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Middle-ear influence on otoacoustic emissions. II: Contributions of posture and intracranial pressure
Hearing Research 140 (2000) 202^211 www.elsevier.com/locate/heares
Middle-ear in£uence on otoacoustic emissions. II: Contributions of posture and intracranial pressure Be¨la Bu«ki a , Aleksander Chomicki b , Monique Dordain b , Jean-Jacques Lemaire b , Hero P. Wit c , Jean Chazal b , Paul Avan b; * a
b
ENT Department, Semmelweis University, Budapest, Hungary Laboratoire de Biophysique sensorielle (EA 2667), Faculte¨ de Me¨decine, Universite¨ d'Auvergne, P.O. Box 38, 63001 Clermont-Ferrand, France c ENT and Audiology Department, AZG, Groningen, The Netherlands Received 17 April 1999; received in revised form 22 October 1999; accepted 26 October 1999
Abstract Although it seems likely that body tilt or surgically provoked variations in intracranial pressure (ICP) can result in variations of intralabyrinthine pressure, the channels for pressure transmission remain controversial and the reasons why evoked otoacoustic emissions (EOAEs) exhibit attendant modifications are unclear. The theoretical framework implemented in the companion paper [Avan et al. part I, 2000] provides sensitive and non-invasive means to identify the middle-ear mechanism(s) entailed in EOAE changes. It was thus applied to analyze the influence of posture on EOAE phases and magnitudes as a function of frequency, in a series of experiments involving body tilt from sitting to supine (0³ or 330³). Controlled ICP variations were surgically carried out in a series of hydrocephalic patients and the resulting EOAE changes were compared to posture data and model predictions. In all cases, the EOAE changes closely resembled those due to an increase in the stiffness of the stapes' annular ligament, in keeping with the assumption that ICP gets transmitted to intralabyrinthine spaces and modifies the hydrostatic load on the stapes, thereby influencing EOAE features. A small additional contribution of middle-ear pressure to EOAE changes was identified in addition to the main stapes component. Dynamical EOAE measurements showed that sudden ICP changes were transmitted to the inner ear within 8^30 s. The high sensitivity of EOAE phases below 2 kHz to ICP changes, together with the absence of any significant confounding middle-ear effect, favors EOAEs for a reliable non-invasive monitoring of ICP and intralabyrinthine pressures. ß 2000 Elsevier Science B.V. All rights reserved. Key words: Posture; Intracranial pressure; Otoacoustic emission; Distortion; Middle-ear impedance; Hydrocephalus
1. Introduction Body tilt from upright to head-down position induces an increase in the intracranial pressure (ICP) of the cerebrospinal £uid (CSF) due to gravity (Davson, 1967 ; Chapman et al., 1990). Hearing is also a¡ected and auditory thresholds (Corso, 1962; Macrae, 1972), sound localization (Lackner, 1974) and auditory threshold microstructure (Horst et al., 1983) have been reported to depend on posture. Such changes originate
* Corresponding author. Tel.: +33 (4) 7360 8015; Fax: +33 (4) 7326 8818; E-mail: [email protected]
likely either from middle- or inner-ear modi¢cations in relation to body position or CSF pressure. Cochlear changes have been con¢rmed by objective measurements of cochlear microphonics (Yoshida and Uemura, 1991) and auditory brainstem-evoked responses (Phillips and Farrell, 1992). Otoacoustic emissions (OAEs) have proven to be posture-sensitive, for example stimulus frequency emissions (Wilson, 1980), spontaneous OAEs (Wilson and Sutton, 1981) and transient-evoked OAEs (TEOAE, Antonelli and Grandori, 1986; Bu«ki et al., 1996). Middle-ear impedance also reacts to posture changes and Casselbrant (1979) then Marchbanks (1982) designed methods to detect tympanic-membrane displacements associated with body tilt. The most parsimonious interpretation of all these ¢ndings is that
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posture-dependent changes of ICP induce variations of intralabyrinthine pressure. There is wide agreement that ICP and intralabyrinthine pressure can be equalized through several possible channels including cochlear aqueduct, vestibular aqueduct, perineural and perivascular spaces (Carlborg et al., 1982). Intralabyrinthine pressure can act directly upon the stapes or the cochlear structures, thereby modifying either sound transmission to the cochlea or sound processing inside the cochlea. Changes of middle-ear impedance may also induce minute alterations of cochlear function by modifying the impedance match at the boundary between middle ear and cochlea. Furthermore, posture also in£uences some, perhaps confounding, middle-ear characteristics other than those associated with the stapes and its ligament: for instance, it is well-known that middle-ear pressure slightly increases with body tilt (Bu«ki et al., 1996; Gaihede and Kjaer, 1998). The issue of pressure relationships between CSF and intralabyrinthine £uids bears an important clinical potential because it opens the possibility to monitor CSF pressure non-invasively through the ear. Patients treated for hydrocephalus can greatly bene¢t from such a monitoring (Moss et al., 1990). Direct objective methods to follow up the e¤cacy of surgically implanted shunting devices consist of either invasive investigation through lumbar puncture, or telemetric measurements requiring expensive sensors (Chapman et al., 1990 ; Miyake et al., 1997). The commercially available tympanic-membrane displacement method of Marchbanks (1982, 1984) provides a simple non-invasive alternative method for CSF pressure monitoring (Reid et al., 1990), although seemingly it su¡ers from some limitations in ageing patients (Phillips and Marchbanks, 1989; Wable et al., 1996). Recently, Bu«ki et al. (1996) have reported that the phases of TEOAE components below 2 kHz are very sensitive to postural changes and variations of ICP produced by surgical manipulations. In all the cases with controlled ICP increase, changes of about 60 daPa were reliably detected by TEOAEs and low-frequency phase shifts proved to be proportional to ICP change. Body tilting is a simple method allowing ICP to be manipulated in subjects for whom invasive measurements are unsuitable. Thus, posture experiments can be helpful to better evaluate the relationships between OAEs and ICP, and OAE detection might serve as an alternative to the tympanic-membrane displacement method of Marchbanks. The contribution of the above-mentioned mechanisms to posture-induced auditory changes remains a matter of controversy. Several channels may transmit CSF pressure to labyrinthine £uids, the venous system may be involved and a¡ect middle-ear impedance as well as intracochlear pressure. Likewise, the degrees of
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patency of the cochlear and vestibular aqueducts and the age-dependence of their patency have raised several arguments (Wlodyka, 1978 ; Phillips and Marchbanks, 1989 ; Gopen et al., 1997 ; Seo et al., 1997). The goal of this work is to address these questions by characterizing the posture e¡ect on OAEs. In the companion paper (Avan et al., 2000), we showed that distortion-product OAEs (DPOAEs) provided a convenient means to analyze middle-ear impedance changes in the mid-frequency range. Indeed, simple manipulations of the middle ear resulting in re£ex contractions of the stapedius muscle, in changes of middle-ear pressure and in increases of tympanic-membrane load, induced clear frequency-dependent shifts in the DPOAE levels and phases. A computer model derived from Zwislocki's (1962) network was used to predict DPOAE changes, from the assumption that each of the aforementioned manipulations a¡ected only a restricted, speci¢c set of parameters. This model correctly accounted for most of the experimental data, thereby explaining why the experimental pro¢les of shifts happened to be characteristic of the mechanical properties of the involved subsystem (stapes sti¡ness, tympanic-membrane sti¡ness or inertia). Accordingly, our aim was to detect DPOAEs after posture changes in human subjects, and to compare their pattern of level and phase shifts to those reported in the companion work for controlled middle-ear modi¢cations. The computerized model derived from Zwislocki's (1962) network, as modi¢ed by Lutman and Martin (1979), was used to adjust hypothetical parameter changes to experimental data from posture manipulations. 2. Materials and methods 2.1. Human subjects Three groups of subjects were included. All of them gave their informed consent to take part in the measurements in the course of either a routine ENT visit or a neurosurgical diagnostic procedure. Group 1 contained the same healthy adults (n = 8; age range 24^39 years) that had already participated in test 1 (stapedius re£ex) described in (Avan et al., 2000). Group 2 was made of other healthy subjects (n = 12; age range 21^63 years). Finally, ¢ve patients with hydrocephalus were extracted from a group of 18 patients for whom several data have been published in (Bu«ki et al., 1996). Group 3 was made of these ¢ve patients (age range 41^76 years). Their TEOAE and ICP data were reprocessed and compared to TEOAE recordings performed in the same ears during postural tests. The experimental procedures were approved by Grant CNAMTS/INSERM 4AIC04.
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2.2. Recordings The middle-ear status was controlled by the same tests as described in the companion work (Avan et al., 2000), and DPOAEs were recorded with the same equipment (Cube Dis, Mimosa Acoustics ; Allen, 1990). Primary-tone frequencies f1 and f2 were swept with f2 varying from 0.5 to 4 kHz (10 steps per octave), whereas the ratio f2/f1 was ¢xed at 1.20. The levels of primaries were 60 dB SPL at f2, 70 dB SPL at f1. The retrospective case study of group 3 ears was performed using TEOAEs instead of DPOAEs because, as already explained in Bu«ki et al. (1996), silence was required in the operating theater so as not to stir the sedated patients and interfere with the scheduled ICP course. In order to ful¢ll this requirement, sound stimuli had to be close to 0 dB SPL allowing TEOAEs to be detected, but not DPOAEs. Recordings were done with a ILO88 equipment (Kemp et al., 1986; setup in Bu«ki et al., 1996). The level and phase of the DPOAE at fd = 2f13f2 were extracted o¥ine from the data¢les stored by the Cube Dis acquisition system. The level of noise background around frequency fd was also available. The signal-to-noise ratio was considered to be acceptable when the DPOAE level exceeded the noise level by more than 12 dB. The magnitude and phase spectra of TEOAEs were obtained from the Fourier transform of the time-domain data¢les stored by the ILO88 equipment. The level and phase shifts of emissions with a postural change were de¢ned as the di¡erences between values before and after the postural change under consideration. As explained in Avan et al., (2000), the primary tones were calibrated in such a way that their levels and absolute phases were always the same in every recording session. Thus, the level and phase shifts of the DPOAE could only be due to the physiological di¡erence between the reference and test conditions. 2.3. Modi¢cations of posture or ICP 2.3.1. Experiment 1 The DPOAEs of the right ears of all the subjects of groups 1 and 2 were recorded in two di¡erent postures, sitting then head-down. This last posture was obtained with the help of a tilting table forming an adjustable angle a with the horizontal plane. The subjects lay £at on their back, and a was set at 330³. The eight subjects of group 1 had already been tested for stapedius re£ex in response to contralateral high-pass noise (corner frequency 3 kHz) at a level of 20 dB above re£ex threshold (Avan et al., 2000). They were instructed to swallow after every posture change, so as to keep stable their middle-ear pressure, as evaluated by tympanometry (Madsen ZO73, frequency of probe tone 226 Hz). These
data were augmented with an intermediate measurement carried out in group 2 for a = 0³. In contrast with the subjects of group 1, those of group 2 were not instructed to swallow and their middle-ear pressure could vary with posture. Data processing consisted of plotting DPOAE level and phase shifts with reference to the sitting position, against frequency fd. Frequency pro¢les were obtained for 330³ vs. sitting with stable middle-ear pressure (group 1; n = 8) and for 0³ vs. sitting and 330³ vs. sitting (group 2; n = 12). The DPOAE shifts due to body tilt were compared in group 2 for a = 0³ vs. 330³, as a function of frequency. The frequency pro¢les of group 1 were compared to those induced by stapedius re£ex activation in group 1. 2.3.2. Experiment 2 Frequencies f2 and f1 were ¢xed (with f2 around 1.2^ 1.3 kHz) and a continuous monitoring of DPOAEs was carried out in the 12 subjects of group 2 (one DPOAE sample every 4 s). In the meantime, they were sitting on the tilting table for about 100 s, then, within less than 4 s, they were moved to supine position (a = 0³) for the next 100 s, then to head-down (a = 330³) for the next 100 s, and ¢nally back to sitting posture (100 s). Special care was taken to minimize the movements of the ear probe while the subject and the table moved. The Cube Dis system made it possible to monitor simultaneously the levels and phases of the acoustic signal in the ear canal at f1 and f2. Data were discarded and the test redone later whenever some characteristics of one of the primary levels were found to drift (by more than 0.5 dB for the level, or 10³ for the phase). The levels and phases of the DPOAEs were plotted against time. Average time plots were obtained across ears, after normalizing the DPOAE shifts with respect to two reference values, namely 0% (baseline in sitting position) and 100% (plateau reached after moving to supine or head-down position). The values for baseline and plateau were computed from the mean of 10 consecutive points taken in a stable interval, more than 40 s after any posture change. 2.3.3. Retrospective case study Data from patients tested for hydrocephalus and included in a previous study (Bu«ki et al., 1996) were selected according to two criteria. In the ¢rst place, their TEOAEs had been recorded along with a diagnostic test involving direct infusion of saline (80 ml/h) into CSF through a lumbar puncture. This so-called perfusion test produced a controlled increase in ICP that was monitored continuously using a piezoresistive probe, as reported in (Bu«ki et al., 1996). The day before the perfusion test, TEOAEs had been recorded in the same ear in response to body tilt, following the same protocol as for experiment 1 in the present work. The second crite-
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rion required that the TEOAE spectra are rich enough that TEOAE shifts produced by ICP changes could be reliably computed at many frequencies. The ¢ve patients of group 3 met these criteria (out of 18 tested in Bu«ki et al., 1996). To bridge the gap between DPOAE and TEOAE data, we needed to assume that level and phase shifts depended little on the nature of OAEs (TEOAEs or DPOAEs). This was checked on the data from four patients of group 1, who were submitted to posture changes from sitting to 30³ head-down while DPOAEs, then TEOAEs were recorded. 2.3.4. Network model predictions The computer model described in the companion work (Avan et al., 2000) was used to predict the pro¢les of phase and level shifts of emissions, assuming that posture mainly in£uenced the sti¡ness of the annular ligament of the stapes. This sti¡ness was represented by capacitance Cst, varying from in¢nity to 0.25 WF, in the analog electrical network of Zwislocki, 1962 and Lutman and Martin, 1979. The value of Cst was assumed to be very large in the reference sitting posture ( s 1 mF), and its ¢nal value was supposed to decrease with increasing hydrostatic pressure, that is, with decreasing angle of the tilting table, from 0 to 330³. Unfortunately, the relationships between Cst and ICP, as well as between ICP and angle of tilt, are di¤cult to ascertain in a quantitative manner: for example, Bu«ki et al. (1996) reported a large intersubject variance in the slope of the linear regression of OAE shifts vs. ICP, and Chapman et al. (1990) described strongly non-linear and subject-dependent variations of ICP as a function of the angle of body tilt. Therefore, no attempt could be made to obtain a quantitative assessment of the change in stapes ligament sti¡ness, and the only reason for the choice of Cst value was that visual optimization of model predictions was achieved. In addition to a Cst decrease, an increase in middleear pressure was considered for group 2 subjects moving from sitting to head-down posture, as tympanometry showed that middle-ear pressure varied by about +35 daPa in this case (Bu«ki et al., 1996). To account for it, the DPOAE shifts were also computed when (C0, Cd1, Cd2, Cd3) were modi¢ed in addition to Cst, by a multiplicative factor between 1 and 1/6, as tested in the companion paper (Avan et al., 2000). 3. Results Control DPOAE recordings for experiment 1 were already described in Avan et al. (2000). The levels obtained with the continuous monitoring of experiment 2 were very similar and signal-to-noise ratios exceeded
Fig. 1. Superimposed examples of two individual pro¢les for DPOAE phase shift (top) and level shift (bottom) against frequency, for body tilt (from sitting to 30³ head-down, open circles for ear 1, closed circles for ear 2) vs. stapedius muscle contractions elicited by loud contralateral noise (open diamonds for ear 1, closed diamonds for ear 2).
12 dB as required, except during the ¢rst 4 s following a posture change. 3.1. Experiment 1 (postures, comparison with stapedius) Individual posture tests gave phase shifts very similar to those induced by stapedius muscle contractions. Fig. 1 (top panel) shows two examples of phase-shift pro¢le with frequency. Both presented low-frequency dominant e¡ects, with di¡erent corner frequencies for the two ears, namely 1.3 and 1.6 kHz for the heavy and thin lines, respectively. Stapedius (diamonds) and posture e¡ects (circles) resembled each other in the two cases. When the same comparison was performed for level shifts (Fig. 1, bottom panel, same symbols), the correspondence was less good because the distance between the stapedius and posture plots could reach 2 dB, with the stapedius shifts being more negative than the posture ones. When posture was changed from sitting to headdown (a = 330³) while middle-ear pressure was ¢xed, the average shift of DPOAE level was close to zero above 1 kHz (Fig. 2, lower left panel; thin lines for average þ 1 S.D.). Below 1 kHz, it was negative and of the order of 1 dB. S.D.s were close to 2 dB. The average phase shift (Fig. 2, upper left panel, same symbols as on bottom diagram) corresponded to a lead in head-down position. The largest phase shifts were obtained below 1 kHz and reached about 25³. As fre-
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Fig. 2. (left panels) Average DPOAE phase shift (top) and level shift (bottom) against frequency for posture change in the ears of group 1 (n = 8) (from sitting to 30³ head-down), and average þ 1 S.D. (thin lines). (right panels) For comparison, average DPOAE phase and level shifts against frequency in the same ears for stapedius muscle contractions, and average þ 1 S.D. (thin lines) (from Avan et al., 2000). The heavy lines on both diagrams represent the predictions of the computerized model. As explained in (Avan et al., 2000), the model prediction for DPOAE level shift had to be referred to the dashed baseline (in the lower right panel), i.e. shifted down by 1.5 dB, to account for a possible e¡erent olivocochlear e¡ect elicited by the contralateral noise.
quency increased above 1 kHz, the phase shift decreased to insigni¢cant values around 1.7 kHz. S.D.s were of the order of 15³. On the right panels, Fig. 2 recalls the average DPOAE shifts reported in the companion work (Avan et al., 2000) when re£ex contractions of the stapedius muscle were triggered at 20 dB above re£ex threshold in the same ears (closed circles on phase- and level-shift diagrams). Although the sizes of posture and stapedius e¡ects di¡ered slightly, their two pro¢les were qualitatively very similar. The average level shifts also exhibited similar pro¢les, except for a vertical shift of about 31.5 dB on the stapedius re£ex plot (Fig. 2, lower right panel). Avan et al. (2000) suggested that this 1.5 dB contribution might be due to an additional suppression of DPOAEs due to activation of the crossed olivocochlear bundle by contralateral noise. Intersubject di¡erences consisted of two components, a slight shift of the frequency corresponding to the maximum phase lead, which varied from 0.78 to 1.22 kHz, and a variation of the size of e¡ects. Maximum phase shifts varied from 74 to 10³, whereas the largest level shifts varied from 34 to 31 dB. For the subset of data from group 2 (supine, a = 0³, vs. sitting), the average phase shift (Fig. 3, top, open circles) was positive at all frequencies, and it presented two clear peaks of similar size (19^23³) separated by a trough. The lower-frequency peak was broad and centered around fd = 0.75 kHz. The other one concerned a
Fig. 3. (top) Average DPOAE phase shifts from sitting to supine (dashed line, open circles) and from supine to head-down (330³; continuous line, closed circles) in the 12 ears of group 2. All S.D.s were 6 10³. (bottom) Model predictions for combinations of Cst and eardrum capacitance changes (Cst minimum = 2.5 WF, dashed line; Cst minimum = 1.75 WF, continuous line). Recall that model predictions were shown to be inaccurate at lower frequencies for positive middle-ear pressure e¡ect, as it is the case here (Avan et al., 2000).
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Fig. 4. Example of DPOAE phase (top) and level (bottom) shifts as derived from continuous monitoring, while the subject was sitting (from 0^100 s), moved to supine position, kept this position from about 110 to 210 s, moved to head-down position (from about 210 to 310 s) and eventually went back to sitting position (after 320 s). The thin horizontal lines on the top diagram indicate the plateau values of DPOAE phase after the posture was kept stable for 30 s to 1 min. It can be noted that the plateau values for DPOAE level were less stable than for phase: in particular, the level after 300 s did not come back to its initial value. For this series of measurements, frequency f2 was set at 1.3 kHz, with f2/f1 = 1.20, and primary levels were 60 dB SPL at f2 and 70 dB SPL at f1.
narrow frequency interval around fd = 1.1 kHz. Level shifts were negative and very small below 1.2 kHz, whereas no level change was observed at higher frequencies. When the posture moved from supine to head-down (a = 330³), the size of the e¡ects increased. The pro¢le of average phase shifts exhibited one broad peak, reaching 27³ around 0.87^0.93 kHz (Fig. 3, closed circles), that is, at a slightly higher frequency than the corresponding lower-frequency peak of the ¢rst posture change. The previously observed second narrow peak seemed to be replaced by a bulge on the pro¢le around the same frequencies. The level shifts were close to 31 dB at low frequencies.
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Fig. 5. Normalized average phase shift of DPOAE as a function of time, over the 32 s interval following posture change from sitting to recumbent (closed circles) and average þ 1 S.D. (thin lines). Meanwhile, no signi¢cant level shift was recorded in most ears. Noisy data were not taken into account, thus the average was computed from 9^10 values only (out of 12 ears) for times 4, 8 and 12 s.
the level shift was about 31.5 dB. From a = 0³ to 330³, the phase shift of this ear increased by 48³, whereas the level decreased by an additional 3 dB. When back to sitting posture, the phase recovered its initial value (marked by the thin horizontal line) whereas the level di¡ered from it by 32 dB. In many ears, no level shift was visible in clear relation to any posture change, and in the long term, levels often tended to drift slowly. These drifts were likely related to slight and gradual movements of the probe tip with posture changes, that did not seem to a¡ect phase measurements nor primary-tone characteristics. Fig. 5 shows the average normalized phase shift dur-
3.2. Experiment 2 (continuous monitoring) Using the value of f2 and f1 that produced the maximum shift in experiment 1, continuous measurements were made of the DPOAE at 2f13f2 while posture varied (Fig. 4). Sharp phase or level changes were visible just during a posture change (from sitting to supine, around 100 s, then from head-down to sitting, after 300 s) and corresponded to noisy data. Sharp changes could also occur brie£y when a subject could not help swallowing. After each position had been kept for about 30 s or less, DPOAE level and phase reached stable plateaus. For the example of Fig. 4, the phase shift from sitting to supine plateaued at 16³, whereas
Fig. 6. Example of comparison of DPOAE vs. TEOAE shifts in the same ear, when the body was tilted from sitting to head-down. In this ear, TEOAE exhibited only ¢ve peaks at di¡erent frequencies in the range 0.6^3.5 kHz.
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Fig. 7. Example of TEOAE phase shift against frequency for the right ear of a subject whose body was tilted from sitting to supine position (open symbols), and who was later submitted to a 160 daPa increase in CSF pressure in the course of a hydrocephalus diagnosis procedure in the operating theater (closed symbols). The TEOAE frequency spectrum in this ear was broad enough for the signal-to-noise ratio to exceed 12 dB at most sample frequencies between 1 and 3 kHz. No signi¢cant level shift was recorded throughout posture and perfusion tests.
ing the ¢rst 32 s after posture was moved from sitting to supine (0³). The plateau was reached (within 5%) after 20^28 s, with a small intersubject variance. No simple monotonic function, such as an exponential one, provided a correct ¢t for experimental data. Between 12 and 20 s after the posture change, the phase shift tended to slow down or even decrease. When posture moved from a = 0³ to 330³, the ¢rst data point after 4 s was often noisy and the plateau had already been reached after 8 s, within 10%, in all subjects. 3.3. Retrospective case study Since this case study had to use TEOAE recordings, a control of the e¡ects of posture change, from sitting to head-down, was performed on both DPOAEs and TEOAEs for four subjects of group 2. A typical example is presented on Fig. 6 (DPOAEs : lines, TEOAE peaks, closed circles). An obvious disadvantage of TEOAEs in this example was that their shifts could be determined only at the ¢ve frequencies corresponding to the main peaks in the TEOAE spectrum, whereas DPOAEs were sampled at 10 points per octave. Nevertheless, a reasonably good agreement (within 10³ and 1 dB) was observed between the results of the two types of emissions in all four ears. The TEOAE spectra in the ¢ve ears of group 3 were such that at least 10 frequency components were identi¢ed with signal-to-noise ratios larger than 12 dB at more than three consecutive frequency samples (one point every 48.8 Hz with the ILO88 system). Thus we considered that it was reliable to compute the phase and level shifts of TEOAE components by direct comparison of the magnitude and phase spectra derived from the Fourier transform of the time-domain
TEOAEs, in head-down vs. sitting position, and in lower vs. higher ICP during the perfusion test. An example of phase shift pro¢les against frequency is depicted on Fig. 7 (open circles, posture test; closed circles, perfusion test with an 160 daPa ICP increase in between the two TEOAE recordings). A close correspondence was observed between the two pro¢les, with only a few isolated discrepancies of 10^14³. The size of the posture e¡ect was slightly smaller than that due to CSF pressure increase. The other individual phase pro¢les for posture change and ICP increase also exhibited good matches. Indeed, in all ears, the maximum shifts were reached at the same frequencies within 50 Hz; the corner frequencies of the shift pro¢les, de¢ned as the ¢rst frequencies with a shift 6 half its maximum value, coincided within 50 Hz except in one ear (because its phase shifts due to posture change were too close to zero, the assessment of the corner frequency was ambiguous on the pro¢le). As the available ICP changes varied widely (i.e. from 60 to 310 daPa), no conclusion as to the sizes of posture vs. ICP e¡ects could be derived; maximum phase shifts due to posture varied from 0³ to 70³ and those due to ICP increase from 40³ to 70³. No reliable TEOAE component was found below 0.9 kHz, so that the tested frequency interval was restricted to 0.9^3 kHz in all ears. Level shifts with posture change and ICP increase always remained very small or absent in this frequency range. 3.4. Model predictions The lumped-element electrical network model of Zwislocki (1962) was used as already shown in (Bu«ki et al., 1996) and (Avan et al., 2000), ¢rst assuming an isolated increase in annular ligament sti¡ness. The superposition of the computed phase and level shifts with experimental data (see Fig. 2, left panels, bold lines) was optimal when Cst was adjusted to 1.5 WF for a = 330³. The computed shifts due to modi¢cations of forward and reverse transmission were very similar at all frequencies, for example at 0.8 kHz, vPforward = 12.8³, vPreverse = 9.7³. As middle-ear pressure could not be controlled when the posture of group 2 subjects was altered, the actual physiological situation was likely to involve a small middle-ear pressure gradient in supine posture (not exceeding +35 daPa as reported by Bu«ki et al., 1996; of the order of +22 daPa according to Gaihede and Kjaer, 1998). In order to account for this gradient, a decrease in the capacitances representing eardrum sti¡nesses was combined with the change of Cst. Whereas Cst varied from in¢nity to either 2.5 WF (for a = 0³) or 1.75 WF (for a = 330³), C0, Cd1, Cd2 and Cd3 were divided by 1.3. With this simulation of middle-ear pressure increase, an
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additional peak appeared in the phase- and level-shift pro¢les, around fd = 1.2 kHz (Fig. 3, bottom). For a = 0³, the size of the additional peak was similar to that of the lower-frequency peak associated with Cst decrease (as observed in Fig. 3, open symbols) representing the real-ear data in a = 0³ vs. sitting position. For a = 330³, the main Cst e¡ect grew rapidly so that the additional peak appeared as a mere bulge on the high-frequency slope of the phase pro¢le (see Fig. 3, top, closed symbols for real-ear data). It was noticeable on Fig. 3 (bottom) that the predicted main peak was shifted towards higher frequencies when Cst decreased (in keeping with the experimental data shown on Fig. 3, top). Model predictions did not accurately match experimental data below 1 kHz, as already pointed out in the companion paper (Avan et al., 2000) for positive pressure changes similar to the present ones. In summary, the e¡ect of posture on DPOAE levels and phases in man closely resembled that induced by stapedius muscle re£ex triggered by contralateral noise. It consisted of a phase lead at low frequencies, together with a weak decrease of DPOAE levels. This e¡ect was correctly modelled qualitatively, using the lumped-element middle-ear equivalent electrical network of Zwislocki (1962), assuming that posture acted mainly on capacitance Cst representing the sti¡ness of the stapes' annular ligament. As middle-ear pressure was left free to vary with posture in the second group of subjects, a small additional e¡ect appeared within a restricted frequency interval slightly above 1 kHz when the posture e¡ect was weak. This contribution matched that predicted by Zwislocki's model when assuming that middle-ear pressure a¡ected eardrum sti¡nesses. The temporal course of DPOAE changes after a sudden posture change revealed that the transmission of the alleged resulting ICP change to cochlear liquids and stapes sti¡ness occurred within seconds for head-down vs. sitting move. When ICP was surgically manipulated in motionless patients, OAE changes mimicked those obtained by postural changes. 4. Discussion Although posture e¡ects on hearing have been welldocumented through numerous audiological methods, either subjective (Corso, 1962; Macrae, 1972; Horst et al., 1983) or objective ones (Casselbrant, 1979; Wilson, 1980 ; Marchbanks, 1982; Antonelli and Grandori, 1986 ; Phillips and Farrell, 1992; Bu«ki et al., 1996), their possible origins have not been established clearly. In particular, it is di¤cult to ascertain whether these effects are a re£ection of middle- or inner-ear modi¢cations, or a combination of two. Nevertheless, it seems likely that attendant variations of the hydrostatic pres-
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sure within intralabyrinthine compartments are a key element of the auditory e¡ects of posture, and posture undoubtedly a¡ects ICP primarily. Therefore, our study of some auditory e¡ects of posture aimed at opening a possibility to address the issue of relationships between ICP and intralabyrinthine pressure. This issue is interesting for fundamental reasons. Several studies of human temporal bones have tentatively addressed the regulation of hydrostatic pressure in the labyrinthine spaces, in relation to possible channels connecting these spaces to the CSF compartment. The patency of the most evident of these channels through the temporal bone, the cochlear aqueduct, has been examined in several publications. Wlodyka (1978) derived from histological studies that the patency of the cochlear aqueduct seemed to decrease with age, so that it was found to be blocked in about 70% temporal bones from subjects s 60 years, whereas 82% aqueducts were patent below 20 years. In contrast, more recent extensive studies (Gopen et al., 1997; Seo et al., 1997) have shown that the percentage of blocked cochlear aqueduct does not vary signi¢cantly with age and that about 30% appear to be fully patent, while 40^ 50% are just ¢lled with loose connective tissue. Thus, most cochlear aqueducts would be likely to transmit low-frequency pressure waves from CSF to labyrinthine compartments in most subjects regardless of age, as long as the wave frequency is 6 20 Hz (Gopen et al., 1997). Intralabyrinthine pressure measurements also bear potentially important practical consequences for neurosurgeons, because the possibility to monitor ICP through indirect audiological methods seems much more cost-e¡ective than direct invasive or telemetric monitoring systems (Chapman et al., 1990; Miyake et al., 1997). Marchbanks (1982, 1984) designed a tympanic-membrane displacement system (MMS 100 ) and reported promising results in hydrocephalus. Recently, Bu«ki et al. (1996) showed that OAEs react to posture or ICP changes in a systematic and very sensitive manner, thereby opening a new possibility to monitor patients with hydrocephalus or any other pressure-related neurosurgical or auditory pathology. The present DPOAE data con¢rmed the ¢ndings of Bu«ki et al. (1996) with TEOAEs. The main advantage of the DPOAE technique was that many di¡erent frequencies were probed rapidly, whereas only a few TEOAE spectral components could be found in the frequency range of interest (e.g. ¢ve on Fig. 6). The general framework established in the companion work (Avan et al., 2000) was successfully applied to analyzing the causes of posture-induced DPOAE changes. The vector analysis of DPOAE shifts revealed that the main posture-induced changes exhibited the same `signature' as those characterizing stapedius muscle con-
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tractions. It seems straightforward to attribute the increase in incremental sti¡ness of the stapes' annular ligament to the displacement of the stapes from its resting position by pressure increase in scala vestibuli (Casselbrant, 1979; Marchbanks, 1984; Bu«ki et al., 1996). The retrospective analysis of TEOAE data from hydrocephalic patients in the operating theater established that controlled, isolated ICP changes and posture changes led to identical pro¢les of emission shifts. This ¢nding con¢rms, ¢rstly, that ICP is the key element for all auditory modi¢cations associated with posture and secondly, that some transmission channel does transmit ICP variations to intralabyrinthine spaces. As the OAEs of all the subjects of the present work proved to react to posture or ICP changes, it is likely that at least one transmission channel was patent enough to transmit ICP changes. These functional data therefore support the most recent anatomical observations of temporal bones by Gopen et al. (1997) and Seo et al. (1997). The computer version of Zwislocki's (1962) model of the middle ear provided a re¢ned interpretation of posture data, in that the small additional change observed in several DPOAE pro¢les (from sitting to supine position) could be attributed to a middle-ear pressure increase in supine position. This e¡ect is well-known though of unclear origin, perhaps an increased volume of middle-ear mucosa, according to Gaihede and Kjaer (1998). The predictions of Zwislocki's model were ¢ne enough to account for the small di¡erence in the frequencies of maximum DPOAE phase shift visible on Fig. 3 (from 0.75 to 0.87^0.93 kHz). This model also con¢rmed that DPOAE phase shifts due to posture or ICP should remain signi¢cant and easily detectable well above 1 kHz, so that pressure monitoring may be more e¡ective using phase rather than level information. The DPOAE method disclosed new pieces of information as to the patency and the dynamics of channels connecting CSF and intralabyrinthine compartments. Continuous DPOAE recordings showed that large pressure changes resulted in rapid auditory modi¢cations, within less than 8 s, whereas smaller pressure variations (likely to be of the order of 100 daPa) might be transmitted more slowly to the cochlea. Pressure changes in the cochlea would be identical to CSF ones if the transmission channels were fully patent. It is very unlikely because gushers are rarely observed during stapedectomy ; the observation that the cochlear aqueduct is often ¢lled up with loose connective tissue (Gopen et al., 1997 ; Seo et al., 1997) would favor the hypothesis that liquid £ow is impossible and that viscous damping contributes to ¢ltering ICP waves. Assuming that the ICP variation due to a rapid posture change would be a square wave, the onset of intracochlear pressure is expected to be exponential, with a half-life proportional
to the viscous drag through the aqueduct and roundwindow compliance. No exponential was observed, but it must be noted that the temporal pro¢le of ICP change with posture is unknown, and possibly not a square wave : it probably explains why intralabyrinthine pressure exhibited a complex variation. It was possible to conclude that even minor ICP changes were fully re£ected through the ear after about half a minute, and often less. This ¢nding supports the recommendations of Marchbanks (1993) concerning ICP measurements with the MMS 10 system and shows that they are conservative. In conclusion, this study and the companion manuscript (Avan et al., 2000) stress the interest of considering the vector characteristics of OAEs generally, and point out their very high sensitivity to minute changes in middle-ear impedance: according to Davson (1967) and Chapman et al. (1990), ICP increase when moving from sitting to supine position hardly exceeds 100 daPa, although it was easily detected by DPOAEs in all subjects. Likewise, Bu«ki et al. (1996) using TEOAEs found that 60 daPa increases in ICP were consistently detected. OAEs seem to be a reliable tool to study ICP changes non-invasively through the ear: as such, they open new possibilities in neurosurgical monitoring, and perhaps also in audiology (e.g. for Menie©re's disease). Posture experiments provided a convenient atraumatic method to elicit ICP and intracochlear pressure changes in normal subjects, and despite the complexity of the resulting physiological modi¢cations, could be considered to alter mainly the sti¡ness of the stapes' annular ligament via increased intralabyrinthine pressure. However, given the large intersubject variability of the magnitude of ICP changes as a function of body position (Chapman et al., 1990) on the one hand, and of the magnitude of OAE responses to ICP changes (Bu«ki et al., 1996), on the other hand a fully quantitative assessment of ICP would probably require individual calibration of OAEs in the presence of surgically controlled ICP changes, as performed by Bu«ki et al. (1996). Acknowledgements This work was funded by Grant 99023 from CIESApape (PAI Balaton) to P. Avan and B. Bu«ki, and Grants CNAMTS/INSERM 4AIC04 and OTKA T022194. References Allen, J.B., 1990. Cube Dis User Manual. Bell Laboratories. Antonelli, A., Grandori, F., 1986. Long-term stability, in£uence of the head position and modelling considerations for evoked otoacoustic emissions. Scand. Audiol. Suppl. 25, 97^108.
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B. Bu«ki et al. / Hearing Research 140 (2000) 202^211 Avan, P., Bu«ki, B., Maat, B., Dordain, M., Wit, H.P., 2000. Middleear in£uence on otoacoustic emissions. I: Noninvasive investigation of the human transmission apparatus and comparison with model results. Hear. Res. 140, 189^201. Bu«ki, B., Avan, P., Lemaire, J.J., Dordain, M., Chazal, J., Ribari, O., 1996. Otoacoustic emissions: a new tool for monitoring intracranial pressure changes through stapes displacements. Hear. Res. 94, 125^139. Carlborg, B., Densert, B., Densert, O., 1982. Functional patency of the cochlear aqueduct. Ann. Otol. 91, 209^215. Casselbrant, M., 1979. Indirect determination of variations in the inner ear pressure in man, an experimental study. Acta Otolaryngol. (Stockh.) Suppl. 362, 7^57. Chapman, P.H., Cosman, E.R., Arnold, M.A., 1990. The relationship between ventricular £uid pressure and body position in normal subjects and subjects with shunts: a telemetric study. Neurosurgery 26, 181^189. Corso, J.F., 1962. Bodily position and auditory threshold. Percept. Motor Skills 14, 449. Davson, H., 1967. Physiology of the Cerebrospinal Fluid. J. and A. Churchill, London. Gaihede, M., Kjaer, D., 1998. Positional changes and stabilization of middle ear pressure. Auris Nasus Larynx 25, 255^259. Gopen, Q., Rosowski, J.J., Merchant, S.N., 1997. Anatomy of the normal human cochlear aqueduct with functional implications. Hear. Res. 107, 9^22. Horst, J.W., Wit, H.P. and Ritsma, R.J., 1983. Psychophysical aspects of cochlear acoustic emissions (`Kemp tones'). In: Klinke, R. and Hartmann, R. (Eds.), Hearing, Physiological Bases and Psychophysics. Springer Verlag, Berlin, pp. 89^96. Kemp, D.T., Bray, P., Alexander, L., Brown, A.M., 1986. Acoustic emission cochleography - practical aspects. Scand. Audiol. Suppl. 25, 71^94. Lackner, J.R., 1974. Changes in auditory localization during body tilt. Acta Otolaryngol. (Stockh.) 77, 19^28. Lutman, M.E., Martin, A.M., 1979. Development of an electroacoustic analogue model of the middle ear and acoustic re£ex. J. Sound Vibr. 64 (1), 133^157. Marchbanks, R.J., 1982. A new system for measuring tympanic membrane displacement. Hear. Aid J. 35, 14^17. Marchbanks, R.J., 1984. Measurement of tympanic membrane displacement arising from aural cardiovascular activity, swallowing, and intra-aural muscle re£ex. Acta Otolaryngol. (Stockh.) 98, 119^ 129.
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Marchbanks, R.J., 1993. MMS 10 Tympanic Displacement Analyser in Research and Clinical Practice, the Users Handbook. MMS. Macrae, J.H., 1972. E¡ects of body position on the auditory system. J. Speech Hear. Res. 15, 330^339. Miyake, H., Ohta, T., Kajimoto, Y., Matsukawa, M., 1997. A new ventriculoperitoneal shunt with a telemetric intracranial pressure sensor: clinical experience with 94 patients with hydrocephalus. Neurosurgery 40, 931^935. Moss, S.M., Marchbanks, R.J., Burge, D.M., 1990. Non-invasive assessment of ventricular shunt function using tympanic membrane displacement measurement technique. Z. Kinderchir. 45 (I), 26^28. Phillips, A.J., Farrell, G., 1992. The e¡ect of posture on three objective audiological measures. Br. J. Audiol. 26, 339^345. Phillips, A.J., Marchbanks, R.J., 1989. E¡ects of posture and age on tympanic membrane displacement measurements. Br. J. Audiol. 23, 279^284. Reid, A., Marchbanks, R.J., Burge, D.M., Martin, A.M., Bateman, D.E., Pickard, J.D., Brightwell, A.P., 1990. The relationship between intracranial pressure and tympanic membrane displacement. Br. J. Audiol. 24, 123^129. Seo, T., Adachi, O., Sakagami, M., Ryu, J.H., Kohut, R.I. and Hinojosa, R., 1997. Patency of the cochlear aqueduct and inner ear symptoms: A human temporal bone study. In: Popelka, G. (Ed.), Assoc. Res. Otolaryngol. Abs. XXth, pp. 157. Wable, J., Collet, L. and Chery-Croze, S., 1996. Age-related changes in perilymphatic pressure: preliminary results. In: Ernst, A., Marchbanks, R. and Samii, M. (Eds.), Intracranial and Intralabyrinthine Fluids, Basic Aspects and Clinical Applications. Springer, Berlin, pp. 191^198. Wilson, J.P., 1980. Evidence for a cochlear origin for acoustic reemissions, threshold ¢ne structure and tonal tinnitus. Hear. Res. 2, 233^252. Wilson, J.P., Sutton, G.J., 1981. Acoustic correlates of tonal tinnitus. Ciba Found. Symp. 85, 82^107. Wlodyka, J., 1978. Studies on cochlear aqueduct patency. Ann. Otol. Rhinol. Laryngol. 87, 22^27. Yoshida, M., Uemura, T., 1991. Transmission of cerebrospinal £uid pressure changes to the inner ear and its e¡ect on cochlear microphonics. Eur. Arch. Otorhinolaryngol. 248, 139^143. Zwislocki, J.J., 1962. Analysis of the middle-ear function. I: Input impedance. J. Acoust. Soc. Am. 34, 1514^1523.
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Middle-ear in£uence on otoacoustic emissions. II: Contributions of posture and intracranial pressure Be¨la Bu«ki a , Aleksander Chomicki b , Monique Dordain b , Jean-Jacques Lemaire b , Hero P. Wit c , Jean Chazal b , Paul Avan b; * a
b
ENT Department, Semmelweis University, Budapest, Hungary Laboratoire de Biophysique sensorielle (EA 2667), Faculte¨ de Me¨decine, Universite¨ d'Auvergne, P.O. Box 38, 63001 Clermont-Ferrand, France c ENT and Audiology Department, AZG, Groningen, The Netherlands Received 17 April 1999; received in revised form 22 October 1999; accepted 26 October 1999
Abstract Although it seems likely that body tilt or surgically provoked variations in intracranial pressure (ICP) can result in variations of intralabyrinthine pressure, the channels for pressure transmission remain controversial and the reasons why evoked otoacoustic emissions (EOAEs) exhibit attendant modifications are unclear. The theoretical framework implemented in the companion paper [Avan et al. part I, 2000] provides sensitive and non-invasive means to identify the middle-ear mechanism(s) entailed in EOAE changes. It was thus applied to analyze the influence of posture on EOAE phases and magnitudes as a function of frequency, in a series of experiments involving body tilt from sitting to supine (0³ or 330³). Controlled ICP variations were surgically carried out in a series of hydrocephalic patients and the resulting EOAE changes were compared to posture data and model predictions. In all cases, the EOAE changes closely resembled those due to an increase in the stiffness of the stapes' annular ligament, in keeping with the assumption that ICP gets transmitted to intralabyrinthine spaces and modifies the hydrostatic load on the stapes, thereby influencing EOAE features. A small additional contribution of middle-ear pressure to EOAE changes was identified in addition to the main stapes component. Dynamical EOAE measurements showed that sudden ICP changes were transmitted to the inner ear within 8^30 s. The high sensitivity of EOAE phases below 2 kHz to ICP changes, together with the absence of any significant confounding middle-ear effect, favors EOAEs for a reliable non-invasive monitoring of ICP and intralabyrinthine pressures. ß 2000 Elsevier Science B.V. All rights reserved. Key words: Posture; Intracranial pressure; Otoacoustic emission; Distortion; Middle-ear impedance; Hydrocephalus
1. Introduction Body tilt from upright to head-down position induces an increase in the intracranial pressure (ICP) of the cerebrospinal £uid (CSF) due to gravity (Davson, 1967 ; Chapman et al., 1990). Hearing is also a¡ected and auditory thresholds (Corso, 1962; Macrae, 1972), sound localization (Lackner, 1974) and auditory threshold microstructure (Horst et al., 1983) have been reported to depend on posture. Such changes originate
* Corresponding author. Tel.: +33 (4) 7360 8015; Fax: +33 (4) 7326 8818; E-mail: [email protected]
likely either from middle- or inner-ear modi¢cations in relation to body position or CSF pressure. Cochlear changes have been con¢rmed by objective measurements of cochlear microphonics (Yoshida and Uemura, 1991) and auditory brainstem-evoked responses (Phillips and Farrell, 1992). Otoacoustic emissions (OAEs) have proven to be posture-sensitive, for example stimulus frequency emissions (Wilson, 1980), spontaneous OAEs (Wilson and Sutton, 1981) and transient-evoked OAEs (TEOAE, Antonelli and Grandori, 1986; Bu«ki et al., 1996). Middle-ear impedance also reacts to posture changes and Casselbrant (1979) then Marchbanks (1982) designed methods to detect tympanic-membrane displacements associated with body tilt. The most parsimonious interpretation of all these ¢ndings is that
0378-5955 / 00 / $ ^ see front matter ß 2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 5 9 5 5 ( 9 9 ) 0 0 2 0 2 - 6
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posture-dependent changes of ICP induce variations of intralabyrinthine pressure. There is wide agreement that ICP and intralabyrinthine pressure can be equalized through several possible channels including cochlear aqueduct, vestibular aqueduct, perineural and perivascular spaces (Carlborg et al., 1982). Intralabyrinthine pressure can act directly upon the stapes or the cochlear structures, thereby modifying either sound transmission to the cochlea or sound processing inside the cochlea. Changes of middle-ear impedance may also induce minute alterations of cochlear function by modifying the impedance match at the boundary between middle ear and cochlea. Furthermore, posture also in£uences some, perhaps confounding, middle-ear characteristics other than those associated with the stapes and its ligament: for instance, it is well-known that middle-ear pressure slightly increases with body tilt (Bu«ki et al., 1996; Gaihede and Kjaer, 1998). The issue of pressure relationships between CSF and intralabyrinthine £uids bears an important clinical potential because it opens the possibility to monitor CSF pressure non-invasively through the ear. Patients treated for hydrocephalus can greatly bene¢t from such a monitoring (Moss et al., 1990). Direct objective methods to follow up the e¤cacy of surgically implanted shunting devices consist of either invasive investigation through lumbar puncture, or telemetric measurements requiring expensive sensors (Chapman et al., 1990 ; Miyake et al., 1997). The commercially available tympanic-membrane displacement method of Marchbanks (1982, 1984) provides a simple non-invasive alternative method for CSF pressure monitoring (Reid et al., 1990), although seemingly it su¡ers from some limitations in ageing patients (Phillips and Marchbanks, 1989; Wable et al., 1996). Recently, Bu«ki et al. (1996) have reported that the phases of TEOAE components below 2 kHz are very sensitive to postural changes and variations of ICP produced by surgical manipulations. In all the cases with controlled ICP increase, changes of about 60 daPa were reliably detected by TEOAEs and low-frequency phase shifts proved to be proportional to ICP change. Body tilting is a simple method allowing ICP to be manipulated in subjects for whom invasive measurements are unsuitable. Thus, posture experiments can be helpful to better evaluate the relationships between OAEs and ICP, and OAE detection might serve as an alternative to the tympanic-membrane displacement method of Marchbanks. The contribution of the above-mentioned mechanisms to posture-induced auditory changes remains a matter of controversy. Several channels may transmit CSF pressure to labyrinthine £uids, the venous system may be involved and a¡ect middle-ear impedance as well as intracochlear pressure. Likewise, the degrees of
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patency of the cochlear and vestibular aqueducts and the age-dependence of their patency have raised several arguments (Wlodyka, 1978 ; Phillips and Marchbanks, 1989 ; Gopen et al., 1997 ; Seo et al., 1997). The goal of this work is to address these questions by characterizing the posture e¡ect on OAEs. In the companion paper (Avan et al., 2000), we showed that distortion-product OAEs (DPOAEs) provided a convenient means to analyze middle-ear impedance changes in the mid-frequency range. Indeed, simple manipulations of the middle ear resulting in re£ex contractions of the stapedius muscle, in changes of middle-ear pressure and in increases of tympanic-membrane load, induced clear frequency-dependent shifts in the DPOAE levels and phases. A computer model derived from Zwislocki's (1962) network was used to predict DPOAE changes, from the assumption that each of the aforementioned manipulations a¡ected only a restricted, speci¢c set of parameters. This model correctly accounted for most of the experimental data, thereby explaining why the experimental pro¢les of shifts happened to be characteristic of the mechanical properties of the involved subsystem (stapes sti¡ness, tympanic-membrane sti¡ness or inertia). Accordingly, our aim was to detect DPOAEs after posture changes in human subjects, and to compare their pattern of level and phase shifts to those reported in the companion work for controlled middle-ear modi¢cations. The computerized model derived from Zwislocki's (1962) network, as modi¢ed by Lutman and Martin (1979), was used to adjust hypothetical parameter changes to experimental data from posture manipulations. 2. Materials and methods 2.1. Human subjects Three groups of subjects were included. All of them gave their informed consent to take part in the measurements in the course of either a routine ENT visit or a neurosurgical diagnostic procedure. Group 1 contained the same healthy adults (n = 8; age range 24^39 years) that had already participated in test 1 (stapedius re£ex) described in (Avan et al., 2000). Group 2 was made of other healthy subjects (n = 12; age range 21^63 years). Finally, ¢ve patients with hydrocephalus were extracted from a group of 18 patients for whom several data have been published in (Bu«ki et al., 1996). Group 3 was made of these ¢ve patients (age range 41^76 years). Their TEOAE and ICP data were reprocessed and compared to TEOAE recordings performed in the same ears during postural tests. The experimental procedures were approved by Grant CNAMTS/INSERM 4AIC04.
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2.2. Recordings The middle-ear status was controlled by the same tests as described in the companion work (Avan et al., 2000), and DPOAEs were recorded with the same equipment (Cube Dis, Mimosa Acoustics ; Allen, 1990). Primary-tone frequencies f1 and f2 were swept with f2 varying from 0.5 to 4 kHz (10 steps per octave), whereas the ratio f2/f1 was ¢xed at 1.20. The levels of primaries were 60 dB SPL at f2, 70 dB SPL at f1. The retrospective case study of group 3 ears was performed using TEOAEs instead of DPOAEs because, as already explained in Bu«ki et al. (1996), silence was required in the operating theater so as not to stir the sedated patients and interfere with the scheduled ICP course. In order to ful¢ll this requirement, sound stimuli had to be close to 0 dB SPL allowing TEOAEs to be detected, but not DPOAEs. Recordings were done with a ILO88 equipment (Kemp et al., 1986; setup in Bu«ki et al., 1996). The level and phase of the DPOAE at fd = 2f13f2 were extracted o¥ine from the data¢les stored by the Cube Dis acquisition system. The level of noise background around frequency fd was also available. The signal-to-noise ratio was considered to be acceptable when the DPOAE level exceeded the noise level by more than 12 dB. The magnitude and phase spectra of TEOAEs were obtained from the Fourier transform of the time-domain data¢les stored by the ILO88 equipment. The level and phase shifts of emissions with a postural change were de¢ned as the di¡erences between values before and after the postural change under consideration. As explained in Avan et al., (2000), the primary tones were calibrated in such a way that their levels and absolute phases were always the same in every recording session. Thus, the level and phase shifts of the DPOAE could only be due to the physiological di¡erence between the reference and test conditions. 2.3. Modi¢cations of posture or ICP 2.3.1. Experiment 1 The DPOAEs of the right ears of all the subjects of groups 1 and 2 were recorded in two di¡erent postures, sitting then head-down. This last posture was obtained with the help of a tilting table forming an adjustable angle a with the horizontal plane. The subjects lay £at on their back, and a was set at 330³. The eight subjects of group 1 had already been tested for stapedius re£ex in response to contralateral high-pass noise (corner frequency 3 kHz) at a level of 20 dB above re£ex threshold (Avan et al., 2000). They were instructed to swallow after every posture change, so as to keep stable their middle-ear pressure, as evaluated by tympanometry (Madsen ZO73, frequency of probe tone 226 Hz). These
data were augmented with an intermediate measurement carried out in group 2 for a = 0³. In contrast with the subjects of group 1, those of group 2 were not instructed to swallow and their middle-ear pressure could vary with posture. Data processing consisted of plotting DPOAE level and phase shifts with reference to the sitting position, against frequency fd. Frequency pro¢les were obtained for 330³ vs. sitting with stable middle-ear pressure (group 1; n = 8) and for 0³ vs. sitting and 330³ vs. sitting (group 2; n = 12). The DPOAE shifts due to body tilt were compared in group 2 for a = 0³ vs. 330³, as a function of frequency. The frequency pro¢les of group 1 were compared to those induced by stapedius re£ex activation in group 1. 2.3.2. Experiment 2 Frequencies f2 and f1 were ¢xed (with f2 around 1.2^ 1.3 kHz) and a continuous monitoring of DPOAEs was carried out in the 12 subjects of group 2 (one DPOAE sample every 4 s). In the meantime, they were sitting on the tilting table for about 100 s, then, within less than 4 s, they were moved to supine position (a = 0³) for the next 100 s, then to head-down (a = 330³) for the next 100 s, and ¢nally back to sitting posture (100 s). Special care was taken to minimize the movements of the ear probe while the subject and the table moved. The Cube Dis system made it possible to monitor simultaneously the levels and phases of the acoustic signal in the ear canal at f1 and f2. Data were discarded and the test redone later whenever some characteristics of one of the primary levels were found to drift (by more than 0.5 dB for the level, or 10³ for the phase). The levels and phases of the DPOAEs were plotted against time. Average time plots were obtained across ears, after normalizing the DPOAE shifts with respect to two reference values, namely 0% (baseline in sitting position) and 100% (plateau reached after moving to supine or head-down position). The values for baseline and plateau were computed from the mean of 10 consecutive points taken in a stable interval, more than 40 s after any posture change. 2.3.3. Retrospective case study Data from patients tested for hydrocephalus and included in a previous study (Bu«ki et al., 1996) were selected according to two criteria. In the ¢rst place, their TEOAEs had been recorded along with a diagnostic test involving direct infusion of saline (80 ml/h) into CSF through a lumbar puncture. This so-called perfusion test produced a controlled increase in ICP that was monitored continuously using a piezoresistive probe, as reported in (Bu«ki et al., 1996). The day before the perfusion test, TEOAEs had been recorded in the same ear in response to body tilt, following the same protocol as for experiment 1 in the present work. The second crite-
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rion required that the TEOAE spectra are rich enough that TEOAE shifts produced by ICP changes could be reliably computed at many frequencies. The ¢ve patients of group 3 met these criteria (out of 18 tested in Bu«ki et al., 1996). To bridge the gap between DPOAE and TEOAE data, we needed to assume that level and phase shifts depended little on the nature of OAEs (TEOAEs or DPOAEs). This was checked on the data from four patients of group 1, who were submitted to posture changes from sitting to 30³ head-down while DPOAEs, then TEOAEs were recorded. 2.3.4. Network model predictions The computer model described in the companion work (Avan et al., 2000) was used to predict the pro¢les of phase and level shifts of emissions, assuming that posture mainly in£uenced the sti¡ness of the annular ligament of the stapes. This sti¡ness was represented by capacitance Cst, varying from in¢nity to 0.25 WF, in the analog electrical network of Zwislocki, 1962 and Lutman and Martin, 1979. The value of Cst was assumed to be very large in the reference sitting posture ( s 1 mF), and its ¢nal value was supposed to decrease with increasing hydrostatic pressure, that is, with decreasing angle of the tilting table, from 0 to 330³. Unfortunately, the relationships between Cst and ICP, as well as between ICP and angle of tilt, are di¤cult to ascertain in a quantitative manner: for example, Bu«ki et al. (1996) reported a large intersubject variance in the slope of the linear regression of OAE shifts vs. ICP, and Chapman et al. (1990) described strongly non-linear and subject-dependent variations of ICP as a function of the angle of body tilt. Therefore, no attempt could be made to obtain a quantitative assessment of the change in stapes ligament sti¡ness, and the only reason for the choice of Cst value was that visual optimization of model predictions was achieved. In addition to a Cst decrease, an increase in middleear pressure was considered for group 2 subjects moving from sitting to head-down posture, as tympanometry showed that middle-ear pressure varied by about +35 daPa in this case (Bu«ki et al., 1996). To account for it, the DPOAE shifts were also computed when (C0, Cd1, Cd2, Cd3) were modi¢ed in addition to Cst, by a multiplicative factor between 1 and 1/6, as tested in the companion paper (Avan et al., 2000). 3. Results Control DPOAE recordings for experiment 1 were already described in Avan et al. (2000). The levels obtained with the continuous monitoring of experiment 2 were very similar and signal-to-noise ratios exceeded
Fig. 1. Superimposed examples of two individual pro¢les for DPOAE phase shift (top) and level shift (bottom) against frequency, for body tilt (from sitting to 30³ head-down, open circles for ear 1, closed circles for ear 2) vs. stapedius muscle contractions elicited by loud contralateral noise (open diamonds for ear 1, closed diamonds for ear 2).
12 dB as required, except during the ¢rst 4 s following a posture change. 3.1. Experiment 1 (postures, comparison with stapedius) Individual posture tests gave phase shifts very similar to those induced by stapedius muscle contractions. Fig. 1 (top panel) shows two examples of phase-shift pro¢le with frequency. Both presented low-frequency dominant e¡ects, with di¡erent corner frequencies for the two ears, namely 1.3 and 1.6 kHz for the heavy and thin lines, respectively. Stapedius (diamonds) and posture e¡ects (circles) resembled each other in the two cases. When the same comparison was performed for level shifts (Fig. 1, bottom panel, same symbols), the correspondence was less good because the distance between the stapedius and posture plots could reach 2 dB, with the stapedius shifts being more negative than the posture ones. When posture was changed from sitting to headdown (a = 330³) while middle-ear pressure was ¢xed, the average shift of DPOAE level was close to zero above 1 kHz (Fig. 2, lower left panel; thin lines for average þ 1 S.D.). Below 1 kHz, it was negative and of the order of 1 dB. S.D.s were close to 2 dB. The average phase shift (Fig. 2, upper left panel, same symbols as on bottom diagram) corresponded to a lead in head-down position. The largest phase shifts were obtained below 1 kHz and reached about 25³. As fre-
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Fig. 2. (left panels) Average DPOAE phase shift (top) and level shift (bottom) against frequency for posture change in the ears of group 1 (n = 8) (from sitting to 30³ head-down), and average þ 1 S.D. (thin lines). (right panels) For comparison, average DPOAE phase and level shifts against frequency in the same ears for stapedius muscle contractions, and average þ 1 S.D. (thin lines) (from Avan et al., 2000). The heavy lines on both diagrams represent the predictions of the computerized model. As explained in (Avan et al., 2000), the model prediction for DPOAE level shift had to be referred to the dashed baseline (in the lower right panel), i.e. shifted down by 1.5 dB, to account for a possible e¡erent olivocochlear e¡ect elicited by the contralateral noise.
quency increased above 1 kHz, the phase shift decreased to insigni¢cant values around 1.7 kHz. S.D.s were of the order of 15³. On the right panels, Fig. 2 recalls the average DPOAE shifts reported in the companion work (Avan et al., 2000) when re£ex contractions of the stapedius muscle were triggered at 20 dB above re£ex threshold in the same ears (closed circles on phase- and level-shift diagrams). Although the sizes of posture and stapedius e¡ects di¡ered slightly, their two pro¢les were qualitatively very similar. The average level shifts also exhibited similar pro¢les, except for a vertical shift of about 31.5 dB on the stapedius re£ex plot (Fig. 2, lower right panel). Avan et al. (2000) suggested that this 1.5 dB contribution might be due to an additional suppression of DPOAEs due to activation of the crossed olivocochlear bundle by contralateral noise. Intersubject di¡erences consisted of two components, a slight shift of the frequency corresponding to the maximum phase lead, which varied from 0.78 to 1.22 kHz, and a variation of the size of e¡ects. Maximum phase shifts varied from 74 to 10³, whereas the largest level shifts varied from 34 to 31 dB. For the subset of data from group 2 (supine, a = 0³, vs. sitting), the average phase shift (Fig. 3, top, open circles) was positive at all frequencies, and it presented two clear peaks of similar size (19^23³) separated by a trough. The lower-frequency peak was broad and centered around fd = 0.75 kHz. The other one concerned a
Fig. 3. (top) Average DPOAE phase shifts from sitting to supine (dashed line, open circles) and from supine to head-down (330³; continuous line, closed circles) in the 12 ears of group 2. All S.D.s were 6 10³. (bottom) Model predictions for combinations of Cst and eardrum capacitance changes (Cst minimum = 2.5 WF, dashed line; Cst minimum = 1.75 WF, continuous line). Recall that model predictions were shown to be inaccurate at lower frequencies for positive middle-ear pressure e¡ect, as it is the case here (Avan et al., 2000).
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Fig. 4. Example of DPOAE phase (top) and level (bottom) shifts as derived from continuous monitoring, while the subject was sitting (from 0^100 s), moved to supine position, kept this position from about 110 to 210 s, moved to head-down position (from about 210 to 310 s) and eventually went back to sitting position (after 320 s). The thin horizontal lines on the top diagram indicate the plateau values of DPOAE phase after the posture was kept stable for 30 s to 1 min. It can be noted that the plateau values for DPOAE level were less stable than for phase: in particular, the level after 300 s did not come back to its initial value. For this series of measurements, frequency f2 was set at 1.3 kHz, with f2/f1 = 1.20, and primary levels were 60 dB SPL at f2 and 70 dB SPL at f1.
narrow frequency interval around fd = 1.1 kHz. Level shifts were negative and very small below 1.2 kHz, whereas no level change was observed at higher frequencies. When the posture moved from supine to head-down (a = 330³), the size of the e¡ects increased. The pro¢le of average phase shifts exhibited one broad peak, reaching 27³ around 0.87^0.93 kHz (Fig. 3, closed circles), that is, at a slightly higher frequency than the corresponding lower-frequency peak of the ¢rst posture change. The previously observed second narrow peak seemed to be replaced by a bulge on the pro¢le around the same frequencies. The level shifts were close to 31 dB at low frequencies.
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Fig. 5. Normalized average phase shift of DPOAE as a function of time, over the 32 s interval following posture change from sitting to recumbent (closed circles) and average þ 1 S.D. (thin lines). Meanwhile, no signi¢cant level shift was recorded in most ears. Noisy data were not taken into account, thus the average was computed from 9^10 values only (out of 12 ears) for times 4, 8 and 12 s.
the level shift was about 31.5 dB. From a = 0³ to 330³, the phase shift of this ear increased by 48³, whereas the level decreased by an additional 3 dB. When back to sitting posture, the phase recovered its initial value (marked by the thin horizontal line) whereas the level di¡ered from it by 32 dB. In many ears, no level shift was visible in clear relation to any posture change, and in the long term, levels often tended to drift slowly. These drifts were likely related to slight and gradual movements of the probe tip with posture changes, that did not seem to a¡ect phase measurements nor primary-tone characteristics. Fig. 5 shows the average normalized phase shift dur-
3.2. Experiment 2 (continuous monitoring) Using the value of f2 and f1 that produced the maximum shift in experiment 1, continuous measurements were made of the DPOAE at 2f13f2 while posture varied (Fig. 4). Sharp phase or level changes were visible just during a posture change (from sitting to supine, around 100 s, then from head-down to sitting, after 300 s) and corresponded to noisy data. Sharp changes could also occur brie£y when a subject could not help swallowing. After each position had been kept for about 30 s or less, DPOAE level and phase reached stable plateaus. For the example of Fig. 4, the phase shift from sitting to supine plateaued at 16³, whereas
Fig. 6. Example of comparison of DPOAE vs. TEOAE shifts in the same ear, when the body was tilted from sitting to head-down. In this ear, TEOAE exhibited only ¢ve peaks at di¡erent frequencies in the range 0.6^3.5 kHz.
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Fig. 7. Example of TEOAE phase shift against frequency for the right ear of a subject whose body was tilted from sitting to supine position (open symbols), and who was later submitted to a 160 daPa increase in CSF pressure in the course of a hydrocephalus diagnosis procedure in the operating theater (closed symbols). The TEOAE frequency spectrum in this ear was broad enough for the signal-to-noise ratio to exceed 12 dB at most sample frequencies between 1 and 3 kHz. No signi¢cant level shift was recorded throughout posture and perfusion tests.
ing the ¢rst 32 s after posture was moved from sitting to supine (0³). The plateau was reached (within 5%) after 20^28 s, with a small intersubject variance. No simple monotonic function, such as an exponential one, provided a correct ¢t for experimental data. Between 12 and 20 s after the posture change, the phase shift tended to slow down or even decrease. When posture moved from a = 0³ to 330³, the ¢rst data point after 4 s was often noisy and the plateau had already been reached after 8 s, within 10%, in all subjects. 3.3. Retrospective case study Since this case study had to use TEOAE recordings, a control of the e¡ects of posture change, from sitting to head-down, was performed on both DPOAEs and TEOAEs for four subjects of group 2. A typical example is presented on Fig. 6 (DPOAEs : lines, TEOAE peaks, closed circles). An obvious disadvantage of TEOAEs in this example was that their shifts could be determined only at the ¢ve frequencies corresponding to the main peaks in the TEOAE spectrum, whereas DPOAEs were sampled at 10 points per octave. Nevertheless, a reasonably good agreement (within 10³ and 1 dB) was observed between the results of the two types of emissions in all four ears. The TEOAE spectra in the ¢ve ears of group 3 were such that at least 10 frequency components were identi¢ed with signal-to-noise ratios larger than 12 dB at more than three consecutive frequency samples (one point every 48.8 Hz with the ILO88 system). Thus we considered that it was reliable to compute the phase and level shifts of TEOAE components by direct comparison of the magnitude and phase spectra derived from the Fourier transform of the time-domain
TEOAEs, in head-down vs. sitting position, and in lower vs. higher ICP during the perfusion test. An example of phase shift pro¢les against frequency is depicted on Fig. 7 (open circles, posture test; closed circles, perfusion test with an 160 daPa ICP increase in between the two TEOAE recordings). A close correspondence was observed between the two pro¢les, with only a few isolated discrepancies of 10^14³. The size of the posture e¡ect was slightly smaller than that due to CSF pressure increase. The other individual phase pro¢les for posture change and ICP increase also exhibited good matches. Indeed, in all ears, the maximum shifts were reached at the same frequencies within 50 Hz; the corner frequencies of the shift pro¢les, de¢ned as the ¢rst frequencies with a shift 6 half its maximum value, coincided within 50 Hz except in one ear (because its phase shifts due to posture change were too close to zero, the assessment of the corner frequency was ambiguous on the pro¢le). As the available ICP changes varied widely (i.e. from 60 to 310 daPa), no conclusion as to the sizes of posture vs. ICP e¡ects could be derived; maximum phase shifts due to posture varied from 0³ to 70³ and those due to ICP increase from 40³ to 70³. No reliable TEOAE component was found below 0.9 kHz, so that the tested frequency interval was restricted to 0.9^3 kHz in all ears. Level shifts with posture change and ICP increase always remained very small or absent in this frequency range. 3.4. Model predictions The lumped-element electrical network model of Zwislocki (1962) was used as already shown in (Bu«ki et al., 1996) and (Avan et al., 2000), ¢rst assuming an isolated increase in annular ligament sti¡ness. The superposition of the computed phase and level shifts with experimental data (see Fig. 2, left panels, bold lines) was optimal when Cst was adjusted to 1.5 WF for a = 330³. The computed shifts due to modi¢cations of forward and reverse transmission were very similar at all frequencies, for example at 0.8 kHz, vPforward = 12.8³, vPreverse = 9.7³. As middle-ear pressure could not be controlled when the posture of group 2 subjects was altered, the actual physiological situation was likely to involve a small middle-ear pressure gradient in supine posture (not exceeding +35 daPa as reported by Bu«ki et al., 1996; of the order of +22 daPa according to Gaihede and Kjaer, 1998). In order to account for this gradient, a decrease in the capacitances representing eardrum sti¡nesses was combined with the change of Cst. Whereas Cst varied from in¢nity to either 2.5 WF (for a = 0³) or 1.75 WF (for a = 330³), C0, Cd1, Cd2 and Cd3 were divided by 1.3. With this simulation of middle-ear pressure increase, an
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additional peak appeared in the phase- and level-shift pro¢les, around fd = 1.2 kHz (Fig. 3, bottom). For a = 0³, the size of the additional peak was similar to that of the lower-frequency peak associated with Cst decrease (as observed in Fig. 3, open symbols) representing the real-ear data in a = 0³ vs. sitting position. For a = 330³, the main Cst e¡ect grew rapidly so that the additional peak appeared as a mere bulge on the high-frequency slope of the phase pro¢le (see Fig. 3, top, closed symbols for real-ear data). It was noticeable on Fig. 3 (bottom) that the predicted main peak was shifted towards higher frequencies when Cst decreased (in keeping with the experimental data shown on Fig. 3, top). Model predictions did not accurately match experimental data below 1 kHz, as already pointed out in the companion paper (Avan et al., 2000) for positive pressure changes similar to the present ones. In summary, the e¡ect of posture on DPOAE levels and phases in man closely resembled that induced by stapedius muscle re£ex triggered by contralateral noise. It consisted of a phase lead at low frequencies, together with a weak decrease of DPOAE levels. This e¡ect was correctly modelled qualitatively, using the lumped-element middle-ear equivalent electrical network of Zwislocki (1962), assuming that posture acted mainly on capacitance Cst representing the sti¡ness of the stapes' annular ligament. As middle-ear pressure was left free to vary with posture in the second group of subjects, a small additional e¡ect appeared within a restricted frequency interval slightly above 1 kHz when the posture e¡ect was weak. This contribution matched that predicted by Zwislocki's model when assuming that middle-ear pressure a¡ected eardrum sti¡nesses. The temporal course of DPOAE changes after a sudden posture change revealed that the transmission of the alleged resulting ICP change to cochlear liquids and stapes sti¡ness occurred within seconds for head-down vs. sitting move. When ICP was surgically manipulated in motionless patients, OAE changes mimicked those obtained by postural changes. 4. Discussion Although posture e¡ects on hearing have been welldocumented through numerous audiological methods, either subjective (Corso, 1962; Macrae, 1972; Horst et al., 1983) or objective ones (Casselbrant, 1979; Wilson, 1980 ; Marchbanks, 1982; Antonelli and Grandori, 1986 ; Phillips and Farrell, 1992; Bu«ki et al., 1996), their possible origins have not been established clearly. In particular, it is di¤cult to ascertain whether these effects are a re£ection of middle- or inner-ear modi¢cations, or a combination of two. Nevertheless, it seems likely that attendant variations of the hydrostatic pres-
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sure within intralabyrinthine compartments are a key element of the auditory e¡ects of posture, and posture undoubtedly a¡ects ICP primarily. Therefore, our study of some auditory e¡ects of posture aimed at opening a possibility to address the issue of relationships between ICP and intralabyrinthine pressure. This issue is interesting for fundamental reasons. Several studies of human temporal bones have tentatively addressed the regulation of hydrostatic pressure in the labyrinthine spaces, in relation to possible channels connecting these spaces to the CSF compartment. The patency of the most evident of these channels through the temporal bone, the cochlear aqueduct, has been examined in several publications. Wlodyka (1978) derived from histological studies that the patency of the cochlear aqueduct seemed to decrease with age, so that it was found to be blocked in about 70% temporal bones from subjects s 60 years, whereas 82% aqueducts were patent below 20 years. In contrast, more recent extensive studies (Gopen et al., 1997; Seo et al., 1997) have shown that the percentage of blocked cochlear aqueduct does not vary signi¢cantly with age and that about 30% appear to be fully patent, while 40^ 50% are just ¢lled with loose connective tissue. Thus, most cochlear aqueducts would be likely to transmit low-frequency pressure waves from CSF to labyrinthine compartments in most subjects regardless of age, as long as the wave frequency is 6 20 Hz (Gopen et al., 1997). Intralabyrinthine pressure measurements also bear potentially important practical consequences for neurosurgeons, because the possibility to monitor ICP through indirect audiological methods seems much more cost-e¡ective than direct invasive or telemetric monitoring systems (Chapman et al., 1990; Miyake et al., 1997). Marchbanks (1982, 1984) designed a tympanic-membrane displacement system (MMS 100 ) and reported promising results in hydrocephalus. Recently, Bu«ki et al. (1996) showed that OAEs react to posture or ICP changes in a systematic and very sensitive manner, thereby opening a new possibility to monitor patients with hydrocephalus or any other pressure-related neurosurgical or auditory pathology. The present DPOAE data con¢rmed the ¢ndings of Bu«ki et al. (1996) with TEOAEs. The main advantage of the DPOAE technique was that many di¡erent frequencies were probed rapidly, whereas only a few TEOAE spectral components could be found in the frequency range of interest (e.g. ¢ve on Fig. 6). The general framework established in the companion work (Avan et al., 2000) was successfully applied to analyzing the causes of posture-induced DPOAE changes. The vector analysis of DPOAE shifts revealed that the main posture-induced changes exhibited the same `signature' as those characterizing stapedius muscle con-
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tractions. It seems straightforward to attribute the increase in incremental sti¡ness of the stapes' annular ligament to the displacement of the stapes from its resting position by pressure increase in scala vestibuli (Casselbrant, 1979; Marchbanks, 1984; Bu«ki et al., 1996). The retrospective analysis of TEOAE data from hydrocephalic patients in the operating theater established that controlled, isolated ICP changes and posture changes led to identical pro¢les of emission shifts. This ¢nding con¢rms, ¢rstly, that ICP is the key element for all auditory modi¢cations associated with posture and secondly, that some transmission channel does transmit ICP variations to intralabyrinthine spaces. As the OAEs of all the subjects of the present work proved to react to posture or ICP changes, it is likely that at least one transmission channel was patent enough to transmit ICP changes. These functional data therefore support the most recent anatomical observations of temporal bones by Gopen et al. (1997) and Seo et al. (1997). The computer version of Zwislocki's (1962) model of the middle ear provided a re¢ned interpretation of posture data, in that the small additional change observed in several DPOAE pro¢les (from sitting to supine position) could be attributed to a middle-ear pressure increase in supine position. This e¡ect is well-known though of unclear origin, perhaps an increased volume of middle-ear mucosa, according to Gaihede and Kjaer (1998). The predictions of Zwislocki's model were ¢ne enough to account for the small di¡erence in the frequencies of maximum DPOAE phase shift visible on Fig. 3 (from 0.75 to 0.87^0.93 kHz). This model also con¢rmed that DPOAE phase shifts due to posture or ICP should remain signi¢cant and easily detectable well above 1 kHz, so that pressure monitoring may be more e¡ective using phase rather than level information. The DPOAE method disclosed new pieces of information as to the patency and the dynamics of channels connecting CSF and intralabyrinthine compartments. Continuous DPOAE recordings showed that large pressure changes resulted in rapid auditory modi¢cations, within less than 8 s, whereas smaller pressure variations (likely to be of the order of 100 daPa) might be transmitted more slowly to the cochlea. Pressure changes in the cochlea would be identical to CSF ones if the transmission channels were fully patent. It is very unlikely because gushers are rarely observed during stapedectomy ; the observation that the cochlear aqueduct is often ¢lled up with loose connective tissue (Gopen et al., 1997 ; Seo et al., 1997) would favor the hypothesis that liquid £ow is impossible and that viscous damping contributes to ¢ltering ICP waves. Assuming that the ICP variation due to a rapid posture change would be a square wave, the onset of intracochlear pressure is expected to be exponential, with a half-life proportional
to the viscous drag through the aqueduct and roundwindow compliance. No exponential was observed, but it must be noted that the temporal pro¢le of ICP change with posture is unknown, and possibly not a square wave : it probably explains why intralabyrinthine pressure exhibited a complex variation. It was possible to conclude that even minor ICP changes were fully re£ected through the ear after about half a minute, and often less. This ¢nding supports the recommendations of Marchbanks (1993) concerning ICP measurements with the MMS 10 system and shows that they are conservative. In conclusion, this study and the companion manuscript (Avan et al., 2000) stress the interest of considering the vector characteristics of OAEs generally, and point out their very high sensitivity to minute changes in middle-ear impedance: according to Davson (1967) and Chapman et al. (1990), ICP increase when moving from sitting to supine position hardly exceeds 100 daPa, although it was easily detected by DPOAEs in all subjects. Likewise, Bu«ki et al. (1996) using TEOAEs found that 60 daPa increases in ICP were consistently detected. OAEs seem to be a reliable tool to study ICP changes non-invasively through the ear: as such, they open new possibilities in neurosurgical monitoring, and perhaps also in audiology (e.g. for Menie©re's disease). Posture experiments provided a convenient atraumatic method to elicit ICP and intracochlear pressure changes in normal subjects, and despite the complexity of the resulting physiological modi¢cations, could be considered to alter mainly the sti¡ness of the stapes' annular ligament via increased intralabyrinthine pressure. However, given the large intersubject variability of the magnitude of ICP changes as a function of body position (Chapman et al., 1990) on the one hand, and of the magnitude of OAE responses to ICP changes (Bu«ki et al., 1996), on the other hand a fully quantitative assessment of ICP would probably require individual calibration of OAEs in the presence of surgically controlled ICP changes, as performed by Bu«ki et al. (1996). Acknowledgements This work was funded by Grant 99023 from CIESApape (PAI Balaton) to P. Avan and B. Bu«ki, and Grants CNAMTS/INSERM 4AIC04 and OTKA T022194. References Allen, J.B., 1990. Cube Dis User Manual. Bell Laboratories. Antonelli, A., Grandori, F., 1986. Long-term stability, in£uence of the head position and modelling considerations for evoked otoacoustic emissions. Scand. Audiol. Suppl. 25, 97^108.
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B. Bu«ki et al. / Hearing Research 140 (2000) 202^211 Avan, P., Bu«ki, B., Maat, B., Dordain, M., Wit, H.P., 2000. Middleear in£uence on otoacoustic emissions. I: Noninvasive investigation of the human transmission apparatus and comparison with model results. Hear. Res. 140, 189^201. Bu«ki, B., Avan, P., Lemaire, J.J., Dordain, M., Chazal, J., Ribari, O., 1996. Otoacoustic emissions: a new tool for monitoring intracranial pressure changes through stapes displacements. Hear. Res. 94, 125^139. Carlborg, B., Densert, B., Densert, O., 1982. Functional patency of the cochlear aqueduct. Ann. Otol. 91, 209^215. Casselbrant, M., 1979. Indirect determination of variations in the inner ear pressure in man, an experimental study. Acta Otolaryngol. (Stockh.) Suppl. 362, 7^57. Chapman, P.H., Cosman, E.R., Arnold, M.A., 1990. The relationship between ventricular £uid pressure and body position in normal subjects and subjects with shunts: a telemetric study. Neurosurgery 26, 181^189. Corso, J.F., 1962. Bodily position and auditory threshold. Percept. Motor Skills 14, 449. Davson, H., 1967. Physiology of the Cerebrospinal Fluid. J. and A. Churchill, London. Gaihede, M., Kjaer, D., 1998. Positional changes and stabilization of middle ear pressure. Auris Nasus Larynx 25, 255^259. Gopen, Q., Rosowski, J.J., Merchant, S.N., 1997. Anatomy of the normal human cochlear aqueduct with functional implications. Hear. Res. 107, 9^22. Horst, J.W., Wit, H.P. and Ritsma, R.J., 1983. Psychophysical aspects of cochlear acoustic emissions (`Kemp tones'). In: Klinke, R. and Hartmann, R. (Eds.), Hearing, Physiological Bases and Psychophysics. Springer Verlag, Berlin, pp. 89^96. Kemp, D.T., Bray, P., Alexander, L., Brown, A.M., 1986. Acoustic emission cochleography - practical aspects. Scand. Audiol. Suppl. 25, 71^94. Lackner, J.R., 1974. Changes in auditory localization during body tilt. Acta Otolaryngol. (Stockh.) 77, 19^28. Lutman, M.E., Martin, A.M., 1979. Development of an electroacoustic analogue model of the middle ear and acoustic re£ex. J. Sound Vibr. 64 (1), 133^157. Marchbanks, R.J., 1982. A new system for measuring tympanic membrane displacement. Hear. Aid J. 35, 14^17. Marchbanks, R.J., 1984. Measurement of tympanic membrane displacement arising from aural cardiovascular activity, swallowing, and intra-aural muscle re£ex. Acta Otolaryngol. (Stockh.) 98, 119^ 129.
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Marchbanks, R.J., 1993. MMS 10 Tympanic Displacement Analyser in Research and Clinical Practice, the Users Handbook. MMS. Macrae, J.H., 1972. E¡ects of body position on the auditory system. J. Speech Hear. Res. 15, 330^339. Miyake, H., Ohta, T., Kajimoto, Y., Matsukawa, M., 1997. A new ventriculoperitoneal shunt with a telemetric intracranial pressure sensor: clinical experience with 94 patients with hydrocephalus. Neurosurgery 40, 931^935. Moss, S.M., Marchbanks, R.J., Burge, D.M., 1990. Non-invasive assessment of ventricular shunt function using tympanic membrane displacement measurement technique. Z. Kinderchir. 45 (I), 26^28. Phillips, A.J., Farrell, G., 1992. The e¡ect of posture on three objective audiological measures. Br. J. Audiol. 26, 339^345. Phillips, A.J., Marchbanks, R.J., 1989. E¡ects of posture and age on tympanic membrane displacement measurements. Br. J. Audiol. 23, 279^284. Reid, A., Marchbanks, R.J., Burge, D.M., Martin, A.M., Bateman, D.E., Pickard, J.D., Brightwell, A.P., 1990. The relationship between intracranial pressure and tympanic membrane displacement. Br. J. Audiol. 24, 123^129. Seo, T., Adachi, O., Sakagami, M., Ryu, J.H., Kohut, R.I. and Hinojosa, R., 1997. Patency of the cochlear aqueduct and inner ear symptoms: A human temporal bone study. In: Popelka, G. (Ed.), Assoc. Res. Otolaryngol. Abs. XXth, pp. 157. Wable, J., Collet, L. and Chery-Croze, S., 1996. Age-related changes in perilymphatic pressure: preliminary results. In: Ernst, A., Marchbanks, R. and Samii, M. (Eds.), Intracranial and Intralabyrinthine Fluids, Basic Aspects and Clinical Applications. Springer, Berlin, pp. 191^198. Wilson, J.P., 1980. Evidence for a cochlear origin for acoustic reemissions, threshold ¢ne structure and tonal tinnitus. Hear. Res. 2, 233^252. Wilson, J.P., Sutton, G.J., 1981. Acoustic correlates of tonal tinnitus. Ciba Found. Symp. 85, 82^107. Wlodyka, J., 1978. Studies on cochlear aqueduct patency. Ann. Otol. Rhinol. Laryngol. 87, 22^27. Yoshida, M., Uemura, T., 1991. Transmission of cerebrospinal £uid pressure changes to the inner ear and its e¡ect on cochlear microphonics. Eur. Arch. Otorhinolaryngol. 248, 139^143. Zwislocki, J.J., 1962. Analysis of the middle-ear function. I: Input impedance. J. Acoust. Soc. Am. 34, 1514^1523.
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