J Am Acad Audiol 17:45–68 (2006)

Electrocochleography in the Evaluation of Patients with Ménière’s Disease/ Endolymphatic Hydrops

John A. Ferraro* John D. Durrant†

Abstract Electrocochleography (ECochG) has evolved as an important tool in the diagnosis/assessment/monitoring of Ménière’s disease/endolymphatic hydrops (MD/ELH).This manuscript provides an update on the use of ECochG for these purposes.The material presented includes descriptions of the components of the electrocochleogram; ECochG recording approaches and parameters; how to prepare for an exam, including subject/patient considerations; construction and placement of a tympanic membrane recording electrode; and interpretation the electrocochleogram. Various approaches aimed at improving ECochG’s sensitivity and specificity to MD/ELH also are described. These approaches go beyond simple measurement of the now-conventional summating potential (SP)/action potential (AP) magnitude ratio to include the SP magnitude to tonebursts, the SP/AP area ratio, and the AP latency difference to clicks of opposing polarity.

Key Words: Action potential, auditory brainstem response, auditory evoked potentials, broadband click, cochlear microphonic, electrocochleography, extratympanic, Ménière’s disease/endolymphatic hydrops, summating potential, toneburst, transtympanic, tympanic membrane, tymptrode

Abbreviations: ABR = auditory brainstem response; AC = alternating current; AP = action potential; AEP = auditory ; BBC = broadband click; CM = cochlear microphonic; ECochG = electrocochleography; ET = extratympanic; MD/ELH = Ménière’s disease/endolymphatic hydrops; SP = summating potential; TM = tympanic membrane; TT = transtympanic

Sumario La electrococleografía (ECochG) ha evolucionado como una importante her- ramienta en el diagnóstico, evaluación y monitoreo de la enfermedad de Ménière-hydrops endolinfático (MD/HEL). Este manuscrito aporta una actu- alización en el uso de la ECochG para estos propósitos. El material presentado incluye descripción de los componentes del electrococleograma; parámetros y enfoques de registro del ECochG; cómo prepararse para un examen, incluyendo consideraciones para el sujeto/paciente; construcción y colocación de un electrodo de registro en la membrana timpánica, e interpretación del electrococleograma. Se describen también varios enfoques orientados a mejo- rar la sensibilidad y la especificidad de la ECochG en la MD/HEL. Estos enfoques van más allá de la simple medición de la convencional tasa de mag- nitud del potencia de suma (SP)/potencial de acción (AP), e incluyen la magnitud del SP para bursts tonales, la tasa de área de SP/AP y la diferencia de laten- cia del AP a clics de polaridad opuesta.

* and Speech Department, University of Kansas Medical Center; †Department of Communication Science and Disorders, University of Pittsburgh

John A. Ferraro, Ph.D., Hearing and Speech Department, University of Kansas Medical Center, 39th and Rainbow Blvd., Kansas City, KS 66160-7605; Phone: 913-588-5937; Fax: 913-588-5923; E-mail: [email protected]

45 Journal of the American Academy of /Volume 17, Number 1, 2006

Palabras Clave: Potencial de acción, respuesta del tallo cerebral, potenciales evocados auditivos, clic de banda ancha, microfónica coclear, electrococleografía, extra-timpánico, enfermedad de Ménière/hydrops endolinfático, potencial de suma, burst tonal, trans-timpánico, membrana timpánica, electrodo para-timpánico Abreviaturas: ABR = respuesta auditiva del tallo cerebral; AC = corriente alterna; AP = potencial de acción; AEP = potencial evocado auditivo; BBC = clic de banda ancha, CM = microfónica coclear; ECochG = electrococleografía; ET = extra- timpánico; MD/ELH = enfermedad de Ménière/hydrops endolinfático; SP = potencial de suma; TM = membrana timpánica; TT = trans-timpánico

s the term implies,“Electrocochleography” in Figure 1, an “electrocochleogram” may (ECochG) is a technique for recording comprise the cochlear microphonic (CM), Athe electrical events of the . cochlear summating potential (SP), and AP, The clinical application of ECochG, however, recorded independently or in various is confined to the stimulus-related cochlear combinations. Although the tracings in this potentials and often includes measurement figure were recorded in response to broadband of the whole nerve or compound action clicks, tonal stimuli also are commonly used potential (AP) of the auditory nerve. As shown to evoke the components of interest. ECochG emerged as a clinical tool in the 1970s, even though attempts to record the CM from humans date back almost to the time of its discovery in the cat by Wever and Bray (1930) (e.g., Fromm et al, 1935; Andreev et al, 1939; Perlman and Case, 1941; Lempert et al, 1947; Lempert et al, 1950). The SP was described in animals in 1950 (Davis et al, 1950; von Bekesy,1950) but received little to no attention in humans until much later (e.g., Eggermont, 1976; Gibson et al, 1977; Gibson, 1978). The first recordings of human auditory nerve APs are credited to Ruben and his colleagues (1960), who performed their measurements on patients undergoing otologic surgery. Increased attention to all auditory evoked potentials (AEPs) began to occur in the early 1970s, following the discovery and clinical application of the auditory brainstem response (ABR). The development and Figure 1. Electrocochleograms evoked by broad- refinement of noninvasive recording band click stimuli. Top tracings show responses to rar- techniques also facilitated the clinical efaction (R) and condensation (C) polarity clicks. application of AEPs, including ECochG. Adding R and C responses (middle tracing) enhances The technical capability to record cochlear the Summating Potential (SP) and auditory nerve and auditory nerve potentials in humans has Action Potential (AP), which are not phase-locked to the stimulus. Subtracting R and C responses (bottom led to a variety of clinical applications for tracing) enhances the Cochlear Microphonic (CM) ECochG, chief among them being a tool in (from American Speech-Language-Hearing Associa- the diagnosis/assessment/ monitoring of tion, 1988, p. 9, based on data from Coats, 1981). Ménière’s disease/ endolymphatic hydrops

46 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

(MD/ELH) and the assessment/monitoring such features would render the CM an ideal of treatment strategies for these disorders. The tool for human clinical applications. In reality, material for this article has been organized to however, the utility of the CM in differential include brief descriptions of the salient diagnosis of versus auditory nerve features of the components of an disorders has yet to be established. Although electrocochleogram, and how ECochG is reductions in CM magnitude have been recorded, interpreted and used clinically, reported for various disorders such as especially with reference to the above MD/ELH (Gibson and Beagley, 1976), these application. Much of this information is features tend to reflect general rather than derived from recent chapters by the authors specific cochlear pathology. Furthermore, on ECochG (Ferraro, 2000; Ferraro and examination of the CM with confidence that Durrant, 2002), and the reader is referred to the recording represents the true potential these chapters for supplemental reading in remains challenging in the clinical setting. this area. Since the CM mimics the waveform of the evoking signal (just as the voltage output of ECOCHG COMPONENTS a microphone), it is difficult to separate from stimulus artifact. etailed descriptions of the CM, SP, and DAP are abundant in the hearing science SP literature and beyond the scope of this article. However, be assured that the practice of The SP is a complex response comprising performing ECochG should not be attempted several components. Like the CM, the SP is without a thorough and working knowledge stimulus related, generated by the hair cells of auditory . The following of the organ of Corti, and a reflection of the section summarizes the salient features of the displacement-time pattern of the cochlear CM, SP, and AP, especially as related to partition. However, whereas the CM mirrors clinical ECochG. the stimulus waveform (i.e., time history), the SP displays a rectified, direct current CM (DC) version of this pattern more representative of the stimulus envelope The CM is an alternating current (AC) (Dallos, 1973). The SP appears as a voltage that reflects the instantaneous unidirectional shift in the CM baseline, the displacement of the along polarity of which is dictated by an interactive some distance within the cochlea (Ferraro effect between stimulus parameters (i.e., and Durrant, 2002). This distance is defined frequency and intensity) and the location of by the effective site and method of the the recording electrode. When recorded from recording, and the conditions of the stimulus. the tympanic membrane (TM) or ear canal, As reflected by the CM, the organ of Corti acts the SP is often seen as a downward (negative) (in a limited way) as a microphone, but here deflection persisting for the duration of the the tranducers are numerous as each acoustic stimulus (see Figure 1). produces a receptor potential that is Because of its complexity, the role of the substantially AC (but not exclusively; see SP in hearing function remains unclear. As section on SP below). In animals, the CM is DC responses to AC stimuli, however, at least perhaps the most thoroughly investigated some of its components are thought to electrical potential of the inner ear, but it represent nonlinearities associated with the certainly remains to be fully understood. The transduction processes in the cochlea (Tasaki historical popularity of the CM in the et al, 1954; Whitfield and Ross, 1965; Davis, laboratory derives from its link to cochlear 1968; Engebretson and Eldridge, 1968; Dallos transduction, from well-demonstrated et al, 1972; Gulick et al, 1989; Ruth, 1994). sensitivity to the health of the cochlear Whether or not the SP actually reflected partition, and, certainly, because it can be intracellular receptor potentials was recorded from within or near the cochlea. uncertain for a period of time following its This latter factor is facilitated by the CM’s discovery. However, SP-like potentials have considerable magnitude compared to other since been observed inside hair cells, and it electrical phenomena associated with the is now clear and that the SP is not an auditory periphery. One would think that epiphenomenon (e.g., Dallos, 1973). It also

47 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006 has long been known that the SP is also highest in this region, phase shifts caused by sensitive to mechanical and electrical biasing cochlear mechanics are minimal. (Durrant and Dallos, 1972; Durrant and Gans, The AP, like the CM, is an AC voltage. 1977). The nonlinear nature of the SP has However, unlike either of the cochlear made it useful for monitoring certain clinical potentials whose waveforms reflect the conditions such as MD/ELH, which may displacement-time pattern of the cochlear augment nonlinearities in the transduction partition (i.e., the CM and SP), the AP process. This application will be discussed waveform is characterized by a series of brief, later. predominantly negative peaks representative of the distribution of underlying neural AP firings. At suprathreshold stimulus levels, the first and largest of these peaks is referred The AP recorded via ECochG represents to as N1. N1 is virtually the same component the summed response of numerous, at times as wave I of the ABR and, as such, arises from thousands of, auditory nerve fibers firing the distal portion of the auditory nerve synchronously.When evoked by click stimuli, (Moller and Janetta, 1983). AP peaks beyond the term “whole nerve AP” is applied since, N1 (such as N2 and N3) are analogous to theoretically, the click has a nearly flat corresponding ABR components (i.e., waves spectrum over the frequency range of interest II and III) but have received little if any and thus vibrates essentially the entire clinical attention in ECochG. basilar membrane. As recorded clinically, For clinical purposes, AP magnitude and however, and regardless of the stimulus, the latency appear to be the most useful features. AP is clearly a compound action potential— The former is a reflection of the number of -the response of a population of neurons nerve fibers firing. Since the afferent fibers rather than a single unit. A stimulus with a of the auditory nerve primarily innervate narrower bandwidth, such as a toneburst, the inner hair cells (Spoendlin, 1966), AP excites a more limited segment of the magnitude also can be viewed as a reflection membrane and, consequently, a more of inner hair cell output. AP latency , which restricted population of nerve fibers. Here, is analogous to the “absolute latency” for then, the term “whole-nerve” can be ABR components, represents the time misleading. More important is the fact that between stimulus onset and the peak of N1. these very different stimuli—clicks and This value incorporates stimulus travel time tonebursts—fail to achieve their respective from the output of the transducer to the inner objectives. That is, the spectrum of the click ear, traveling wave propagation time along that actually reaches the cochlea generally is the basilar membrane and time consumed far from flat, due to combined earphone, ear activating synaptic transmission between canal, and middle ear response hair cells and first order neurons. As with all characteristics. Likewise, the cochlear waves of the ABR, reductions in signal response to tonebursts is far from discrete, intensity at suprathreshold levels for the AP due to their spectra and limited cochlear are accompanied by absolute latency resolution (Durrant, 1986). Thus, clicks do not prolongations and reductions in N1 excite the “whole” nerve, and even tonebursts magnitude leading to eventual disappearance excite several points of vibration along the into the electrical noise floor. basilar membrane. Since its initial recording in humans in A high degree of synchrony of neural 1960, the AP has been the most widely firings is essential to producing a well-defined studied product of ECochG. Early interest AP,which accounts for the popularity of click in the AP, however, was directed toward the and brief/abrupt-onset tonebursts as evoking development of an electrophysiological index stimuli. In either case, however, the response of hearing status in children (Cullen et al., to moderately intense stimulation (i.e., 70 1972). This effort was overshadowed by the dB nHL or more) tends to be dominated by ABR for such purposes, primarily because neural contributions from the basal or high- wave V of the ABR appeared to be more frequency end of the cochlea (Kiang, 1965), sensitive and easier to measure than the AP- at least in normal ears and pathological ears N1. As AEP applications and technology have with no worse than moderate hearing loss. evolved over the years, the use of the AP to Since the velocity of the traveling wave is the assess and monitor cochlear and auditory

48 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant nerve function has received renewed ET recordings are performed with an attention, especially in surgical settings. In electrode resting against the skin of the ear addition, the use of a combined AP-ABR canal or surface of the TM. For the latter approach for assessing retrocochlear status site, the procedure may be referred to as in hard-of-hearing subjects is gaining “tympanic (or TM) ECochG” (Ferraro and popularity.Finally,an important application Ferguson, 1989), even though this approach of the AP that will be discussed in more detail is still considered to be ET. Pioneering work later in this paper involves the measurement in ET recordings was performed by Sohmer of its magnitude in comparison to that of the and Feinmesser (1967), Coats and Dickey SP in patients suspected of having MD/ELH. (1970), and Cullen et al (1972), among others. Although ET ECochG can be performed using ECOCHG RECORDING APPROACHES a needle electrode in the skin of the ear canal, this option is rarely chosen. Therefore, virtually all ET recordings are noninvasive Transtympanic versus Extratympanic and, by virtue of this feature, have been better ECochG accepted in the United States than TT techniques. Examples of currently popular ET The terms “transtympanic” (TT) and electrodes are shown in Figure 2. “extratympanic” (ET) refer to the two general Both TT and ET approaches to ECochG approaches for recording ECochG. TT ECochG have advantages and disadvantages. The is an invasive procedure that involves passing primary advantage of the TT approach is the a needle electrode through the TM to rest on close proximity of the recording electrode to the cochlear promontory.A ball electrode on the response generators, which produces the round window can also be used when the components of large magnitude with middle ear space is exposed during surgery. relatively little signal averaging. The major TT approaches to ECochG were introduced in limitations of TT ECochG relate to its the late 1960s (e.g., Yoshie et al, 1967; Aran invasiveness. Such procedures must be and LeBert, 1968) and are still used widely performed by or require the assistance of a in countries other than the United States. physician and are therefore limited to a medical setting. In addition, penetrating the TM with a needle is painful to the patient, even when local anesthetics are used. These disadvantages certainly have limited the use of TT ECochG in the United States. By comparison, ECochG responses recorded from ET sites require more signal averaging and tend to yield smaller component magnitudes than TT recordings. The biggest advantage of ET approaches, thus, is that they can be performed in nonmedical settings with minimal discomfort to the patient, obviating the need for sedation/local anesthesia—and a physician. Another factor that has facilitated the use of ET ECochG relates to advances in electrode design (discussed in following section) and the practice of using the TM as a recording site. The TM offers a good and practical compromise between ear canal and TT placements with respect to component Figure 2. Photographs of extratympanic ECochG magnitudes and, consequently, signal electrodes. Tymptrode (modified version of electrode averaging time (Ruth and Lambert, 1989; described by Stypulkoswski and Staller [1987]) (top Ferraro, Thedinger, et al, 1994; Ferraro, left), Lilly wick electrode (top right), and Bio-Logic ECochGtrode (middle) are placed at the surface of the Blackwell, et al, 1994; Schoonhoven et al, tympanic membrane. Gold-foil TIPtrode (bottom) 1995). Perhaps most importantly for clinical rests in the ear canal. From Ferraro (2000, p. 429). purposes, however, the waveform patterns

49 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006

that lead to the interpretation of the TT if you were the patient? electrocochleogram tend to be preserved in TM recordings (Ferraro, Thedinger, et al, ECOCHG RECORDING PARAMETERS 1994). When performed correctly,TM ECochG should cause minimal-to-no discomfort to the election of recording parameters for patient. However, the technique of placing an SECochG varies according to the electrode on the highly sensitive TM can components of interest. Since these sometimes result in more patient discomfort components generally occur within a latency than is customary for other, noninvasive ET epoch of 5 msec following stimulus onset, approaches (but certainly not as much as is they can be considered to be in the family of usually associated with TT ECochG). “early-latency” or “short-latency” AEPs (Picton Given the advantages and disadvantages et al, 1974). As members of the same family, of both approaches, the decision to perform ECochG components and the ABR can be ET or TT ECochG often depends on the recorded using similar parameters. A notable traditional practices, personnel, and attitudes exception occurs in the selection of the of the clinic. Obviously, TT recordings are bandpass of the preamplifier for ECochG dependent on the availability of a physician when the SP is of interest. That is, the filter who has the time and interest to perform setting must be wide enough to accommodate the examination. While a physician is not both a quasi-steady-state DC component (the needed for ET ECochG, placing an electrode SP) and an AC component with a on the TM is certainly a more delicate fundamental frequency of approximately 1 maneuver than attaching surface electrodes kHz (the AP). Other differences between to the scalp or resting them in the ear canal. ECochG and ABR recording parameters With proper instruction and materials, involve the electrode array and the number however, this procedure is relatively easy to of samples to be averaged. For ECochG, the learn and well within the scope of professional latter is dependent on the choice of recording practice for audiologists (American Speech- approaches, with TT requiring considerably Language-Hearing Association, 1990). fewer repetitions than ET.Table 1 illustrates Unfortunately,one factor that is virtually suitable ET (TM) protocol for recording the overlooked in the decision to perform TT or SP and AP together, which often is done when ET ECochG is the attitude/preference of the ECochG is used in the diagnosis of MD/ELH. patient. Given the choice with an A description of these parameters is provided understanding of the benefits and limitations below. of each approach, which one would you choose

Table 1. Extratympanic (Tympanic) ECochG Recording Protocol Electrode Array

Primary (+) Tympanic Membrane Secondary (-) Contralateral Mastoid or Earlobe Common Nasion Recording Parameters

Timebase 10 milliseconds Amplification 50,000 X Analog Filter Bandpass 5 Hz--3000 Hz Repetitions 750--1000 Stimuli

Type Broadband Clicks (BBC), Tonebursts (TB) Duration of Electrical Pulse (BBC) 100 microseconds Frequency (TB) 1000 Hz, 2000 Hz Envelope (TB) 2 millisecond linear rise/fall, 10 millisecond plateau Polarity Rarefaction, Condensation (BBC); Alternating (TB) Repetition Rate 11.3/second Beginning Level 80 dB nHL

50 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

Electrode Array converter also must be taken into account. Thus, amplification/sensitivity settings may If your preference is an electrode array vary from laboratory to laboratory and also that displays the AP as a downward among evoked potential units from different (negative) deflection. The primary electrode manufacturers. However, the manipulation of (i.e., the electrode connected to the these variables to provide settings +/noninverting input of the differential appropriate to recording conditions generally preamplifier) should rest on the TM. Sites for is easily accomplished. The goal here is to the secondary (-/inverting) electrode include amplify enough to extract a good (and real) the vertex of the scalp, high forehead, response without triggering the artifact contralateral earlobe, or mastoid process. We rejection routine inordinately throughout the prefer the earlobe or mastoid for the location recording. of the secondary (-) electrode simply because electrodes tend to be easier to attach and Analog Filter Settings secure to these sites. The nasion, ipsilateral earlobe, or ipsilateral mastoid may serve as Adaptation notwithstanding, the SP, as sites for the electrode connected to the fundamentally a DC potential, could last as “common” or “ground” input to the long as the stimulus of any duration. Ideally, preamplifier. If you prefer the AP to be then, a DC recording amplifier is needed to displayed as an upward deflection (such as in record this component. However, particularly the way conventional ABR components are for the amount of gain needed, such amplifiers displayed), simply reverse the + and - inputs are notoriously unstable for to the preamplifier. electrophysiological recordings. Fortunately, the SP, as evoked for practical/clinical Timebase purposes, is only quasi-steady-state, permitting the use of the AC-coupled As indicated above, ECochG components amplifiers typically found in commercially generally occur within the first few manufactured AEP units. Indeed, the click milliseconds after stimulus onset. For brief evokes a rather brief transient DC component transient stimuli (such as clicks), we use a that is readily recorded with low-pass cutoffs timebase (or signal averaging window) of 10 in the vicinity of 5–100 Hz, depending upon msec, which also allows for visualization of filter characteristics. Such recordings (i.e., ABR components that follow N1. For longer using familiar ABR settings) can be duration stimuli (such as tonebursts), the accomplished without significant distortion timebase should extend beyond the duration of the SP-AP complex for purposes of of the stimulus envelope so that the entire measuring the SP/AP magnitude ratio response is observable within the averaging (Durrant and Ferraro, 1991). However, when window (recalling that both the SP and CM recording the SP to tonebursts, this approach persist for the duration of the stimulus). creates a DC-step-like waveform, and, even if only quasi-steady-state, the waveform is Amplification Factor likely to be significantly distorted unless the low-frequency cutoff of the amplifier is low Amplification factor is selected to (generally 10 Hz or below, depending on maximize the signal-to-noise ratio for a given duration of the sound and the filter recording condition. The amount needed for characteristics). suitable recordings of the SP and/or AP for The low-pass (or high-frequency cutoff) ET measurements generally ranges between setting of the filter should be set to allow 20,000 and 100,000X, whereas the factor for transmission of the AC components of TT recordings can be much lower (by 5 to 10 interest. In the case of the AP-N1, 3000 Hz times). In part, selection of this parameter is is a suitable setting as the fundamental based on the level of the electrical noise floor, frequency of this component is approximately which comprises several elements (i.e., 1000 Hz. Filter settings for CM recordings myogenic and electroencephalographic would depend on the frequencies of the activity,electrical artifact from the equipment evoking stimuli (and thus the resultant and/or testing environment). The sensitivity responses). setting of the computer’s analog-to-digital

51 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006

Repetitions more attention later. Although the click continues to remain The number of individual responses popular, toneburst stimuli also have been needed to extract a well-defined used in several ECochG studies involving electrocochleogram from the background MD/ELH populations (e.g., Levine et al, 1992; noise generally varies with recording Orchik et al, 1993; Ferraro, Blackwell, et al, conditions, and also the subject’s degree of 1994; Ferraro, Thedinger, et al, 1994; Koyuncu hearing loss. The former depends on the et al, 1994; Margolis et al, 1995). Tone bursts recording approach. That is, TT recordings provide a higher degree of response require considerably fewer repetitions than frequency-specificity than clicks (depending ET approaches. More repetitions may be on stimulus envelope and duration), which necessary for subjects with hearing loss than can be useful for monitoring cochlear status normally hearing subjects, especially if the in progressive disorders where hearing may loss is in the 1–4 kHz range. In our not be affected at all frequencies. In addition, experience, when sensorineural hearing loss the use of longer stimuli allows for better in these frequencies exceeds 50–60 dB HL, the visualization of the SP and CM (Durrant and use of ET ECochG in MD/ELH populations Ferraro, 1991). is questionable. The basis for this statement A lack of standardization regarding is that losses of this magnitude reduce the stimulus parameters presents a problem output of the population of hair cells when using tonebursts to record ECochG contributing to the responses of interest and components and other AEPs. Most studies render them too small for reliable ET employ signals of only one or two frequencies; recordings. On the other hand, when hearing stimulus envelopes are different, and there loss precludes the identification of wave I in is no standardized approach to defining the presence of wave V in the conventionally stimulus intensity. These inconsistencies recorded ABR, ECochG can be very useful make it difficult to compare data from (Ferraro and Ferguson, 1989). different studies/clinics. For tone bursts, we use an envelope with a linear rise-fall time Stimuli of 1–2 msec and a plateau of 10 msec or longer. Shorter plateaus (e.g., 5 msec) can As mentioned earlier, the broadband click sometimes be used to inhibit (but generally (BBC) is a popular stimulus for short-latency not eliminate) interference by ABR AEPs because it excites synchronous components (Levine et al, 1992). discharges from a large population of neurons Stimulus polarity depends on the initial to produce well-defined peaks in the response. deflection of the transducer diaphragm and In addition, 100 msec is a popular choice for is an important factor for ECochG. Presenting the duration of the electrical pulse driving the clicks or tonebursts in alternating polarity transducer because the first spectral null for inhibits the presence of stimulus artifact and a click of this duration occurs at 10,000 Hz CM, as their phases are locked to the signal. (i.e., 1/100 msec). In reality, the frequency Stimulus artifact can sometimes be large range of the transducer is usually lower than enough to obscure early ECochG components, 10,000 Hz and the acoustic signal receives and CM generally overshadows both the SP additional filtering by the outer and middle and AP features that are problematic when ears. Thus, the spectrum of the stimulus these latter two components potentials are the reaching the cochlea is far from flat, and components of interest. Alternating stimulus considerably narrower than 10,000 Hz. polarity can be applied to help overcome this Since the duration of both the CM and SP problem. However, recording separate are stimulus dependent, the brevity of the responses to condensation and rarefaction click makes it a less-than-ideal stimulus for clicks then adding them together off-line may studying either of these potentials. Despite be a more preferable solution, since certain this limitation, the use of clicks has proven subjects with MD/ELH display abnormal effective in evoking the SP-AP complex for latency differences between AP-N1 latencies ECochG applications related to MD/ELH, to condensation versus rarefaction clicks even though the duration of the SP is (Margolis and Lilly,1989; Levine et al, 1992; abbreviated under these conditions (Durrant Margolis et al, 1992; Margolis et al, 1995; and Ferraro, 1991). This feature will receive Orchik et al, 1997; Sass et al, 1997).

52 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

As with the majority of signal-averaged electrophysiological response from the nontest AEPs, it is important for ECochG that the ear is very small. In addition, ECochG cochlear/neural responses to one stimulus be components are generated prior to crossover complete before the next stimulus is of the auditory pathway.Finally,the potential introduced. This requirement allows for for crossover stimulation can be further considerable latitude in the selection of minimized by the use of tubal insert stimulus repetition rate for click-evoked AEPs. earphones. For ECochG, however, increasing this rate A final note regarding stimuli relates to beyond 10–30/second may cause unacceptable stimulus artifact, which can be quite large for adaptation of the AP (Suzuki and Yamane, ECochG. The nature of ET (especially TM) 1982). Click repetition rates on the order of electrodes is that they tend to have high 100/second cause extensive (nearly total) impedance and are vulnerable to radiation adaptation of the AP while leaving the SP from the transducer and other electrical relatively unaffected (Gibson et al, 1977; sources in the environment. The following Coats, 1981). Unfortunately, the use of such factors can help to inhibit such artifact: using fast rates has not proven to be very successful a tubal insert transducer; separating the in the clinic, in part because the AP transducer from the electrode cables as much contribution is not completely eliminated and as possible; braiding the electrode cables; the SP may also be reduced under extreme testing subjects in a shielded sound booth conditions (e.g., click rates greater than 90/sec) with the examiner and AEP unit located (Harris and Dallos, 1979; Durrant, 1986). In outside of the booth; plugging the AEP unit addition, rapid clicks presented at loud levels into an isolated socket equipped with a true- tend to be very annoying for patients. earth ground; using a grounded cable for the When ECochG is performed to help primary electrode (such cables are diagnose MD/ELH, the stimulus should be commercially available); turning off the lights intense enough to evoke a well-defined SP- in the testing room and unplugging AP complex. Thus, stimulus presentation unnecessary electronic equipment (it also typically begins at a level near the maximum may be necessary to turn off the lights in output of the stimulus generator. the examiner room); encasing the transducer Unfortunately,as mentioned earlier, the lack in grounded Mu metal shielding. of standardization for AEP stimuli regarding signal calibration and dB reference is true for PREPARING FOR AN EXAMINATION both tonebursts and BBCs. Common references include dB hearing level (HL, or hearing threshold level [HTL]), dB normal Recording Approach hearing level (nHL), dB sensation level (SL), and dB peak equivalent sound pressure level Virtually all ECochG recordings (pe SPL). Since the latter one is determined performed in the authors’ clinics/laboratories by matching the SPL of a transient signal to are ET and made from the TM because of the that of a continuous sinusoid, it represents the advantages this site offers over other locations only physical measure of intensity of the along the ear canal (i.e., increased component three common references. It may be necessary magnitudes, more stable/repeatable to calibrate ECochG signals in both nHL and responses, and reduced testing time because pe SPL. As with conventional audiometry, less signal averaging is needed) nHL values are referenced against normal (Stypulkowski and Staller, 1987; Ruth et al., subjects. For dB pe SPL, an oscilloscope is 1988; Ruth and Lambert, 1989; Ferraro and used to match the level of the click to that of Ferguson, 1989; Ruth, 1990; Arsenault and a continuous sinusoid (e.g., a 1000 Hz signal). Benitez, 1991). Given our preference for TM Consistent with the findings of Stapells et al ECochG, the following information (1982), 0 dB nHL for clicks corresponds to emphasizes this particular approach. approximately 30 dB pe SPL. The use of high stimulus levels raises the Subject/Patient Considerations question of the need for masking to assure unilateral stimulation of the intended ear. Most patients are unfamiliar with This concern is irrelevant for ECochG, ECochG and therefore confused as to what it however, since the magnitude of any is, why they need it, how it will be performed,

53 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006 and whether or not it will be painful. For the As with most audiometric examinations, lay person (i.e., most patients) the lengthy both ears should be tested, even if unilateral term “electrocochleography” adds to this disease is suspected. Comparison between confusion. Instructions to the patient can affected and unaffected sides in particular can begin on the way to the testing room with an provide important diagnostic information. assurance that the examination is We always test the affected side first in case noninvasive and painless, that the test will the patient becomes restless as the take approximately one hour, and they can examination progresses. sleep through it if they wish. The patient also is informed as to why their physician has Construction and Placement of the requested this examination (e.g., to help TM Electrode (Tymptrode) determine if there is too much fluid in the inner ear). Engaging patients in conversation The photograph of ET electrodes in at this point and watching them walk also Figure 2 includes the tymptrode (originally provides some insight regarding the status of described by Stypulkowski and Staller, 1987, their hearing and balance, although the and modified by Ferraro and Ferguson, 1989), results of other auditory and vestibular the Lilly wick electrode (Lilly and Black, testing should be available in their files. Once 1989), the TM-ECochGtrode manufactured by in the sound booth, the patient is placed in Bio-Logic, and the gold-foil TIPtrode, which a supine position on an examining bed or has long been available for ear canal semireclined in an examination chair or recordings. The latter three electrodes are recliner. Good and comfortable head and neck commercially available. The tymptrode can be support is particularly important. Eyeglasses fabricated using the “store bought” materials and/or earrings are removed (usually by the listed below (see Durrant, 1990; Ferraro, patient), and food/chewing gum/candy/etc. 1992; and Ferraro, 1997): must be swallowed or discarded. When the • medical grade silicon (SilasticTM) patient is comfortable and attentive, he or she tubing (0.058” inner diameter, 0.077” is informed that devices called electrodes outer diameter; will be attached to the scalp, a small, sponge- • TeflonTM-insulated silver wire or cotton-tipped electrode will be inserted (0.008” bare diameter, 0.011” along the ear canal to rest on the TM, and an insulated diameter); earplug will be used to hold the electrode in • a wad of cotton; place and deliver click and beeping-type • electrode gel (not paste or cream); sounds to the ear. The patient should be • fine, needle-nosed forceps; alerted that the TM electrode might feel • 1 cc disposable tuberculin syringe strange and maybe a little uncomfortable, with needle; but that it should not be particularly painful. • copper microalligator clip soldered to If pain should occur, repositioning the the end of an electrode cable. electrode usually helps. In very rare instances Briefly, the procedure for constructing (i.e., less than 0.5% in the first author’s the tymptrode involves cutting the wire and experience), the exam may have to be tubing into segments a few centimeters longer terminated, or an ear canal electrode used than the ear canal, threading the wire instead of the tymptrode. The procedures for through the tubing, scraping the Teflon preparing the skin and placing the surface insulation off of both ends of the wire, hooking electrodes are identical to those used for one of the bared ends into the cotton wad, and conventional ABR examinations. Prior to stuffing the hooked portion of the cotton back inserting the tymptrode, otoscopy is into the tubing with fine forceps. A small performed to assess the patency of the ear portion of the cotton extends beyond the canal and normalcy of the TM. Cerumen tubing to serve as the electrode tip. Figure 3 removal may be necessary to visualize the TM is a drawing of the tymptrode constructed as and clear a pathway along the ear canal large described above. Tymptrodes, at this stage, enough for the electrode. If either the ear can be made and stockpiled for indefinite canal or TM appear abnormal or damaged, periods of time. Immediately prior to use, ECochG is not advisable in general, and the cotton tip of the tymptrode is impregnated certainly not without consulting the patient’s with electrode gel using the tuberculin physician. syringe. We attach the microalligator clip of

54 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

electrophysiological monitoring. It also helps to ask the patient when they feel that the electrode is touching the TM. Even with an otoscope, it is difficult to actually see the point of contact between the tymptrode tip and TM in most cases. However, monitoring the electrophysiological noise floor during electrode placement helps to achieve proper contact. The noise floor, peak-clipping, and cyclic activity associated with an “open-line” condition drop dramatically,and the baseline EEG becomes more stable when the TM is contacted. Repositioning and sometimes reinsertion of the tymptrode may be necessary to achieve proper contact. However, using both visual and electrophysiological monitoring provides the best opportunity for Figure 3. Components of the “tymptrode” electrode success on the “first try.” used for surface recordings from the tympanic mem- brane. Once the tymptrode is in place, the foam tip of the sound delivery tube is compressed and inserted into the ear canal alongside the electrode tubing. Care must be taken to not push the electrode further against the TM the electrode cable to the other, bared end of when inserting the earplug. Although the the wire, before inserting the tymptrode. materials that comprise the tymptrode are With the test ear is facing up, the relatively soft and flexible (which allows the tymptrode is inserted into the entrance of tip to compress or bend at the TM rather the ear canal and gently advanced (by hand than penetrate the membrane), such a or using the fine forceps) until the tip touches condition usually causes discomfort to the the TM. Contact is confirmed via otoscopy and patient. Only a portion of the transducer earplug needs to be inserted into the canal to hold the tymptrode in place and deliver the signal for ECochG applications. Figure 4 is a schematic representation of the tymptrode and sound delivery tube in place. Even with the most delicate contact, the TM does react somewhat in most cases by displaying a slight blushing spot at the point of contact with the tymptrode. In hundreds of subjects and patients examined by the authors, this condition has never proven to be an untoward reaction, clears up within minutes or hours, and may even be a useful indicator of exactly where the electrode was situated.

INTERPRETATION OF THE ELECTROCOCHLEOGRAM

s with most AEPs, component magnitude Aand temporal features form the bases for interpreting the electrocochleogram. Figure 5 depicts normal TM recordings to alternating polarity clicks (which enhances the SP and AP at the expense of the CM). Figure 4. Schematic illustration of the tymptrode in Component magnitudes can be measured as place. Modified from Ferraro (1992, p. 28). absolute values (defined by single points)

55 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006

Figure 5. ECochG recordings from the tympanic membrane to clicks presented in alternating polarity at 80 dB nHL. The magnitudes of the Summating Potential (SP) and Action Potential (AP) can be measured from peak- to-trough (left panel), or with reference to a baseline value (right panel). Magnitude/time scale is 1.25 micro- volts/1 millisecond per gradation. Insert phone delay is 0.90 milliseconds. From Ferraro (2000, p. 435).

(left panel) or using a baseline reference may favor one approach over the other, but (right panel). The authors are split on which it probably is the best idea, above all else, to of these two approaches is best, showing that try to be as consistent as possible across even authorities of similar background and measures in the normative sample and generally similar views can still have differing clinical patients. Here, for simplicity, the opinions on how to interpret an single-point approach is adopted, in which electrocochleogram. In this instance, rights case, the normal SP measured from the TM and wrongs are difficult to define, particularly in response to 80 dB nHL clicks may be under the electrically “noisy” circumstances expected to range from 0.1–1.0 microvolts, of minimally/non-invasive recording with a mean of 0.4 microvolts. AP magnitudes conditions in awake patients. The first author can be as large as 5.0 microvolts, although our finds the single-point calculations to be the mean value is approximately 2.0 microvolts. more useful and potentially reliable as it AP-N1 latency is measured from stimulus minimizes the judgmental factor of defining onset to the peak of N1 and, as mentioned an unstable or electrically skewed baseline earlier in this manuscript, should be identical common to ET recordings in general. to the absolute latency of ABR wave I. At 80 Theoretically, this approach is subject to no dB nHL, normal N1 latencies generally range more or no less noise than single points from 1.3–1.7 msec with a mean of chosen to represent the SP and AP approximately 1.5 msec. Since a tubal insert magnitudes. However, the second author earphone was used to deliver the stimulus, prefers using a value representing the the above latency values have been corrected average through a millisecond or two of for the 0.9 msec delay attributable to the baseline before the response. At least for one sound tube. Although labeled in Figure 5, of the measurements, the noise can be N2 has received little interest for ECochG reduced (the average being inherently a applications. “variance reducer”). This method is equally Also as shown in Figure 5, we measure useful in determining the SP magnitude for SP and AP magnitudes from the leading edge tonebursts, for the same reason in both of both components. The resultant values are cases—minimizing bias by some noise peak. then used to derive the SP/AP magnitude In the final analysis, individual circumstances ratio, which is a key measure when ECochG

56 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

Figure 6. ECochG recording from the tympanic membrane to a 2,000 Hz toneburst (alternating polarity, 80 dB nHL, 2 msec rise/fall, 10 msec plateau). Action Potential (AP) and its first negative peak (N1) are seen at the onset of the response. Summating Potential (SP) persists as long as the stimulus. SP magnitude is meas- ured at midpoint of response (point B), with reference to a baseline value (point A). From Ferraro, Blackwell, et al. (1994, p. 19). is used to help diagnose and monitor promontory responses (note magnitude MD/ELH. This value tends to occur within a scales), the corresponding patterns of the TM relatively small range (i.e., 0.1–0.5), especially and TT recordings at each frequency are in comparison to the individual magnitudes virtually identical (as indicated earlier in of both the SP and AP (Ferraro and Krishnan, this manuscript). 1997). Although clicks and tonebursts are the Figure 6 depicts a normal waveform stimuli of choice for ECochG, it is important evoked by an 80 dB nHL, 2000 Hz toneburst to note that comparisons among studies from (2 msec rise/fall, 10 msec plateau, alternating different laboratories/clinics remain difficult polarity). Recall that for tonebursts the SP at best. This problem persists because of a persists as long as the stimulus and therefore lack of consistency and standardization is not seen as a small shoulder preceding the regarding such aspects as choice of recording AP (which is still seen near the onset of the approach, recording and stimulus parameters, response). To minimize the influence of the stimulus calibration, and measurement AP, SP magnitude is measured at the preferences. All of these conditions continue midpoint of the waveform with reference to to necessitate the establishment of laboratory- baseline magnitude. The polarity of the SP /clinic-specific norms for ECochG. depends on whether this voltage is above (positive SP) or below (negative SP) the ECOCHG’S ROLE IN THE baseline voltage. Figure 7 illustrates EVALUATION OF MD/ELH toneburst SPs at several frequencies recorded from both the TM and promontory (TT) of the lthough much has been learned about same normally hearing subject. Three AMD (or idiopathic ELH) since its initial important features should be noted from description in the literature over 140 years these tracings: (1) The polarities of the SPs ago (Ménière, 1861), the true pathophysiology may vary slightly across frequencies. (2) of this disorder(s) continues to be elusive. As Despite these slight variations, the a result, neither a cure nor an effective magnitudes of toneburst-SPs in normal ears treatment strategy that works for all patients are very small, which renders the actual has been developed. The symptoms upon polarity of the SP in this population which diagnosis of MD/ELH is based include somewhat inconsequential. (3) Although the recurrent, spontaneous vertigo, hearing loss, magnitudes of the TM responses are aural fullness, and tinnitus (American approximately one-quarter that of the Academy of Otolaryngology—Head and Neck

57 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006

Figure 7. Transtympanic (TT) and Tympanic Membrane (TM) electrocochleograms evoked by tonebursts of dif- ferent frequencies presented at 80 dB nHL (2 msec rise fall, 10 msec plateau). Stimulus frequency in kHz indi- cated at the right of each waveform. Despite differences in magnitudes (see magnitude scale), TT and TM response patterns are virtually identical. From Ferraro, Blackwell, et al, (1994, p. 20).

Surgery Committee on Hearing and mechanical (Gibson et al, 1977) and/or Equilibrium, 1995). However, the presence electrical (Durrant and Dallos, 1972, 1974; and severity of these symptoms tend to vary Durrant and Gans, 1977) has not been over time both among and within patients. resolved, and other factors such as The capricious nature of this disorder makes biochemical and/or vascular changes may it difficult to diagnose and evaluate with a also be responsible (Eggermont, 1976; Goin high degree of specificity and/or sensitivity. et al; 1982; Staller, 1986). Regardless of the As mentioned throughout this paper, specific pathophysiology,measurement of the ECochG has emerged as one of the more SP to help diagnose, assess, and monitor powerful tools in the diagnosis, assessment, MD/ELH has emerged as a primary, and and monitoring of MD/ELH, primarily probably the most popular, application for through the measurement of the SP and AP. ECochG. In particular, it is now well documented that Although it is the enlargement of the SP the electrocochleograms of patients with magnitude that often characterizes the MD/ELH often display abnormally enlarged electrocochleograms of patients with SP magnitudes (e.g., Schmidt et al, 1974; MD/ELH, the consistency of this finding when Gibson et al, 1977; Gibson, 1978; Moriuchi and using click stimuli improves when this value Kumagami, 1979; Morrison et al, 1980; Coats, is compared to the magnitude of AP-N1 to 1981, 1986; Kitahara et al, 1981; Goin et al., form the SP/AP magnitude ratio (Eggermont, 1982; Kumagami et al, 1982; Ferraro et al, 1976; Coats, 1981; Coats, 1986). An enlarged 1983; Ferraro et al, 1985; Staller, 1986; SP/AP magnitude ratio to click stimuli, Dauman et al, 1988; Ruth et al, 1988; Ferraro therefore, would be considered a positive and Krishnan, 1997). The conventional finding for ELH. This feature is illustrated in rationale for this finding is that an increase Fig. 8, which displays the click-evoked in endolymph volume creates mechanical electrocochleogram of a patient with MD/ELH biasing of vibration of the organ of Corti to on the left side. As can be seen from these which, again, the SP is sensitive. Whether the tracings, the left SP/AP magnitude ratio nature of this increased distortion is (when measured using the “single point”

58 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

Figure 8. ECochG tracings to broadband clicks (alternating polarity,80 dB nHL) from a patient with endolym- phatic hydrops. Affected side (left) shows a magnitude-enlarged summating potential (SP), and SP/action potential (AP) magnitude ratio. SP-AP relationship on the unaffected side (right) is within normal limits.

method), is approximately 21/2 times larger in the general Ménière’s population is only than the normal right ratio. Figure 9 displays approximately 55%–65% and has been normal and abnormal toneburst-evoked reported to be as low as 20% (Gibson et al, electrocochleograms (2000 Hz, 2 msec r/f, 10 1977; Coats, 1981; Kitahara et al, 1981; msec plateau) from another MD/ELH patient. Kumagami et al, 1982; Margolis et al, 1995; For these measurements, SP magnitude Pou et al, 1996; Ferraro and Tibbils, 1999). represents the difference between baseline and These statistics demand a continuing search midpoint voltages (recalling that the SP persists for ways to make ECochG more sensitive, for the duration of the stimulus).The left panel particularly for patients whose symptoms are displays an enlarged, negative SP from the not “classic” and for whom the clinical profile affected left ear, whereas the right response is is unclear (Campbell et al, 1992). barely measurable and well within normal The episodic nature of MD/ELH certainly limits. It also should be noted for toneburst plays a role in the sensitivity of any diagnostic responses that the measurement of interest is tool used for this disorder. In addition, the magnitude of the SP trough rather than the MD/ELH is characterized by various SP/AP magnitude ratio. Indeed, it often is the stages during its evolution within a given case that the AP to tonebursts may not even be patient, which manifest differently visible in the face of an abnormally enlarged SP. electrophysiologically (Aran et al, 1984; Although the specificity of ECochG in Horner and Cazals, 1988). Thus, one might the diagnosis of MD/ELH has been reported expect the sensitivity of ECochG to vary to be higher than 90% (Ferraro et al, 1983; Pou according to when the test was administered et al, 1996; Murphy et al, 1997), the incidence in the course of the disease. In support of of an enlarged SP and SP/AP magnitude ratio this notion, Ferraro et al (1985) found positive

59 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006

Figure 9. ECochG tracings to a 2,000 Hz toneburst (alternating polarity, 80 dB nHL, 2 msec rise/fall, 10 msec plateau) from another patient with endolymphatic hydrops. Affected side (left panel) displays an enlarged SP trough, while SP magnitude on unaffected side (right panel) is very small and within normal limits. AP-N1 com- ponent is seen at the onset of the response to toneburst stimuli. electrocochleograms in over 90% of patients asymptomatic and then retest them when who had active symptoms at the time of symptoms are present. Comparing testing that included aural fullness and electrocochleograms under these conditions hearing loss. Pou et al (1996) observed often reveals differences that are changes in the SP-AP relationship as a diagnostically significant. function of degree of hearing loss. Such loss Additional evidence for the close may be initially episodic but also tends to relationship between ECochG and the acute progress with duration of disease. Given these status of the inner ear can be seen in cases associations, one way to make ECochG more involving intraoperative ECochG monitoring sensitive is to test patients when they are in patients undergoing endolymphatic experiencing symptoms. Unfortunately, the decompression/shunt surgery for treatment practicality of this idea is questionable given of MD/ELH. Although still controversial, the fluctuating nature of the disorder decompression or shunting of the (especially in its early stages), the general endolymphatic sac is an option for patients operating hours of most clinics, and the who fail nonsurgical treatments. During such inability and/or unwillingness of patients to surgeries, instantaneous measurements of complete an examination during an “attack.” the mechanoelectrical processes of the inner Nonetheless, testing patients during or as ear can be achieved via ECochG (Gibson et soon as possible after an episode will al, 1988; Gibson and Arenberg, 1991; Arenberg significantly improve the chances of obtaining et al, 1993; Wazen, 1994; Mishler et al, 1994). a positive electrocochleogram if indeed the Figure 10 exemplifies intraoperative changes patient has MD/ELH. We also have found it in the electrocochleogram induced by probing helpful, especially in the early stages of the for the endolymphatic duct in a patient with disorder, to test patients when they are MD/ELH. The uppermost tracings display

60 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

an enlarged SP and SP/AP magnitude ratio. difference between responses to condensation However, the SP becomes smaller and versus rarefaction clicks (as described earlier remains that way after a metal probe is in this chapter). Figure 12 illustrates this passed into (and therefore decompresses) the procedure. The AP-N1 latency difference (LD) duct (bottom three tracings). Probing of between clicks of opposite polarity for this surrounding tissue did not alter the MD/ELH patient was 0.75 msec, which was electrocochleogram. Figure 11 displays considerably above the upper limit 0.38 msec selected tracings measured from another seen in normal ears. The basis for comparing patient undergoing endolymphatic sac AP-N1 latencies to clicks of opposite polarity decompression surgery.A noticeable reduction relates to changes in the velocity of the in the SP/AP magnitude ratio to click stimuli, traveling wave in an endolymph-loaded and the SP magnitude to tonebursts were cochlea. That is, the vibratory cycle of the observed when the sac was decompressed. cochlear partition under such conditions may Although not always the case, this particular be abnormally restricted (or enhanced) in patient reported an improvement in one direction over the other. If this condition symptoms following surgery. occurs, the velocity of the traveling wave (on which the AP-N1 latency is dependent) will Beyond the SP/AP Magnitude Ratio differ if the initial movement of the cochlear partition is upwards (as with rarefaction Other approaches to increasing the clicks) versus downwards (as with sensitivity of ECochG have been directed condensation clicks). toward the parameters associated with Another interesting feature in Figure 12 recording and interpreting the is that the AP-N1 latency difference is obscured electrocochleogram, and looking beyond when responses to rarefaction and condensation comparatively simple measures of SP clicks are combined (lowest tracing). This magnitude. An example of such a method approach is analogous to presenting clicks in involves measuring the AP-N1 latency alternating polarity. What appears instead is

Figure 10. ECochG recordings measured at various events during endolymphatic sac decompression surgery. Note the reduction in SP magnitude in the “Probe passed into duct” tracing, which illustrates the relationship between the electrocochleogram and the acute status of the endolymphatic system. This feature is used to help to differentiate the location of the endolymphatic duct from surrounding tissue during surgery. From Gibson and Arenberg (1991, p. 300).

61 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006

Figure 11. ECochG tracings recorded during endolymphatic shunt decompression surgery: baseline tracing (1), drilling on mastoid (2), probing for endolymphatic duct (3), inserting prosthesis (4), closing (5). Tracing 5 shows a reduction in the summating potential (SP)/action potential (AP) magnitude ratio compared to tracing 1. Trac- ings 1–5 are in response to clicks, whereas tracings 6–7 were recorded to tonebursts at the onset of surgery and display an enlarged SP magnitude. From Ferraro (2000, p. 446).

an abnormally widened SP-AP complex. It is left panel are from a normal subject, whereas interesting to note that Morrison et al (1980) the right tracings are from an MD/ELH reported a widening of the SP-AP duration in patient. The shaded portions of the top Ménière’s patients over 20 years ago. This tracings in both panels represent the area of finding was attributed to an “after-ringing” of SP,which was defined by the onset of the SP the CM caused by endolymphatic hydrops. In (baseline) and that point in the tracing where light of recent studies, it may be more likely that the waveform returned to the baseline differences in AP-N1 latency to condensation magnitude. Despite its label, this versus rarefaction clicks accounted for the measurement also includes the areas of widened SP-AP complex observed by Morrison components other than the SP (such as the et al (who used click stimuli presented in AP-N1, and often AP-N2). The shaded alternating polarity). portions of the lower tracings represent the Even though the underlying mechanisms AP-N1 area. The results from this study may be unclear, the above studies suggest that revealed that virtually all MD/ELH patients the width (i.e., duration) of the SP-AP complex with enlarged SP/AP magnitude ratios also may be important to consider in the have enlarged SP/AP area ratios. However, interpretation of the electrocochleogram. enlarged area ratios also were seen in several Ferraro and Tibbils (1999) explored this patients suspected of having MD/ELH but notion by combining both magnitude and whose SP/AP magnitude ratios were within duration features of the response to measure normal limits. Subsequent research in our the “areas” of the SP and AP. Area laboratory using data from 138 patients with measurements were accomplished using a MD/ELH has shown that measurement of special software routine that allowed us to the SP/AP area ratio significantly improves measure the “area under the curve” defined the diagnostic sensitivity of ECochG in by a straight line connecting two cursor comparison to the SP/AP magnitude ratio points. Figure 13 displays representative (Devaiah et al, 2003). tracings from this study.The waveforms in the Given the above findings, we routinely

62 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

Figure 12. ECochG tracings to broadband clicks presented in opposing polarity from a patient with Meniere’s disease. Top tracing evoked with condensation-polarity clicks; middle tracing evoked with rarefaction-polarity clicks. The latency difference of 0.75 milliseconds between AP-N1 components to condensation versus rarefac- tion clicks is a positive finding for endolymphatic hydrops since it is greater than 0.38 milliseconds. This fea- ture is obscured if the condensation and rarefaction tracings are combined to derive the response to alternat- ing clicks (bottom tracing). From Margolis et al (1995, p. 52).

Figure 13. Measurement of the areas of the summating potential (SP) and action potential (AP) to click stim- uli to derive the SP/AP area ratio. Area values are obtained using a software routine that allows for measure- ment of the “area under a curve” defined by a straight line that connects two cursor points. Shaded portions represent these areas. Tracings in the top and bottom left panels are from the affected side of a subject with endolymphatic hydrops and display an enlarged SP/AP area ratio. Normal tracings on the right are from the unaffected side. From Ferraro and Tibbils (1999, p. 24).

63 Journal of the American Academy of Audiology/Volume 17, Number 1, 2006 include measurement of the SP/AP area ratio Obviously, more research in this area is in the interpretation of electrocochleograms. needed to ascertain ECochG’s sensitivity to However, we continue to measure the SP/AP cochlear versus vestibular hydrops, assuming magnitude ratio to clicks, the SP magnitude that these conditions can exist independently. to tonebursts (1000 and 2000 Hz), and the N1 As we continue to learn more about the latency difference to clicks of opposite polarity. infrastructure and physiology of the inner ear, The question as to which of these it is likely that even more basic mechanisms measurements (or combination of will be revealed to account for normal and measurements) is most sensitive to MD/ELH impaired hair-cell transduction in general. remains to be answered. To address this Molecular biological bases, perhaps even issue, we have begun an outcome study involving genetic coding or related processes involving several hundred patients seen for may play a role in altering these mechanisms ECochG examinations in our clinic during the in individuals with MD/ELH to produce the past five years. This project involves assessing changes in the SP and other features of the the relationship between the results of an electrocochleogram described above. ECochG examination (i.e., the individual measurements described above) and the SUMMARY subsequent diagnosis and treatment of the patient. At this time, the jury is still out CochG has emerged as an important tool regarding the measurement(s) that is most Ein the diagnosis, assessment, and sensitive to MD/ELH. monitoring of MD/ELH despite continuing A final note regarding the specificity of debate on the best ways to record and ECochG relates to enlarged SP/AP magnitude interpret responses. In this case, the “best ratios in conditions other than MD/ELH. In ways” are those that optimize the sensitivity particular, this feature also has been reported and specificity of ECochG in the evaluation for perilymphatic fistulae (Kobayashi et al, of MD/ELH—while causing minimal 1993; Ackley et al, 1994; Campbell and Abbas, discomfort to the patient. The following is a 1993, 1994). Thus, it may be the case that any summary of the features described in this change in cochlear fluid pressure that biases manuscript that should be considered in the cochlear transduction, and therefore the SP, selection of ECochG parameters to achieve will affect the SP/AP relationship (Storms this goal. et al, 1996). However, as implied in earlier • Although ECochG components discussion, definitive proof of this mechanism include the CM, SP, and AP, remains to be seen. Eggermont (1976) measurement of the SP and AP questioned the hydromechanical rationale continues to offer the most useful over two decades ago, suggesting information in the evaluation of consideration of possible biochemical changes MD/ELH. While the CM may indeed underlying or triggered by the fluid pressure have other valuable applications changes—ionic diffusion gradients can be (e.g., in the diagnosis of auditory altered by osmosis and vice versa. neuropathy), its utility for MD/ELH Yamasoba et al (1993) observed enlarged purposes has yet to be established. SPs in cases of idiopathic low-frequency • The authors prefer an ET recording hearing losses, namely patients who have no approach for ECochG that involves balance-related or other symptoms placing the primary electrode on the characteristic of MD/ELH. This finding external surface of the TM. This site suggests that a positive electrocochleogram offers a good compromise between may be a manifestation of “cochlear hydrops.” TT and other ET sites regarding Indeed, we have seen numerous patients who component magnitudes, preservation fit this profile. That is, a positive of diagnostic patterns, and testing electrocochleogram in the face of hearing time, and can be performed by loss, aural fullness, and tinnitus, but not audiologists in a nonmedical setting accompanied by vertigo. Likewise, we also with minimal-to-no discomfort to the have observed negative electrocochleograms patient. in dizzy patients whose auditory symptoms • The stimulus and signal averaging were minimal at the time of testing but who parameters associated with ECochG were eventually diagnosed with MD/ELH. should be chosen to favor

64 Electrocochleography in the Evaluation of Patients/Ferraro and Durrant

measurement of the SP and AP, MD/ELH, enlarged SP/AP recorded together or separately,and magnitude ratios also have been in response to both BBCs and reported in cases of perilymphatic tonebursts. fistulae and apparent cochlear • The lack of standardized stimuli and hydrops. This finding suggests that stimulus calibration approaches for the conditions to which ECochG may ECochG continues to necessitate the be most specific are changes in establishment of laboratory-/clinic- cochlear fluid pressure. specific normative data. • The relationship between ECochG • Stimulus and other artifact can be a results and symptoms and also to bigger problem for TM-ECochG than the acute status of the ear (as for other AEPs because of the observed in intraoperative recordings sensitivity/fragility of recording site, and conditions other than MD/ELH the construction, sensitivity, and that cause changes in cochlear fluid stability of the recording electrode, pressure), serves to underscore the and lowering the low-frequency general truism of ECochG, and all cutoff of the analog filter to allow AEP measures for that matter: they for measurement of the SP are functional indicators and not component. Several suggestions are pathognomonic of a particular offered in this manuscript to help disorder/disease. Fortunately for the inhibit such artifact. diagnostician, an increased SP/AP • Although the SP/AP magnitude ratio magnitude and/or area ratio, or to BBCs appears to be highly specific abnormally prolonged AP-N1 latency to MD/ELH (i.e., patients that display difference to BBCs of opposing an enlarged ratio are usually polarity are rare in retrocochlear diagnosed with this disorder), the cases and other disorders of hearing. sensitivity of this measurement (i.e., Thus, a positive electrocochleogram the likelihood of finding an enlarged certainly points strongly to a cochlear SP/AP magnitude ratio in someone disorder and most likely an etiology who has MD/ELH) in the general of MD/ELH. MD/ELH population is not as high. This finding demands a continued REFERENCES search for other features of the electrocochleogram that may improve Ackley RS, Ferraro JA, Arenberg IK. (1994) Diagnosis of patients with perilymphatic fistula. Semin Hear ECochG’s sensitivity.These features 15:37–41. may include the SP magnitude to tonebursts, the SP/AP area ratio to American Academy of Otolaryngology–-Head and Neck Surgery. Committee on Hearing and BBCs, and the latency difference Equilibrium. (1995) Guidelines for the diagnosis and between the AP-N1 components to evaluation of therapy in Meniere’s disease. Otolaryngol BBCs of opposing polarity.Although Head Neck Surg 113:181-185. our data suggest that measurement American Speech-Language-Hearing Association. of the SP/AP area ratio may offer the (1988) The short latency auditory evoked potentials: most sensitivity among the above a tutorial paper by the Working Group on Auditory Evoked Potential Measurements of the Committee values, additional research is needed on Audiologic Evaluation. to verify this finding. • There is a significant relationship American Speech-Language-Hearing Association. (1990) Competencies in auditory evoked potential between ECochG results and the measurement and clinical applications. Working symptoms the patient displays at Group on Auditory Evoked Potential Measurements the time of testing. Thus, one way to of the Committee on Audiologic Evaluation. Suppl 2. make ECochG more sensitive is to Andreev AM, Aropova AA, Gersuni SV.(1939) On elec- test patients when they are trical properties in the human cochlea. J Physiol symptomatic, even though the USSR 22:206–212. practicality of this strategy often is Aran JM, Lebert G. (1968) Les responses nerveuse limited. cochleaires chex l’homme, image du fonctionnement • Although, as indicated above, de l’oreille et nouveau test d’audiometrie objectif. Revue de Laryngologie, Otologie, Rhinologie (Bordeaux) ECochG is highly specific to 89:361–365.

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