were asked to rate this change on a visual analog scale from 0 to 100. These patients also completed the DHI again, and the neurologist completed the UPDRS motor score. We cannot exclude the possibility for a central origin such as brainstem ischemia that could have caused the dizziness in our patients. However, we feel such a central cause was unlikely among the patients described here, in light of both their subjective complaints (isolated position-dependent vertigo), their physical examination (no accompanying signs pointing to a brainstem lesion) and the therapeutic effects of the DixeHallpike maneuver. We did not perform the alternate head jerk to evaluate for potential central causes for vertigo, and we did not perform a CT or MRI as part of our study, but such tests would be useful to perform in any patients with vertigo that is not readily explained by a peripheral cause. Ethical approval was waived.
3. Statistical analysis We searched for factors related to the presence of BPPV in PD patients. The relation between BPPV and age, gender, DHI, disease duration, monthly frequency of falls, UPDRS score and Hoehn and Yahr score was assessed univariately. The Fisher’s exact test was used for nominal variables (gender), the ManneWhitney U test for continuous data because of the difference in population sizes. Continuous variables were disease duration, frequency of falls, UPDRS score, Hoehn and Yahr score and DHI. Change in DHI score in treated BPPV patients was tested with the Wilcoxon signed-rank test. The two most strongly related factors (based on the lowest p value of the univariate relation) were included in a multivariate logistic regression model to adjust for each other. 4. Results We sent an invitation letter to 803 PD patients, 305 of whom (38%) responded positively (186 men (61%)), mean age 70.5 years (SD 9.5 years), median disease duration 4.8 years (range 0e42 years), median UPDRS-score 21 (range 3e108), and median DHI score 22 (range 0e100). Eighty patients (26%) reported more than one fall per month. There were 58 patients in Hoehn and Yahr
1111
stadium 1, 194 in stadium 2, 26 in stadium 3, 9 in stadium 4 and 18 patients in stadium 5. Among the responders 151 patients (49%) reported episodic dizziness, 12 of whom appeared to have a classical BPPV, and an additional four had atypical BPPV. Taken together, among patients with PD and dizziness, 10.6% had BPPV. A further 32 (10.5%) patients had a history suggestive for BPPV, but no objective signs during testing. None of the patients who denied dizziness turned out to have objective signs of BPPV. 57 patients (38%) had symptomatic orthostatic hypotension of whom three also had a classical and two an atypical BPPV. We acknowledge that there could be a difference between patients with positional dizziness with or without nystagmus (as some of the latter may not represent BPPV at all), and future research should address this issue in larger numbers of patients. The 16 BPPV patients were treated with a canalith-reposition maneuver and were re-examined three months later. Ten of them (63%) had remained free of symptoms for three months after treatment, three patients reported mild improvement in dizziness complaints, while three patients indicated no or only slight improvement. Overall the median DHI in these BPPV patients decreased significantly after treatment (median before treatment: 41, range 6e92, median after treatment: 24, range 0e74; p ¼ 0.01). Patients with classical or atypical BPPV (n ¼ 16) had a median disease duration of 4 years (range 1e18 years) and their Hoehn and Yahr scores were 1 (n ¼ 4), 2 (n ¼ 9) and 5 (n ¼ 3). BPPV patients didn’t differ from non-BPPV PD-patients with respect to sex (50% versus 39%, p ¼ 0.43), age (median 73 years versus 72 years, p ¼ 0.87), of Hoehn and Yahr score (both groups had a median score of 2, p ¼ 0.88) or frequency of falls (p ¼ 0.38). The DHI score was significantly higher in patients with BPPV (median 41) compared to patients without BPPV (median 22, p < 0.07) (Table 1). Only the presence of dizziness and the DHI-score were related to the presence of BPPV. In the multivariate logistic regression model, DHI was not longer related to the presence of BPPV when dizziness was included in the model (coefficient 0.43, p ¼ 0.21). 5. Discussion These results show that overall, 5.3% of patients with PD have BPPV, and 10.8% of patients who self-report dizziness have objective signs of BPPV. Moreover, our results indicate that BPPV can be treated easily in this population, with complete relief of symptoms in the majority of patients. Dizziness in PD is usually attributed to orthostatic hypotension. Although the majority of dizzy patients in our population also had signs of OH, we raise attention to the possibility that BPPV may additionally contribute to episodic dizziness. Three earlier case reports alerted to this possibility [21], but the present study is the
Table 1 Characteristics of Parkinson’s patients (n ¼ 305).
Dizziness (%) Disease duration (median (minemax)) Men (%) Hoehn & Yahr (median (minemax)) Age (median (minemax)) Frequency of falls (once per month (%)) DHI (median (minemax)) DHI <30 (%)
BPPV þ (16)
BPPVe(287)
P-value
16 (100%) 4 (1e18)
135 (47%) 5 (0e42)
<0.001 0.69
8 (50%) 2 (1e5)
176 (61%) 2 (0e5)
0.43 0.88
73 (66e85) 6 (38%) 41 (6e92) 6 (38%)
DHI ¼ Dizziness Handicap Inventory (DHI) [17].
72 (38e92)
0.87
74 (26%)
0.38
22 (0e100) 181 (64%)
0.07 0.06
1112
E. van Wensen et al. / Parkinsonism and Related Disorders 19 (2013) 1110e1112
first to give an indication of the possible prevalence (almost 11% in this cohort). We admit that this prevalence is only an indication, because the response rate to our initial questionnaire was only 38%. Selection bias can therefore not be excluded, for example because patients with BPPV or another form of dizziness were more likely to respond, or the bias among non-responders may have act in the opposite direction, such that patients with greater disease severity and more complaints did not respond. We were reassured to find that we only found objective signs of BPPD among those patients who self-reported dizziness. It is therefore unlikely that we missed a large proportion of patients with BPPV among non-responders who declined to participate because they experienced no dizziness. In other words, a first pragmatic step to screen for BPPD is to simply ask for subjective dizziness. A DHI is not necessary for this purpose, since the scores did not independently predict the presence of BPPV. Patients who self-report dizziness can then be examined further to test for BPPV, using the DixeHallpike maneuver. In patients with a history suggestive for BPPV but with a negative DixeHallpike maneuver, we did not repeat this diagnostic procedure. Repeating the DixeHallpike maneuver could have resulted in a higher prevalence rate, and this could be considered in clinical practice to avoid missing BPPD. A further selection bias may have been introduced by the fact that we invited patients to come to the hospital to participate, which may have favored inclusion of less severely affected ones. However, we found no relation with disease severity, although the numbers of affected patients were perhaps too small to reliably exclude an influence of disease severity. It is worth noting that among the 16 individual cases, disease severity ranged widely, with a DHI ranging from 6 to 92. Leaving BPPV untreated can lead to complicating situations, such as falls during transfers from a seated or recumbent position [22]. Our results indicate that in patients with PD, BPPV can be treated easily using a canalith-reposition maneuver, with complete relief of symptoms in the majority of patients that lasted for at least three months. Only three patients experienced no or only slight improvement. Repeating one of the canalith reposition maneuver could perhaps further improve the overall therapeutic efficacy. The high therapeutic success (even among patients who had themselves not sought medical attention for dizziness) underscores the importance of actively screening for dizziness, and to treat BPPV accordingly. Similarly, screening instruments and therapeutic options are available for those patients whose dizziness can be attributed to orthostatic hypotension [23]. Acknowledgment This study was supported by the Gelre Hospital in Apeldoorn. We would like to thank our colleague-neurologists in the hospitals in Deventer and Zutphen for their support and especially Sylvia Masius for her support and all the food and beverage. Appendix Author roles E. van Wensen: Writing of the first draft, conception, organization and execution of research project. R. B. van Leeuwen: Writing of the first draft, conception, organization and execution of research project. H.J. van der Zaag-Loonen: Statistical analysis and Review and Critique of manuscript. S. Masius-Olthof: Organization and execution of research project. B.R. Bloem: Conception of research project and Review and Critique of manuscript.
Financial Disclosures E. van Wensen: received payment by Abbot for contributions for the National Steering Committee Navigat PD. R. B. van Leeuwen: reports no disclosures. H.J. van der Zaag-Loonen: reports no disclosures. S. Masius-Olthof: reports no disclosures. Prof. Bloem: Has served as an editorial board member of Movement Disorders, currently serves as an editorial board member of Physiotherapy Canada, is Associate Editor for the Journal of Parkinson’s disease, received honoraria from serving on the scientific advisory board for Boehringer Ingelheim, Glaxo-Smith-Kline, Danone and Solvay, and received research support from the Netherlands Organization for Scientific Research, the Michael J Fox Foundation, the Prinses Beatrix Foundation, the Stichting Internationaal Parkinson Fonds and the Alkemade Keuls fonds. References [1] Carpenter MG, Allum JH, Honegger F, Adkin AL, Bloem BR. Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatr 2004;75:1245e54. [2] Bloem BR, Hausdorff JM, Visser JE, Giladi N. Falls and freezing in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord 2004;19:871e84. [3] Latt MD, Lord SR, Morris JG, Fung VS. Clinical and physiological assessments for elucidating falls risk in Parkinson’s disease. Mov Disord 2009;24: 1280e9. [4] Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA. Predictors of future falls in Parkinson disease. Neurology 2010;75:116e24. [5] Allcock LM, Rowan EN, Steen IN, Wesnes K, Kenny RA, Burn DJ. Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat Disord 2009;15:110e5. [6] Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM. Dual tasking, gait rhythmicity, and Parkinson’s disease: which aspects of gait are attention demanding? Eur J Neurosci 2005;22:1248e56. [7] Kim S, Horak FB, Carlson-Kuhta P, Park S. Postural feedback scaling deficits in Parkinson’s disease. J Neurophysiol 2009;102:2910e20. [8] Davis LE. Dizziness in elderly men. J Am Geriatr Soc 1994;42:1184e8. [9] Katsarkas A. Dizziness in aging: a retrospective study of 1194 cases. Otolaryngol Head Neak Surg 1994;110:296e301. [10] Oghalai JS, Manolidis S, Bath JL, Stewart MG, Jenkins HA. Unrecognized benign paroxysmal positional vertigo in elderly patients. Otolaryngol Head Neck Surg 2000;122:630e4. [11] Tinetti ME, Williams CS, Gill TM. Health, functional and psychological outcomes among older persons with chronic dizziness. J Am Geriatr Soc 2000;48: 417e21. [12] Grimby A, Rosenhall U. Healthrelated quality of life and dizziness in old age. Gerontology 1995;41:286e98. [13] Strupp M, Brandt T. Diagnosis and treatment of vertigo and dizziness. Dtsch Arztebl Int 2008;105:173e80. [14] Buki B, Simon L, Garab S, Lundberg YW, Junger H, Straumann D. Sitting-up vertigo and trunk retropulsion in patients with benign positional vertigo but without positional nystagmus. J Neurol Neurosurg Psychiatr 2011;82: 98e104. [15] Tirelli G, D’Orlando E, Giacomarra V, Russoulo M. Benign positional vertigo without detectable nystagmus. The Laryngoscope 2001;111:1053e6. [16] Haynes DS, Resser JR, Labadie RF, Girasole CR, Kovach BT, Scheker LE, et al. Treatment of benign positional vertigo using the Semont maneuver: efficacy in patients presenting without nystagmus. The Laryngoscope 2002;112: 796e801. [17] Jacobson GP, Newman CW. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Sug 1990;116:424e7. [18] Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 2008;23:2129e70. [19] Furman J, Cass S. Benign paroxysmal positional vertigo. N Engl J Med 1999;341:1590e6. [20] von Brevern M, Seelig T, Radtke A, Tiel-Wilck K, Neuhauser H, Lempert T. Short-term efficacy of Epley’s manoeuvre: a double-blind randomised trial. J Neurol Neurosurg Psychiatr 2006;77:980e2. [21] Shachie V, Aranke BS, KApil D, Sethi. Benign paroxysmal positional vertigo in Parkinson’s disease. Neurology 2003;61:1156. [22] Ganança FF, Gazzola JM, Ganança CF, Caovilla HH, Ganança MM, Cruz OL. Elderly falls associated with benign paroxysmal positional vertigo. Braz J Otorhinolaryngol 2010; JaneFeb;76:113e20. [23] Thijs RD, Bloem BR, van Dijk JG. Falls, faints, fits and funny turns. J Neurol 2009;256:155e67.
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Benign paroxysmal positional vertigo in Parkinson’s disease E. van Wensen a, *, R.B. van Leeuwen a, H.J. van der Zaag-Loonen a, S. Masius-Olthof a, B.R. Bloem b a b
Gelre Hospitals, Apeldoorn, A. Schweitzerlaan 31, 7334 DZ Apeldoorn, The Netherlands Radboud University Nijmegen Medical Centre, Donders Institute for Brain, Cognition and Behavior, Department of Neurology, Nijmegen, The Netherlands
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 February 2013 Received in revised form 16 July 2013 Accepted 23 July 2013
Background: Dizziness is a frequent complaint of patients with Parkinson’s disease (PD), and orthostatic hypotension (OH) is often thought to be the cause. We studied whether benign paroxysmal positional vertigo (BPPV) could also be an explanation. Aim: To assess the prevalence of benign paroxysmal positional vertigo in patients with Parkinson’s disease, with and without dizziness. Methods: 305 consecutive outpatients with PD completed the Movement Disorders Society-sponsored revision of the Unified Parkinsons’ Disease Rating Scale-motor score, the Dizziness Handicap Inventory, the DixeHallpike maneuver and a test for orthostatic hypotension. When positive for benign paroxysmal positional vertigo, a repositioning maneuver was performed. Patients were followed for three months to determine the clinical response. Results: 305 patients responded (186 men (61%), mean age 70.5 years (Standard Deviation 9.5 years)), of whom 151 (49%) complained of dizziness. 57 (38%) of the dizzy patients appeared to have orthostatic hypotension; 12 patients (8%) had a classical but previously unrecognized benign paroxysmal positional vertigo. A further four patients (3%) had a more atypical presentation of benign paroxysmal positional vertigo. Three months after treatment, 11 (92%) of patients with classical benign paroxysmal positional vertigo were almost or completely without complaints. We found no ‘hidden’ benign paroxysmal positional vertigo among patients without dizziness. The prevalence of benign paroxysmal positional vertigo among all patients with PD was 5.3%. Conclusion: Among Parkinson patients with symptoms of dizziness, up to 11% may have benign paroxysmal positional vertigo, which can be treated easily and successfully. Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.
Keywords: Parkinson’s disease Dizziness BPPV Orthostatic hypotension DixeHallpike maneuver
1. Introduction Balance disorders and falls are common in patients with Parkinson’s disease (PD). The pathophysiology is complex and multifactorial. Contributing factors that are reported frequently include freezing of gait, abnormal postural reflexes, frontal executive dysfunction and environmental factors [1e7]. Much less attention has focused on the possible role of periods of dizziness preceding a fall. Many patients with PD complain of dizziness, and in most cases this is attributed to orthostatic hypotension. Benign Paroxysmal Positional Vertigo (BPPV) is another cause of episodic dizziness, but it has rarely been associated with falls in PD. BPPV is a common condition, especially in the elderly [8e10]. It causes marked
* Corresponding author. Tel.: þ31 641290005; fax: þ31 555818234. E-mail addresses: [email protected], [email protected] (E. van Wensen).
disability, and has a great impact on the quality of life (QoL) [11,12]. BPPV can be diagnosed easily, and it is readily treatable. However, many affected patients remain undiagnosed, and both patients and caregivers are commonly unaware of the presence of BPPV [10]. It would be interesting to compare our present findings in Parkinson patients to baseline population rates for BPPV in a similar elderly cohort, but no prior study has reported this. The study of Ogholai et al. [10] comes closest to our approach, and the percentage of unrecognized benign paroxysmal positional vertigo in their hands ranged from 9% in an inner-city geriatric population up to 39% among patients aged 70 years or older in a dizziness clinic. We hypothesize that BPPV is often not recognized in patients with PD, and that its presence contributes to falls and poor QoL in this patient group. It is conceivable that PD patients are prone to develop BPPV, because their global hypokinesia and bradykinesia (leading to slower head movements) might facilitate earlier development of canalolithiasis or cupulolithiasis, causing BPPV. Indeed, reduced mobility e as occurs in patients with prolonged
1353-8020/$ e see front matter Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.parkreldis.2013.07.024
E. van Wensen et al. / Parkinsonism and Related Disorders 19 (2013) 1110e1112
bed rest e is associated with more frequent development of BPPV [13], but whether this applies to PD patients remains speculative. Another hypothesis is that BPPD in PD patients could result from head trauma secondary to the frequent falls that are common in PD patients. We therefore aimed to examine how many patients with PD have BPPV (classical and atypical [14e16]), how often this had remained undetected, and what factors would predict the presence of BPPV in PD patients. 2. Methods In an observational study we investigated the prevalence of BPPV in an unselected cohort of consecutive outpatients with PD who visited a large Dutch community hospital between 2004 and 2010. Inclusion criteria were a diagnosis of PD according to the UK Brain Bank criteria, and being able to visit the outpatient clinic. Exclusion criterion was a diagnosis of BPPV in the last year. All outpatients with a known diagnosis of PD from the registry of two regional hospitals received a standardized questionnaire. This questionnaire included demographic details and disease characteristics (including disease duration, frequency of falls and medication use). Patients also completed the Dizziness Handicap Inventory (DHI), which is a validated questionnaire to assess the impact of dizziness on daily life [17]. The DHI has a score range of 0e100, with higher scores representing more severe impairments by dizziness. During a hospital visit, patients were examined by a neurologist with experience in movement disorders. Examinations included the UPDRS- MDS motor-score [18] and orthostatic hypotension (blood pressure assessment both in the supine position and in the upright position every minute for a total of 3 min). An experienced vestibular technician performed the DixeHallpike maneuver [19] and diagnosed the patient according to the following combination of symptoms and signs: no dizziness or nystagmus: no BPPV; dizziness and classical nystagmus: classical BPPV; dizziness but no nystagmus: atypical BPPV; no dizziness but positive nystagmus: atypical BPPV; no dizziness and no nystagmus, but a classical history for BPPV: historical BPPV. Patients with classical or atypical BPPV were treated with a canalith-reposition maneuver [20] and clinically re-examined after three months. At this time, the effect of treatment was evaluated by asking patients whether they had experienced any improvement or deterioration, and if so, they were asked to rate this change on a visual analog scale from 0 to 100. These patients also completed the DHI again, and the neurologist completed the UPDRS motor score. We cannot exclude the possibility for a central origin such as brainstem ischemia that could have caused the dizziness in our patients. However, we feel such a central cause was unlikely among the patients described here, in light of both their subjective complaints (isolated position-dependent vertigo), their physical examination (no accompanying signs pointing to a brainstem lesion) and the therapeutic effects of the DixeHallpike maneuver. We did not perform the alternate head jerk to evaluate for potential central causes for vertigo, and we did not perform a CT or MRI as part of our study, but such tests would be useful to perform in any patients with vertigo that is not readily explained by a peripheral cause. Ethical approval was waived.
3. Statistical analysis We searched for factors related to the presence of BPPV in PD patients. The relation between BPPV and age, gender, DHI, disease duration, monthly frequency of falls, UPDRS score and Hoehn and Yahr score was assessed univariately. The Fisher’s exact test was used for nominal variables (gender), the ManneWhitney U test for continuous data because of the difference in population sizes. Continuous variables were disease duration, frequency of falls, UPDRS score, Hoehn and Yahr score and DHI. Change in DHI score in treated BPPV patients was tested with the Wilcoxon signed-rank test. The two most strongly related factors (based on the lowest p value of the univariate relation) were included in a multivariate logistic regression model to adjust for each other. 4. Results We sent an invitation letter to 803 PD patients, 305 of whom (38%) responded positively (186 men (61%)), mean age 70.5 years (SD 9.5 years), median disease duration 4.8 years (range 0e42 years), median UPDRS-score 21 (range 3e108), and median DHI score 22 (range 0e100). Eighty patients (26%) reported more than one fall per month. There were 58 patients in Hoehn and Yahr
1111
stadium 1, 194 in stadium 2, 26 in stadium 3, 9 in stadium 4 and 18 patients in stadium 5. Among the responders 151 patients (49%) reported episodic dizziness, 12 of whom appeared to have a classical BPPV, and an additional four had atypical BPPV. Taken together, among patients with PD and dizziness, 10.6% had BPPV. A further 32 (10.5%) patients had a history suggestive for BPPV, but no objective signs during testing. None of the patients who denied dizziness turned out to have objective signs of BPPV. 57 patients (38%) had symptomatic orthostatic hypotension of whom three also had a classical and two an atypical BPPV. We acknowledge that there could be a difference between patients with positional dizziness with or without nystagmus (as some of the latter may not represent BPPV at all), and future research should address this issue in larger numbers of patients. The 16 BPPV patients were treated with a canalith-reposition maneuver and were re-examined three months later. Ten of them (63%) had remained free of symptoms for three months after treatment, three patients reported mild improvement in dizziness complaints, while three patients indicated no or only slight improvement. Overall the median DHI in these BPPV patients decreased significantly after treatment (median before treatment: 41, range 6e92, median after treatment: 24, range 0e74; p ¼ 0.01). Patients with classical or atypical BPPV (n ¼ 16) had a median disease duration of 4 years (range 1e18 years) and their Hoehn and Yahr scores were 1 (n ¼ 4), 2 (n ¼ 9) and 5 (n ¼ 3). BPPV patients didn’t differ from non-BPPV PD-patients with respect to sex (50% versus 39%, p ¼ 0.43), age (median 73 years versus 72 years, p ¼ 0.87), of Hoehn and Yahr score (both groups had a median score of 2, p ¼ 0.88) or frequency of falls (p ¼ 0.38). The DHI score was significantly higher in patients with BPPV (median 41) compared to patients without BPPV (median 22, p < 0.07) (Table 1). Only the presence of dizziness and the DHI-score were related to the presence of BPPV. In the multivariate logistic regression model, DHI was not longer related to the presence of BPPV when dizziness was included in the model (coefficient 0.43, p ¼ 0.21). 5. Discussion These results show that overall, 5.3% of patients with PD have BPPV, and 10.8% of patients who self-report dizziness have objective signs of BPPV. Moreover, our results indicate that BPPV can be treated easily in this population, with complete relief of symptoms in the majority of patients. Dizziness in PD is usually attributed to orthostatic hypotension. Although the majority of dizzy patients in our population also had signs of OH, we raise attention to the possibility that BPPV may additionally contribute to episodic dizziness. Three earlier case reports alerted to this possibility [21], but the present study is the
Table 1 Characteristics of Parkinson’s patients (n ¼ 305).
Dizziness (%) Disease duration (median (minemax)) Men (%) Hoehn & Yahr (median (minemax)) Age (median (minemax)) Frequency of falls (once per month (%)) DHI (median (minemax)) DHI <30 (%)
BPPV þ (16)
BPPVe(287)
P-value
16 (100%) 4 (1e18)
135 (47%) 5 (0e42)
<0.001 0.69
8 (50%) 2 (1e5)
176 (61%) 2 (0e5)
0.43 0.88
73 (66e85) 6 (38%) 41 (6e92) 6 (38%)
DHI ¼ Dizziness Handicap Inventory (DHI) [17].
72 (38e92)
0.87
74 (26%)
0.38
22 (0e100) 181 (64%)
0.07 0.06
1112
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first to give an indication of the possible prevalence (almost 11% in this cohort). We admit that this prevalence is only an indication, because the response rate to our initial questionnaire was only 38%. Selection bias can therefore not be excluded, for example because patients with BPPV or another form of dizziness were more likely to respond, or the bias among non-responders may have act in the opposite direction, such that patients with greater disease severity and more complaints did not respond. We were reassured to find that we only found objective signs of BPPD among those patients who self-reported dizziness. It is therefore unlikely that we missed a large proportion of patients with BPPV among non-responders who declined to participate because they experienced no dizziness. In other words, a first pragmatic step to screen for BPPD is to simply ask for subjective dizziness. A DHI is not necessary for this purpose, since the scores did not independently predict the presence of BPPV. Patients who self-report dizziness can then be examined further to test for BPPV, using the DixeHallpike maneuver. In patients with a history suggestive for BPPV but with a negative DixeHallpike maneuver, we did not repeat this diagnostic procedure. Repeating the DixeHallpike maneuver could have resulted in a higher prevalence rate, and this could be considered in clinical practice to avoid missing BPPD. A further selection bias may have been introduced by the fact that we invited patients to come to the hospital to participate, which may have favored inclusion of less severely affected ones. However, we found no relation with disease severity, although the numbers of affected patients were perhaps too small to reliably exclude an influence of disease severity. It is worth noting that among the 16 individual cases, disease severity ranged widely, with a DHI ranging from 6 to 92. Leaving BPPV untreated can lead to complicating situations, such as falls during transfers from a seated or recumbent position [22]. Our results indicate that in patients with PD, BPPV can be treated easily using a canalith-reposition maneuver, with complete relief of symptoms in the majority of patients that lasted for at least three months. Only three patients experienced no or only slight improvement. Repeating one of the canalith reposition maneuver could perhaps further improve the overall therapeutic efficacy. The high therapeutic success (even among patients who had themselves not sought medical attention for dizziness) underscores the importance of actively screening for dizziness, and to treat BPPV accordingly. Similarly, screening instruments and therapeutic options are available for those patients whose dizziness can be attributed to orthostatic hypotension [23]. Acknowledgment This study was supported by the Gelre Hospital in Apeldoorn. We would like to thank our colleague-neurologists in the hospitals in Deventer and Zutphen for their support and especially Sylvia Masius for her support and all the food and beverage. Appendix Author roles E. van Wensen: Writing of the first draft, conception, organization and execution of research project. R. B. van Leeuwen: Writing of the first draft, conception, organization and execution of research project. H.J. van der Zaag-Loonen: Statistical analysis and Review and Critique of manuscript. S. Masius-Olthof: Organization and execution of research project. B.R. Bloem: Conception of research project and Review and Critique of manuscript.
Financial Disclosures E. van Wensen: received payment by Abbot for contributions for the National Steering Committee Navigat PD. R. B. van Leeuwen: reports no disclosures. H.J. van der Zaag-Loonen: reports no disclosures. S. Masius-Olthof: reports no disclosures. Prof. Bloem: Has served as an editorial board member of Movement Disorders, currently serves as an editorial board member of Physiotherapy Canada, is Associate Editor for the Journal of Parkinson’s disease, received honoraria from serving on the scientific advisory board for Boehringer Ingelheim, Glaxo-Smith-Kline, Danone and Solvay, and received research support from the Netherlands Organization for Scientific Research, the Michael J Fox Foundation, the Prinses Beatrix Foundation, the Stichting Internationaal Parkinson Fonds and the Alkemade Keuls fonds. References [1] Carpenter MG, Allum JH, Honegger F, Adkin AL, Bloem BR. Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatr 2004;75:1245e54. [2] Bloem BR, Hausdorff JM, Visser JE, Giladi N. Falls and freezing in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord 2004;19:871e84. [3] Latt MD, Lord SR, Morris JG, Fung VS. Clinical and physiological assessments for elucidating falls risk in Parkinson’s disease. Mov Disord 2009;24: 1280e9. [4] Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA. Predictors of future falls in Parkinson disease. Neurology 2010;75:116e24. [5] Allcock LM, Rowan EN, Steen IN, Wesnes K, Kenny RA, Burn DJ. Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat Disord 2009;15:110e5. [6] Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM. Dual tasking, gait rhythmicity, and Parkinson’s disease: which aspects of gait are attention demanding? Eur J Neurosci 2005;22:1248e56. [7] Kim S, Horak FB, Carlson-Kuhta P, Park S. Postural feedback scaling deficits in Parkinson’s disease. J Neurophysiol 2009;102:2910e20. [8] Davis LE. Dizziness in elderly men. J Am Geriatr Soc 1994;42:1184e8. [9] Katsarkas A. Dizziness in aging: a retrospective study of 1194 cases. Otolaryngol Head Neak Surg 1994;110:296e301. [10] Oghalai JS, Manolidis S, Bath JL, Stewart MG, Jenkins HA. Unrecognized benign paroxysmal positional vertigo in elderly patients. Otolaryngol Head Neck Surg 2000;122:630e4. [11] Tinetti ME, Williams CS, Gill TM. Health, functional and psychological outcomes among older persons with chronic dizziness. J Am Geriatr Soc 2000;48: 417e21. [12] Grimby A, Rosenhall U. Healthrelated quality of life and dizziness in old age. Gerontology 1995;41:286e98. [13] Strupp M, Brandt T. Diagnosis and treatment of vertigo and dizziness. Dtsch Arztebl Int 2008;105:173e80. [14] Buki B, Simon L, Garab S, Lundberg YW, Junger H, Straumann D. Sitting-up vertigo and trunk retropulsion in patients with benign positional vertigo but without positional nystagmus. J Neurol Neurosurg Psychiatr 2011;82: 98e104. [15] Tirelli G, D’Orlando E, Giacomarra V, Russoulo M. Benign positional vertigo without detectable nystagmus. The Laryngoscope 2001;111:1053e6. [16] Haynes DS, Resser JR, Labadie RF, Girasole CR, Kovach BT, Scheker LE, et al. Treatment of benign positional vertigo using the Semont maneuver: efficacy in patients presenting without nystagmus. The Laryngoscope 2002;112: 796e801. [17] Jacobson GP, Newman CW. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Sug 1990;116:424e7. [18] Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 2008;23:2129e70. [19] Furman J, Cass S. Benign paroxysmal positional vertigo. N Engl J Med 1999;341:1590e6. [20] von Brevern M, Seelig T, Radtke A, Tiel-Wilck K, Neuhauser H, Lempert T. Short-term efficacy of Epley’s manoeuvre: a double-blind randomised trial. J Neurol Neurosurg Psychiatr 2006;77:980e2. [21] Shachie V, Aranke BS, KApil D, Sethi. Benign paroxysmal positional vertigo in Parkinson’s disease. Neurology 2003;61:1156. [22] Ganança FF, Gazzola JM, Ganança CF, Caovilla HH, Ganança MM, Cruz OL. Elderly falls associated with benign paroxysmal positional vertigo. Braz J Otorhinolaryngol 2010; JaneFeb;76:113e20. [23] Thijs RD, Bloem BR, van Dijk JG. Falls, faints, fits and funny turns. J Neurol 2009;256:155e67.