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Long Term Auditory Follow-Up of Preterm Infants after Neonatal Hearing

Screening

Article · July 2019

DOI: 10.24966/NCP-878X/100034

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 de Graaff-Korf KS, et al., J Neonatol Clin Pediatr 2019, 6: 034
DOI: 10.24966/NCP-878X/100034

HSOA Journal of
Neonatology and Clinical Pediatrics
Research Article

Long-Term Auditory Follow-Up of Conclusion

ABR of the better ear at three months PTA in preterm reliably
Preterm Infants after Neonatal seems to predict all types of HL in later childhood as well as the
Hearing Screening hearing level in children with SNHL at follow-up. In case of ANSD the
VRA was not predictive for the severity of HL at follow-up. Further re-
KS de Graaff-Korf1*, MR Benard2, P van Dommelen3 and HLM search is necessary to substantiate these findings in preterm infants.
van Straaten1 Keywords: Auditory brainstem response; Follow-up; Hearing Loss;
Preterm Infants
Department of Neonatology, Isala Women and Children’s Hospital, The
1

Netherlands
2
Pento Speech and Hearing Center Zwolle, Audiologist in Zwolle, Abbreviations
The Netherlands
SNHL - Sensori Neural Hearing Loss
3
Department of Child Health, TNO, Leiden, The Netherlands
CHL - Conductive Hearing Loss
Abstract ANSD - Auditory Neuropathy Spectrum Disorder
PTA - Post Term Age
Background
TOST - Two One-Sided Tests
Since introduction of neonatal Automated Auditory Brainstem Re-
AABR - Automated Auditory Brainstem Response
sponse (AABR) hearing screening in Neonatal Intensive Care Unit
(NICU) graduates, Hearing Loss (HL) is established during the first ABR - Auditory Brainstem Response
few months of age. The diagnostic Auditory Brainstem Response NICU - Neonatal Intensive Care Unit
(ABR) is used as the gold standard in establishing HL after birth. Aim
of this study was to investigate the predictive value of better ear ABR
HL - Hearing Loss
findings at three months Post Term Age (PTA) in preterm infants with VRA - Visual Reinforcement Audiometry
bilateral Sensori Neural (SNHL) or Conductive Hearing Loss (CHL). IVH - Intra Ventricular Hemorrhage
In Preterms with bilateral Auditory Neuropathy Spectrum Disorder
(ANSD) the predictive value of Visual Reinforcement Audiometry
NEC - Necrotising Entero Colitis
(VRA) was investigated.
Introduction
Methods
When Hearing Loss (HL) is diagnosed in the neonatal period it
Outcome data of graduates of a level III NICU, who didn’t pass is essential that interventions are started as early as possible. This
AABR neonatal hearing screening between 2004-2016 were ana-
enables early habilitation, including guidance of parents and fitting
lyzed retrospectively. At follow-up type and hearing level of gradu-
ates with bilateral HL was established. Hearing level was investigat-
of hearing aids, cochlear implants or bone-conduction devices at an
ed at the age of two years using VRA and at four and eight years of early age. This can help the child with normal speech and language
age using play-audiometry. The Two One-Sided Tests equivalence acquisitionwhich leads to improved school achievement, self-esteem
procedure for paired means was applied with the magnitude of the and psychosocial adaption [1,2].
region of similarity equal to 10dB.
A two-step Automated Auditory Brainstem Response (AABR)
Results neonatal hearing screening program was gradually introduced in all
In all 32 cases ABR at three months PTA correctly predicted the Neonatal Intensive Care Units (NICU) in the Netherlands between
final type of HL. In 8 SNHL children initial ABR was equivalent with 1998 and 2001 as a first step towards nation-wide neonatal hearing
the four and eight year’s play-audiometry (p<0.05). In eight SNHL screening [3]. After repetitive referral, audiological diagnostic tests
and 15 ANSD children,VRA levels didn’t reflect significantly play-au- were performed at a Speech and Hearing center to establish neonatal
diometry levels. Almost all cases (89%, N=8/9) with non-syndromic
HL as soon as possible,with in three months Post Term Age (PTA).
CHL recovered properly.
This correction for gestational age is extremely relevant, especially in
*Corresponding author: KS de Graaff-Korf, Department of Neonatology, Isala NICU graduates with an extremely low gestational age. Besides the
Women and Children’s Hospital, The Netherlands, E-mail: [email protected] fact that the stage of the ontogenetic development is related to the du-
Citation: de Graaff-Korf KS, Benard MR, van Dommelen P, van Straaten HLM ration of pregnancy it is reported in literature that the ongoing process
(2019) Long-Term Auditory Follow-Up of Preterm Infants after Neonatal Hearing of myelination of the auditory pathway may be delayed or deviant in
Screening. J Neonatol Clin Pediatr 6: 034. infants who are born prematurely [4-6]. Therefore, we want to inves-
Received: July 11, 2019; Accepted: July 23, 2019; Published: July 30, 2019 tigate the predictive value of the initial diagnostic ABR findings in the
better ear at three months PTA versus the Visual Reinforcement Au-
Copyright: © 2019 de Graaff-Korf KS, et al. This is an open-access article dis- diometry (VRA) results at two years and the play-audiometry results
tributed under the terms of the Creative Commons Attribution License, which at four and eight years of age, with regard to the type and severity of
permits unrestricted use, distribution, and reproduction in any medium, provided
the original author and source are credited. bilateral HL.
Citation: de Graaff-Korf KS, Benard MR, van Dommelen P, van Straaten HLM (2019) Long-Term Auditory Follow-Up of Preterm Infants after Neonatal Hearing
Screening. J Neonatol Clin Pediatr 6: 034.

• Page 2 of 5 •

Methods for paired means was applied with the magnitude of the region of sim-
ilarity equal to 10dB. The null hypothesis was that the differences in
Outcome data from graduates of a single center level III NICU who mean dB levels for the different tests were not equal. P-values <0.05
did not pass AABR neonatal hearing screening between 2004-2016 were considered significant.
were retrospectively analyzed. Although the NICU hearing screening
program was established in 2001, it is only since 2004 that all the pro- Within the group of patients with etiologically temporary conduc-
cedures and measurement protocols are standardized and well doc- tive HL we defined the ABR level to be predictive if at least 75% have
umented. Auditory retesting was performed at approximately three normal hearing (<35dB) on the play-audiometry (at four and eight
months PTA in two dedicated referral Audiological Centers (Pento years).
Speech and Hearing Centres Zwolle and Hengelo, the Netherlands).
This included an extensive diagnostic ABR, Oto-Acoustic Emissions Results
(OAE) and impedance audiometry, to diagnose the severity and type A total of 62 NICU graduates failed neonatal AABR screening of
of HL. During follow-up VRA and play-audiometry were used to in- which 59 (N꞊59/62) bilaterally and three (N꞊3/62) unilaterally (Figure
vestigate possible progression of HL. The quality and timing of this 1). All three graduates with unilateral AABR failure had no HL at
program is guaranteed by the central regulation and registration of diagnostic testing.
data at the Department of Child Health, TNO, Leiden, The Nether-
lands [7]. For this study, auditory follow-up data were collected from Long term follow-up data were available for 34 (N꞊34/59) new-
NICU graduates with established bilateral HL at approximately three borns with diagnosed bilateral HL at a PTA of three months. In 14
months PTA. The data included the results of impedance audiome- (N=14/59) no HL was diagnosed and in 11 (N꞊11/59) the follow-up
try, OAE, diagnostic ABR, VRA at two years, and play-audiometry dataset was in complete due to referral to Speech and Hearing Centers
at four and eight years of age. Informed consent (oral) was obtained outside the region.
from the parents or legal guardians of all participating patients. This
The type and severity of bilateral HL could be diagnosed in 34
study was approved by the Medical Ethics Committee of the Isala
NICU graduates: Nine (N꞊9/34) had CHL, eight (N꞊8/34) had SNHL,
Hospital, Zwolle, The Netherlands (reference number 190508).
15 (N꞊15/34) had ANSD and two (N꞊2/34) had a combination of
Types of hearing loss ANSD and SNHL.

For this study, a distinction is made between Conductive Hear- In this study the last two patients with combined HL were not in-
ing Loss (CHL), Sensori Neural Hearing Loss (SNHL) and Auditory cluded in the results, leaving follow-up data of 32 infants for analysis
Neuropathy Spectrum Disorder (ANSD). (Table 1).

Diagnostic audiological tests

ABR: Auditory brainstem response audiometry reflects the neuronal
activity between the cochlea and the brainstem in response to acoustic
stimuli [8]. Interacoustics Eclipse EP15 (Interacoustics A/S, Middel-
fart, Denmark) was used to measure the ABR responses.

VRA: Visual Reinforcement Audiometry (VRA) is based on the ori-

entation reflex towards a new sound source. It is a subjective audito-
rytest that requires cooperation of the child and parents. Interacoustics
Affinity/AC440 was used (Interacoustics A/S, Middelfart, Denmark)
to present the acoustical stimuli.

Play-audiometry: Play-audiometry is an auditory examination of

children based on conditioned responses. The child is taught to per- Figure 1: Study enrollment.
form an action only when he or she hears a sound. The test determines
the minimal intensity of a warble tone at least at 0.5, 1,2 and 4 kHz
at which the child is able to detect the stimulus [9]. The tones were Characteristics NICU graduates N = 32
presented through a headphone/insert earphone and a bone-conductor. Gestationalage, mean, weeks 32 (24 - 41)
The bone-conductor was placed on the mastoid bone thus obtaining Birthweight, mean, grams 1912 (665 - 4210)
a pure tone audiogram. Interacoustics Affinity/AC440 (Interacoustics Gender, male, number (%) 17/32 (53)
A/S, Middelfart, Denmark) was used to present the acoustical stimuli. Hospitalization NICU, mean, days 29 (1 - 78)

Statistical analysis Mechanicalventilation, number (%) 24/32 (75)

Mechanicalventilation, mean, days 9 (1 - 34)
For this study, the difference between the better ear ABR level IVH, number (%) 11/32 (34)
at three months PTA and the betterear at play-audiometry (at four NEC, number (%) 1/32 (3)
and eight years) or the difference between VRA (at two years) and Sepsis (bloodculture proven), number (%) 5/32 (16)
play-audiometry (at four and eight years) was investigated.
IVH: Intraventricular Hemorrhage
NEC: Necrotizing Enterocolitis.
R Version 3.5.1 with library equivalence was used for statistical
Figure 1: Indicates the baseline characteristics supplemented with perinatal risk fac-
analysis. The Two One-Sided Tests (TOST) equivalence procedure tors for HL in NICU graduates.

Volume 6 • Issue 2 • 100034

J Neonatol Clin Pediatr ISSN: 2378-878X, Open Access Journal
DOI: 10.24966/NCP-878X/100034

Citation: de Graaff-Korf KS, Benard MR, van Dommelen P, van Straaten HLM (2019) Long-Term Auditory Follow-Up of Preterm Infants after Neonatal Hearing
Screening. J Neonatol Clin Pediatr 6: 034.

• Page 3 of 5 •

Overall, at follow-up there was no change in type of HL in 32

(100%, N꞊32/32) NICU graduates. Figures 2, 3 and 4 show the follow
up results for each type of HL in box plots.

Sensori Neural hearing loss

In the eight SNHL graduates the observed differences in means
between the ABR level at three months PTA and play-audiometry
level at four years of age fell within the equivalence bounds of 10dB
and was therefore considered practically equivalent, because both
one-sided tests were statistically rejected (p=0.036). Similar conclu- Figure 4: The follow-up results for CHL in boxplots.
sion could be drawn from the ABR level with the play-audiometry
level at eight years of age (p=0.036).
Discussion
In contrast, the observed differences in means between the VRA
level at two years of age in the SNHL group and play-audiometry In this preliminary study the long-term follow-up results at four
level at four and eight years of age did not fall within the equivalence and eight years of age of NICU graduates after neonatal established
bounds of 10dB (resp. p=0.34 and p=0.41) (Figure 2). HL showed that the initial ABR at the PTA of three months was accu-
rate in predicting the final stage of all types of HL.

In NICU graduates with SNHL the initial ABR and not the VRA
was significantly accurate in predicting the severity of HL at four and
eight years of age.

ANSD was set as no response at all above a stimulus level of

>90dB while OAE’s and/or cochlear microphonics are present.
Therefore no level of HL could be established by definition at three
months PTA from ABR in children with ANSD. Also in this ANSD
groupVRA results showed unequal dB levels with play-audiometry at
Figure 2: The follow-up results for SNHL in boxplots. four and eight years of age. In 53% of these children VRA levels were
>10dB better than play-audiometry. This means that hearing levels-
established by VRA were not predictive for hearing levels at four and
Auditory neuropathy spectrum disorder eight years follow-up.
The most common diagnosis in our study population was ANSD None of the children with CHL had congenital malformations in
(N=15/32). In accordance with the definition of ANSD, ABR hear- the auditory pathway. Nearly all cases recovered from a probably
ing levels at a PTA of three months could not be set in this patient temporary CHL. In one case, CHL was mild and persistent without
group. The observed differences in means between the VRA level at deterioration due to a chronic middle ear infection.
two years of age and play-audiometry level at four and eight years of
age did not fall within the equivalence bounds of 10dB and was not These findings are of importance in the process of parental guid-
considered practically equivalent, because both one-sided tests were ing. In the SNHL group ABR findings at three months PTA supports
not statistically rejected (resp. p=0.21 and p=0.93). In eight (53%, future hearing type and level findings while in children with ANSD
N=8/15) children with ANSD VRA hearing levels were better (>10 uncertainty about the level of HL is long lasting.
dB) compared to play-audiometry levels at four and eight years of age To our best knowledge this is the first study that takes the PTA
(Figure 3). of the preterm infant at the time of the initial diagnostic ABR into
account as a more physiological milestone for the premature new
born when investigating long-term follow-up results. Due to the re-
cent introduction of neonatal hearing screening, follow-up studies are
limited and mostly refer to a (near) term population of newborns. The
follow-up period in these studies ranges from six months to six years
of age [5,6,10-15]. This study is unique in its insight into data after a
lengthy follow-up period, i.e. four and eight years. These follow-up
data were related to the PTA of three months which is in terms of
pathophysiology more suitable to very preterm newborns. The diag-
Figure 3: The follow-up results for ANSD in boxplots. nostic ABR is used as the gold standard in establishing HL after birth
[4]. From literature it is known that in premature infants the ongoing
Conductive HL process of myelination of the auditory pathway is delayed or alterat-
ed [5,6,16-18]. Eventually the maturational delay catches up at the
In almost all cases (89%, N= 8/9) with non-syndromic CHL, the postconceptional age of 40-42 weeks, which is normally the full-term
HL recovered below 35dB according to the VRA and play-audiome- age of healthy newborns [16-18]. Coenraad, et al., showed a pro-
try at four or eight years of age (Figure 4). longed I-V interval at ABR, combined with normal ABR thresholds,

Volume 6 • Issue 2 • 100034

J Neonatol Clin Pediatr ISSN: 2378-878X, Open Access Journal
DOI: 10.24966/NCP-878X/100034
Citation: de Graaff-Korf KS, Benard MR, van Dommelen P, van Straaten HLM (2019) Long-Term Auditory Follow-Up of Preterm Infants after Neonatal Hearing
Screening. J Neonatol Clin Pediatr 6: 034.

• Page 4 of 5 •

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