Eur Arch Otorhinolaryngol DOI 10.1007/s00405-014-3041-3
Fatigue during an episode of benign paroxysmal positional vertigo Lea Pollak · Rafael Stryjer
Received: 9 December 2013 / Accepted: 30 March 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract Fatigue is characterized by weariness unrelated to exertion levels. It has been reported in chronic neurological diseases such as multiple sclerosis, Parkinson disease and stroke. Patients with benign paroxysmal positional vertigo (BPPV) often complain about fatigue during a vertigo attack. No attention has been paid to this symptom in the literature so far. We were interested to evaluate the frequency and factors influencing fatigue in BPPV. Patients treated for idiopathic BPPV during the years 2011–2012 were prospectively evaluated for the presence of fatigue. During the first visit, patients were asked to complete two questionnaires based on their experience during the last week: the Fatigue severity scale and the Hospital anxiety and depression scale. Patients’ demographic data and BPPV characteristics were registered. Among 172 patients treated for BPPV, 40 (23.2 %) reported fatigue. The mean fatigue score was 4.73 ± 1.98 indicating moderate fatigue. No correlation was found between fatigue and anxiety or fatigue and depression. Fatigue scores were inversely related to age (r = −0.36, p = 0.020) and were not dependent on the type of BPPV, its recurrence, background diseases, gender, duration of vertigo or the presence of autonomic symptoms. Moderate fatigue is quite common during an attack of BPPV. It seems to be a genuine symptom of the entity
L. Pollak Department of Neurology, The Assaf Harofeh Medical Center, Zerifin, Affiliated to the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel L. Pollak (*) Kibutz Galuyot 4, 74012 Ness Ziona, Israel e-mail: [email protected]
R. Stryjer Psychiatric Hospital Beer Yacov, Zerifin, Israel
that might worsen patients’ distress. For severe or persistent fatigue treatment with fatigue relieving drugs such as amantadine, methylphenidate or modafinil could be tried in the future. Keywords Benign paroxysmal positional vertigo · Acute attack · Fatigue
Introduction Benign paroxysmal positional vertigo (BPPV), one of the most frequent causes of peripheral vestibular dysfunction, is characterized by short attacks of vertigo induced by head position changes [1–3]. It is considered to be caused by canalithiasis and/or cupulolithiasis. Otoconial debris becomes detached from the utricular macula and enters one of the semicircular canals of the vestibular labyrinth. Movement of the head in the plane of the canal results in inappropriate stimulation of the sensory hair cells and vertigo. Loosening of the otoconia from the macula may be precipitated by head trauma or an inner ear disorder but the majority of BPPV cases are idiopathic . Particle repositioning maneuvers, aimed to remove the otoconia from the involved semicircular canal, are highly effective in treatment of BPPV [4, 5]. In practice, we often meet BPPV patients who complain about tiredness and fatigue in addition to vertigo. No attention has been paid to this symptom in the literature so far. Fatigue in BPPV might be primary or secondary to other associated symptoms, duration of vertigo or mood changes. Fatigue is a common complaint in neurological diseases [6, 7]. It is characterized by weariness unrelated to exertion levels and is usually not ameliorated by rest. It has been well characterized in chronic disorders such as multiple
sclerosis, postpoliomyelitis, Parkinson disease, spinocerebellar atrophy, central nervous system lupus erythematosus and stroke [8–15]. Fatigue in acute diseases has been less often investigated . In view of patients’ recurrent complaints we were interested to evaluate the frequency and factors influencing fatigue during a BPPV attack.
Methods Patients treated for idiopathic BPPV at a dizziness clinic during the years 2011–2012 were prospectively evaluated for the presence of fatigue. Those who reported fatigue, spontaneously or upon questioning, were included. Patients with a history of significant internal, surgical, neurological or psychiatric disease and patients receiving medication known to cause fatigue were a priori excluded. Mild health problems such as controlled hypertension, infrequent migraine attacks, state after minor surgical or orthopedic procedure was not an exclusion factor. The diagnosis of BPPV was established by a positive Dix–Hallpike or roll test [3, 4]. Duration of symptoms prior to treatment and associated autonomic symptoms such as nausea, vomiting, fainting, sweating or diarrhea were registered. The patients were then asked to complete two questionnaires based on their experience during the last week: the Fatigue severity scale (FSS) and the Hospital anxiety and depression scale (HADS) [17–20]. FSS is a nine-item questionnaire evaluating the impact of fatigue with answers ranging from 1 (strongly agree) to 7 (strongly disagree). Scores between 4 and 4.9 are considered to reflect moderate fatigue while scores 5 and above reflect severe fatigue. The HADS is used to assess levels of anxiety and depression. Seven statements are relevant to generalized anxiety and seven to depression. The maximum score for each is 21. A score of 11–21 indicates a probable mood disorder and score of 8–10 is suggestive of mild mood changes while values of 0–7 are considered normal. The FSS and HADS were shown to have a good internal consistency, reliability and validity. Consecutively, the patients were treated by an appropriate particle repositioning maneuver (Epley maneuver for posterior and barbecue treatment for horizontal canal BPPV) [4, 5]. Patients were again examined within 1 week after the treatment. If necessary, the treatment was repeated at 3–7 day intervals until disappearance of nystagmus on testing. The study was performed in accordance with the Helsinki declaration and approved by the local ethics committee.
Eur Arch Otorhinolaryngol Table 1 Characteristics of BPPV patients with fatigue Mean age (years) Gender Males/females Type of BPPV Posterior canal (% of patients) Horizontal canal Bilateral Autonomic symptoms (% of patients) Mean duration of vertigo (weeks) Number of treatments One (% of patients) Two Three and more
57.3 ± 13.4 11/29 87.5 7.5 5 47.5 7.7 ± 15.7 55 20 25
Statistical methods Paired sample test (paired t test) was applied for comparison of means (i.e., questionnaire scores in men and women and in patients with first versus recurrent attack). Pearson correlation test was used to examine association of numerical variables (i.e., correlations between individual questionnaire scales, correlations between age or symptom duration and questionnaire scales). One-way ANOVA (analysis of variance) was applied for investigating the differences of numerical data in multiple groups (i.e., questionnaire scores according to the type of BPPV or number of treatments).
Results Incidence of fatigue Among 172 patients treated for BPPV, 40 (23.2 %) reported fatigue associated with vertigo attack and were included in the study. Their characteristics are summarized in Table 1. Fatigue severity The mean fatigue score in a BPPV patient was 4.73 ± 1.98. The average anxiety score was 1.27 ± 0.9 and depression score 1.04 ± 0.82. Fatigue and mood No correlation was found between fatigue and anxiety or fatigue and depression. Anxiety levels were correlated with levels of depression (r = 0.44, p = 0.004).
Eur Arch Otorhinolaryngol Fig. 1 Dependence of fatigue on age in BPPV patients
Fatigue and patients’ demographics Fatigue scores were inversely related to age, i.e., older individuals reported less fatigue than young patients (r = −0.36, p = 0.020) (Fig. 1). Young individuals were more anxious than older patients (r = −0.47, p = 0.002). No interdependence was found between gender and fatigue, anxiety or depression. Fatigue, anxiety or depression was not influenced by background disease. Fatigue and BPPV characteristics The fatigue, anxiety or depression scales did not depend on the type of BPPV. The presence of vegetative symptoms did not influence the degree of fatigue, anxiety or depression. Patients with a first attack of BPPV did not differ from those with recurrent BPPV in respect to fatigue and mood. The duration of symptoms prior to treatment did not influence fatigue, but anxiety was more pronounced in patients with longer symptom duration (r = 0.39, p = 0.03).
Discussion Twenty-three percent of BPPV patients in this study reported moderate fatigue. This is not a negligible number, since 40 % of patients with multiple sclerosis, one-third of patients with Parkinson disease and 30 % of patients after stroke reported fatigue to be one of their most disabling symptoms [8, 10, 11]. The pathophysiology of fatigue in central nervous system disorders has not been clarified and is probably the result of multiple factors . Homeostatic dysregulation such as cerebral glycogen depletion, increased brain
temperature, accumulation of ammonia, inflammatory cytokines, increased serotonin or decreased dopamine, all have been stated to play a role in perception of fatigue [21– 23]. Structural lesions of the hypothalamus, basal ganglia and cortex have been reported to be associated with fatigue [6, 24–26]. In addition to hemispheric lesions, fatigue has been noted in posterior fossa lesions such as postoperative states, posterior head injury and Arnold Chiari malformation [6, 27]. It has been proposed that fatigue might be linked to damage to the reticular formation and the ascending serotonergic tone as well as the substance P. A brainstem fatigue generator model has been proposed in postpoliomyelitis fatigue and postviral fatigue syndromes . It implicates viral damage to the dopaminergic pathways of the ascending reticular activating system. The vestibular nuclei have abundant connections with the activating reticular system and cerebellum. Inappropriate vestibular input might, therefore, contribute to the feeling of fatigue through its influence on distinct neural mediators in the brainstem. In our study, fatigue was not dependent on the type of BPPV, its recurrence, background diseases, gender, duration of vertigo or the presence of autonomic symptoms. Paradoxically, age seemed to have a protective effect on fatigue since older patients experienced less fatigue. In community studies, the relationship between age and fatigue is not consistent except that fatigue is rare before adolescence . Hypothetically, aging of synaptic transmission might explain the decreased influence of abnormal stimulation of pathways in the brainstem and the lower impact of BPPV on fatigue in elderly. Younger patients were more anxious than older patients, but anxiety or depression was not found to influence the level of fatigue. In addition to humeral factors, psychological factors such as mood, perception of effort, motivation and
expectation are well-recognized etiological factor of fatigue [6, 29–31]. In our study, fatigue was not influenced by mood. Anxiety was higher in patients with longer duration of symptoms but the anxiety and depression scales were not increased. This is a quite surprising finding since BPPV patients usually seem to be emotionally upset and extremely anxious during their attack. In a previous study we compared patients with a first attack of acute vestibular dysfunctions to patients with other nonvestibular neurological deficits . Patients with vertigo reported significantly more anxiety than nonvestibular patients, 77 % having severe or moderate anxiety as measured by the HADS. The rate of depression and the premorbid anxiety was similar in both groups. However, only 33 % of vestibular patients had BPPV while the remainder consisted of patients with labyrinthitis or vertebrobasilar stroke. This and the fact that the study was performed in a hospital setting, as opposed to the outpatient clinic in the present study, might explain the differences in anxiety levels. In another work, we explored the beliefs and emotional reactions of patients with BPPV during an attack and following treatment in an outpatient setting . The mean anxiety levels, measured by the State-Trait Anxiety Inventory (STAI), were 39.4 (range 20–80) indicating a quite low anxiety levels as well. Lately, several studies have investigated the radiological correlates of fatigue [6, 34]. While no specific changes have been found on traditional magnetic resonance imaging (MRI), functional imaging techniques such as functional MRI (fMRI) and positron emission tomography (FDGPET) have shown some changes attributable to fatigue. Patients with multiple sclerosis with fatigue had less functional cerebral activation in regions involved in motor planning and execution on fMRI when compared with multiple sclerosis patients without fatigue . Decreased glucose metabolism in putamen, prefrontal and premotor cortex has been found in MS patients with fatigue on FDG-PET scans. In the future, neuroimaging might also be helpful in elucidation of fatigue in diseases of the posterior fossa such as vestibular lesions.
Conclusion Moderate fatigue is quite common during an attack of BPPV. The presence of fatigue is not related to the type or recurrence of BPPV, autonomic signs or mood. It seems to be a genuine symptom of the entity and might worsen patients’ distress. For severe or persistent fatigue treatment with fatigue relieving drugs such as amantadine, methylphenidate or modafinil could be tried in the future.
Eur Arch Otorhinolaryngol Conflict of interest The authors have no competing interests to report.
References 1. Neuhauser HK (2007) Epidemiology of vertigo. Curr Opin Neurol 20:40–46 2. Honrubia V, House M (2001) Mechanism of posterior semicircular canal stimulation in patients with benign paroxysmal positional vertigo. Acta Otolaryngol 121:232–240 3. von Brevern M, Lezius F, Tiel-Wilck K, Tiel-Wilck K, Radtke A, Lempert T (2004) Benign paroxysmal positional vertigo: current status of medical management. Otolaryngol Head Neck Surg 130:381–382 4. Parnes LS, Agrawall SK, Atlas J (2003) Diagnosis and management of benign paroxysmal positional vertigo (BPPV). CMAK 169:681–693 5. Richard W, Bruintjes TD, Oostenbrink P, van Leeuwen RB (2005) Efficacy of the Epley maneuver for posterior canal BPPV: a long-term, controlled study of 81 patients. Ear Nose Throat 84:22–25 6. Chaudhury A, Behan OP (2004) Fatigue in neurological diseases. Lancet 363:978–988 7. Kluger BM, Krupp LB, Enoka RM (2013) Fatigue and fatigability in neurologic illness. Neurology 80:409–416 8. Krupp L (2006) Fatigue is intrinsic to multiple sclerosis (MS) and is the most commonly reported symptom of the disease. Mult Scler 12:367–368 9. Friedman JH, Brown RG, Comella C, Garber CE, Krupp LB, Lou JS et al (2007) Fatigue in Parkinson’s disease: a review. Mov Disord 22:297–308 10. Alves G, Wentzel-Larsen T, Larsen JP (2004) Is fatigue an independent and persistent symptom in patients with Parkinson disease? Neurology 63:1908–1911 11. Lerdal A, Bakken LN, Kouwenhoven SE, Pedersen G, Kirk evold M, Finset A et al (2009) Poststroke fatigue: a review. J Pain Symptom Manage 38:928–949 12. Radman N, Staub F, Aboulafia-Brakha T, Berney A, Bogousslavsky J, Annoni JM (2012) Poststroke fatigue following minor infarcts. A prospective study. Neurology 79:1422–1427 13. Tersteeg IM, Koopman FS, Stolwijk-Swuste JM, Beelen A, Nollet F (2001) A 5-year longitudinal study of fatigue in patients with late-onset sequelae of poliomyelitis. Arch Phys Med Rehabil 92:899–904 14. Brusse E, Brusse-Keizer MGJ, Duidenvoorden HJ, van Swieten JC (2011) Fatigue in spinocerebellar ataxia. Patient self-assessment of an early and disabling symptom. Neurology 76:953–959 15. Omdal R, Mellgren SI, Koldingsnes W, Jacobsen EA, Husby G (2002) Fatigue in patients with systemic lupus erythematosus: lack of associations to serum cytokines, antiphospholipid antibodies, or other disease characteristics. J Rheumatol 29:482–486 16. Lerdal A, Bakken LN, Rasmussen EF, Beiermann C, Ryen S, Pynten S et al (2011) Physical impairment, depressive symptoms and pre-stroke fatigue are related to fatigue in the acute phase after stroke. Disabil Rehabil 33:334–342 17. Schwartz JE, Jandorg L, Krupp LB (1993) The measurement of fatigue: a new instrument. J Psychosom Res 17:753062 18. Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD (1989) The fatigue severity scale: application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 46:1121–1123 19. Zigmond AS, Snaith RP (1983) The Hospital Anxiety and Depression Scale. Acta Psychiatr Scand 67:361–370
Eur Arch Otorhinolaryngol 20. Bjelland I, Dahl AA, Haug TT, Neckelmann D (2002) The validity of the Hospital Anxiety and Depression Scale. An updated literature review. J Psychosom Res 52:69–77 21. Foley TE, Fleshner M (2008) Neuroplasticity of dopamine circuits after exercise: implications for central fatigue. Neuromolecular Med 10:67–80 22. Meeusen R, Watson P, Hasegawa H, Roelands B, Piacentini MF (2006) Central fatigue: the serotonin hypothesis and beyond. Sports Med 36:881–909 23. Nybo L (2008) Hyperthermia and fatigue. J Appl Physiol 104:871–878 24. Chaudhuri A, Behan PO (2000) Fatigue and basal ganglia. J Neurol Sci 179:34–42 25. Bradley LA, Alarcon GS (1999) Is Chiari malformation associated with increased levels of substance P and clinical symptoms in persons with fibromyalgia? Arthritis Rheum 60:471–473 26. Scott LV, Dinan TG (1999) The neuroendocrinology of chronic fatigue syndrome: focus on the hypothalamic-pituitary-adrenal axis. Funct Neurol 14:3–11 27. Bruno RL, Crenage SJ, Fick NM (1998) Parallels between postpolio fatigue and chronic fatigue syndrome: a common pathophysiology? Am J Med 105:66S–73S
28. Lewis G, Wessely S (1992) The epidemiology of fatigue: more questions than answers. J Epidemiol Community Health 46:92–97 29. Lamers F, Hickie I, Merikangas KR (2013) Prevalence and correlates of prolonged fatigue in a U.S. Sample of adolescents. Am J Psychiatry 170:502–510 30. Lam RW, Malhi GS, McIntyre RS, Demyttenaere K, Gorwood P, Michalak EE et al (2013) Fatigue and occupational functioning in major depressive disorder. Aust NZ J Psychiatry (Epub ahead of print) 31. Grafman J, Schwartz V, Dale JK, Scheffers M, Houser C, Straus SE (1993) Analysis of neuropsychological functioning in patients with chronic fatigue syndrome. J Neurol Neurosurg Psychiatry 56:684–689 32. Pollak L, Klein C, Stryjer R, Kossych V, Rabey JM (2003) Anxiety in the first attack of vertigo. Otolaryngol Head Neck Surg 128:829–834 33. Pollak L, Segal P, Stryjer R, Goldberg Stern H (2012) Beliefs and emotional reactions in patients with benign paroxysmal positional vertigo: a longitudinal study. Am J Otolaryngol 33:221–225 34. DeLuca J, Genova HM, Capili EJ, Wylie GR (2009) Func tional neuroimaging of fatigue. Phys Med Rehabil Clin N Am 20:325–337