Otology & Neurotology 35:323Y328 Ó 2014, Otology & Neurotology, Inc.

Benign Paroxysmal Positional VertigoVToward New Definitions Be´la Bu¨ki Department of Otolaryngology, County Hospital Krems, Austria

utriculus, the ampulla of the inferior canal. It is argued that in these cases, depending on their behavior (free-floating or sticking to the cupula) and the precise position of the inferior ampulla, either no nystagmus or a slow downbeat nystagmus should ensue when the patient is positioned from sitting to a Dix-Hallpike position. Such scenarios could hypothetically explain commonly seen clinical entities such as ‘‘subjective BPPV’’ and/or cases with a peripheral positional downbeat nystagmus. Key Words: NystagmusVOtoconiaVParoxysmalV PositionalVVertigo. Otol Neurotol 35:323Y328, 2014.

Objective: To review new clinical data and theories concerning atypical positional nystagmus in vertical canal benign paroxysmal positional vertigo (BPPV). Data Sources: Peer reviewed, clinical papers describing nystagmus provoked by positioning in cases with BPPV. Study Selection: Basic scientific articles detailing 3D anatomical reconstructions of the inner ear. Conclusion: In BPPV, it is hypothetically possible that otoconia become dislocated but do not fall into the common crus of the vertical canals or into the horizontal canal; in these cases, they may gravitate toward the most inferior part of the

Currently, the diagnostic criteria of benign paroxysmal positional vertigo (BPPV) consist of vertical-torsional positional nystagmus evoked by the Dix-Hallpike maneuver or a predominantly horizontal positional nystagmus after rolling the head sideways from the supine position. More recent studies reported atypical nystagmus patterns seen in cases of BPPV that do not fit these classic criteria. There are some newer theories, based upon anatomic and clinical data, which suggest that some variants of BPPV may cause chronic complaints without positional nystagmus and that the inferior semicircular canal may frequently be involved in generation of peripheral positional downbeat nystagmus. Downbeat nystagmus suspected of peripheral origin, until now, has been attributed exclusively to the superior canals. Recently, Cambi et al. (1) suggested it otherwise in their article (see below). Thus, the goal of this review is to evaluate the accumulating evidence concerning atypical nystagmus in BPPV and to review whether these new results agree with accepted theories on the origin of BPPV. Of course, the explanations and hypotheses below are not directly provable but then so are most of the explanations given for the various varieties of BPPV.

Current Definitions of BPPV Variants Labyrinthine otoconia maintenance is a tightly regulated process (2). As a result of age-related degeneration, otoconia may escape the macula and subsequently dissolve, except when they are confined to a small space with pathologically high calcium concentration (3). When dislodged from the utricular macula, freely moving otoconia may float into any canal or be attached to any cupula of the ampullae, thereby causing canalolithiasis and/or cupulolithiasis of the individual canal (for a review, see Parnes et al. (4)). The relative geometrical arrangement of the utricular macula in relation to the semicircular canal (SCC) openings has been used to explain the timing of the attacks and the different frequencies by which the individual SCCs are affected (Fig. 1). Debris-induced movements of the endolymph cause nystagmus in the plane of the involved canal (Ewald’s first law (5)) and in the same direction, as if the endolymph would move because of head acceleration (for review, see (6)). In the supine position, the common crus of the vertical semicircular canals opens immediately below the utricular macula (7). It has been theorized (8,9), that in the supine position, such while sleeping, dislodged debris may fall into the vertical canals (Fig. 2). Upon wakening and sitting up in the morning, the patient thus involuntarily removes the debris from the superior (anterior) canal, and simultaneously, the otoconia in the

Address correspondence and reprint requests to Be´la Bu¨ki, M.D., Ph.D., HNO-Abteilung, LKH Krems, Mitterweg 10, A-3500 Krems an der Donau, Austria; E-mail: [email protected] The author discloses no conflict of interest.


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Today, diagnosis of BPPV requires the detection of positional nystagmus provoked by Dix-Hallpike positioning, when the vertical semicircular canals are involved, or nystagmus invoked by a supine, horizontal roll with the involvement of the horizontal semicircular canals. According to currently accepted criteria, superior canalolithiasis should evoke a transient downbeat nystagmus, posterior canalolithiasis, a transient upbeat-geotropic nystagmus in the Dix-Hallpike position. Horizontal canalolithiasis goes with geotropic, cupulolithiasis with apogeotropic horizontal nystagmus in lateral supine position (4,6).

FIG. 1. Explanation of sketches used in this review. UM: Utricular macula, SC: superior canal ampulla, HC: horizontal canal ampulla, IC: inferior (posterior) canal ampulla. The caudal part of the utricular macula is floating on a thin membrane (7).

inferior (posterior) canal move further in the direction of the cupula and become trapped in the most inferior region of the SCC, which is closed by the cupula on the utricular side. In this case, it is possible to remove the debris from the inferior canal by a ‘‘backward somersault’’ roll, and this is the basis of the Epley maneuver (10). Thus, the Epley maneuver is basically a backward somersault carried out with a U-turn in the middle. In supine position, the opening of the long arm of the horizontal canal is also below the utricular macula, but it is directed sideways, and as a result, free-floating debris is less likely to enter, accounting for the relative infrequency of horizontal canal BPPV. This also explains why in cases of horizontal BPPV, spontaneous recovery may occur when the patient turns over in bed.

Superior Canal Canalo/CupulothiasisVDoes It Exist at All? Concerning the genesis of BPPV from the superior canal, several questions arise. First, if mechanical attachment of debris onto the cupula occurs, on which side of the cupula does this happen? In the Dix-Hallpike position, the utricular macula is immediately above the cupula of the superior canal, so it is possible that acute dislocation of the otoconia during a Dix-Hallpike maneuver may cause a sudden superior cupulothiasis on the utricular side inducing a sustained downbeat nystagmus (Fig. 3). However, from the canal side, it would be difficult to float debris onto the superior cupula. It would require first a canalolithiasis and then a head turning in the supine position; it is thus widely agreed that superior canalo/ cupulolithiasis may be very rare if it exists at all (for a thorough discussion of this topic, see (11)). Regardless, if it does exist, then in superior canal cupulolithiasis, the positioning of the patient from sitting in the Dix-Hallpike position should theoretically elicit the movements of debris in the same direction in canalolithiasis and cupulolithiasis: the nystagmus should be an apogeotropic downbeat nystagmus with a small torsional fast-phase,

FIG. 2. Relative positions of the vertical semicircular canals and the utricular macula in supine position (left) and during sitting up (right). In supine position (during sleep), the opening of the vertical canals is below the macula, and detached otoconia may fall into the vertical canals. During sitting up, the superior canal may be inadvertently freed from debris; otoconial mass in the posterior canal becomes trapped in the most inferior part of the canal. Arrows show the hypothetical movements of the debris. Otology & Neurotology, Vol. 35, No. 2, 2014

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FIG. 3. The effect of gravity (arrows) on the anterior cupula in cupulolithiasis: in sitting (A) and in Dix-Hallpike position (B), a downbeatapogeotropic nystagmus ensues.

which beats toward the affected ear, which is the upper ear in the Dix-Hallpike position in this case. Also, it should be possible to elicit the nystagmus with DixHallpike testing to either side (10). Inferior Canal CupulolithiasisVMore Questions Inferior canalolithiasis occurs when the dislodged otoconia enter the common crus, the common opening of the vertical canals, if the debris dislodgement occurs when patient is lying in supine position. If floating otoconia miss this opening or when patients liberate themselves involuntarily during turning over in bed, or when otoconia dislodge during the day when the patient is in the supine position, the short arm and the upper surface of the inferior cupula should catch the debris. This is because in the upright position, the utricular macula is above the inferior ampulla, the latter being the most inferior part of the vestibulum, the fluid compartment housing the macula. One can easily speculate that otoconia, which are present in the vestibulum, should be deposited on the inferior cupula, on its utricular (short arm) side. Schuknecht was the first to observe basophilic deposits on the utricular side of the posterior cupula (12), whereas Oas later coined the expression ‘‘short arm canalolithiasis’’ (9), and Buckingham discussed this using anatomic reconstructions (8). It is thus likely that with inferior cupulolithiasis in upright position, the debris

adhering to the inferior cupula should deflect it downward, away from the utricle (Fig. 4A). Over time, the cupula can adapt itself to this constant pathologic downward displacement. In this scenario, what happens to the cupula after positioning the patient from sitting to a Dix-Hallpike position? It is known, that the anatomic angle of attachment of the inferior cupula to the utriculus varies (13,14). During positioning, depending on the exact anatomic angle of the ampulla and the angle of the head hanging position, theoretically either nothing changes with Dix-Hallpike positioning (the cupula remains downward deflected) and no nystagmus is seen (Fig. 4B), or in the case of a more inferiorly attached ampulla and/or more inferiorly head hanging position, the cupula swings over and deflects upward, toward the utriculus, causing a slight, prolonged downbeat nystagmus (Fig. 4D). Such a downbeat nystagmus should be indistinguishable from a hypothetical contralateral superior (anterior) canalolithiasis. Also, such a downbeat nystagmus caused by the inferior cupula could hypothetically be elicited bilaterally, from both Dix-Hallpike positions and also in a straight head-hanging position. Considering the inferior position of the ampulla in question, one is tempted to speculate that this scenario occurs frequently, perhaps even more frequently than canalolithiasis, when the debris has to hit the opening of the common crus. Otology & Neurotology, Vol. 35, No. 2, 2014

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FIG. 4. Variants of posterior cupulolithiasis and short arm canalolithiasis (vertical arrows: effects of gravity). A, Posterior cupulolithiasis in sitting, the cupula is chronically downward deflected. B, Posterior cupulolithiasis in Dix-Hallpike position. In a case of an anatomically less inferior connecting ampulla and in less pronounced Dix-Hallpike position, the cupula, which is already deflected in sitting, does not change its position during the provocative maneuver, no nystagmus ensues. C, In short arm canalolithiasis, the debris falls off the cupula in DixHallpike position. D, In a case of perhaps more inferiorly connecting ampulla and/or more pronounced head hanging position, the cupula may swing upward and be deflected toward the utriculus, thereby eliciting a slight downbeat nystagmus.

Inferior Canal Short Arm CanalolithiasisVA Hypothesis When the concrements gravitate into the short arm of the inferior canal but do not attach themselves to the cupula (short arm canalolithiasis) (8,9), they may move to-and-fro in the short arm, causing slight dizziness when bending forward, or looking up, while in the Dix-Hallpike position, they should simply move back to the utriculus, without causing cupular deflection and nystagmus (Fig. 4C). Clinical Syndromes Peripheral Positional Downbeat Nystagmus Because positional downbeat nystagmus may be caused by a number of central etiologies, including posterior fossa tumor, cerebellar or spinocerebellar degeneration, multiple sclerosis, Arnold-Chiari malformation, lithium toxicity, or paraneoplastic disease (10), it can only be considered ‘‘peripheral’’ when all these pathologies have been reliably excluded. When a peripheral BPPV was postulated in such cases, it was conventionally interpreted as caused by a superior canal pathology (15,16). For instance, Bertholon et al. (17) studied ‘‘idiopathic’’ positional downbeat nystagmus when no central cause could be found and attributed it to refractory superior canalolithiasis. Recent work by Cambi et al. (1) studied peripheral positional downbeat nystagmus elicited by a Dix-Hallpike or a straight head hanging position. According to the authors, this kind of

benign and spontaneously improving nystagmus may be more frequent than previously thought and may not be caused by superior canal cupulo-canalolithiasis. In this article, the positional downbeat nystagmus was encountered approximately as frequently as horizontal canal involvement in other patient groups with BPPV. Although the authors could not definitively prove that nystagmus was caused by ipsilateral inferior cupulolithiasis, as opposed to contralateral superior canal involvement, they had a strong argument in favor of this hypothesis: they noticed a high association (30%) of downbeat nystagmus, when it could be lateralized, to previous or subsequent inferior canalolithiasis on the same side (personal communication from authors). This implies that the peripheral downbeat nystagmus was related to freely moving particles in the utriculus on the side with the ear down when provoking the peripheral downbeat nystagmus and not on the contralateral side as it should be with a putative superior cupula or canal involvement. If posterior cupulolithiasis caused positional downbeat nystagmus by the mechanism described previously, this would also explain the missing reversal of nystagmus when the patient was returned to the sitting position, which has been a source of confusion to many (11). BPPV Without Nystagmus Neurotologists frequently see patients with ‘‘subjective’’ BPPV, with complaints of positional vertigo (e.g.,

Otology & Neurotology, Vol. 35, No. 2, 2014

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ATYPICAL NYSTAGMUS IN BPPV when bending forward, lying down, sitting up or turning over in bed) but without objective positional nystagmus. There have been efforts to characterize this entity and measure the effectiveness of reposition maneuvers (18Y22). Multiple authors made efforts to explain the absence of nystagmus in subjective BPPV. As possible causes of ocular fixation, subtle nystagmus missed by the observer or the too small size of otoconia was proposed (18,20,22). We suggest here, as explained above, that nystagmus should be absent in many cases of posterior cupulolithiasis (and in the remaining ones, peripheral downbeat nystagmus would be logical). Buki et al. (23) has proposed that nystagmus should not be anticipated in cases of posterior short arm posterior canalolithiasis either. In this study, short vertigo and abnormal trunk oscillations during and after sitting up could be documented in cases with BPPV symptoms but without positional nystagmus (23). This ‘‘sitting-up’’ vertigo was typically unilateral, that is, it predominantly occurred either in the right anterior-left posterior (RALP) or in the left anterior-right posterior (LARP) plane during sitting up from the right or left Dix-Hallpike position. Based on this finding, it was argued that other mechanisms, such as orthostatic dysregulation, changes in intracranial pressure or increased motion sensitivity were improbable causes. Hypothetically, this so-called ‘‘type 2 BPPV’’ might be elicited by inferior canal short arm canalolithiasis: during examination in the head hanging position, no nystagmus ensues, but the chronically downward deflected cupula acts in an exaggerated fashion when sitting up. During this maneuver, patients experience a sensation of stumbling forward, thereby causing retropulsion. Furthermore, when sitting up, free moving debris falling back onto the cupula may cause identifiable trunk sway for a brief second. For therapy, repetitive sit-ups from the Dix-Hallpike position are recommended in such cases. The head hanging position during this maneuver should liberate the short arm of the inferior canal from canaloliths and move them out from the constricted ampullar endolymphatic space with a high microdomain Ca++-concentration. In many cases, strong vegetative symptoms (sweating, nausea, and even retching) may emerge at the beginning of the training; however, with repetitive maneuvers, these unpleasant symptoms soon disappear. It should be emphasized that in the present article, we offer theories, not facts, and that there could be multiple explanations for unusual combinations of eye movements and dizziness that do not relate to the inner ear. In the clinical setting, apart from central pathologies, differential diagnosis of positional vertigo should include migraine (24), phobic postural vertigo (25), and chronic subjective dizziness (26), the latter 2 groups being anxiety-related entities. However, it may be important to think about patients with BPPV symptoms without classical positional nystagmus. In a recent article, for instance, Jeong et al. recruited 100 consecutive patients with a diagnosis of idiopathic BPPV for a study. During the procedure of selection, 84 patients who reported a typical history suggestive of BPPV but did not exhibit


positional nystagmus were excluded (27). It is certainly a question to be answered if patients with similar ‘‘subjective’’ BPPV complaints do, in fact, have BPPV or not. Perhaps our suggestion concerning a hypothetical mechanism may stimulate this debate. CONCLUSION In BPPV, small particles of otoconia dislodged in an upright position, or particles which did not fall into the opening of the canals, gravitate to the most inferior parts of the vestibulum and, here, maintained for longer period in the high Ca++ concentration of the ampullary space, chronically stimulate the cupula with particular head motions. Such particles may become adherent to the cupula and cause a chronic downward deflection. Then, depending of the anatomy and on the extent of the headhanging position, either no positional nystagmus or a peripheral downbeat nystagmus might be observed in the Dix-Hallpike position. If the particles remain free in the short arm, they may simply float out of the short arm in the head hanging position, again resulting in no nystagmus. In such symptomatic cases, repetitive sit-ups may cure the patients. Acknowledgments: The author thanks Prof. Lawrence R. Lustig, Department of OtolaryngologyYHead and Neck Surgery, University of California San Francisco, for the useful comments and generous help during manuscript preparation. The author also thanks the two anonymous reviewers for the motivated, meticulous work and suggestions.

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Otology & Neurotology, Vol. 35, No. 2, 2014

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Benign paroxysmal positional vertigo--toward new definitions.

To review new clinical data and theories concerning atypical positional nystagmus in vertical canal benign paroxysmal positional vertigo (BPPV)...
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