electrophysiology to quality of life
Klop, W.M.C.
Citation
Klop, W. M. C. (2009, April 8). Exploring the capabilities of modern cochlear implants : from electrophysiology to quality of life. Retrieved from https://hdl.handle.net/1887/13726
Version: Corrected Publisher’s Version
License: Licence agreement concerning inclusion of doctoral thesis in the Institutional Repository of the University of Leiden
Downloaded from: https://hdl.handle.net/1887/13726
Chapter 1
Introduction and outline of the thesis
1. Electrical hearing
Djourno and Eyries’ well-known publication1 in 1957 marked a new era by suggesting that activation of the auditory periphery through a monopolar electrode was practical, and capable of providing physiologically useful information to the central auditory pathway. Two decades later, multi-channel devices were introduced to utilize the tonotopic organization of the cochlea. The assumption was that each individual channel could activate a restricted part of the deafened cochlea, just as sound within a restricted frequency band could activate a restricted part of the normal cochlea.2
Nowadays, all multi-channel cochlear implant systems have the same basic components and functions in common with the “Chorimac”, developed in the mid- seventies by Bertin for Chouard.3 Typically, these prosthetic devices consist of an external microphone, a speech processor, and an intra-scalar electrode array (figure 1.1).
Figure 1.1: Graphical presentation of the basic components of a cochlear implant system.
The incoming sound is captured by the microphone and sent to a speech processor.
Speech is filtered into a number of frequency bands and the temporal envelope of each band is extracted. This so-called envelope extraction mechanism usually determines the amplitudes of the various frequency bands. A specific speech coding strategy then codes the amplitude information.
The early speech processors tended to use feature extraction strategies (F0/F1/
F2) or the compressed analogue (CA) approach. As these traditional speech-coding strategies had limitations, Wilson et al.4 introduced the Continuous Interleaved Sampling (CIS) strategy to improve sampling rate and to reduce the electrode interaction by presenting the signal in brief pulses to each electrode in a non- overlapping sequence. The CIS is currently one of the main strategies and its principle underlies the speech coding strategies in most commercially available devices.
As the speech processing strategy encodes the auditory signal it is transmitted via a radio frequency signal across the skin to the internal implant. The internal electronics of the internal implant further processes the coded information into electrical pulses, which are sent to the electrode array. The electrode array is implanted into the scala tympani of the cochlea, usually through a cochleostomy in the vicinity of the round window membrane. In this way, the electrode contacts are distributed along the cochlear duct. The electrical pulses are then delivered to the appropriate electrode in the intracochlear array. The particular electrode that is stimulated depends on the frequency of the channel, since all multi- channel cochlear implants exploit the place mechanism for encoding frequency in the cochlea.
One of the key elements for the understanding of electrical hearing is the intracochlear stimulation of the auditory nerve. While normal hearing is due to stimulation of the hair cells in the cochlea, electrical hearing results from direct stimulation of the auditory nerve fibres. In order to gain more insight into this type of stimulation process, many experimental and computational model studies have been performed. Generally, three primary stimulus dimensions govern how cochlear implants transfer information to auditory nerve fibres.5 Firstly, varying the stimulus level alters the population of excited fibres and changes the firing and stochastic characteristics of that population. Secondly, the stimulus pulse rate
can affect temporal resolution. Finally, the place of stimulation, using multiple electrode arrays, can excite different fiber subpopulations.
To obtain better control of the electrode-nerve interface, an important question has to be answered: can we optimize the information transfer from electrode to the auditory nerve fibres with a modern multi- channel cochlear implant by modulating level, rate and/or place of stimulation? In the past ten years there has, therefore, been an enormous increase in publications that deal with optimizing the information transfer in cochlear implants.6-9
Research conducted at the Leiden ORL department focused merely on the place of stimulation. It was recognized in modeling10-13, as well as in clinical studies14 that benefits should result from placing an array closer to the cell bodies. In that way, the ability of an electrode to selectively activate the neurons in the cochlea improves. Spatial selectivity describes how much the neural region stimulated by one channel protrudes into regions that are normally covered by other channels.15 Ideally, each electrode contact stimulates a separate sub-population of nerve fibers. However, in most cases deafness is caused by absence or degeneration of sensory hair cells in the cochlea. Damage to the hair cells results in loss of nerve fibres.16 A schematic illustration of the peripheral auditory system for cases of normal and profoundly-impaired hearing is shown in figure 1.2. The electrode array is represented as a xylophone. In normal hearing, “the xylophone” ideally uses the tonotopic organization of the uniformly divided fibres of the auditory nerve, with no overlap.
As to profoundly impaired hearing, the bottom panel of figure 1.2 clearly illustrates three practical problems encountered with cochlear implantation.
Firstly, with neural degradation fewer and unequally divided nerve fibers remain in the cochlea. Secondly, the configuration of the multi-electrode array leads to electrical interaction in-between the electrodes. Thirdly, stimulation of
“different” populations of nerve fibres by adjacent electrodes of the electrode array practically leads to considerable overlap between those populations. Thus, instead of a perfect representation of the tonotopic organization of the cochlea, the modern multi-cochlear implant lacks spatial selectivity and shows channel interaction, leading to a less optimal processing of sounds and speech.
Apex Low frequencies
Base High frequencies Nerve fibres
Overlap Apex
Low frequencies
Base High frequencies
Neural degeneration A
B
Figure 1.2: Multi channel cochlear implant. The xylophone represents the multi- electrode array using the tonotopic organization of the cochlea. The vertical grey lines represent nerve fibers. A: Idealized situation with perfect selectivity and no cochlear pathology. B: Because of the neural degeneration in the deafened cochlea and overlap of the excitation patterns of each electrode, the cochlear implant lacks spatial selectivity and shows channel interaction.
2. Objective measurement of Cochlear Implant function
A broad spectrum of measures is used to evaluate the processing of sounds and speech in cochlear implant patients. Many characteristics of the neural responses elicited by a cochlear implant can be verified through objective measurements.
Objective measurements are measurement techniques that do not rely on patient participation and can be supplemental to behavioral data. Objective measures in the field of cochlear implantation can be divided into two categories: electrical measures and electrophysiological measures. Electrical measures have been developed to evaluate the function of the implant electronics and the electrode output and comprise an internal implant electronics test, testing the radio frequency coupling, electrode impedance telemetry, compliance voltage telemetry and electrical field imaging. Such measures provide valuable information that can be used to confirm device function and investigate the integrity of the electrode, both at the time of cochlear surgery and postoperatively.17 However, it is beyond the scope of this thesis to elucidate the electrical measures involved in cochlear implantation.
Electrophysiological measures are those that involve interaction with (human) physiology. Although there are several potential clinical applications of objective electrophysiological measures, the most immediate is to determine whether the responses can be used to facilitate the programming of the cochlear implant processor. The most commonly used measures in cochlear implant research are the electrically evoked stapedial reflex (eSR), electrically evoked auditory brainstem response (eABR) and electrically evoked compound action potential (eCAP).
The eSR elicits the acoustic reflex by means of electrical stimulation in cochlear implant recipients and has been established since 1986.18 It is a quick, non- invasive procedure which can provide a guideline for setting levels of maximum stimulation19,20, although it is not possible to record the eSR in a substantial cohort of patients (~30%), especially in small children.
The first definitive description of the acoustical auditory brainstem response (ABR) in humans was reported in 1971 by Jewett and Willingston.21 Since then, the generator sites of the classic seven waves (I-VII) arising in the first 10 ms after presentation of the click stimulus have been extensively described. In 1979, Starr and Brackmann22 reported comparable brainstem responses in humans to
electrical stimulation (eABRs) with a single monopolar electrode in the scala tympani.
Figure 1.3: Example of an electrical Auditory Brainstem Response (eABR). The eABR signal is the response of the auditory brainstem due to an electrical stimulus. The vertical axis shows the eABR signal at increasing current levels (A). The horizontal axis represents time (ms) after stimulus onset. Different peaks present different parts of the auditory pathway.
In the past, eABR was used quite often during assessment of cochlear implant candidates. The presence of a brain stem response confirms that auditory nerve fibres are receiving and reacting to electrical stimulation, and is therefore an effective check of the status of the auditory pathway and, later in the process, of the function of the implant (figure 1.3). The eABR measured after implantation can also be used to help program the speech processor. However, the most significant limitation is that the eABR has a very small amplitude and is easily affected by muscle artifacts. Most clinical uses of the eABR can now be accomplished more easily using the eCAP. The latter signal consists of summed responses of nerve fibres excited by current pulses, and recorded with a recording electrode positioned close to the cochlear nerve or intracochlearly (figure 1.4).
Figure 1.4: Example of an electrical Compound Action Potential (eCAP) recorded with Neural Response Imaging (NRI). The vertical axis shows the eCAP at increasing stimulus levels (A). The horizontal axis represents time (s) from stimulus onset.
A typical eCAP consists of a triphasic waveform with a small positive peak (P0) followed by a negative trough (N1) followed by a positive peak (P1).
The eCAP from an intracochlear electrode of the Ineraid cochlear implant was first described by Brown et al.23 These findings initiated the inclusion of the Neural Response Telemetry (NRT) recording system into the Nucleus CI24M implant.24 This device was capable of two-way telemetry across the skin without the need for a percutaneous plug. The other implant manufacturers followed with similar designs. Neural Response Imaging (NRI) was introduced in the Advanced Bionics CII device25 and Auditory Nerve Response Telemetry (ART) in the MedEl PulsarCI100 device.26
Because the eCAP is an early-latency (100-300s after stimulus onset) evoked potential, separating it from the stimulus artifact is a challenge. This stimulus artifact is often large enough to saturate the recording amplifier. Techniques used to reduce stimulus artifact typically involve manipulations of the stimulus. The NRI system by Advanced Bionics© commonly delivers the stimulus pulses in alternating polarity. The NRT software of the Cochlear Corporation© generally uses a masker probe technique to cancel the stimulus artifact.23 It is helpful to understand how these artifact reduction protocols work to optimize stimulation and recording parameters. Figure 1.5 describes and illustrates both algorithms.
Figure 1.5: Two commonly used techniques for artifact reduction: alternating polarity and forward masking.
The alternating polarity technique measures responses for negative-leading (cathodic) and positive-leading (anodic) biphasic pulses. The neural response evoked by the stimulus should not reverse polarity as the stimulus polarity changes. Upon averaging responses from both polarities, the majority of the stimulus artifact cancels out, leaving the neural response.
The second method, forward masking, makes use of the refractory properties of the auditory nerve. A high-level masker puts the nerve in a refractory state, so that the subsequent probe fails to elicit a response (MP). This waveform is subtracted from the probe (P) alone to eliminate the probe artifact. This subtraction introduces an inverted masker and masker response. To remove this, the response to the masker alone (M) is added, producing the desired neural response.
In the last decade, there has been a steady increase in the number of studies addressing the clinical utility of eCAP measures. So far, main applications are (1), the objective verification of device function, (2) the objective verification of auditory nerve function, and (3) assistance in programming the speech processor in individuals.24, 27-30
Thus, it may be concluded that objective measures provide basic knowledge about the electrode-nerve interface and the functioning of the CI system However, the merit of a CI is not determined by a perfect transfer of electrical current to the auditory nerve, but by its contribution to oral communication, social interaction and daily life. Subjective tools are preferable when assessing the aforementioned aspects of communication and well-being.
3. Subjective measurement of Cochlear Implant function
Evaluating cochlear Implant function by looking at a broad range of health domains, including communication, psychological and social domains, is a possible means to identify shortcomings of a cochlear implant program and to provide a starting point for improvements. But, how do we evaluate the benefits of cochlear implants in such a heterogeneous population? What constitutes the success of a cochlear implant? When single electrode cochlear implants were used clinically in the 1970s, pre- and postoperative evaluation was done partly through psychological assessment, and test batteries for speech perception were not formalized. As speech perception performance improved with the multiple-channel cochlear implants, the relatively simple tests of closed-set speech perception became less important. To address these problems, a subcommittee of the American Academy of Otolaryngology- Head and Neck Surgery selected a minimum battery of speech perception tests for adults with CI. This battery consists of one monosyllabic word recognition test, the Consonant-Nucleus Consonant (CNC) word list31 and a sentence test, the Hearing in Noise Test (HINT).32
In the Netherlands, speech perception scores are obtained using the Dutch Society of Audiology (NVA) CNC word lists.33 These lists are used in routine clinical practice for speech audiometry, as well as for hearing aid and cochlear implant evaluation.
Results of the NVA-test are typically expressed as phonemes correct; it is optional to use word scores to allow comparison with other (English) word tests. At our hospital, the performance of cochlear implant users is usually evaluated at a speech level of 65 dB SPL, but levels of 55 en 75 dB SPL are used in addition.
As the speech perception scores with multiple-channel cochlear implants have improved, there is a growing need to evaluate performance not only in quiet, but also in conditions that are more difficult. Therefore, when the average phoneme score in quiet exceeds 50%, patients are also tested in noise. For this purpose, the standard NVA speech-shaped noise is combined with speech presented at a fixed level of 65 dB SPL. Speech scores in noise are assessed at maximally four signal-to- noise ratios (SNR), starting with an SNR of +10 dB and continuing at +5, 0 and -5 dB SNR until the phoneme score is lower than 30%.
The Dutch sentence test34 –used in normal clinical practice to assess speech discrimination in noise– appeared to be unsuitable for CI-patients. Due to the test design, this test can only be administered if all words of a sentence can be discriminated correctly in quiet. This turned out to be too difficult for most CI-patients.
To measure performance in real life conditions, a speech-tracking task without the help of lip-reading can be completed.35 In speech tracking, selected everyday texts are presented live (of 100 to 110 words, 7 to 10 words per phrase). At the completion of one text, the number of words is divided by the time needed to finish the text, to give a word-per-minute (wpm) rate. The initial group of patients implanted in our centre demonstrated steadily increasing scores (up to 66 wpm on the average over 3 months), subjectively reflecting the increased ease of listening.25
Although speech perception scores are very important indicators of how a CI benefits a patient, other outcomes may also provide essential information on the benefits of a CI. In general, hearing is of fundamental human significance in communication and thereby in social and emotional functioning. In contrast, impaired hearing may result in withdrawal from social life, depression, and anxiety.36 It might also hamper an individual’s independence; for instance, if a doorbell cannot be heard or a telephone cannot be used. Thus, rehabilitation of hearing loss not only affects speech perception, but also contributes to self- esteem, daily activities, and social functioning.
The general health status of CI-patients, as well as their health-related quality of life (HRQoL)37, have recently received increasing attention. Most definitions of HRQoL encompass how patients experience and evaluate various aspects of their health, including physical, psychological, and social functioning, physical symptoms, and overall health or well-being. Valid and reliable questionnaires are necessary to measure HRQoL. A good example of a commonly used measure of generic health status in the general population is the SF- 36™.38 The SF-36 is a multi-purpose, short-form health survey with 36 questions. It yields an 8-scale profile of functional health and well-being scores as well as psychometrically- based physical and mental health summary measures. The SF-36 has proven useful in surveys of various populations, in comparing the relative burden of diseases, and in differentiating the health benefits produced by a wide range of different treatments. However, its sensitivity in the hearing-impaired patients has been questioned.39
Disease-specific instruments, such as The Hearing Handicap Inventory for Adults (HHIA)40, Glasgow Benefit Inventory41 and Nijmegen Cochlear Implant Questionnaire (NCIQ)42, have been developed to describe typical aspects of hearing-related disease. The instruments assess treatment effects on hearing loss and deafness. So far, several reports have shown that cochlear implantation has a positive impact on different aspects of quality of life in patients with profound sensorineural hearing loss41,42, although there are few prospective studies that include both generic and disease specific instruments.
When generic HRQoL measures are used, comparisons with other healthcare interventions are possible. Quality-adjusted life years (QALYs) are a special case of such measures that are mostly used in cost-effectiveness analyses.
Cost-effectiveness analyses evaluate health interventions based on the relation between the resources consumed (costs) and the resultant health outcomes (effects). Such analyses provide a quantified assessment of the value provided and seek to describe the impact of an intervention in terms of benefit and costs. QALYs are calculated as follows: time spent in all relevant outcome states, or health states, is multiplied by the value assigned to those particular states, after which the products are added. The values used as the multipliers to calculate QALYs, are numerical judgments of the desirability of the respective health states. These values are called utilities. Most health states have a utility between 0 (death)
and 1 (perfect health). Utilities of very poor health states may even be negative.
Utilities can be assigned by experts or can be elicited from patients or healthy people. Common methods for eliciting utilities are the Time Trade Off method (TTO), Standard Gamble (SG) and the Visual Analogue Scale (VAS).43 In the TTO method, the subject is asked to choose between his remaining life expectancy in the current state (with disease) and a shorter life span in normal health. VAS is a rating scale; the subject is asked to rate the state by placing a mark on a 100-mm horizontal or vertical line, anchored by optimal health and death. The SG reveals an individual’s preference by offering a choice between2 alternatives: living in a health state with certainty or takinga gamble on a new intervention for which the outcome is uncertain.44
SG, TTO, and VAS are feasible methods that have all received recommendation.45 The VAS would be especially appropriate if neither risk nor trade-offs between quality of life and length of life are involved andif weighing different dimensions of quality of life is the onlyaim. In situations where risks or health care choices are involved, the SG and TTO are considered superior. For the SGand TTO methods, an interview setting is recommended. With respect to face validity, some consider the TTO to be the most valid method, because the question it poses ismost closely associated with the type of health care choicesthat need to be made.45-48
For cost-effectiveness analyses from a societal perspective health state classification systems such as the Health Utilities Index (HUI-Mark II and III)49,50, the Australian Assessment of Quality of Life (AQoL) instruments51 and the EuroQol- 5D52 are used. A classification system has also been developed based on the aforementioned SF-36: the SF-6D.53 In these classification systems, patients in a health state complete a descriptive quality-of-life questionnaire. Utilities are assigned to the thus described health states by means of a scoring table, based on preferences elicited in earlier studies from the general public.54 Most of these questionnaires are easy to use, provide descriptive information on sub-domains and assign utilities. Cost-effectiveness of cochlear implantation in adults has been evaluated extensively (Table 1.1).55-62
Table 1.1: Cost-utility of cochlear implantation in adults.
Study Instrument Country N Utility $/QALY
UK Cochlear Implant Study group, 2004 HUI3 U.K. 311 0.2 27,142
Francis et al. 2002 HUI3 U.S. 47 0.24 9,530
Palmer et al., 1999 HUI2 U.S. 37 0.2 14,670
Wyatt et al., 1996 HUI2 U.S. 229 0.204 15,928
Wyatt et al., 1995 VAS-without U.S. 229 0.304 9,000
Summerfield et al., 1995 VAS-without U.K. 105 0.41 7,405
Summerfield et al., 1995 VAS-before U.K. 103 0.23 13,200
Harris et al., 1995 QWB U.S. 7 0.072 31,711
The studies have shown a wide range of costs per qualy (from $7,405 up to $31,711).
This variation is not only due to differences in utility (0.07-0.41), but depends also on the way costs are calculated and on the measurement tools (HUI2-3, VAS and QWB) that are used. Nevertheless, there is general agreement that cochlear implantation is good value for money.60-62 In contrast with this vast number of foreign studies no such studies have been performed in the Netherlands.
4. Overview of the present thesis
Implantation with state of the art, multichannel cochlear implants (CI) that optimize the tonotopic organization of the cochlea aims to improve hearing of deaf patients. The clinical CI program at the Leiden University Medical Centre (LUMC) commenced in 2000 when the first postlingually deafened patient was implanted. Since that first patient, over 250 adults and 80 children have been treated. Initially, all patients were implanted with the Clarion CII HiFocus 1 (Advanced Bionics Corporation). Nowadays, the Cochlear Implant Rehabilitation Centre Leiden Effatha (CIRCLE) uses different state-of-the-art devices from the Advanced Bionics Corporation as well as from the Cochlear Corporation.
Until the start of our clinical CI program, the main part of CI research performed in our centre was carried out on animals and concentrated on the development of a computer model of the implanted guinea pig cochlea.10,11,63 This computer model revealed new insights in the relation between stimulating electrodes and
the auditory nerve response. These developments encouraged the Leiden ORL department to extend the animal model into a human model that can potentially be used for clinical applications.12,13,64
The scientific work mentioned above had one ultimate goal: to improve speech perception and quality of life in hearing impaired patients. Hence, in this thesis we investigated the clinical effectiveness of the current multi-channel cochlear implants in our centre. Whether the new capabilities of our modern cochlear implants could further optimize the information transfer was explored using electrophysiological techniques and evaluated by subjective measurements.
In Chapter two we conducted a prospective assessment of benefits of cochlear implantation in a series of 44 consecutive patients in our centre. The impact of a CI on speech perception performance, health related quality of life and cost- effectiveness in postlingually deafened adults was evaluated. To obtain an insight into the effect of CI on quality of life, measures for clinical relevance were applied.
As the performance of these modern devices continues to improve, the population of hearing-impaired individuals who can benefit from implantation is likely to become more diverse, even including subjects that used to be considered poor CI candidates. Such a specific group, the prelingually deafened adults, is described in Chapter three. Furthermore, outcomes are evaluated in this chapter.
One of the factors that limit the effectiveness of a cochlear implant is likely to be the relatively modest degree of spectral resolution that is available. A greater number of stimulated electrodes should theoretically provide better spectral resolution, while a higher rate of stimulation might improve the temporal resolution.4 Contrary to older single channel processors, modern multi-electrode devices are able to process high rate strategies using temporally interleaved pulses. Chapter four describes a blind crossover study evaluating the effect of the number of electrodes on speech perception in silence and noise using a high-rate stimulation strategy.
Since technical improvements allowed the selection of special populations (prelingually deafened adults, very young patients, multi-disabled patients, patients that still have some benefit from hearing aids) to receive cochlear implants, the need to optimize subjective fitting procedures with objective data
increased. ECAP measurements provided by NRI may allow us to predict more accurately the levels needed to program the speech processor without the need for behavioural data. However, these systems suffer from a stimulus artefact contamination of the eCAP signal. The first priority in successfully recording the eCAP is to find a way to minimize the stimulus artefact in the recorded response.
In Chapter five, a new method for dealing with this problem was tested in a series of animal experiments.
Recording the eCAP using NRI in CI-patients should increase our knowledge about the characteristics of single electrodes and their excitation patterns, and help to optimize CI performance. The results of our high rate study (Chapter four) indicated that it is important to know which electrodes do or do not carry additional information. With the aim of determining the independence of each electrode in a multi-electrode array, we developed an objective equivalent of the dual electrode masker selectivity paradigm.65 The structure of the results to be expected was investigated with a simple quantitative model and tested in clinical patients (Chapter six).
Finally, in Chapter seven, the results and overall conclusions of the studies reported on in this thesis are discussed and practical implications as well as proposals for future research are formulated.
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