Vicky W. Zhang & Bradley McPherson

Centre for Communication Disorders, The University of Hong Kong

Introduction

Since David Kemp published his pioneering work on otoacoustic emissions (OAEs) in 1978, OAEs have attracted a great deal of interest from audiologists, biophysicists, cell biologists, and even engineers throughout the world. The aim of this paper is to review the history of OAE research, and to highlight current OAE studies, in China. The review is the first in English that considers the Chinese contribution to OAE research. The authors have focused on research work from mainland China. Research contributions from Taiwan and Hong Kong are typically published in English-medium scientific journals. However, mainland China publishes over 1360 medical scientific periodicals (see http://www.mlpla.gov.cn/catalog2003/2003c.xls) and many mainland researchers write exclusively for Chinese publications. This review attempts to break through the language barrier and present the non-Chinese reader with an overview of Chinese OAE research work. Of course, we can only highlight a small number of selected publications in this review. Readers interested in exploring the range of Chinese OAE research further are encouraged to search via the Chinese Academic Journal database, which provides abstracts (in both Chinese and English) of articles from over 5,000 publications. Many university libraries around the world subscribe to this service.

It is not an exaggeration to say that the discovery of OAEs has revolutionized the study of the auditory system in China, as it has done elsewhere in the world. Since Jiang published the first Chinese paper describing OAEs in August 1989, there have been over 400 published reports on the topic in Chinese academic journals. The Chinese researchers who make use of OAE techniques have diverse interests - from animal experimentation to genetic research, from clinical audiology to industrial noise protection, from signal analysis and processing to OAE equipment design. This review will examine the Chinese research contribution in the areas of basic clinical OAE parameters, the application of OAEs in professional fields, basic animal experimental and genetic studies, the development of OAE technology in engineering, and will conclude by discussing the possible future directions of Chinese OAE research.

OAE properties in normal hearing subjects

Otoacoustic emissions are acoustical signals that originate from the cochlea, are conducted through the ossicular chain and the tympanic membrane, and can be detected in the ear canal. They may occur spontaneously or be evoked by stimulation. Following a series of early papers that gave OAE reference data for Chinese people (Shi et al.,1989; Xu et al., 1989), more detailed data concerned with OAE parameters in normal hearing young people was subsequently reported (Liu et al., 1996a; Liu et al., 2004; Yu et al., 1999). In 1993, Zhou et al. and Wang et al. published standardized data for OAE parameters in children and older age groups, respectively.

Clinical applications of OAEs

Cochlear damage and consequent hearing loss are often reflected in the alteration of OAE properties. Many Chinese studies have attempted to utilize OAE recordings to assist in the diagnosis of sensorineural hearing loss.

OAEs in adult audiology

(1) OAE properties in the diagnosis of cochlear dysfunction

The main reason that OAEs have become so widely used is their important clinical and diagnostic applications. Since the 1990s, OAEs has been routinely used in clinical otology and audiology in China to provide useful information in the evaluation of cochlear function. They enable the cochlear component of a hearing disorder to be identified and changes in cochlear status to be objectively monitored when this may not be possible using other audiologic methods.

Liu et al. (1998) showed that transient evoked otoacoustic emission (TEOAE) results were significantly abnormal in patients with Meniere’s disease as the OAE amplitude decreased in the low frequency region. After ingestion of glycerol, the main frequencies with observed OAE amplitude in some patients with Meniere’s disease shifted in frequency range (Guo et al., 1998; Liu et al., 1998). The results suggested to the authors that TEOAEs can be used in the diagnosis of Meniere’s disease as a more sensitive method than pure tone audiometry. Also, OAE assessment may be of value in detecting sudden deafness patients (Zhang et al., 1999) and those patients with vertebrobasilar transient ischemic vertigo (Li & Zhong, 1998). Liu and Feng (2003) analyzed the altered features of auditory functions in patients with hereditary nephritis-nerve deafness syndrome (Alport syndrome) and identified, partly through their use of distortion product otoacoustic emission (DPOAE) tests, the location of the pathological changes in Alport syndrome patients as being in the basilar membrane. They suggest that DPOAE assessment can help refine the initial diagnosis and support genetic counselling for Alport syndrome patients and their families. Moreover, by quantifying the presence and absence of TEOAEs and DPOAEs, it has been demonstrated that cochlear function may be affected in patients with severe obstructive sleep apnea (Long et al., 2003). After uvulopalatopharyngoplasty, the presence and amplitude of TEOAEs and DPOAEs can be significantly increased (She et al., 2004). Similarly, DPOAEs can provide valuable information when examining radiation injury to the cochlea after radiotherapy for nasopharyngeal carcinoma (Xiong et al., 2002), monitor the impaired cochlear function caused by hypertension (Chu et al., 2002) and help in the early diagnosis of hearing loss associated with chronic renal failure (Zheng et al., 2000) and in cases of hyperlipidemia (Pan et al., 2000).

(2) OAEs and tinnitus

Another interesting area of clinical OAE research in China concerns the correlation between OAEs and tinnitus. No correlation was found between subjective tinnitus frequencies and those of recorded spontaneous otoacoustic emissions (SOAEs) (Liu et al., 1996b). However, the same authors found that, among 306 ears with tinnitus (with or without hearing loss), in 94.8% of sensorineural hearing loss cases with tinnitus, the DP-gram presented with lower than normal amplitude or was absent within a frequency range associated with elevated pure-tone-threshold. In 59% of cases with normal hearing and tinnitus, the amplitude of DPOAEs at frequencies near the tinnitus frequencies was decreased and there were no detectable SOAEs.

(3) Middle ear effects on the OAEs

OAEs are influenced by the fact that the stimulus must be transmitted to the cochlea via the middle ear and the response must be detected in the ear canal, so it is important to study the interaction of middle-ear status and emission properties. Among subjects with negative middle ear pressure TEOAEs are reduced in amplitude, and it has been found that the stiffness factor affects TEOAE results more markedly than mass and friction factors (Zeng et al., 2000). Liu et al. (2000) explored the influence of differences in middle ear status on DPOAE findings. The results noted that the amplitude of DPOAEs in B type and C type tympanograms was -6.9 to 4.4 dBSPL, and -2.2 to 4.7 dBSPL, respectively. The prevalence of recordable DPOAEs was 13% and 19% in type B and C tympanograms, respectively.

(4) OAEs and noise exposure

In order to study the diagnostic value of OAEs in cases of noise-induced deafness, many studies have been done on different occupational groups exposed to noise. All of these results show that DPOAEs are one of the best diagnostic indicators of early stage noise-induced deafness (Cui et al., 1999; Feng et al., 2004; Long et al., 2004; Xu et al., 2003; Zhang et al., 2000; Zhou et al., 2003). Cui et al. (1999) recorded DPOAEs at four different primary stimulus levels from chronic high-level noise exposed people, and suggested that L1=L2=60 dB SPL is the best primary stimulus level. Han et al. (2004) compared conventional DPOAE, pure tone audiometry and expanded high frequency DPOAE (9-16 kHz) on noise exposed army workers. Their results demonstrated that DPOAE results were more sensitive than pure tone audiometry or expanded high frequency DPOAE. The authors concluded that DPOAEs are a potential screening instrument for the early detection of noise-induced deafness and a useful tool in the Chinese army’s auditory screening program.

(5) Contralateral suppressors and OAEs

To study efferent function more fully and to assess the contralateral auditory pathways in humans, Zheng et al. (1994) applied a TEOAE with and without contralateral noise to study the effects of contralateral suppression on OAEs, in normal hearing subjects. Results of this study revealed that as the intensity of contralateral noise was increased, the suppression effect on OAEs appeared stronger. This phenomenon may be the result of the modulating effect of the medial olivocochlear system on the outer hair cells in cochlea. Similarly, Liang et al. (1996) found that combined OAE and contralateral suppression tests are of great significance in evaluating cochlear status and the efferent function of the central auditory processing mechanisms. In 2000, Wang & Zhong investigated the effects of three kinds of sound stimuli on the amplitude of contralateral acoustic stimulus with DPOAEs. Their results showed that white noise gave a maximal suppression effect, narrow-band noise a reduced effect, while pure tone stimuli had a minimal effect. Suppressive effects on the amplitude of DPOAEs increased with increasing levels of contralateral stimulus.

OAEs and pediatric audiology

The impact of OAEs on the clinical assessment of hearing in infants and children has been especially dramatic. OAE technology has come to play a major role in newborn hearing screening programs because of its minimal time duration, reliability, objectivity and non-invasive nature. Since the 1990s, many Chinese studies have focused on exploring possible models of OAE screening and establishing feasible pass/refer criteria for neonatal hearing screening in China (Gong et al., 2001; Liao et al., 1999; Nie et al., 1999a; Qian, 1996). Generally speaking, OAEs are easily recorded from infants and children with normal cochlear auditory function under good recording conditions. The studies by Qian et al. (1994), Liao et al. (1997) and Zhou et al. (2004) demonstrated that TEOAEs could be successfully recorded from over 90% of full-term neonates. Nie et al. (1999a, 1999b) analyzed the specific properties of TEOAEs and DPOAEs in full-term newborns. Collectively, these findings have created a great deal of enthusiasm in China for using this rapid, reliable technique for universal hearing screening of all neonates.

Chinese studies have found the initial pass rate for neonates varied from 84.6% to 88.3%, and the prevalence of bilateral hearing loss was 2.86-6.04°Î (Guo & Yao, 1996; Nie et al., 1999b; Nie et al., 2003b), with some of the variation due to differences in screening methods in different studies. Yu et al. (2003) explored the factors which may affect DPOAE results in hearing screening, and their results noted that the initial screening outcome was correlated with birth weight, gender and birth order. In addition, Nie et al. (1999a) noted that a 2-day old neonatal group showed a higher passing rate than a 1-day old group, and there was no significant difference in the pass rate between their 2-day group and a +3-day old group. Nie et al. suggested that the optimal initial screening time should be set to 2 days after birth. However, other Chinese researchers consider that 3 days after birth is optimal (Liao et al., 1997; Zhou et al., 2004).

Normally, children have larger OAEs than adults, associated with a greater high frequency spectral content (Qian et al., 1994; Qian & Jiang, 1995). In addition, some Chinese researchers have found that there is a significant difference between right and left ears (Qi et al., 2000), and that pass rates are higher in right ears and for female neonates (Yu et al., 2003). These findings agree with studies in the Western OAE literature.

Risk factors for hearing loss in newborn babies are another critical issue which has attracted many researchers in different disciplines. Nie et al. (2003a) established that there are three high risk indicators associated with newborn hearing loss: family history, craniofacial anomalies, and neonatal intensive care unit history. Others studies have focused on the effect of other risk factors for infant hearing loss, such as hypoxia-ischemic encephalopathy, hyperbilirubinemia, and congenital human cytomegalovirus (Li et al., 2003; Liu, Wang, et al., 1996; Shen et al., 2002; Wang et al., 1999; Zhang et al., 2002; Zhang et al., 2003).

Basic animal experimentation and genetic studies

Although the principle application of OAEs has been their use in the audiological practice, they are also being utilized widely as noninvasive probes of cochlear function, in basic physiological research. In order to investigate micromechanical properties and the electromotility of outer hair cells, a diverse range of animal experiments has been carried out. Jiang et al. (1996) observed DPOAE changes in the guinea pig cochlea after trachea obstruction caused acute anoxia and apnea, and found that there is a relationship between DPOAE amplitude and the oxygen tolerance of cochlear hair cells. In 1997, perilymphatic fistula was induced in healthy guinea pigs to study its effects on DPOAEs (Wang et al., 1997c). The results noted that DPOAE amplitudes decreased significantly immediately after the formation of the fistula, and recurred to near pre-treatment levels in animals whose fistula was repaired. DPOAEs may therefore be viewed as a useful measure in the detection of perilymphatic fistula.

Wang et al. (1997a, 1997b) investigated the effect of a simulated diving procedure on DPOAEs, and also on inner ear actin levels using an immunohistologic method. The results found that there was a decrease in DPOAE amplitude after diving, but the immunohistologic reaction to actin in the cochlea and vestibular ampulla did not show a substantial change. Therefore, the decrease in DPOAE amplitude may be due to the change of impedance at the tympanic membrane and the middle ear pressure change associated with diving, and may cause no damage to the inner ear. The research may provide useful information for further studies in this area of naval medicine.

In addition, to explore the function of the cochlear efferent system, many Chinese researchers have undertaken experiments using guinea pigs. Li et al. (1998) used strychnine to obstruct the oliveocochlear bundle and found that DPOAEs were not reduced after strychnine administration. This indicated that efferent neural activity of the central nervous system does not affect DPOAEs when no contralateral stimulation is present, and confirmed previous Western studies.


OAE techniques have also been used in the detection of the effects of ototoxicity. Chinese researchers have found that DPOAEs can be used as a sensitivity index in ototoxicity research. Tao et al. (2002) studied the protective effect of melatonin on ototoxicity caused by gentamycin exposure. This research team observed the amplitude of DPOAEs and DPOAE input/output function curves, and concluded that melatonin had a protective effect against cochlear ototoxicity caused by gentamycin. Similarly, by observing the changes in DPOAE amplitude and morphology, Qu et al. (2004) found that glutamic acid (Glu) is likely to have toxic effects on both inner and outer ear hair cells.

The identification of deafness genes is an essential step in understanding the molecular mechanisms involved in hearing and hearing loss. Localization and cloning of deafness genes only began recently in China. To date, one deafness gene (GJB3) has been cloned in China (at the National Laboratory of Medical Genetics of China, Central South University China). The GJB3 gene was mapped to human chromosome 1p33-p35.Mutation analysis revealed that mutations of this gene were associated with high-frequency hearing loss (Xia et al., 1998). A few laboratories are dedicated to mapping new loci and identifying new deafness genes for nonsyndromic hearing loss. They are supported by the National Natural Science Foundation of China and other funding bodies. Researchers are now working on the molecular genetics involved in nonsyndromic prelingual deafness, and trying to detect mutations in related genes, such as GJB2, _-tectorin, myosin7A, myosin15, PDS, OTOF and tRNASeur. Xiao & Xie (2002) investigated the frequency of the seven genes and examined the molecular and epidemiological characteristics of these in Chinese patients. In developing research into the genomics of inherited deafness in China, the following basic data collection was emphasized by these researchers: epidemiological surveys and registration; collection, maintenance and banking of the data; and genetic material resources. By identifying the genes responsible for hearing impairment, more insight may be gained into the molecular process of hearing and the pathology of hearing loss in China and elsewhere.

Medical engineering research and OAEs

The successful clinical application of OAE tests requires advanced signal processing capabilities and the use of accurate and reliable instruments for OAE recording. Nowadays, a wide variety of commercial OAE instruments are available, ranging from handheld devices providing a simple indication of OAE presence or absence to elaborate clinical and research machines offering multiple OAE measures. All of these achievements depend on developments in the medical engineering field.

Zheng et al. (1997) described an active homomorphic model of the auditory periphery system based on an electroacoustic analog. The active ability is induced by a controlled voltage source, and the model includes the auditory canal, middle ear and the inner ear. The calculated results show that this model has the same frequency selection characteristics as a real cochlea, and it can produce TEOAEs and DPOAEs which are remarkably similar to those obtained from real human ears. The authors also made a thorough study to measure the parameters obtained using this homomorphic model, and acquired simulated TEOAE results which bear characteristics similar to actual clinical data (Zheng et al., 2002).

Ways to reduce the initial OAE artifact and increase the signal to noise ratio of OAE recordings have been actively considered by Chinese medical engineers in the past 10 years. Chai et al. (1999a) and Gong et al. (2001a, 2001b) proposed discrete wavelet transform methods, which not only reduce the stimulus artifact but also enhance the recognizable response. Digital filtering and correlation function processing techniques were proposed by Jiang et al. (1996), Ye et al. (2002) and Ye, Ye & Cao (2002) proposed using an algorithm based on the frequency coherent spectrum and cross-spectrum to optimally evaluate the TEOAE response.

In addition, Li et al. (1999) found that by short time Fourier transformation the exponent of the artifact decayed rapidly while the frequency distribution of the TEOAE was similar to that of the stimulating signal. The TEOAE signal and artifact may be separated and recognized more effectively by this method. The time-frequency distribution method for analysis of TEOAE signals was also studied by Chai et al. (1998), Chai and Zhuang (1999b) and Chai et al. (2000). This group considered that a cone-shaped kernel distribution is the optimal computing method for recording the time-frequency representations of TEOAEs, and also analyzed the correlation between tone-burst OAEs and TEOAEs using the cone-shaped kernel distribution method. Similarly, in order to improve the detection of TEOAEs, Ye et al. (2003) demonstrated the potential advantages of a new method called singularity detection technology, which is based on wavelet transform modulus maxima reconstruction. This method was found to be much more effective than the traditional ensemble averaging method, especially when only few test stimulus sweeps were applied.

Moreover, Chinese medical engineers have helped to develop new diagnostic applications for OAE technology. In 1998, Zheng et al. presented a new spectrum analysis method, based on Marple’s autoregressive mathematical model technique, for TEOAE data. This procedure could determine the type of hearing loss (high frequency, mid frequency, or low frequency) directly. The obtained diagnostic results were essentially the same as those obtained by DP-gram. Later, Zheng et al. (1999) and Gong et al. (2002a) investigated the application of the continuous wavelet transform and the approximate entropy method in locating defective cochlear regions so as to aid in the diagnosis of hearing loss.

From the beginning of Chinese OAE research, many kinds of imported instruments have been used by Chinese research institutes and audiology clinics. In addition, Chinese engineers have designed their own OAE equipment. In 1994, Weng et al. successfully developed an OAE probe coupled to a conventional bone-conduction earphone for stimulus presentation. This probe could be connected to auditory evoked potential instrumentation and allowed this equipment to be used for OAE test purposes. To reduce the initial artifact associated with TEOAE testing, Gong et al. (2002b) proposed employing a predictor-subtractor-restorer filter, which can not only reduce the signal artifact but also enhance useful high frequency TEOAE information. As for OAE recording systems, South China University and Tsinghua University are the two main institutes to have developed this type of equipment in China (Du & Ren, 1999; Liu et al., 2002). Now, the “HS-OAE” system designed by Tsinghua University has met China National Standards approval and is being regularly used in hearing clinics in some areas of China.

Future directions in Chinese OAE research

It has been more than 20 years since OAEs were first identified. Not only has this technique enhanced our understanding of normal cochlear processes, it has provided us with an objective, accurate, and simple assessment tool for studying these processes. However, there are still many areas that require much additional research, and some of these areas are the focus of Chinese researchers. With the steady increase in the number of Chinese hospitals with universal neonatal hearing screening programs, it is likely that there will be much further research activity in this field. OAE screening techniques still have limitations. Firstly, conventional OAE tests mainly provide information about mid-frequency (1-4 kHz) cochlear status, and information concerning potential low frequency and high frequency hearing loss is lacking. Secondly, noise is still a problem in the detection of OAE signals. Therefore, developing advanced methods for increasing the signal to noise ratio may be an important task for researchers. Thirdly, optimal screening procedures that combine OAE and auditory brainstem evoked response testing to both detect auditory neuropathy (Li et al., 2001; Li & Sun 2003; Liu et al., 2003; Ni et al., 2000; Xu et al., 2002; Wang et al., 2002) and reduce false positive rates is potentially another major issue for future research.

With the rapid development of professional education in audiology in China, more and more audiologists will become involved in research in the OAE field. They will bring new ideas and vigor to the development of this technique in China. As Chinese researchers develop more international collaborations it can be hoped that Chinese research will come to make a wider impact in our field.


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