Otology & Neurotology 35:495Y500 Ó 2014, Otology & Neurotology, Inc.
Pseudo-Spontaneous and Head-Shaking Nystagmus in Horizontal Canal Benign Paroxysmal Positional Vertigo *Sun-Uk Lee, †Hyo-Jung Kim, and ‡Ji-Soo Kim *Department of Neurology, Ajou University College of Medicine, Ajou University Hospital, Suwon; ÞKangwon National University College of Medicine, Medical Research Institute, Seoul National University Bundang Hospital, Seongnam; and þDepartment of Neurology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, Republic of Korea
(28/41, 68.3%, p = 0.028) but in either direction without directional preponderance in geotropic type (p = 0.659). Of the 90 patients who underwent horizontal head-shaking, 27 (30.0%) showed HSN that was more common in apogeotropic than in geotropic type (22/44 [50.0%] versus 5/46 [10.9%], p G 0.001). Patients with apogeotropic HC-BPPV showed predominantly contralesional HSN (19/22 [86.4%], p = 0.001), whereas patients with geotropic type did not show any directional preponderance of HSN (contralesional in 2 and ipsilesional in 3). Conclusion: HSN is more common and mostly contralesional in apogeotropic HC-BPPV. HSN may be a lateralizing sign in apogeotropic HC-BPPV. Different prevalence and patterns of HSN in apogeotropic and geotropic HC-BPPV suggest dissimilar cupular dynamics in those disorders. Key Words: Benign paroxysmal positional vertigoVHead-shaking nystagmusVNystagmusVVertigo.
Objectives: To determine the characteristics and diagnostic value of pseudo-spontaneous and head-shaking nystagmus (HSN) in benign paroxysmal positional vertigo involving the horizontal semicircular canal (HC-BPPV). Study Design: Retrospective case series review. Methods: After excluding 19 patients with canal paresis, abnormal head impulse test, recent history of peripheral or central vestibular disorders, or poor cooperation, we retrospectively recruited 127 patients with HC-BPPV from January 2009 to July 2012. The patients included 69 geotropic and 58 apogeotropic types. We analyzed the pattern of pseudo-spontaneous nystagmus and HSN according to the lesion side. Results: Pseudo-spontaneous nystagmus was observed in 87 (87/127, 68.5%) patients, both in geotropic (46/69, 66.7%) and apogeotropic (41/58, 70.7%) types without difference in the prevalence between the types (p = 0.627). Pseudo-spontaneous nystagmus beat more to the lesion side in apogeotropic type
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Address correspondence and reprint requests to Ji-Soo Kim, M.D., Ph.D., Department of Neurology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 300 Gumidong, Bundang-gu, Seongnam-si, Gyeonggi-do, 463-707, Republic of Korea; E-mail: [email protected] This study was supported by a grant of Korea Medical Device Industrial Cooperative Association. Author contributions Dr. Lee wrote the manuscript and analyzed and interpreted the data. Ms. H. J. Kim analyzed and interpreted the data and revised the manuscript. Dr. Kim conducted the design and conceptualization of the study, interpretation of the data, and drafting and revision of the manuscript. Disclosure Dr. Lee and H. J. Kim report no disclosures. Dr. J. S. Kim serves as an Associate Editor of Frontiers in Neuro-otology and on the Editorial Boards of the Journal of Korean Society of Clinical Neurophysiology, Research in Vestibular Science, Journal of Clinical Neurology, Frontiers in Neuro-ophthalmology, Journal of Neuroophthalmology, Case Reports in Ophthalmological Medicine, and World Journal of Neurology; and received research support from SK Chemicals, Co. Ltd.
Head shaking may reveal central as well as peripheral vestibular dysfunction by generating nystagmus (1). Horizontal head shaking usually induces nystagmus beating to the intact or healthier side in patients with unilateral or asymmetrical peripheral vestibular disorders. This headshaking nystagmus (HSN) of the peripheral type is explained by the following: 1) asymmetrical vestibular inputs due to Ewald’s second law, which states that the excitatory stimuli are more effective than the inhibitory ones in inducing vestibular responses (1Y3); and 2) central velocity storage mechanisms (1,4). Benign paroxysmal positional vertigo (BPPV) is characterized by short-lasting vertigo that develops when the dependent position of the head is changed (5,6). BPPV is explained by free floating otolithic debris in the endolymph of the semicircular canal (canalolithiasis) or debris near or attached to the cupula (cupulolithiasis) (7,8). In BPPV involving the horizontal semicircular canal (HC-BPPV), 495
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2 different types have been recognized according to the patterns of nystagmus induced when the head is turned to either side while supine. In geotropic HC-BPPV, the evoked nystagmus beat to the ground and is explained by otolithic debris in the canal (9). In contrast, the evoked nystagmus beating toward the ceiling in apogeotropic HC-BPPV has been ascribed to otolithic debris attached or near to the cupula within the ampulla (3,10). Patients with either type of HC-BPPV may show spontaneous nystagmus in the sitting position, which is also referred to pseudo-spontaneous because it showed positional modulations and disappearance with resolution of HCBPPV (10Y13). The direction of pseudo-spontaneous nystagmus also has been known to have a lateralizing value in HC-BPPV (10Y12). In HC-BPPV, the otolithic debris in the endolymph or attached to the cupula may alter the dynamics of the endolymph or the cupula during horizontal head shaking and generate HSN. Accordingly, analyzing the patterns of HSN may provide a clue to the altered dynamics of the endolymph or cupula in HC-BPPV. However, no study has attempted systematic analysis of HSN in patients with HC-BPPV. In this study, we analyzed the patterns of pseudo-spontaneous nystagmus and HSN in a large number of patients with either geotropic or apogeotropic type of HC-BPPV. MATERIALS AND METHODS Patients We reviewed the medical records of 146 patients (47 men and 99 women; age range, 34Y92 yr; mean age T SD, 65.0 T 12.4) with HC-BPPV. The age did not differ between men and women (66.1 T 12.8 versus 65.0 T 12.4, p = 0.586). The recruitment was performed using our data base that represents all vestibular patients seen at the Dizziness Clinic of Seoul National University Bundang Hospital from January 2009 to July 2012. The patients included 76 geotropic and 70 apogeotropic types. The right ear was involved in 80 patients (55.2%). The diagnosis of HC-BPPV was based on the following: 1) a history of brief episodes of positional vertigo, 2) directionchanging horizontal nystagmus beating toward the ground (geotropic nystagmus) or to the ceiling (apogeotropic nystagmus) in head turned to either side in the supine position, and 3) absence of identifiable central nervous system disorders that could otherwise explain the positional vertigo and nystagmus. To exclude patients with underlying peripheral vestibular disorders or central positional nystagmus, all patients also received detailed neurotologic examinations including spontaneous and gaze-evoked nystagmus, horizontal head impulse, horizontal and vertical smooth pursuit and saccades, limb ataxia, and balance function in addition to routine neurologic examinations. Even in patients with isolated vertigo, those with central ocular motor signs, limb ataxia, severe imbalance, or no response to repeated canalith repositioning maneuvers were arranged for MRIs. We also excluded patients who showed positive horizontal head impulse test (HIT) as determined at the bedside, documented caloric paresis on bithermal caloric tests, other neurologic deficits indicating central pathologies, and history of continuous vertigo that suggested peripheral or central vestibulopathy within one year. This was to avoid bias
from including the patients with asymmetric canal responses because of peripheral or central vestibulopathies other than BPPV. Although canal paresis or a positive HIT may result from HC-BPPV itself (14,15), we excluded those cases with canal paresis or positive HIT to avoid bias from including patients with underlying vestibulopathy. After excluding 19 patients with canal paresis (n = 12), abnormal head impulse test (n = 2), previous history of other vestibulopathies (n = 2, one with Me´nie`re’s disease and the other with lateral medullary infarction) and poor cooperation during video-oculography (n = 3), we retrospectively analyzed the patterns of pseudo-spontaneous nystagmus and HSN in 127 patients.
Neurotologic Evaluation After measuring the pseudo-spontaneous nystagmus in sitting position, patients lay supine from sitting (lying-down nystagmus) and turned their heads to either side while supine (head-turning nystagmus) to induce positional nystagmus. Then, the patients were moved from a supine to sitting position, and the head was bent down (head-bending nystagmus) (16). We excluded the patients with BPPV involving the posterior or anterior canals. Nystagmus was first observed without fixation using a videoFrenzel goggle system (SLMED, Seoul, Republic of Korea). The affected ear was determined by comparing the intensity of the nystagmus, with an assumption that the induced nystagmus is more intense when the head is rotated to the affected side in the geotropic type and to the intact side in the apogeotropic type. When the decision was inconclusive because of near symmetrical nystagmus, the direction of lying-down or head-bending nystagmus was also considered. In recent studies, the lying-down nystagmus mostly beat to the intact ear (10,12,17,18), whereas the head-bending nystagmus beat to the lesion side in geotropic HCBPPV (10,16). In apogeotropic type, the directions of lying-down and head-bending nystagmus were mostly opposite to those induced in the geotropic type. Eye movements were also recorded using 3-dimensional videooculography (SMI, Teltow, Germany). Spontaneous nystagmus was recorded both with and without fixation while sitting. After spontaneous nystagmus was subsided, HSN was induced using a passive head-shaking maneuver. The head was shaken in a sinusoidal pattern at the frequency of 2.8 Hz paced to the sound of a metronome. We measured the mean slow-phase velocity (SPV) of the first 3 beats of HSN. HSN was observed until it disappeared. The presence of HSN was defined only when the SPV of the induced nystagmus exceeded the values observed in normal controls after subtracting the SPV of pseudo-spontaneous nystagmus (horizontal HSN Q3 degrees per second; vertical HSN Q2 degrees per second; torsional HSN Q2 degrees per second), and when the nystagmus lasted more than 5 seconds (19). The head impulse test was performed manually with a rapid rotation of the head at an approximate amplitude of 20 degrees in the yaw plane with a high acceleration. Bedside head impulse test was considered abnormal if a corrective saccade was present (20). Two patients with abnormal HIT were excluded. Bithermal caloric tests were performed by irrigating the ears for 25 seconds with 50 ml of cold and hot water (30-C and 44-C, respectively). Asymmetry of vestibular function was calculated using Jongkees’ formula. Canal paresis was defined as a response difference of 25% or more between the ears (19), and 12 patients with canal paresis were also excluded. No patients took any medications that could affect the vestibular function during the evaluation.
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PSEUDO-SPONTANEOUS AND HSN IN HC-BPPV
FIG. 1. Pseudo-spontaneous nystagmus. Pseudo-spontaneous nystagmus was observed both in geotropic and apogeotropic types without difference in the prevalence between the types. The pseudo-spontaneous nystagmus more commonly beat to the lesion side in apogeotropic type but without directional preponderance in geotropic type.
Statistical Analysis Statistical analyses were performed with SPSS (version 18.0, Chicago, IL, USA). The clinical variables were compared using the W2 test (2 tailed), independent sample t test, and binomial test.
RESULTS Pseudo-Spontaneous Nystagmus Pseudo-spontaneous nystagmus was observed in 87 (87/127, 68.5%) patients with HC-BPPV, both in geotropic (46/69, 66.7%) and apogeotropic (41/58, 70.7%) types without difference in the prevalence between the types (p = 0.627, W2 test; Fig. 1). Pseudo-spontaneous nystagmus was mostly mild with the mean SPV ranging from 0.2 to 4.6 degrees per second (mean T SD = 1.3 T 0.9 degrees per second). Only 46 (52.9%) of the 87 patients showed mean SPV of pseudo-spontaneous nystagmus more than 1.0 degrees per second. The pseudospontaneous nystagmus more commonly beat to the lesion side (28/41, 68.3%, p = 0.028, binomial test) in apogeotropic type but either to the intact (25/46, 54.3%) or lesioned (21/46, 45.7%) side without directional preponderance (p = 0.659, binomial test) in the geotropic group (Fig. 1). Head-Shaking Nystagmus Of the 90 patients who underwent horizontal head shaking, 27 (30.0%) showed horizontal HSN. Maximum SPV of horizontal HSN ranged from 3.1 to 9.9 degrees per second (mean T SD = 4.8 T 1.9 degrees per second), and its duration varied from 5 to more than 15 seconds. HSN was more commonly observed in the apogeotropic than in the geotropic type (22/44 [50.0%] versus 5/46 [10.9%], p G 0.001, W2 test, Fig. 2). Patients with apogeotropic BPPV showed
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predominantly contralesional HSN (19/22, 86.4%, p = 0.001, binomial test, Fig. 2) with a mean SPV at 4.4 T 1.4 degrees per second, whereas the patients with geotropic type did not show any directional preponderance of HSN (mean SPV T SD = 6.8 T 2.8 degrees per second, contralesional in 2 and ipsilesional in 3, Fig. 2). HSN was induced in only 3 (6.5%) of the 46 patients with pseudo-spontaneous nystagmus from geotropic HC-BPPV and in 17 (41.5%) of the 41 patients with pseudo-spontaneous nystagmus from apogeotropic type (p G 0.001, W2 test). Of interest, 8 of 28 patients with ipsilesional pseudo-spontaneous nystagmus from the apogeotropic type had HSN in the opposite (contralesional) direction of the pseudo-spontaneous nystagmus (Fig. 3, Video, Supplemental Digital Content 1, http://links.lww.com/MAO/A192, which demonstrates reversed HSN). No differences were found in the clinical features between the groups with and without HSN except the types of HC-BPPV (independent sample t test, W2 test; Table 1). DISCUSSION Pseudo-spontaneous nystagmus is explained by the 30-degree inclination of the horizontal semicircular canal from the horizontal plane (12). In our patients, pseudospontaneous nystagmus more frequently beats to the affected side in the apogeotropic type, which is consistent with the previous explanation of the pseudo-spontaneous nystagmus in apogeotropic HC-BPPV (10Y12). However, the direction of pseudo-spontaneous nystagmus was either ipsilesional or contralesional in geotropic HC-BPPV. The occurrence and direction of pseudo-spontaneous nystagmus in geotropic HC-BPPV would depend on the position of the otolithic debris in the horizontal canal before
FIG. 2. Head-shaking nystagmus (HSN). HSN was more common in apogeotropic than in geotropic type. HSN mostly beat to the intact side in apogeotropic type, whereas HSN showed no directional preponderance in geotropic one. Otology & Neurotology, Vol. 35, No. 3, 2014
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assuming the head upright position and should be interpreted with caution. Our patients with HC-BPPV frequently showed HSN, which was more common and mostly directed to the intact side in the apogeotropic type. The frequent occurrence of HSN in our HC-BPPV patients without any identified underlying vestibulopathy indicates asymmetric vestibular inputs during horizontal head-shaking in HC-BPPV, probably because of otolithic debris in the horizontal semicircular canal. In unilateral or asymmetric peripheral vestibular dysfunction, the HSN beating away from the lesion side is explained by accumulated vestibular asymmetry favoring the intact side in the central velocity storage mechanism (21). In the horizontal semicircular canal, deflection of the cupula toward the utricle (utriculopetal) activates it, whereas the utriculofugal deflection results in inhibition. Because the inhibitory vestibular nerve firing rate cannot decrease below zero while the firing rate may increase up to 350 to 400 Hz with stimulation, the excitatory stimuli are more effective than the inhibitory ones in inducing vestibular responses (Ewald’s second law) (3). In persons with symmetrical peripheral vestibular function, the oppositely directed inputs from both ears would be cancelled out during horizontal head shaking because of the push-and-pull actions of the cupulae on both sides. However, in patients with unilateral or asymmetrical peripheral vestibular dysfunction, the net vestibular input (excitatoryYinhibitory input) would be less in the (more severely) damaged ear during each cycle of head shaking, and this asymmetry would be amplified during head shaking because of accumulation in the central velocity storage mechanism (1,4). Then, the
FIG. 3. Recording of pseudo-spontaneous, head-shaking (HSN), and head-turning nystagmus in a patient with apogeotropic benign paroxysmal positional vertigo involving the left horizontal semicircular canal. A, The pseudo-spontaneous nystagmus beat to the involved left side while HSN beat to the healthy right side. B, The patient shows apogeotropic nystagmus in the head turned position while supine, which was more intense when the head was turned to the unaffected right side.
TABLE 1.
Comparison of clinical features according to the presence of HSN HSN (+) (n = 27)
Age, yr (SD) Sex (%, women) Lesion side (%, Right) Presence of SN (%) Direction of SN (%, ipsilesional) Mean SPV of SN (O/s, SD) Subtype of HC-BPPV (%, apogeotropic)
64.4 (11.4) 19/27 (65.1) 16/27 (59.3) 20/27 (74.1) 12/20 (60.0)
HSN (-) (n = 63) 65.8 (11.8) 41/63 (70.4) 32/63(50.8) 45/63 (71.4) 23/45 (51.1)
p 0.589 0.626 0.461 0.797 0.507
0.87 (0.78) 0.86 (0.93) 0.944 22/27 (81.5%) 22/63 (34.9%) G0.001
HC-BPPV indicates horizontal canal benign paroxysmal positional vertigo; HSN, head-shaking nystagmus; SN, pseudo-spontaneous nystagmus; SPV, slow-phase velocity.
accumulated vestibular asymmetry finally discharges as nystagmus beating away from the lesion side after head shaking (HSN). In our patients with HC-BPPV, HSN was more frequent and mostly contralesional in the apogeotropic type, whereas HSN was less common and either ipsilesional or contralesional in the geotropic type. These findings indicate decreased vestibular inputs from the involved ear during the horizontal head shaking in patients with apogeotropic HCBPPV. Because the apogeotropic HC-BPPV is explained by otolithic debris attached or near to the cupula in the anterior arm of the horizontal canal, these otolithic debris may have influenced the cupular dynamics during horizontal head shaking. In view of the decreased vestibular inputs from the affected side, we may presume interruption or decreased transfer of the endolymph flow to the cupula because of mechanical blockage by the otolithic debris. That is, the otolithic debris near the inlet of the ampulla may have played a role as a check valve, and thus allowed the endolymph to enter the ampulla and caused cupular deviation during initial rotation in one direction. In contrast, subsequent rotation in the opposite direction would move the mass into the ball-valve position, cutting off endolymph flow from the ampulla and preventing any cupular movement. After the first few head rotations, once the pressure has risen in the ampulla, the pressure accumulation within the ampulla would equal the force exerted by endolymph moving toward the ampulla, preventing any further inflow and tightly sealing the ball-valve into the ampullary neck. The presence of a ball-valve essentially acts as a semicircular canal plugging, leaving only one functioning ear. This would result in asymmetric velocity storage and a typical HSN beating away from the canal-plugged ear (Fig. 4) (1,4). In contrast, the rare occurrence and no directional preponderance of HSN in the geotropic type indicate that otolithic debris in the canal generally do not exert a significant impact on the fluid dynamics of the endolymph during head-shaking. In previous reports, HSN usually indicates underlying vestibular asymmetry because of peripheral or central vestibular dysfunction. Indeed, HSN is one of the most sensitive signs of vestibular neuritis and may also be
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FIG. 4. A proposed mechanism for head-shaking nystagmus (HSN) in apogeotropic benign paroxysmal positional vertigo involving the left horizontal semicircular canal. After head-shaking, the otoconial debris near the inlet of the ampulla block the endolymph flow. By sealing off the inlet of the ampulla, the otolithic debris may exert a canal plugging effect, which would leave only the right ear to function, and lead to right beating HSN.
observed in lesions involving the brainstem and cerebellum (1,4,19,21Y23). Our study shows that HSN may be induced by deranged cupular dynamics because of mechanical restriction and is not necessarily indicative of underlying vestibular dysfunction in HC-BPPV. HSN was also described in HC-BPPV in a previous study (10). In our patients with apogeotropic HC-BPPV, the HSN predominantly beats to the intact side. In HC-BPPV, the involved side is usually determined by comparing the intensity of nystagmus observed in the head-turned position to either side. In the apogeotropic type, the induced nystagmus is usually more intense when the head is turned to the intact side (2,24). However, the intensity of nystagmus is often inconclusive or misleading. In those cases, the direction of pseudo-spontaneous, head-bending and lying-down nystagmus aid in lateralization. Our study adds the direction of HSN to the list of lateralizing signs in apogeotropic HC-BPPV. Of interest, 8 of 28 patients with ipsilesional pseudospontaneous nystagmus had HSN in the opposite direction of the pseudo-spontaneous nystagmus. HSN in the opposite direction of spontaneous nystagmus is usually regarded a central sign and has been described in lateral medullary or cerebellar infarctions (19,23). Our study shows that this phenomenon may occur in apogeotropic HC-BPPV. Our study has some limitations. First of all, it is a retrospective single-center study. Second, although we excluded patients with underlying unilateral or asymmetrical vestibular dysfunction, as was determined with horizontal head impulse and caloric tests, these tests may be negative in compensated unilateral or asymmetrical vestibulopathies.
Accordingly, HSN may have resulted from underlying compensated vestibulopathy (25,26). Third, we did not reevaluate HSN after resolution of BPPV. However, the chance of false negative head impulse and bithermal caloric tests seems reasonably low in patients with HSN. CONCLUSION Pseudo-spontaneous nystagmus beats more to the lesion side in apogeotropic HC-BPPV but in either direction in the geotropic type. HSN was more common and mostly contralesional in apogeotropic HC-BPPV. The different prevalence and patterns of HSN in apogeotropic and geotropic HC-BPPV suggest dissimilar cupular dynamics in those disorders. The direction of HSN seems to be more useful than the direction of pseudo-spontaneous nystagmus for determining the affected side of apogeotropic HC-BPPV. REFERENCES 1. Takahashi S, Fetter M, Koenig E, Dichgans J. The clinical significance of head-shaking nystagmus in the dizzy patient. Acta Otolaryngol 1990;109:8Y14. 2. Leigh RJ, Zee DS. The Neurology of Eye Movements. 4th ed. New York, NY: Oxford University Press, 2006. 3. Baloh RW, Honrubia V, Konrad HR. Ewald’s second law reevaluated. Acta Otolaryngol 1977;83:475Y9. 4. Choi KD, Kim JS. Head-shaking nystagmus in central vestibulopathies. Ann NY Acad Sci 2009;1164:338Y43. 5. Dix MR, Hallpike CS. The pathology, symptomatology and diagnosis of certain common disorders of the vestibular system. Proc R Soc Med 1952;45:341Y54. Otology & Neurotology, Vol. 35, No. 3, 2014
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6. Lee SH, Kim JS. Benign paroxysmal positional vertigo. J Clin Neurol 2010;6:51Y63. 7. Schuknecht HF. Cupulolithiasis. Arch Otolaryngol 1969;90:765Y78. 8. Hall SF, Ruby RR, McClure JA. The mechanics of benign paroxysmal positional vertigo. J Otolaryngol 1979;8:151Y8. 9. Baloh RW, Jacobson K, Honrubia V. Horizontal semicircular canal variant of benign positional vertigo. Neurology 1993;43:2542Y9. 10. Nuti D, Mandala` M, Salerni L. Lateral canal paroxysmal positional vertigo revisited. Ann N Y Acad Sci 2009;1164:316Y23. 11. Asprella-Libonati G. Pseudo-spontaenous nystagmus: a new sign to diagnose the affected side in lateral semicircular canal benign paroxysmal positional vertigo. Acta Otorhinolaryngol Ital 2008;28:73Y8. 12. Asprella Libonati G. Diagnostic and treatment strategy of the lateral semicircular canal canalolithiasis. Acta Otorhinolaryngol Ital 2005; 25:277Y83. 13. Bisdorff AR, Debatisse D. Localizing signs in positional vertigo due to lateral canal cupulolithiasis. Neurology 2001;57:1085Y8. 14. Strupp M, Brandt T, Steddin S. Horizontal canal benign paroxysmal positioning vertigo: reversible ipsilateral caloric hypoexcitability caused by canalolithiasis? Neurology 1995;45:2072Y6. 15. Heidenreich KD, Beaudoin K, White JA. Can active lateral canal benign paroxysmal positional vertigo mimic a false-positive head thrust test? Am J Otolaryngol 2009;30:353Y5. 16. Lee SH, Choi KD, Jeong SH, Oh YM, Koo JW, Kim JS. Nystagmus during neck flexion in the pitch plane in benign paroxysmal positional vertigo involving the horizontal canal. J Neurol Sci 2007;256:75Y80. 17. Koo JW, Moon IS, Shim WS, Moon SY, Kim JS. Value of lyingdown nystagmus in the lateralization of horizontal semicircular
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Otology & Neurotology, Vol. 35, No. 3, 2014
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Pseudo-Spontaneous and Head-Shaking Nystagmus in Horizontal Canal Benign Paroxysmal Positional Vertigo *Sun-Uk Lee, †Hyo-Jung Kim, and ‡Ji-Soo Kim *Department of Neurology, Ajou University College of Medicine, Ajou University Hospital, Suwon; ÞKangwon National University College of Medicine, Medical Research Institute, Seoul National University Bundang Hospital, Seongnam; and þDepartment of Neurology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, Republic of Korea
(28/41, 68.3%, p = 0.028) but in either direction without directional preponderance in geotropic type (p = 0.659). Of the 90 patients who underwent horizontal head-shaking, 27 (30.0%) showed HSN that was more common in apogeotropic than in geotropic type (22/44 [50.0%] versus 5/46 [10.9%], p G 0.001). Patients with apogeotropic HC-BPPV showed predominantly contralesional HSN (19/22 [86.4%], p = 0.001), whereas patients with geotropic type did not show any directional preponderance of HSN (contralesional in 2 and ipsilesional in 3). Conclusion: HSN is more common and mostly contralesional in apogeotropic HC-BPPV. HSN may be a lateralizing sign in apogeotropic HC-BPPV. Different prevalence and patterns of HSN in apogeotropic and geotropic HC-BPPV suggest dissimilar cupular dynamics in those disorders. Key Words: Benign paroxysmal positional vertigoVHead-shaking nystagmusVNystagmusVVertigo.
Objectives: To determine the characteristics and diagnostic value of pseudo-spontaneous and head-shaking nystagmus (HSN) in benign paroxysmal positional vertigo involving the horizontal semicircular canal (HC-BPPV). Study Design: Retrospective case series review. Methods: After excluding 19 patients with canal paresis, abnormal head impulse test, recent history of peripheral or central vestibular disorders, or poor cooperation, we retrospectively recruited 127 patients with HC-BPPV from January 2009 to July 2012. The patients included 69 geotropic and 58 apogeotropic types. We analyzed the pattern of pseudo-spontaneous nystagmus and HSN according to the lesion side. Results: Pseudo-spontaneous nystagmus was observed in 87 (87/127, 68.5%) patients, both in geotropic (46/69, 66.7%) and apogeotropic (41/58, 70.7%) types without difference in the prevalence between the types (p = 0.627). Pseudo-spontaneous nystagmus beat more to the lesion side in apogeotropic type
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Address correspondence and reprint requests to Ji-Soo Kim, M.D., Ph.D., Department of Neurology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 300 Gumidong, Bundang-gu, Seongnam-si, Gyeonggi-do, 463-707, Republic of Korea; E-mail: [email protected] This study was supported by a grant of Korea Medical Device Industrial Cooperative Association. Author contributions Dr. Lee wrote the manuscript and analyzed and interpreted the data. Ms. H. J. Kim analyzed and interpreted the data and revised the manuscript. Dr. Kim conducted the design and conceptualization of the study, interpretation of the data, and drafting and revision of the manuscript. Disclosure Dr. Lee and H. J. Kim report no disclosures. Dr. J. S. Kim serves as an Associate Editor of Frontiers in Neuro-otology and on the Editorial Boards of the Journal of Korean Society of Clinical Neurophysiology, Research in Vestibular Science, Journal of Clinical Neurology, Frontiers in Neuro-ophthalmology, Journal of Neuroophthalmology, Case Reports in Ophthalmological Medicine, and World Journal of Neurology; and received research support from SK Chemicals, Co. Ltd.
Head shaking may reveal central as well as peripheral vestibular dysfunction by generating nystagmus (1). Horizontal head shaking usually induces nystagmus beating to the intact or healthier side in patients with unilateral or asymmetrical peripheral vestibular disorders. This headshaking nystagmus (HSN) of the peripheral type is explained by the following: 1) asymmetrical vestibular inputs due to Ewald’s second law, which states that the excitatory stimuli are more effective than the inhibitory ones in inducing vestibular responses (1Y3); and 2) central velocity storage mechanisms (1,4). Benign paroxysmal positional vertigo (BPPV) is characterized by short-lasting vertigo that develops when the dependent position of the head is changed (5,6). BPPV is explained by free floating otolithic debris in the endolymph of the semicircular canal (canalolithiasis) or debris near or attached to the cupula (cupulolithiasis) (7,8). In BPPV involving the horizontal semicircular canal (HC-BPPV), 495
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2 different types have been recognized according to the patterns of nystagmus induced when the head is turned to either side while supine. In geotropic HC-BPPV, the evoked nystagmus beat to the ground and is explained by otolithic debris in the canal (9). In contrast, the evoked nystagmus beating toward the ceiling in apogeotropic HC-BPPV has been ascribed to otolithic debris attached or near to the cupula within the ampulla (3,10). Patients with either type of HC-BPPV may show spontaneous nystagmus in the sitting position, which is also referred to pseudo-spontaneous because it showed positional modulations and disappearance with resolution of HCBPPV (10Y13). The direction of pseudo-spontaneous nystagmus also has been known to have a lateralizing value in HC-BPPV (10Y12). In HC-BPPV, the otolithic debris in the endolymph or attached to the cupula may alter the dynamics of the endolymph or the cupula during horizontal head shaking and generate HSN. Accordingly, analyzing the patterns of HSN may provide a clue to the altered dynamics of the endolymph or cupula in HC-BPPV. However, no study has attempted systematic analysis of HSN in patients with HC-BPPV. In this study, we analyzed the patterns of pseudo-spontaneous nystagmus and HSN in a large number of patients with either geotropic or apogeotropic type of HC-BPPV. MATERIALS AND METHODS Patients We reviewed the medical records of 146 patients (47 men and 99 women; age range, 34Y92 yr; mean age T SD, 65.0 T 12.4) with HC-BPPV. The age did not differ between men and women (66.1 T 12.8 versus 65.0 T 12.4, p = 0.586). The recruitment was performed using our data base that represents all vestibular patients seen at the Dizziness Clinic of Seoul National University Bundang Hospital from January 2009 to July 2012. The patients included 76 geotropic and 70 apogeotropic types. The right ear was involved in 80 patients (55.2%). The diagnosis of HC-BPPV was based on the following: 1) a history of brief episodes of positional vertigo, 2) directionchanging horizontal nystagmus beating toward the ground (geotropic nystagmus) or to the ceiling (apogeotropic nystagmus) in head turned to either side in the supine position, and 3) absence of identifiable central nervous system disorders that could otherwise explain the positional vertigo and nystagmus. To exclude patients with underlying peripheral vestibular disorders or central positional nystagmus, all patients also received detailed neurotologic examinations including spontaneous and gaze-evoked nystagmus, horizontal head impulse, horizontal and vertical smooth pursuit and saccades, limb ataxia, and balance function in addition to routine neurologic examinations. Even in patients with isolated vertigo, those with central ocular motor signs, limb ataxia, severe imbalance, or no response to repeated canalith repositioning maneuvers were arranged for MRIs. We also excluded patients who showed positive horizontal head impulse test (HIT) as determined at the bedside, documented caloric paresis on bithermal caloric tests, other neurologic deficits indicating central pathologies, and history of continuous vertigo that suggested peripheral or central vestibulopathy within one year. This was to avoid bias
from including the patients with asymmetric canal responses because of peripheral or central vestibulopathies other than BPPV. Although canal paresis or a positive HIT may result from HC-BPPV itself (14,15), we excluded those cases with canal paresis or positive HIT to avoid bias from including patients with underlying vestibulopathy. After excluding 19 patients with canal paresis (n = 12), abnormal head impulse test (n = 2), previous history of other vestibulopathies (n = 2, one with Me´nie`re’s disease and the other with lateral medullary infarction) and poor cooperation during video-oculography (n = 3), we retrospectively analyzed the patterns of pseudo-spontaneous nystagmus and HSN in 127 patients.
Neurotologic Evaluation After measuring the pseudo-spontaneous nystagmus in sitting position, patients lay supine from sitting (lying-down nystagmus) and turned their heads to either side while supine (head-turning nystagmus) to induce positional nystagmus. Then, the patients were moved from a supine to sitting position, and the head was bent down (head-bending nystagmus) (16). We excluded the patients with BPPV involving the posterior or anterior canals. Nystagmus was first observed without fixation using a videoFrenzel goggle system (SLMED, Seoul, Republic of Korea). The affected ear was determined by comparing the intensity of the nystagmus, with an assumption that the induced nystagmus is more intense when the head is rotated to the affected side in the geotropic type and to the intact side in the apogeotropic type. When the decision was inconclusive because of near symmetrical nystagmus, the direction of lying-down or head-bending nystagmus was also considered. In recent studies, the lying-down nystagmus mostly beat to the intact ear (10,12,17,18), whereas the head-bending nystagmus beat to the lesion side in geotropic HCBPPV (10,16). In apogeotropic type, the directions of lying-down and head-bending nystagmus were mostly opposite to those induced in the geotropic type. Eye movements were also recorded using 3-dimensional videooculography (SMI, Teltow, Germany). Spontaneous nystagmus was recorded both with and without fixation while sitting. After spontaneous nystagmus was subsided, HSN was induced using a passive head-shaking maneuver. The head was shaken in a sinusoidal pattern at the frequency of 2.8 Hz paced to the sound of a metronome. We measured the mean slow-phase velocity (SPV) of the first 3 beats of HSN. HSN was observed until it disappeared. The presence of HSN was defined only when the SPV of the induced nystagmus exceeded the values observed in normal controls after subtracting the SPV of pseudo-spontaneous nystagmus (horizontal HSN Q3 degrees per second; vertical HSN Q2 degrees per second; torsional HSN Q2 degrees per second), and when the nystagmus lasted more than 5 seconds (19). The head impulse test was performed manually with a rapid rotation of the head at an approximate amplitude of 20 degrees in the yaw plane with a high acceleration. Bedside head impulse test was considered abnormal if a corrective saccade was present (20). Two patients with abnormal HIT were excluded. Bithermal caloric tests were performed by irrigating the ears for 25 seconds with 50 ml of cold and hot water (30-C and 44-C, respectively). Asymmetry of vestibular function was calculated using Jongkees’ formula. Canal paresis was defined as a response difference of 25% or more between the ears (19), and 12 patients with canal paresis were also excluded. No patients took any medications that could affect the vestibular function during the evaluation.
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PSEUDO-SPONTANEOUS AND HSN IN HC-BPPV
FIG. 1. Pseudo-spontaneous nystagmus. Pseudo-spontaneous nystagmus was observed both in geotropic and apogeotropic types without difference in the prevalence between the types. The pseudo-spontaneous nystagmus more commonly beat to the lesion side in apogeotropic type but without directional preponderance in geotropic type.
Statistical Analysis Statistical analyses were performed with SPSS (version 18.0, Chicago, IL, USA). The clinical variables were compared using the W2 test (2 tailed), independent sample t test, and binomial test.
RESULTS Pseudo-Spontaneous Nystagmus Pseudo-spontaneous nystagmus was observed in 87 (87/127, 68.5%) patients with HC-BPPV, both in geotropic (46/69, 66.7%) and apogeotropic (41/58, 70.7%) types without difference in the prevalence between the types (p = 0.627, W2 test; Fig. 1). Pseudo-spontaneous nystagmus was mostly mild with the mean SPV ranging from 0.2 to 4.6 degrees per second (mean T SD = 1.3 T 0.9 degrees per second). Only 46 (52.9%) of the 87 patients showed mean SPV of pseudo-spontaneous nystagmus more than 1.0 degrees per second. The pseudospontaneous nystagmus more commonly beat to the lesion side (28/41, 68.3%, p = 0.028, binomial test) in apogeotropic type but either to the intact (25/46, 54.3%) or lesioned (21/46, 45.7%) side without directional preponderance (p = 0.659, binomial test) in the geotropic group (Fig. 1). Head-Shaking Nystagmus Of the 90 patients who underwent horizontal head shaking, 27 (30.0%) showed horizontal HSN. Maximum SPV of horizontal HSN ranged from 3.1 to 9.9 degrees per second (mean T SD = 4.8 T 1.9 degrees per second), and its duration varied from 5 to more than 15 seconds. HSN was more commonly observed in the apogeotropic than in the geotropic type (22/44 [50.0%] versus 5/46 [10.9%], p G 0.001, W2 test, Fig. 2). Patients with apogeotropic BPPV showed
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predominantly contralesional HSN (19/22, 86.4%, p = 0.001, binomial test, Fig. 2) with a mean SPV at 4.4 T 1.4 degrees per second, whereas the patients with geotropic type did not show any directional preponderance of HSN (mean SPV T SD = 6.8 T 2.8 degrees per second, contralesional in 2 and ipsilesional in 3, Fig. 2). HSN was induced in only 3 (6.5%) of the 46 patients with pseudo-spontaneous nystagmus from geotropic HC-BPPV and in 17 (41.5%) of the 41 patients with pseudo-spontaneous nystagmus from apogeotropic type (p G 0.001, W2 test). Of interest, 8 of 28 patients with ipsilesional pseudo-spontaneous nystagmus from the apogeotropic type had HSN in the opposite (contralesional) direction of the pseudo-spontaneous nystagmus (Fig. 3, Video, Supplemental Digital Content 1, http://links.lww.com/MAO/A192, which demonstrates reversed HSN). No differences were found in the clinical features between the groups with and without HSN except the types of HC-BPPV (independent sample t test, W2 test; Table 1). DISCUSSION Pseudo-spontaneous nystagmus is explained by the 30-degree inclination of the horizontal semicircular canal from the horizontal plane (12). In our patients, pseudospontaneous nystagmus more frequently beats to the affected side in the apogeotropic type, which is consistent with the previous explanation of the pseudo-spontaneous nystagmus in apogeotropic HC-BPPV (10Y12). However, the direction of pseudo-spontaneous nystagmus was either ipsilesional or contralesional in geotropic HC-BPPV. The occurrence and direction of pseudo-spontaneous nystagmus in geotropic HC-BPPV would depend on the position of the otolithic debris in the horizontal canal before
FIG. 2. Head-shaking nystagmus (HSN). HSN was more common in apogeotropic than in geotropic type. HSN mostly beat to the intact side in apogeotropic type, whereas HSN showed no directional preponderance in geotropic one. Otology & Neurotology, Vol. 35, No. 3, 2014
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assuming the head upright position and should be interpreted with caution. Our patients with HC-BPPV frequently showed HSN, which was more common and mostly directed to the intact side in the apogeotropic type. The frequent occurrence of HSN in our HC-BPPV patients without any identified underlying vestibulopathy indicates asymmetric vestibular inputs during horizontal head-shaking in HC-BPPV, probably because of otolithic debris in the horizontal semicircular canal. In unilateral or asymmetric peripheral vestibular dysfunction, the HSN beating away from the lesion side is explained by accumulated vestibular asymmetry favoring the intact side in the central velocity storage mechanism (21). In the horizontal semicircular canal, deflection of the cupula toward the utricle (utriculopetal) activates it, whereas the utriculofugal deflection results in inhibition. Because the inhibitory vestibular nerve firing rate cannot decrease below zero while the firing rate may increase up to 350 to 400 Hz with stimulation, the excitatory stimuli are more effective than the inhibitory ones in inducing vestibular responses (Ewald’s second law) (3). In persons with symmetrical peripheral vestibular function, the oppositely directed inputs from both ears would be cancelled out during horizontal head shaking because of the push-and-pull actions of the cupulae on both sides. However, in patients with unilateral or asymmetrical peripheral vestibular dysfunction, the net vestibular input (excitatoryYinhibitory input) would be less in the (more severely) damaged ear during each cycle of head shaking, and this asymmetry would be amplified during head shaking because of accumulation in the central velocity storage mechanism (1,4). Then, the
FIG. 3. Recording of pseudo-spontaneous, head-shaking (HSN), and head-turning nystagmus in a patient with apogeotropic benign paroxysmal positional vertigo involving the left horizontal semicircular canal. A, The pseudo-spontaneous nystagmus beat to the involved left side while HSN beat to the healthy right side. B, The patient shows apogeotropic nystagmus in the head turned position while supine, which was more intense when the head was turned to the unaffected right side.
TABLE 1.
Comparison of clinical features according to the presence of HSN HSN (+) (n = 27)
Age, yr (SD) Sex (%, women) Lesion side (%, Right) Presence of SN (%) Direction of SN (%, ipsilesional) Mean SPV of SN (O/s, SD) Subtype of HC-BPPV (%, apogeotropic)
64.4 (11.4) 19/27 (65.1) 16/27 (59.3) 20/27 (74.1) 12/20 (60.0)
HSN (-) (n = 63) 65.8 (11.8) 41/63 (70.4) 32/63(50.8) 45/63 (71.4) 23/45 (51.1)
p 0.589 0.626 0.461 0.797 0.507
0.87 (0.78) 0.86 (0.93) 0.944 22/27 (81.5%) 22/63 (34.9%) G0.001
HC-BPPV indicates horizontal canal benign paroxysmal positional vertigo; HSN, head-shaking nystagmus; SN, pseudo-spontaneous nystagmus; SPV, slow-phase velocity.
accumulated vestibular asymmetry finally discharges as nystagmus beating away from the lesion side after head shaking (HSN). In our patients with HC-BPPV, HSN was more frequent and mostly contralesional in the apogeotropic type, whereas HSN was less common and either ipsilesional or contralesional in the geotropic type. These findings indicate decreased vestibular inputs from the involved ear during the horizontal head shaking in patients with apogeotropic HCBPPV. Because the apogeotropic HC-BPPV is explained by otolithic debris attached or near to the cupula in the anterior arm of the horizontal canal, these otolithic debris may have influenced the cupular dynamics during horizontal head shaking. In view of the decreased vestibular inputs from the affected side, we may presume interruption or decreased transfer of the endolymph flow to the cupula because of mechanical blockage by the otolithic debris. That is, the otolithic debris near the inlet of the ampulla may have played a role as a check valve, and thus allowed the endolymph to enter the ampulla and caused cupular deviation during initial rotation in one direction. In contrast, subsequent rotation in the opposite direction would move the mass into the ball-valve position, cutting off endolymph flow from the ampulla and preventing any cupular movement. After the first few head rotations, once the pressure has risen in the ampulla, the pressure accumulation within the ampulla would equal the force exerted by endolymph moving toward the ampulla, preventing any further inflow and tightly sealing the ball-valve into the ampullary neck. The presence of a ball-valve essentially acts as a semicircular canal plugging, leaving only one functioning ear. This would result in asymmetric velocity storage and a typical HSN beating away from the canal-plugged ear (Fig. 4) (1,4). In contrast, the rare occurrence and no directional preponderance of HSN in the geotropic type indicate that otolithic debris in the canal generally do not exert a significant impact on the fluid dynamics of the endolymph during head-shaking. In previous reports, HSN usually indicates underlying vestibular asymmetry because of peripheral or central vestibular dysfunction. Indeed, HSN is one of the most sensitive signs of vestibular neuritis and may also be
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FIG. 4. A proposed mechanism for head-shaking nystagmus (HSN) in apogeotropic benign paroxysmal positional vertigo involving the left horizontal semicircular canal. After head-shaking, the otoconial debris near the inlet of the ampulla block the endolymph flow. By sealing off the inlet of the ampulla, the otolithic debris may exert a canal plugging effect, which would leave only the right ear to function, and lead to right beating HSN.
observed in lesions involving the brainstem and cerebellum (1,4,19,21Y23). Our study shows that HSN may be induced by deranged cupular dynamics because of mechanical restriction and is not necessarily indicative of underlying vestibular dysfunction in HC-BPPV. HSN was also described in HC-BPPV in a previous study (10). In our patients with apogeotropic HC-BPPV, the HSN predominantly beats to the intact side. In HC-BPPV, the involved side is usually determined by comparing the intensity of nystagmus observed in the head-turned position to either side. In the apogeotropic type, the induced nystagmus is usually more intense when the head is turned to the intact side (2,24). However, the intensity of nystagmus is often inconclusive or misleading. In those cases, the direction of pseudo-spontaneous, head-bending and lying-down nystagmus aid in lateralization. Our study adds the direction of HSN to the list of lateralizing signs in apogeotropic HC-BPPV. Of interest, 8 of 28 patients with ipsilesional pseudospontaneous nystagmus had HSN in the opposite direction of the pseudo-spontaneous nystagmus. HSN in the opposite direction of spontaneous nystagmus is usually regarded a central sign and has been described in lateral medullary or cerebellar infarctions (19,23). Our study shows that this phenomenon may occur in apogeotropic HC-BPPV. Our study has some limitations. First of all, it is a retrospective single-center study. Second, although we excluded patients with underlying unilateral or asymmetrical vestibular dysfunction, as was determined with horizontal head impulse and caloric tests, these tests may be negative in compensated unilateral or asymmetrical vestibulopathies.
Accordingly, HSN may have resulted from underlying compensated vestibulopathy (25,26). Third, we did not reevaluate HSN after resolution of BPPV. However, the chance of false negative head impulse and bithermal caloric tests seems reasonably low in patients with HSN. CONCLUSION Pseudo-spontaneous nystagmus beats more to the lesion side in apogeotropic HC-BPPV but in either direction in the geotropic type. HSN was more common and mostly contralesional in apogeotropic HC-BPPV. The different prevalence and patterns of HSN in apogeotropic and geotropic HC-BPPV suggest dissimilar cupular dynamics in those disorders. The direction of HSN seems to be more useful than the direction of pseudo-spontaneous nystagmus for determining the affected side of apogeotropic HC-BPPV. REFERENCES 1. Takahashi S, Fetter M, Koenig E, Dichgans J. The clinical significance of head-shaking nystagmus in the dizzy patient. Acta Otolaryngol 1990;109:8Y14. 2. Leigh RJ, Zee DS. The Neurology of Eye Movements. 4th ed. New York, NY: Oxford University Press, 2006. 3. Baloh RW, Honrubia V, Konrad HR. Ewald’s second law reevaluated. Acta Otolaryngol 1977;83:475Y9. 4. Choi KD, Kim JS. Head-shaking nystagmus in central vestibulopathies. Ann NY Acad Sci 2009;1164:338Y43. 5. Dix MR, Hallpike CS. The pathology, symptomatology and diagnosis of certain common disorders of the vestibular system. Proc R Soc Med 1952;45:341Y54. Otology & Neurotology, Vol. 35, No. 3, 2014
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