Abstract
Objectives. To study the efficacy of otoacoustic emissions (OAEs) as a screening test for hearing impairment in children with acute bacterial meningitis. Hearing tests were performed before discharge from the hospital in an attempt to improve coverage and avoid delays in the diagnosis of postmeningitic hearing loss.
Methods. Children with bacterial meningitis were recruited from 21 centers. In the 48 hours before discharge from the hospital, all patients underwent a thorough audiologic assessment consisting of transient evoked OAEs, auditory brainstem responses (ABRs), otoscopy, and tympanometry. Hearing loss was defined as ABR threshold ≥30 dB. The results of OAE screening were compared with the gold standard of ABR threshold.
Results. Of 124 children recruited, we were able to perform both OAEs and ABRs on 110 children. Seven (6.3%) of the 110 children had ABR threshold ≥30 dB; 2 had sensorineural hearing loss and 5 had conductive hearing loss. At follow-up, hearing loss persisted in both cases of sensorineural hearing loss and no new cases were identified. All 7 children with hearing loss failed the OAE screening test. Ninety-four children with normal hearing thresholds passed the test, and 9 failed. Thus, the screening test had a sensitivity of 1.00 (95% confidence interval, 0.59 to 1.00), a specificity of 0.91 (0.85 to 0.97), a positive predictive value of 0.44 (0.20 to 0.70), and a negative predictive value of 1.00 (0.96 to 1.00).
Conclusions. OAE screening in children recovering from meningitis was found to be feasible and effective. The test was highly sensitive and reasonably specific. Inpatient OAE screening should allow early diagnosis of postmeningitic hearing loss and prompt auditory rehabilitation.
Sensorineural hearing loss is the commonest serious complication of bacterial meningitis in childhood. Approximately 10% of survivors are affected.1,,2 It is therefore suggested that all children who have had meningitis be tested for hearing loss.3,,4 In the United Kingdom, it is recommended that a hearing assessment should be performed in a pediatric audiology clinic 4 to 6 weeks after the child has been discharged from the hospital.1 In practice, only 75% to 80% of patients have a formal hearing test.5,,6 This is partly because children are not referred to the audiology services and partly because they fail to attend their appointments.6,,7 Furthermore, there is often a considerable delay between discharge from the hospital and the first attendance to the audiology clinic. In many cases this interval is more than 3 months.5,,7 Incomplete audiologic follow-up and delayed assessment have also been reported in several American studies of postmeningitic hearing loss.3,,8,9 Delays in the diagnosis of postmeningitic deafness are a cause for concern because they may prevent optimal auditory rehabilitation. This is particularly important in cases of profound hearing loss, in which cochlear implantation is the only effective treatment. Within a few months of meningitis the cochlear duct may be obliterated by new bone formation, making cochlear implantation ineffective or even impossible.10,,11
Delays in the diagnosis of postmeningitic deafness could be avoided if children with meningitis were screened before discharge from the hospital. This approach should also ensure that more children are tested. However, universal inpatient screening would almost certainly be impractical using conventional techniques. Subjective methods, such as pure tone audiometry and visual reinforcement audiometry, require the cooperation of the patient, and this may not be forthcoming in children recovering from meningitis. Auditory brainstem responses (ABRs) are an electrophysiologic test that can be performed in the recovery stage of meningitis.3,12–14 ABRs may be useful in this situation because they provide an objective measurement of hearing threshold. To some extent, the test can also differentiate between lesions of the auditory nerves, the cochlea, and the middle ear. However, interpretation of ABRs requires expertise, and it can be time-consuming and expensive. Furthermore, young children sometimes require sedation, or even general anesthesia, before ABRs can be performed.15
Detection of transient evoked otoacoustic emissions (OAEs) is a newer audiologic technique that can be used as a screening test for hearing impairment in children. OAEs are minute sound waves that are produced by the healthy cochlea in response to an auditory stimulus.16 In clinical practice, transient evoked OAEs can be recorded from nearly all healthy ears but are abolished in those with lesions of the cochlea.17,,18 OAEs are also abolished in some ears with conductive hearing loss.19 OAEs are essentially an all-or-nothing phenomenon. This means that the test cannot be used to measure hearing thresholds, or to distinguish between cochlear and conductive hearing loss. OAEs do, however, have great potential as a screening test. This is because the all-or-nothing nature of OAEs means that most healthy ears produce an emission, whereas those with hearing defects simply fail to produce a response. Testing for OAEs is also noninvasive, and quick and simple to perform. Furthermore, OAE screening has been shown to be cost-effective when compared with ABRs.20
The aim of this study was to determine whether OAEs could be used as a predischarge screening test for hearing loss in children recovering from acute bacterial meningitis. To be clinically useful, the screening test would need to identify all children with hearing loss, without causing too many children with normal hearing to fail. In practice, the screening test would be used to determine which patients need urgent referral for diagnostic assessment and determination of hearing threshold.
In this study we evaluated the use of an OAE screening program against the gold standard of ABRs. The analysis was performed as part of a multicenter prospective study of hearing loss during meningitis.21
METHODS
Between November 1993 and April 1995, children with newly diagnosed bacterial meningitis were recruited from 21 hospitals in a defined area of England and Wales. All study participants underwent repeated audiologic testing, the details of which are published elsewhere.21 The study was approved by local ethics committees, and informed consent was obtained for all participants.
In the 48 hours before discharge from the hospital, patients were tested by transient evoked OAEs, ABRs, otoscopy, and tympanometry. All tests were performed and analyzed by one experienced investigator (M.P.R.). OAEs were recorded using the QuickScreen program on the ILO88 System (Otodynamics, Hatfield, UK) as previously described.21 The presence or absence of an OAE was determined using a limited-frequency screening criterion (pass = signal-to-noise ratio ≥3 dB on one or more bandwidths).22If OAEs were absent, the entire test procedure was repeated to exclude methodologic failure.
ABRs were recorded on a Sapphire 2A EP System (Medelec, Old Woking, UK) and wave V thresholds were estimated to the nearest 10 dB normal hearing level (nHL). Sedation was not used. Children were also assessed by otoscopy and tympanometry. Ears were classified as having hearing loss if the ABR wave V threshold was ≥30 dB nHL. Impairments were deemed to be conductive if the ear had evidence of an effusion and produced a type B tympanogram. Otherwise, a sensorineural hearing loss was diagnosed.
We performed audiologic follow-up on children who had hearing loss at the time of discharge from the hospital. These children were assessed by OAEs, ABR, and tympanometry on 3 occasions during the following 9 months. All children enrolled in the study were referred for local audiologic follow-up. We were informed of the results of these assessments.
The performance of OAEs was compared with the result of ABRs in the 48 hours before discharge from the hospital, and values were obtained for the sensitivity and specificity of the test. Positive and negative predictive values were also calculated. Ninety-five percent confidence intervals were calculated for each statistic using exact binomial values.23
RESULTS
One hundred twenty-four children with acute bacterial meningitis were recruited. This represents >80% of the cases of childhood meningitis that occurred in the defined area during the study period. Children in the study population did not differ in severity of illness from those who were not studied. The causative organisms wereNeisseria meningitidis (92 children, 74%),Streptococcus pneumoniae (18 children, 15%), andHaemophilus influenzae type b, Listeria monocytogenes, and group B streptococcus (one case each). In the remaining 11 cases (8%) no pathogen was identified. The ages of the children ranged from 6 weeks to 15 years (median, 2.1 years). We were able to perform both OAEs and ABRs in 110 children (89%). Of the remaining children, 4 were discharged from the hospital before the tests could be performed, 4 would not tolerate the ABR procedure, and 6 would not cooperate with either ABRs or OAEs. The children who would not tolerate the tests were aged between 10 months and 3 years. In general, OAEs were quick and easy to measure. The majority of tests could be completed in under 10 minutes and most children did not object to the procedure. In contrast, ABR recordings took at least 30 minutes and many children objected to the procedure.
Seven (6.3%) of the 110 children who could be fully assessed were classified as having hearing loss (ABR threshold ≥30 dB nHL). Two children were diagnosed as having sensorineural hearing loss (both bilateral) and 5 had conductive hearing loss (3 bilateral). The performance of the OAE screening test is shown in Table 1. According to the pass/fail criterion used in this study, all 7 patients with hearing loss did not produce OAEs in the affected ears. Nine children with ABR thresholds <30 dB nHL also failed to produce detectable OAEs in one or both ears. Thus, the sensitivity of OAEs was 1.00 (95% confidence interval, 0.59 to 1.00) and the specificity was 0.91 (0.85 to 0.97). In this population, the positive predictive value of failing the test was 0.44 (95% confidence interval, 0.20 to 0.70) and the negative predictive value was 1.00 (0.96 to 1.00).
Results of OAE Screening in the Study Population
Follow-up data is available for 100 (91%) of the 110 children who underwent inpatient screening. The interval between discharge from the hospital and the first attendance at the local audiology clinic for these children is shown in Fig 1. The median interval was 8 weeks (range, 1 to 34 weeks). Children with hearing loss at the time of discharge from the hospital were followed by both the local audiology services and the study investigators. The results of both sets of follow-up data were consistent. The 2 children with sensorineural deafness have persistent severe to profound cochlear hearing impairments (pure tone averages of 70 and 100 dB nHL in the best ear). Three of the 5 cases of conductive hearing loss have resolved. Children with normal hearing at discharge from the hospital were followed by their local audiology services. Two new cases of conductive hearing loss were reported, but no new cases of sensorineural hearing loss were detected.
Interval between discharge from hospital and first attendance for audiologic follow-up.
DISCUSSION
In this study, we attempted to record OAEs from a large, representative sample of British children in the recovery phase of acute bacterial meningitis. Our main findings were that inpatient OAE screening for postmeningitic hearing loss is both feasible and effective. Regarding the feasibility of OAE screening, we found that the technique was well tolerated by the patients and was considerably easier to perform than ABRs. Technically acceptable recordings were obtained from 90% of the children tested. This attainment rate is comparable to those obtained in OAE screening studies in populations of healthy children and neonates.22,24–26
There have been two previous studies of OAE screening in children with meningitis.20,,27 These have produced conflicting information about the feasibility of the technique in this population. In the first study, Fortnum et al27 attempted to record OAEs from children shortly before discharge from the hospital. They were able to obtain satisfactory recordings from only 28 of the 53 patients studied. The low attainment rate was attributed to poor compliance, and the authors suggested that children in the recovery phase of bacterial meningitis are too irritable to tolerate the test procedure. More recently, François et al20 reported on their experience of OAE screening in 39 young children who were seen in an audiology clinic several weeks after discharge from the hospital. In this study the authors obtained satisfactory OAE recordings from all but 2 of the children. The findings of these two studies suggested that the timing of the screening test may be critical.20However, the high attainment rate in our study shows that children can tolerate the test procedure during the recovery phase of meningitis. It is therefore likely that the variation in attainment rates is because of other factors. There were considerable differences in equipment and technique between the studies, and it may be that the later studies have been more successful because of advances in OAE technology and methodology.22
This study was the first to obtain values for the sensitivity and specificity of OAE screening in children recovering from meningitis. In previous studies the results of OAE screening have not always been compared with an accurate, objective measurement of hearing threshold. In our study, OAEs were compared with the gold standard of ABRs. We found that all children with hearing loss failed to produce OAEs and that 91% of those with normal hearing did produce emissions. In other words, OAE screening had a sensitivity of 1.00 and a specificity of 0.91. Such a high sensitivity is clearly desirable in a screening test. This sensitivity value should, however, be interpreted with some caution because only 7 of the 110 children studied had hearing loss (and only 2 of these had sensorineural deafness). Nevertheless, OAEs have proven effective in identifying cases of postmeningitic hearing loss in a number of previous studies,20,,22,27,28 and there have been no reports of patients with postmeningitic deafness passing an OAE test. Furthermore, OAEs have also been shown to be highly sensitive in screening other populations of children and neonates.17,,18
One type of sensorineural deafness that could be missed by OAE screening is retrocochlear hearing loss, where the pathologic lesion is in the auditory nerves or higher centers.18,,29 Emissions may be produced in retrocochlear hearing loss because the generation of OAEs is not dependent on an intact nervous system. In the past it was often thought that such lesions were responsible for postmeningitic deafness. However, it is now clear from pathologic, experimental, and clinical studies that most, if not all, cases of postmeningitic hearing loss are caused by lesions of the cochlea.21,30–32 It is therefore unlikely that many cases of postmeningitic deafness would be missed by an OAE screening program.
The specificity of OAEs in this study, at 0.91 (95% confidence interval, 0.85 to 0.97), is satisfactory for a screening test of hearing status. The figure is similar to those obtained in studies in which OAEs and ABRs have been compared in neonatal screening programs.24,,26 Similar figures have also been obtained in studies of healthy older children.22,,25
In the past, there have been concerns about the specificity of OAE screening for sensorineural hearing loss because patients with conductive hearing loss may also fail the test.18 It was thought that this would be a particular problem in postmeningitic screening because of a reported association between bacterial meningitis and otitis media with effusion.27 However, in this study, only 5 children failed the OAE screening test because of conductive hearing loss. Moreover, other results from our study suggest that children with acute bacterial meningitis do not have an excess of middle ear effusions.33 Thus, although children with conductive defects may fail an OAE screening test, the numbers involved would not be great.
As well as calculating the sensitivity and specificity of OAE screening, we also obtained positive and negative predictive values for the test. The positive predictive value, which is the proportion of patients who fail the screening test and actually have hearing loss, was 0.44. In other words, more than half of the children who failed the test had normal hearing. Although this may seem disappointing, it should be noted that the positive predictive value of a screening test is dependent on the prevalence of the condition of interest. In this population, hearing loss was uncommon and the positive predictive value was correspondingly low. It should also be noted that only 9 of 103 children with normal hearing failed the test. Thus, the absolute number of children with normal hearing referred for further investigation would not be great. The negative predictive value of the OAE screening test was highly satisfactory at 1.00 (95% confidence interval, 0.96 to 1.00). This reflects the fact that all 94 children who passed the OAE test had normal hearing. The negative predictive value obtained in this study confirms that children who pass the screening test are highly unlikely to have hearing loss, and do not therefore need urgent referral for further investigation.
One of the major findings of this study was that predischarge hearing tests are possible in children recovering from meningitis. We believed it was important to perform inpatient screening because up to 25% of children who have had meningitis do not receive audiologic follow-up.5–7 We reasoned that the proportion of children tested could be increased by performing the tests before the children left the hospital. In fact, >90% of the children in this study did have a follow-up hearing test but this may be explained by the fact that we tried to ensure that follow-up tests were performed as part of the study protocol. We therefore continue to believe that more children would be tested by an inpatient screening program.
Inpatient screening also avoids delays in the diagnosis of postmeningitic hearing loss. This is important because late diagnosis of postmeningitic hearing loss may prevent optimal audiologic rehabilitation. Cochlear implantation, for example, can partially restore hearing in postmeningitic deafness, but the procedure may be ineffective if not performed promptly.10,,11 One British study found that 40% of children referred to the audiology services had to wait more than 3 months for their first hearing test.7 In our study half the children waited for more than 2 months. It is clear that inpatient OAE screening could identify those at risk of sensorineural deafness and prevent these excessive delays.
In the past there have been isolated reports of postmeningitic hearing loss developing after a patient has been discharged from the hospital. Cases have even been described in which deafness develops several years after the illness.1 If hearing loss were to develop after discharge from the hospital, this would undoubtedly limit the usefulness of inpatient screening. Fortunately, the evidence suggests that sensorineural hearing loss rarely develops at this late stage. For instance, there have been no cases of late deafness in a number of prospective studies.3,,13,14 Other reports have shown that sensorineural deafness usually develops early in the course of the disease.21,,34 Hearing loss can, in fact, be detected within hours of admission to the hospital. It therefore seems that the development of deafness weeks or months after meningitis is an unlikely event. For these reasons we believe that inpatient screening should not miss many cases of sensorineural hearing loss.
Another phenomenon that could lessen the value of early OAE screening is reversible postmeningitic deafness. During the 1980s several investigators found that up to one-third of patients with bacterial meningitis had a hearing defect that lasted for several weeks or months and then resolved.3,12–14 The cause of this reversible hearing loss was uncertain. Some authors believed that the condition was sensorineural,12,,13 whereas others, such as Dodge et al,3 thought that it was conductive. Clearly, if reversible hearing loss is sensorineural, a large number of children would be identified by an inpatient screening program and then referred for urgent audiologic assessment and possible cochlear implantation. Fortunately, most of the evidence suggests that reversible hearing loss is conductive rather than sensorineural.1,,33,35 In any event, reversible hearing loss is unlikely to be confused with permanent postmeningitic deafness at the time of diagnostic audiologic assessment because it tends to be less severe.13 It is therefore unlikely that reversible hearing loss would seriously disrupt an inpatient OAE screening program.
CONCLUSION
We believe that inpatient OAE screening for postmeningitic hearing loss is a promising development. Such an OAE screening program should allow the great majority of children with hearing loss to be identified and referred for urgent audiologic assessment. This assessment should include an accurate determination of hearing threshold by ABRs or audiometry. As in this study, a combination of OAEs, ABRs, otoscopy, and tympanometry should also be used to identify the site of the auditory lesion. Children with confirmed sensorineural hearing loss could then be considered for early cochlear implantation. To date, the number of children with hearing loss that have been tested by OAEs is limited, and it remains possible that some children with postmeningitic hearing loss could pass an OAE screening test. It is also possible that a small number of patients could develop hearing loss after discharge from the hospital. For these reasons, we recommend that children who pass an OAE screening test should continue to be followed-up routinely. As more data is gathered, it may become apparent that children who pass the screening program can be confidently discharged from the hospital without further audiologic follow-up.
In summary, we have shown that OAE screening is feasible in children recovering from bacterial meningitis. The screening test itself is highly sensitive and reasonably specific for postmeningitic hearing loss. We have also demonstrated that inpatient testing for postmeningitic hearing loss is desirable, practical, and safe.
ACKNOWLEDGMENTS
Dr Richardson was supported by grants from the South and West Regional Health Authority and the Bath Unit for Research into Paediatrics.
We wish to thank the pediatricians, audiologists, and microbiologists at the participating centers in the United Kingdom: Basingstoke District Hospital (Basingstoke), Royal United Hospital (Bath), Princess of Wales Hospital (Bridgend), Royal Hospital for Sick Children (Bristol), Southmead Hospital (Bristol), University Hospital of Wales (Cardiff), Llandough Hospital (Cardiff), Cheltenham General Hospital (Cheltenham), West Dorset Hospital (Dorchester), Royal Devon and Exeter Hospital (Exeter), Gloucestershire Royal Hospital (Gloucester), Prince Charles Hospital (Merthyr Tydfil), East Glamorgan Hospital (Pontypridd), Poole Hospital (Poole), St Mary's Hospital (Portsmouth), Salisbury District Hospital (Salisbury), Southampton General Hospital (Southampton), Singleton Hospital (Swansea), Princess Margaret Hospital (Swindon), Taunton and Somerset Hospital (Taunton), and Royal Hampshire County Hospital (Winchester).
Footnotes
- Received March 4, 1998.
- Accepted June 29, 1998.
Reprint requests to (M.P.R.) Paediatric Infectious Diseases Unit, St George's Hospital, London SW17 0QT, United Kingdom.
- ABR =
- auditory brainstem response •
- OAE =
- otoacoustic emission •
- dB nHL =
- decibels normal hearing level
REFERENCES
- Copyright © 1998 American Academy of Pediatrics