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Advances in Medical Sciences 59 (2014) 9094

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Advances in Medical Sciences


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Original Research Article

Second stage of Universal Neonatal Hearing Screening A way for diagnosis and
beginning of proper treatment for infants with hearing loss
Magdalena Lachowska *, Paulina Surowiec, Krzysztof Morawski, Katarzyna Pierchaa,
Kazimierz Niemczyk
Department of Otolaryngology, Hearing Implant Center, Medical University of Warsaw, Warsaw, Poland

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 26 November 2012
Accepted 5 September 2013
Available online 25 March 2014

Purpose: To analyze retrospectively the results of hearing testing in infants at the second stage of the
Polish Universal Neonatal Hearing Screening Program carried out in the Department of Otolaryngology
at the Medical University of Warsaw.
Material/methods: A total of 351 infants referred to our Department for the second stage of UNHS were
included in the study. There were 39.60% infants referred due to positive result of hearing screening at
the rst stage of the Program performed in neonatal units, 55.27% with negative screening but risk
factors present, and 5.13% without any tests due to equipment failure in the maternity unit.
Results: Risk factors were identied in 86.61% of the infants. The most frequent ones were
hyperbilirubinemia (71.51%), premature birth (63.25%), and ototoxic medication (62.11%). Otoacoustic
emission test showed fail results in 17.66% of the infants, and auditory brainstem responses conrmed
hearing loss in 16.81%. Correlation between risk factors and conrmed hearing loss was found for
hyperbilirubinemia, low birth weight, intensive therapy for at least 7 days, low Apgar scores, and
craniofacial abnormalities.
Conclusions: The early identication of infants with hearing loss is essential for early intervention. Not
only infants who fail the initial screening but also the ones with risk factors of hearing impairment
should be referred to the centers that are capable of providing the necessary diagnostic services required
for the second stage of the UNHSP. Those two steps are needed to both minimize the risk of overlooking a
child with hearing loss and properly diagnose hearing impairment.
2014 Medical University of Bialystok. Published by Elsevier Urban & Partner Sp. z o.o. All rights
reserved.

Keywords:
Screening
Hearing loss
Infants
Early detection
Otoacoustic emission
Auditory brainstem response

1. Introduction
High incidence of hearing loss among newborns draws our
attention. Current statistics indicate an overall hearing impairment
rate of 13 in 1000 live births in healthy newborns nursery and 24
in 100 in neonatal intensive care units. Hearing impairment in
children, undiagnosed or diagnosed with delay, may negatively
result in childs language, cognitive, social, emotional, and
academic development. The hearing loss itself and its mentioned
negative results may signicantly affect the childs quality of life.
When hearing impairment is diagnosed early and proper
intervention is undertaken, children with hearing loss are likely

* Corresponding author at: Department of Otolaryngology, Hearing Implant


Center, Medical University of Warsaw, Banacha 1a, 02-097 Warsaw, Poland.
Tel.: +48 22 599 2521; fax: +48 22 599 2523.
E-mail address: mlachowska@wum.edu.pl (M. Lachowska).

to make great progress, and be more successful in life. Recent


advances in technology made the Universal Newborns Hearing
Screening (UNHS) feasible and enabled early intervention of
congenital hearing impairment. It is one of the greatest advances in
medicine of the last century [15].
The Joint Committee on Infant Hearing 2000 Position Statement
[6] with later update in 2007 [7] and supplement in 2013 [8]
includes guidelines for the development of Early Hearing Detection
and Intervention programs. These guidelines specify recommendations for the audiologic tests in infants with negative results of
hearing screening. They also recommend accurate further interventions depending on the nal hearing diagnosis. The audiologic
tests include auditory brainstem response (ABR), otoacoustic
emission (OAE), impedance audiometry including tympanometry
with high frequency probe stimuli, and acoustic reexes.
Polish Universal Neonatal Hearing Screening Program (UNHSP)
started back in 2002. It was initiated by a group of Polish
otorhinolaryngologists and neonatologists with a great support

http://dx.doi.org/10.1016/j.advms.2014.02.002
1896-1126/ 2014 Medical University of Bialystok. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved.

M. Lachowska et al. / Advances in Medical Sciences 59 (2014) 9094

from The Great Orchestra of Christmas Charity Foundation. From


the very beginning, it covered all neonatal units in Poland using
transient evoked otoacoustic emission (TEOAE) as a tool for
hearing screening. TEOAE is performed in all newborns in their
second or third day of life. With years, almost all newborns and
infants (9698.5%) are screened for hearing impairment [9,10]. The
UNHS Program was created to meet three main purposes, that is, to
detect, diagnose and treat. The rst purpose is to detect hearing
loss in newborns before they leave the neonatal units and identify
neonates with normal hearing but with hearing loss risk factors in
their perinatal history. The newborns who do not meet the TEOAE
pass criteria and/or have hearing loss risk factors are referred to the
second stage of the Program the diagnostic process. It is at the
same time the second purpose of the Program, i.e., to verify positive
results from the rst stage, establish nal diagnosis of hearing loss,
and refer patients for treatment. Not only neonates with positive
TEOAE results are referred to the second stage, but also those with
hearing loss risk factors and those that skip TEOAE rst screening
regardless of reasons. According to the Program, no child is missed
from screening at this point and the possibility of overlooking
subjects with hearing loss due to the risk factors in their early life is
limited. The Polish UNHSP is carried out very carefully. It prevents
the exclusion of children with various degrees of hearing
impairment. The third purpose of the Program (third stage) is to
provide the child with hearing aids, and/or introduce proper
treatment, including surgical treatment with cochlear implants
and rehabilitation [9,10].
Before the Polish UNHSP was introduced, there had been an
earlier successful attempt to create a coordinated care system for
children with hearing impairment [11], but it had its limitations.
The problems mainly resulted from the care system of that time,
limited availability of diagnostic equipment and insufcient
technology. Hearing tests in infants and children were limited
mostly to observing the behavioral response to sound, such as a
ringing bell, and to conducting behavioral audiometry for hearing
thresholds detection in children who were old enough to
participate in such tests. The ABR or OAE was not available at
that time, but since then a lot has changed in the Polish medical
care system and in medicine and technology worldwide. Currently,
even the most modern diagnostic equipment is available in Poland.
The use of objective auditory measurements including auditory
threshold detection in infants and young children enabled early
intervention programs such as The Polish UNHSP.
The Polish UNHSP has been proven to achieve its goals and
prevent the adverse consequences of delayed diagnosis of hearing
loss not only on speech and language, but also on cognitive
development [9].
The purpose of this study was to analyze retrospectively the
results of hearing testing in infants at the second stage of the Polish
UNHSP carried out in the Department of Otolaryngology at the
Medical University of Warsaw by means of hearing loss conrming
diagnosis and hearing loss risk factors.
2. Material and methods
In this retrospective study, we analyzed data of 351 infants who
were referred to our Department for the second stage of the Polish
UNHS Program in the years 20072011. Our Department is one of
those in Poland that meets the criteria of the second stage of the
Program diagnosis of hearing loss in infants referred from the
rst stage. At the same time, it also covers the third stage goal
treatment with cochlear implantation in children and their further
speech and language rehabilitation.
We analyzed the following data: presence of hearing loss risk
factors, results of hearing testing at the second stage (conrmation
of hearing loss diagnosis), false-positive results from the rst stage

91

of the program, and correlation between conrmed hearing loss at


the second stage and risk factors.
Data of each subject were collected using a questionnaire, on
the presence of hearing loss risk factors, answered by the parents of
an infant. Infants were considered to be at risk for hearing loss
based on the recommendations of Joint Committee on Infant
Hearing (JCIH), 1994 Position Statement [12]. The JCIH in its 1994
statement listed 10 risk factors that identify infants who are at the
greatest risk for hearing impairment, in an attempt to optimize
infant hearing screening. The risk factors include the following:
1.
2.
3.
4.

Family history of hearing loss


Craniofacial abnormalities
Low birth weight (less than 1500 g)
Postnatal asphyxia (low Apgar scores of 04 at the 1st minute
or 06 at the 5th minute)
5. Hyperbilirubinemia more than 15 mg/l (including serum level
requiring exchange transfusion)
6. Congenital perinatal TORCH infection
7. Bacterial meningitis or bacteriology-proven sepsis
8. Mechanical ventilation lasting 5 days or longer
9. Ototoxic medication
10. Stigma or other ndings associated with a syndrome known to
include a sensorineural and/or conductive hearing loss
(syndrome associated with congenital hearing loss).
Additionally, we considered premature birth (<33 Hbd) and neonate
intensive therapy for at least 7 days as perinatal risk factors and
included them in the questionnaire.
Hearing testing was performed with transient evoked otoacoustic emission and auditory brainstem response. Otoacoustic
emissions are routinely conducted in our Department as part of the
evaluation of infants failing the rst stage of the newborn hearing
screening. For this purpose we use Distortion Product Otoacoustic
Emission (DPOAE). DPOAE are evoked by two pure tones of slightly
different frequencies (F1 and F2) presented to the ear. Five
different pairs of tones were used to test different regions of the
cochlea covering frequency range from 1500 Hz to 6000 Hz. The
pass criterion was set to be at least 6 dB sound-to-noise ratio (SNR).
We routinely use ABR procedure as a part of the second stage
hearing evaluation, not only when appropriate responses to DPOAE
testing are not obtained but in all cases. The acoustic stimuli used
for ABR consisted of broadband clicks with 100 ms duration and
with alternating polarity. The clicks were delivered monaurally by
a handheld TDH-49 headphone, at a rate of 29.4/s. The analysis
time was 20 ms. The electrode impedance was ensured to be below
5 kV. The ABR protocol consisted of testing each ear at 70, 60, 50,
40, 30, and 20 dBnHL with 5 dB steps at threshold. Thresholds, the
lowest intensity level that evokes an electrophysiologic response,
were established to judge the presence or absence of hearing loss. If
a response was not observed at 70 dBnHL, testing was performed at
80 and 90 dBnHL. An infant was considered to have passed the ABR
test if a replicable wave V response was present at least at
35 dBnHL in both ears. Our facility performs ABR frequencyspecic tests, but we do not use it as a part of the diagnostic
evaluation of infants failing the newborn screening. We use those
tests as immediate follow-up in infants who fail the screening at
the second stage in order to establish hearing thresholds for
frequencies of 500 Hz, 1000 Hz and clicks (a click is considered to
cover the frequency range of 20004000 Hz) and start proper
treatment. All subjects were tested while they were in natural
sleep. Sedation was not used.
Statistical analysis was performed using Statistica software
(StatSoft, Inc., 2011, data analysis software system, Version 10,
Oklahoma, USA). This is a retrospective study and no free informed
consent form for this study was needed; subjects identity was not
divulged.

M. Lachowska et al. / Advances in Medical Sciences 59 (2014) 9094

92

Table 2
ABR thresholds results for infants with conrmed hearing loss.
Hearing loss threshold

40 dBnHL
70 dBnHL

Fig. 1. Prevalence of hearing loss risk factors in studied group of infants.

3. Results
In the analyzed group of 351 infants, 194 (55.27%) were males
and 157 (44.73%) were females. One hundred and thirty-nine
(39.60%) infants were referred to our Department due to the failing
result of the hearing screening test at the rst stage of the Program
performed in a neonatal unit (positive hearing screening test
results). One hundred and ten of them, aside from those results,
presented at least one risk factor. Other 194 (55.27%) infants with
negative screening results at the rst stage were referred due the
hearing loss risk factors alone. The last 18 (5.13%) were referred to
the second stage without any tests at the rst stage due to
equipment failure in the maternity unit. The mean age of all infants
tested in our Department was 3.5 months (SD = 0.94).
We identied risk factors in 304 infants (86.61%) and found that
the majority (256 infants, 72.93%) presented with more than one
risk factor. As shown in Fig. 1, the most frequent risk factors
(prevalence in more than 50% of analyzed infants) observed in the
studied group were hyperbilirubinemia (71.51%), premature birth
(63.25%), and ototoxic medication (62.11%). Less frequent (20
50%) risk factors were low birth weight (31.62%), intensive therapy
for at least 7 days (27.07%), and mechanical ventilation for at least
5 days (22.22%).
DPOAE diagnostic test performed in our Department showed
fail results in 62 infants (17.66%). Testing with ABR method to
establish hearing thresholds conrmed hearing loss in 59 infants
(16.81%) (Table 1), unilateral in 32 infants and bilateral in 27
(Table 2). This means that there were false-positive results at the
rst stage of the Program. Of 139 positive results from the rst
stage, 24 (17.26%) were conrmed as hearing loss at the second
stage, which makes 115 to be false positive (82.73% false positive).
Of 194 infants referred due to the risk factors alone, 35 (18.04%)
were diagnosed with hearing loss presenting thresholds
40 dBnHL. All 59 infants with conrmed hearing loss were
further referred to the third stage meeting the third goal of the
Program the proper treatment. Among those 59 infants with

Number of infants
Unilateral
hearing loss

Bilateral
hearing loss

The sum of the


unilateral
and bilateral

32
7

27
6

59
13

hearing loss, 46 presented moderate hearing loss (thresholds


between 40 and 70 dBnHL) and 13 severe hearing loss (thresholds
>70 dBnHL) (Table 2). Unilateral hearing impairment was found in
54.17% of infants with hearing loss.
In the mentioned 18 infants not tested at the rst stage, all
proved to have normal hearing.
Not all risk factors correlated with the conrmed hearing loss.
Such a correlation (p < 0.05) was found for hyperbilirubinemia,
low birth weight, intensive therapy for at least 7 days, low Apgar
scores, and craniofacial abnormalities, as shown in Table 3.
4. Discussion
Early identication of hearing loss offers children the opportunity to develop signicantly improved language skills compared
with those children who are diagnosed later. Therefore, internationally recommended age for the diagnosis of hearing loss in
children is 3 months of age. If hearing loss is conrmed,
intervention should start as soon as possible, preferably before 6
months of age [15,7]. The Polish UNHS Program follows these
steps.
False-positive rates at the rst stage of UNHS remain
considerably high when newborns are screened with TEOAEs
alone [13]. In our study, the false-positive results from the rst
stage reached 82.73% (from 139 positive results from the rst
stage, 24 were conrmed as hearing loss). We attribute this high
rate to the TEOAE screening being performed before hospital
discharge, which is the second or third day of life. At this age, the
presence of uid in the middle ear, which may be amniotic uid, or
negative pressure in an unventilated middle ear cavity, or debris in
the external ear canal of the newborn may signicantly inuence
the results of otoacoustic emission testing, generating falsepositive results [14]. The large number of false-positive results
coming from TEOAE screening at birth is one of the most serious
weaknesses of hearing screening programs not only in Poland
[15,16]. The other explanation may be attributed to a lack of
experience in system management and population-based care,
and/or failures in the systems data entry [5]. On the other hand,
the choice of the TEOAE methods, as the rst screening test to be
used after birth, arises from the necessity for creating an easy test
that is both functional and does not require a specialist with prior
audiologic experience [9,17]. That is why this rst step does not
constitute a diagnosis and is only the initial component of a much
more complex program that includes referral for follow-up testing.

Table 1
Prevalence of positive and negative hearing loss test results in studied group of infants (n = 351). Outcomes of hearing screening at the second and/or third day of life in the
maternity unit (rst stage of the program), and at the second stage of the Program DPOAE as diagnostic test and ABR click to conrm hearing loss. Out of 351 infants referred
to the second stage, 18 (5.13%) were not tested due to equipment failure at the maternity unit.
TEOAE neonatal screening at 2nd3rd day of
life (results from rst stage)

DPOAE diagnostic test at the second stage

ABR diagnostic test at the second stage

Test result

Number of neonates

Test result

Number of infants

Test result

Number of infants

Pass
Refer

194 (55.27%)
139 (39.60%)

Pass
Refer

289 (82.34%)
62 (17.66%)

Normal hearing
Hearing loss

292 (83.19%)
59 (16.81%)

M. Lachowska et al. / Advances in Medical Sciences 59 (2014) 9094

93

Table 3
Correlation between risk factors and conrmed hearing loss (DPOAE and ABR) at the second stage of the Program.
Risk factor

Number of infants with


given risk factor

Tau

Gamma

Hyperbilirubinemia [>15 mg/l]


Premature birth [<33 Hbd]
Ototoxic medication
Low birth weight [<1500 g]
Intensive therapy for at least 7 days
Hyperbilirubinemia (required transfusion)
Mechanical ventilation for at least 5 days
Postnatal asphyxia (low Apgar scores)
Congenital perinatal TORCH infection
Craniofacial abnormalities
Syndrome associated with congenital hearing loss
Family history of hearing loss
Bacterial meningitis
At least 1 risk factor present

251
222
218
111
95
87
78
57
26
12
7
5
5
304

S0.071*
0.011
0.021
0.104*
0.086*
0.007
0.052
0.112*
0.018
0.083*
0.045
0.010
0.054
0.047

0.048*
0.763
0.551
0.004*
0.017*
0.853
0.150
0.002*
0.609
0.020*
0.210
0.774
0.131
0.189

S0.200*
0.030
0.059
0.276*
0.237*
0.021
0.156
0.340*
0.089
0.442*
0.336
0.108
1.000
0.169

0.048*
0.763
0.551
0.004*
0.017*
0.853
0.150
0.002*
0.609
0.020*
0.210
0.774
0.131
0.189

Strong (signicant) correlation: p < 0.05.

However, to improve the quality results of the rst step in newborn


hearing testing, another automated objective test, i.e., automated
ABR (AABR), might be used as proposed by van Straaten et al. [18].
The purpose of hearing screening at birth is to assure early
identication of hearing loss. If infants with hearing loss cannot be
identied by 3 months of age, it is also likely that the goal of
intervention by 6 months of age may not be met.
The second step diagnostic testing procedures is used to
determine the presence, type, and degree of hearing loss followed
by decisions determining appropriate intervention for the hearing
loss [6]. In Poland, all children with positive test result at the rst
step and all children with risk factors of hearing impairment, aside
from the test results, are referred to the otolaryngology departments within 3 months of life for further and more detailed tests
and therapy when indicated. Our Department offers the second
and third steps of the Program. Here infants are tested once again
with otoacoustic emissions and with ABR. If hearing loss is
conrmed, the proper treatment is implemented, including
surgery with cochlear implantation.
High-risk infants with one or more risk factors as dened by the
JCIH have a substantially higher incidence of hearing loss
compared to normal hearing neonates [12]. Out of all the infants
in our study, tested at the second stage of the Program, risk factors
were identied in 86.61% of them, and more than one risk factor in
72.93%. The most frequent risk factors were hyperbilirubinemia,
premature birth, and ototoxic medication. In the 194 infants
referred due to the risk factors alone, 18.04% diagnostic tests
revealed hearing loss. If those children were missed from the
second stage, their normal language development would be
jeopardized. The earliest possible proper treatment delivery is a
critical factor in optimizing outcomes for children with hearing
impairment. As already mentioned, undetected hearing loss has a
negative impact on language development. Children with hearing
loss fall behind their normal hearing peers in language and
academic achievement, which usually results in lower educational
and job opportunities [1,2,4,5]. In their study, Wroblewska-Seniuk
et al. [19] observed no relative difference in the percentage of
infants with and without risk factors in whom the follow-up test
result was positive. The authors reported that the most common
risk factors were the use of ototoxic drugs, low Apgar score, and
prematurity. However, Aiyer and Parikh [20] showed that the most
frequent risk factors observed were hyperbilirubinemia, craniofacial abnormalities, septicaemia/meningitis, and ototoxic medication. Their data suggest that only craniofacial anomaly in infants is
related to the likelihood of hearing loss. In our study, among the
infants with particular risk factors of having hearing loss, the ones
with hyperbilirubinemia, low birth weight, intensive therapy for at

least 7 days, low Apgar scores, and craniofacial abnormalities


proved to correlate with conrmation of hearing loss. If not
referred to the second stage, most of those children would be
undetected and proper diagnosis could be signicantly delayed. It
is essential for hearing impairment to be recognized as early in life
as possible so that the treatment and rehabilitation process can
take full advantage of the plasticity of the developing central
nervous system. To achieve this goal, close cooperation between
maternity units and audiologic centers, with regard to the
reliability and efcacy of UNHSP, is of great importance.
Another factor worth mentioning, found in this study, is a large
fraction of unilateral hearing loss at the second stage of the
Program (54.17% of all infants diagnosed with hearing loss). It
raises a relevant question regarding the responsible etiological
factor and the genetic factor comes rst in mind. More than 80
genes associated with sensorineural hearing loss are described in
the available literature. Some of the genes are associated with
syndromic and some with nonsyndromic hearing impairment at
birth. The most frequent and important in etiology are GJB2,
SLC26A4 gene and mitochondrial 12S rRNA gene mutations
[21,22]. Some of those genes are important in hearing impairment
related to aminoglycosides treatment. In our study, the group with
ototoxic medication as a risk factor was very large (218 infants). In
our Department, like in many other otolaryngology departments in
Poland, genetic testing is not routinely performed as it is not a
standard test in Poland. In most of the hearing centers, if the
genetic testing is performed, it is usually conducted in cooperation
with another department (which has a genetic laboratory) as a
research project. It raises a question about adding genetic
exploration as an integrated part of the newborn hearing
screening. We assume that this combination would be appropriate
and should raise an important discussion about changes in hearing
screening programs.
Another important issue is congenital cytomegalovirus (CMV)
infection. The newborn mass screening programs that are
obligatory in Poland, as an early detection of congenital diseases,
are hypothyreosis, phenylketonuria, cystic brosis, and hearing
testing. As described in this study, hearing screening is conducted
with the use of otoacoustic emissions. The UNHS Program detects
infants with hearing loss, including those with hearing impairment
caused by congenital infections. CMV infection is a very important
factor to be considered in hearing loss. However, only some
children with hearing loss resulting from CMV may be identied
with the Program due to late onset of hearing impairment. Thus,
the majority of the CMV-associated hearing loss cases may remain
undetected for years. Implementation of screening for congenital
CMV infection seems to be rationed and has recently begun to be

94

M. Lachowska et al. / Advances in Medical Sciences 59 (2014) 9094

explored [2325]. It requires a standardized screening test and a


protocol for follow-up of infected children, including treatment for
the children with symptoms and extensive follow-up in asymptomatic CMV infections (late onset hearing loss and other
disabilities). This subject is currently widely discussed in the
available literature [2325].

[7]

[8]

5. Conclusions
[9]

Early detection of hearing loss in infants offers great benet of


improved speech, language, and cognitive development. Not only
infants who fail the initial screening, but also the ones with risk
factors of hearing impairment in their history should be referred to
the centers that provide the necessary diagnostic services required
for the second stage of the UNHS Program. Those two steps are
needed to both minimize the risk of overlooking a child with
hearing loss and properly diagnose hearing impairment. Early
identication of infants with hearing loss is essential for early
intervention. Although it was not a part of this study, adding
genetic exploration as a part of hearing screening program would
help in identifying children with hearing loss or predisposition to
it. It would also provide information that is relevant to the
prognosis for the child. This problem along with screening for
congenital CMV infection in newborns merits more study and
creative multicenter projects to collect data for supporting future
policy decisions. This issue should be widely discussed.

[16]

Conict of interests

[17]

The authors state that there is no conict of interest, including


any nancial interest.

[18]

Financial disclosure
The authors state that there is no nancial support to be
disclosed.
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