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Brainstem electric response audiometry in newborns
Iniernational Journal of Pediatric Otorhinolaryngologv, Elsevier Biomedical Press
4 ( 1982) 3 17-323
317
Brainstem electric response audiometry in newborns H.P. Pauwels, M. Vogeleer, Department
P.A.R. Clement, L. Kaufman.
P.J. Rousseeuw
and
of E.N. T., Centre for Statistics and Operational Research, V. V. (Free University Brussels). Laarbeeklaan 101, 1090 Brussels (Belgium) (Received March 5th, 1982) (Accepted May 19th, 1982)
Summary
Brainstem electric response audiometry (BERA) was performed as a screening procedure for the assessment of hearing of 523 neonates. It is shown that binaural stimulation gives a higher percentage of interpretable records. A statistical analysis was made of CT, (I-III) and CT, (I-V) as a function of gestational age, conceptional age, birth weight, sex, Apgar score, bilirubinaemia and perinatal pathology.
Introduction
Brainstem electric response audiometry (BERA) was first adopted for use in the newborn by Hecox and Galambos [3]. These workers had come to the conclusion that the recording of the various brainstem waves was sufficiently reliable and constant to warrant the use of this technique as an objective testing method in the measurement of the auditory function in neonates. The latency of the various waves in neonate infants varies according to two parameters: (1) as stimulus intensities increase, a decrease in latency is observed, and (2) the maturity of the brainstem plays a role. Salamy and McKean (6) described the decrease in latency of the I-V time. This I-V time declines from the time of birth to the age of one year, when it reaches the adult level. Various authors [1,4,8-lo] presented the change in latency of V as a function of conceptional age, whether the child was born pre-term or at full term. The shortening of the V wave latency during maturation was calculated by these authors, and was found to vary between 0.05 and 0.5 ms/week in the period immediately after birth, depending on the author. The purpose of this study is to determine whether BERG can be carried out as a screening procedure for deafness in the newborn. 0165-5876/82/0000-0000/$02.75
0 1982 Elsevier Biomedical
Press
318
Materials and Methods The babies studied (test subjects, n = 532) were all born in the Brussels Free University (A.Z.-V.U.B.) maternity unit in the course of the year 1980 and in the first 4 months of 1981. No selection criteria were applied. The newborn children were brought in their cots to the E.N.T. unit soon after mealtime. They were tested during sleep. The average duration of the procedure was 16 min [ 121. Gestational age varied between 36 and 42 weeks, and conceptional age between 37 and 43 weeks. The infants were placed in a sound-proof cabin, which contained only the preamplifier. Paste-on surface electrodes were positioned over the mastoid bones and on the forehead. The signal used was a 0.17 ms click produced by a Magnetic Shielddeck Headset MSH 87. The responses of 2000 stimuli were averaged by means of a clinical Madsen of the ERA 74 type. For the second group, a Madsen of the ERA 2550 type was used. In the first group of 300 infants, the left and right ears were tested separately (monaural stimulation), while in the second group of 223 children binaural stimulation was used. Test intensities were 90, 60 and 30 dB HL for the first group, and 90, 70, 50 and 30 dB HL for the second group. The following clinical information could be obtained only in 178 infants of the first group: gestational and conceptional age, weight at birth, perinatal pathology such as asphyxia, Apgar score and presence of a pathological icterus neonatorum.
Rli!SUltS Interpretability
of screening procedure
In the first group interpretable results were obtained on at least one side in 212 infants (70.0%). The criteria used to determine interpretability were the presence of wave III and wave V at 90 dB HL, and the fact that these were again found at the lower stimulation intensities. CT,* averages 2.772 ms (S.D.= 0.21) and CT, * averages 5.126 ms (S.D.= 0.274). Using binaural stimulation (CT, = 5.227 ms) we obtained reliable recordings in 189 (84.0%) of the second group of infants. L-ejt 11sright difference
A statistical analysis of the data collected from the 178 infants of the first group was made. We first checked whether latency times (CT, and CT,) on the left and right sides correlated well, and whether they showed any systematic variation from one another (Table I). This allowed, for each test subject, to use only one variable (left or right) in case the other was missing, or to use the mean value of both left and right ears in case both were available.
* CT, is the latency of wave III minus wave I, while CT, is the latency of wave V minus wave I.
319 TABLE
I
CORRELATION
BETWEEN
There is no systematic Correlation CT, (right)-CT, CT, (right)--CT, Two sided paired CT, (right)-CT, CT, (right)-CT,
variation
THE LATENCIES between
OF THE LEFT AND
THE RIGHT
SIDE
sides.
(left): 0.495 (P =O.OOl) (left): 0.618 (P =O.OOl) f-tests (left): P =0.634 (left): P =O.llO
CT, and CT, as a function of sex CT, was measured in 83 female and 95 male infants, and CT, in 52 female and 63 male infants. Table II shows that CT, is significantly shorter in female babies, while CT, is almost significantly shorter. CT, and CT, as a function of age and birthweight In this case, 3 parameters were used: gestational age, conceptional age and weight at birth. Table III shows that CT, and CT, follow gestational age better than conceptional age (Fig. 1). Clinical parameters The clinical data collected, i.e. perinatal asphyxia, Apgar score and icterus neonatorum, were recorded as binary variables, i.e. they were recorded only insofar as they were pathological or not. From Table IV follows that: (a) With respect to asphyxia, a significant difference was found in the distribution of CT,: a lengthening of latency time was observed in the pathological group, and a one-sided test gave a nearly significant result (P = 0.063). (b) The above observations also hold for the pathological Apgar score (P = 0.072). (c) A significantly higher value of CT, (P = 0.009) was noted in the group of infants who showed an abnormally high level of bilirubinaemia in the postnatal
TABLE
II
CT, AND
CT, CT,
CTs AS A FUNCTION
OF SEX
Sex
n
Mean
F M F M
83 95 52 63
2.72 2.81 5.08 5.15
Significance
P=O.o01 P =0.085
320
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.--Lq-+-a-,
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TABLE
III
CT, AND CI’, AS A FUNCTION
OF AGE. Gestational
Conceptional
age
age
coefficient
-0.151 P =0.031
-0.119 P =0.072
coefficient
-0.312 P =O.OOl
-0.178 P = 0.038
Birth weight
CT, Pearson correlation Significance CT, Pearson correlation Significance
TABLE
-0.306 P =O.cHll
IV
CT, and CT, ARE CORRELATED
WITH
CLINICAL
CT,
DATA
CT,
n
Mean
S.D.
n
Mm
S.D.
ASPHYXIA Not present Present
163 15
2.76 2.91
0.18 0.36
105 10
5.12 5.13
0.28 0.2 1
APGAR Normal Abnormal
158 20
2.76 2.88
0.18 0.34
100 15
5.11 5.20
0.27 0.28
BILIRUBINE Normal Abnormal
160 18
2.77 2.82
0.21 0.19
102 13
5.10 5.29
0.26 0.34
period. Infants with a pathological Apgar score, perinatal asphyxia and bilirubinaemia had a mean gestation age that did not exceed the general mean.
Discussion
The time difference between the various waves (mainly CT, and CT,) is generally adopted as a yardstick of brainstem maturity [lo]. Cox et al. [l] found that CT, showed a tendency to become heterogeneous in the various age groups below 4 months of age. In the literature one finds only a discussion of the variation of wave V as a function of age, while the variation of CT, is never studied [1,3,8-lo]. Our study points to a difference when we take CT, and CT, as a function of gestational age or of conceptional age.
322
A possible explanation could be that the early postnatal period introduces a change in the maturation rate of the brainstem. Depending on the gestational age, CT, falls by 0.024 ms/week, and CT, by 0.068 ms/week (for a gestational age which varies between 36 and 42 weeks). Depending on the conceptional age (37-42 weeks), CT, falls by an average of 0.037 ms/week. The difference between males and females confirms the findings of Cox et al. [l]. However, in our own study this difference is not so considerable.
At the Conference on Newborn Hearing Screening, held in San Francisco in 1971, the consensus was reached that no acceptable technique existed for an objective and reliable screening procedure. Schulman-Galambos and Galambos [9] and Samo and Clemis [7] took the same stand when they described BEBA as the technique that would meet the various criteria for objectivity and reliability, although their view was that BEBA did not meet the criteria of mass screening of a defect that occurs with a frequency of 1: 1000. These authors suggested that only those children who are in the higher risk bracket should qualify for screening. In such a group, the incidence goes up to 1: 50, and this proportion warrants the high technicity of the procedure. If screening, however, is restricted only to the high risk group, one must accept the fact that about 50% of the deaf neonates will be missed. It is a well-recognized fact that during the past ten years the importance of the hereditary group of deaf children is increasing. This group does not represent a high risk group [2,111. Naturally, by screening the babies at birth, the hearing losses which occur during the first year of life, will be missed. Most of these acquired hearing losses will be obvious, e.g. because of a history of infection (otitis media, meningitis, scarlet fever, measles, etc.) or trauma. Whether inherited recessive hearing loss will develop during the first year of life, still remains an open question. When BEIU is used in newborns to evaluate the hearing threshold on both sides, the procedure will be both costly and time consuming [8]. From the results of our first group of infants, it is clear that in a screening procedure (to detect a threshold lower than 50 dB without hearing loss), the number of recordings that elude interpretation is too high (30%) in a once-only test. This is why we switched to the binaural stimulation which enabled us to cut down the number of rejectable recordings by half. The reason for the rejection of recordings was the difficulty of interpretation of the different waves due to unrest of the baby. Because of the high standard of our criteria we had a rejection rate of 16%. These children were retested a few days later before leaving the maternity unit until a satisfactory record was obtained. Pelzman and Patterson [5] have developed a simplified apparatus with the help of the Infant Hearing Assessment Foundation. This equipment was specifically designed to test newborn babies and can be operated by non-specialists. - We feel that this is an avenue that has to be further explored so as to develop an
323
apparatus that would be specifically designed for mass screening. This is the only condition for the development of programs that will meet all the criteria of an objective and reliable screening procedure.
Acknowledgements
This paper was presented at the XIIth World Congress of Oto-, Rhino-, Laryngology, held on June 2 I-27, 198 1, Budapest, Hungary.
References I Cox, C., Hack, M. and Metz, D., Evoked response audiometry normative data from preterm infants, Audiology, 20 (1981) 53-64. 2 Cremers, C.W.R. and Geerts, S.J., Erfehjkheid en Vroegkinderhjke Doofheid of Slechthorendheid, De Tijdstroom, Poperingen (Belgium), 1980, 34 pp. R., Brainstem auditory evoked responses in human infants and adults, 3 Hecox, K. and Galambos, Arch. Otolaryng., 99 (1974) 30-33. B., Schulman-Galambos, C. and Galambos, R., Brainstem auditory evoked responses in 4 Mokotoff, children, Arch. Otolaryn., 103 (1977) 38-43. C.D., Infant hearing assessment-Clinical application by volunteers, 5 Peltzman, Ph. and Patterson, presented at the XVth International Congress of Audiology, Krakow (Poland), Sept. 1980. of the human brainstem potentials during the 6 Salamy, A. and McKean, C.M., Post-natal development first year of life, Electroenceph., clin. Neurophysiol., 40 (1976) 418-426. of neonatal hearing impairment, 7 Samo, C. and Clemis, J., A workable approach to the identification Laryngoscope, 90 (1980) 1313-1320. C. and Galambos, R., Brainstem auditory evoked response in premature infants, 8 Schulman-Galambos, J. Speech Res., 18 (1975) 456-465. C. and Galambos, R., Brainstem evoked response audiometry in newborn 9 Schulman-Galambos, hearing screening, Arch. oto-laryng., 105 (1979). of auditory function in newborn 10 Starr, A., Amlie, R.N., Martin, W.H. and Sanders, S., Developments infants as revealed by auditory potentials, Pediatrics, 60 (1977)83 I-839. N., La deficience auditive et le conseil genetique, Acta oto-rino-laryng. belg., 31 11 Van Regemorter, (1977) 169-182. 12 Vogeleer, M., Pauwels, H.P., Clement, P., Kaufman, L. and Rousseeuw, P.J., Brainstem evoked responses as an audiometric screening procedure in neonates, in press.
4 ( 1982) 3 17-323
317
Brainstem electric response audiometry in newborns H.P. Pauwels, M. Vogeleer, Department
P.A.R. Clement, L. Kaufman.
P.J. Rousseeuw
and
of E.N. T., Centre for Statistics and Operational Research, V. V. (Free University Brussels). Laarbeeklaan 101, 1090 Brussels (Belgium) (Received March 5th, 1982) (Accepted May 19th, 1982)
Summary
Brainstem electric response audiometry (BERA) was performed as a screening procedure for the assessment of hearing of 523 neonates. It is shown that binaural stimulation gives a higher percentage of interpretable records. A statistical analysis was made of CT, (I-III) and CT, (I-V) as a function of gestational age, conceptional age, birth weight, sex, Apgar score, bilirubinaemia and perinatal pathology.
Introduction
Brainstem electric response audiometry (BERA) was first adopted for use in the newborn by Hecox and Galambos [3]. These workers had come to the conclusion that the recording of the various brainstem waves was sufficiently reliable and constant to warrant the use of this technique as an objective testing method in the measurement of the auditory function in neonates. The latency of the various waves in neonate infants varies according to two parameters: (1) as stimulus intensities increase, a decrease in latency is observed, and (2) the maturity of the brainstem plays a role. Salamy and McKean (6) described the decrease in latency of the I-V time. This I-V time declines from the time of birth to the age of one year, when it reaches the adult level. Various authors [1,4,8-lo] presented the change in latency of V as a function of conceptional age, whether the child was born pre-term or at full term. The shortening of the V wave latency during maturation was calculated by these authors, and was found to vary between 0.05 and 0.5 ms/week in the period immediately after birth, depending on the author. The purpose of this study is to determine whether BERG can be carried out as a screening procedure for deafness in the newborn. 0165-5876/82/0000-0000/$02.75
0 1982 Elsevier Biomedical
Press
318
Materials and Methods The babies studied (test subjects, n = 532) were all born in the Brussels Free University (A.Z.-V.U.B.) maternity unit in the course of the year 1980 and in the first 4 months of 1981. No selection criteria were applied. The newborn children were brought in their cots to the E.N.T. unit soon after mealtime. They were tested during sleep. The average duration of the procedure was 16 min [ 121. Gestational age varied between 36 and 42 weeks, and conceptional age between 37 and 43 weeks. The infants were placed in a sound-proof cabin, which contained only the preamplifier. Paste-on surface electrodes were positioned over the mastoid bones and on the forehead. The signal used was a 0.17 ms click produced by a Magnetic Shielddeck Headset MSH 87. The responses of 2000 stimuli were averaged by means of a clinical Madsen of the ERA 74 type. For the second group, a Madsen of the ERA 2550 type was used. In the first group of 300 infants, the left and right ears were tested separately (monaural stimulation), while in the second group of 223 children binaural stimulation was used. Test intensities were 90, 60 and 30 dB HL for the first group, and 90, 70, 50 and 30 dB HL for the second group. The following clinical information could be obtained only in 178 infants of the first group: gestational and conceptional age, weight at birth, perinatal pathology such as asphyxia, Apgar score and presence of a pathological icterus neonatorum.
Rli!SUltS Interpretability
of screening procedure
In the first group interpretable results were obtained on at least one side in 212 infants (70.0%). The criteria used to determine interpretability were the presence of wave III and wave V at 90 dB HL, and the fact that these were again found at the lower stimulation intensities. CT,* averages 2.772 ms (S.D.= 0.21) and CT, * averages 5.126 ms (S.D.= 0.274). Using binaural stimulation (CT, = 5.227 ms) we obtained reliable recordings in 189 (84.0%) of the second group of infants. L-ejt 11sright difference
A statistical analysis of the data collected from the 178 infants of the first group was made. We first checked whether latency times (CT, and CT,) on the left and right sides correlated well, and whether they showed any systematic variation from one another (Table I). This allowed, for each test subject, to use only one variable (left or right) in case the other was missing, or to use the mean value of both left and right ears in case both were available.
* CT, is the latency of wave III minus wave I, while CT, is the latency of wave V minus wave I.
319 TABLE
I
CORRELATION
BETWEEN
There is no systematic Correlation CT, (right)-CT, CT, (right)--CT, Two sided paired CT, (right)-CT, CT, (right)-CT,
variation
THE LATENCIES between
OF THE LEFT AND
THE RIGHT
SIDE
sides.
(left): 0.495 (P =O.OOl) (left): 0.618 (P =O.OOl) f-tests (left): P =0.634 (left): P =O.llO
CT, and CT, as a function of sex CT, was measured in 83 female and 95 male infants, and CT, in 52 female and 63 male infants. Table II shows that CT, is significantly shorter in female babies, while CT, is almost significantly shorter. CT, and CT, as a function of age and birthweight In this case, 3 parameters were used: gestational age, conceptional age and weight at birth. Table III shows that CT, and CT, follow gestational age better than conceptional age (Fig. 1). Clinical parameters The clinical data collected, i.e. perinatal asphyxia, Apgar score and icterus neonatorum, were recorded as binary variables, i.e. they were recorded only insofar as they were pathological or not. From Table IV follows that: (a) With respect to asphyxia, a significant difference was found in the distribution of CT,: a lengthening of latency time was observed in the pathological group, and a one-sided test gave a nearly significant result (P = 0.063). (b) The above observations also hold for the pathological Apgar score (P = 0.072). (c) A significantly higher value of CT, (P = 0.009) was noted in the group of infants who showed an abnormally high level of bilirubinaemia in the postnatal
TABLE
II
CT, AND
CT, CT,
CTs AS A FUNCTION
OF SEX
Sex
n
Mean
F M F M
83 95 52 63
2.72 2.81 5.08 5.15
Significance
P=O.o01 P =0.085
320
‘1rl. : d s
I
-.-I-.-.
I
--l--_.d-__i
I ._._l__,_~~_t+H_~~l_,__.
*
I
I
._J4_q-L\--Y-I
I
.--Lq-+-a-,
:
I
,_.-I-,--_.
-.
:
i
.-.-.
I’
f
14 :l
.--. -/..._..._.-. :_-._ f
I
_-c~_._~~_~___~._~_L~._I
.__.-- I .-._I_,_
-.-.
;’
s
.-._.--I-.
I ._,_,_._,__,__.._~ _i : ._..__. / ._._-. :
go
2
I
a
1
c.__.
.--*-_)+rk-
:
C.-.-l_++-+.
-I-I-#q-I.
tl I
.-..,-._,
_._._.
)
-I--
,-..I_.
0
I
d
I
321
TABLE
III
CT, AND CI’, AS A FUNCTION
OF AGE. Gestational
Conceptional
age
age
coefficient
-0.151 P =0.031
-0.119 P =0.072
coefficient
-0.312 P =O.OOl
-0.178 P = 0.038
Birth weight
CT, Pearson correlation Significance CT, Pearson correlation Significance
TABLE
-0.306 P =O.cHll
IV
CT, and CT, ARE CORRELATED
WITH
CLINICAL
CT,
DATA
CT,
n
Mean
S.D.
n
Mm
S.D.
ASPHYXIA Not present Present
163 15
2.76 2.91
0.18 0.36
105 10
5.12 5.13
0.28 0.2 1
APGAR Normal Abnormal
158 20
2.76 2.88
0.18 0.34
100 15
5.11 5.20
0.27 0.28
BILIRUBINE Normal Abnormal
160 18
2.77 2.82
0.21 0.19
102 13
5.10 5.29
0.26 0.34
period. Infants with a pathological Apgar score, perinatal asphyxia and bilirubinaemia had a mean gestation age that did not exceed the general mean.
Discussion
The time difference between the various waves (mainly CT, and CT,) is generally adopted as a yardstick of brainstem maturity [lo]. Cox et al. [l] found that CT, showed a tendency to become heterogeneous in the various age groups below 4 months of age. In the literature one finds only a discussion of the variation of wave V as a function of age, while the variation of CT, is never studied [1,3,8-lo]. Our study points to a difference when we take CT, and CT, as a function of gestational age or of conceptional age.
322
A possible explanation could be that the early postnatal period introduces a change in the maturation rate of the brainstem. Depending on the gestational age, CT, falls by 0.024 ms/week, and CT, by 0.068 ms/week (for a gestational age which varies between 36 and 42 weeks). Depending on the conceptional age (37-42 weeks), CT, falls by an average of 0.037 ms/week. The difference between males and females confirms the findings of Cox et al. [l]. However, in our own study this difference is not so considerable.
At the Conference on Newborn Hearing Screening, held in San Francisco in 1971, the consensus was reached that no acceptable technique existed for an objective and reliable screening procedure. Schulman-Galambos and Galambos [9] and Samo and Clemis [7] took the same stand when they described BEBA as the technique that would meet the various criteria for objectivity and reliability, although their view was that BEBA did not meet the criteria of mass screening of a defect that occurs with a frequency of 1: 1000. These authors suggested that only those children who are in the higher risk bracket should qualify for screening. In such a group, the incidence goes up to 1: 50, and this proportion warrants the high technicity of the procedure. If screening, however, is restricted only to the high risk group, one must accept the fact that about 50% of the deaf neonates will be missed. It is a well-recognized fact that during the past ten years the importance of the hereditary group of deaf children is increasing. This group does not represent a high risk group [2,111. Naturally, by screening the babies at birth, the hearing losses which occur during the first year of life, will be missed. Most of these acquired hearing losses will be obvious, e.g. because of a history of infection (otitis media, meningitis, scarlet fever, measles, etc.) or trauma. Whether inherited recessive hearing loss will develop during the first year of life, still remains an open question. When BEIU is used in newborns to evaluate the hearing threshold on both sides, the procedure will be both costly and time consuming [8]. From the results of our first group of infants, it is clear that in a screening procedure (to detect a threshold lower than 50 dB without hearing loss), the number of recordings that elude interpretation is too high (30%) in a once-only test. This is why we switched to the binaural stimulation which enabled us to cut down the number of rejectable recordings by half. The reason for the rejection of recordings was the difficulty of interpretation of the different waves due to unrest of the baby. Because of the high standard of our criteria we had a rejection rate of 16%. These children were retested a few days later before leaving the maternity unit until a satisfactory record was obtained. Pelzman and Patterson [5] have developed a simplified apparatus with the help of the Infant Hearing Assessment Foundation. This equipment was specifically designed to test newborn babies and can be operated by non-specialists. - We feel that this is an avenue that has to be further explored so as to develop an
323
apparatus that would be specifically designed for mass screening. This is the only condition for the development of programs that will meet all the criteria of an objective and reliable screening procedure.
Acknowledgements
This paper was presented at the XIIth World Congress of Oto-, Rhino-, Laryngology, held on June 2 I-27, 198 1, Budapest, Hungary.
References I Cox, C., Hack, M. and Metz, D., Evoked response audiometry normative data from preterm infants, Audiology, 20 (1981) 53-64. 2 Cremers, C.W.R. and Geerts, S.J., Erfehjkheid en Vroegkinderhjke Doofheid of Slechthorendheid, De Tijdstroom, Poperingen (Belgium), 1980, 34 pp. R., Brainstem auditory evoked responses in human infants and adults, 3 Hecox, K. and Galambos, Arch. Otolaryng., 99 (1974) 30-33. B., Schulman-Galambos, C. and Galambos, R., Brainstem auditory evoked responses in 4 Mokotoff, children, Arch. Otolaryn., 103 (1977) 38-43. C.D., Infant hearing assessment-Clinical application by volunteers, 5 Peltzman, Ph. and Patterson, presented at the XVth International Congress of Audiology, Krakow (Poland), Sept. 1980. of the human brainstem potentials during the 6 Salamy, A. and McKean, C.M., Post-natal development first year of life, Electroenceph., clin. Neurophysiol., 40 (1976) 418-426. of neonatal hearing impairment, 7 Samo, C. and Clemis, J., A workable approach to the identification Laryngoscope, 90 (1980) 1313-1320. C. and Galambos, R., Brainstem auditory evoked response in premature infants, 8 Schulman-Galambos, J. Speech Res., 18 (1975) 456-465. C. and Galambos, R., Brainstem evoked response audiometry in newborn 9 Schulman-Galambos, hearing screening, Arch. oto-laryng., 105 (1979). of auditory function in newborn 10 Starr, A., Amlie, R.N., Martin, W.H. and Sanders, S., Developments infants as revealed by auditory potentials, Pediatrics, 60 (1977)83 I-839. N., La deficience auditive et le conseil genetique, Acta oto-rino-laryng. belg., 31 11 Van Regemorter, (1977) 169-182. 12 Vogeleer, M., Pauwels, H.P., Clement, P., Kaufman, L. and Rousseeuw, P.J., Brainstem evoked responses as an audiometric screening procedure in neonates, in press.