CLINICAL SCIENCE

(Central) Auditory Processing: the impact of otitis

media
Leticia Reis Borges,I Jorge Rizzato Paschoal,II Maria Francisca Colella-SantosIII
I
University of Campinas (UNICAMP) Faculty of Medical Sciences, Children and Adolescents Health, Campinas/SP, Brazil. II University of Campinas
(UNICAMP), Faculty of Medical Sciences, Otolaryngology, Campinas/SP, Brazil. III University of Campinas (UNICAMP), Faculty of Medical Sciences
Audiologist, Human Communication Disorders, Campinas/SP, Brazil.

OBJECTIVE: To analyze auditory processing test results in children suffering from otitis media in their first five
years of age, considering their age. Furthermore, to classify central auditory processing test findings regarding
the hearing skills evaluated.
METHODS: A total of 109 students between 8 and 12 years old were divided into three groups. The control
group consisted of 40 students from public school without a history of otitis media. Experimental group I
consisted of 39 students from public schools and experimental group II consisted of 30 students from private
schools; students in both groups suffered from secretory otitis media in their first five years of age and
underwent surgery for placement of bilateral ventilation tubes. The individuals underwent complete
audiological evaluation and assessment by Auditory Processing tests.
RESULTS: The left ear showed significantly worse performance when compared to the right ear in the dichotic digits
test and pitch pattern sequence test. The students from the experimental groups showed worse performance when
compared to the control group in the dichotic digits test and gaps-in-noise. Children from experimental group I had
significantly lower results on the dichotic digits and gaps-in-noise tests compared with experimental group II. The
hearing skills that were altered were temporal resolution and figure-ground perception.
CONCLUSION: Children who suffered from secretory otitis media in their first five years and who underwent surgery
for placement of bilateral ventilation tubes showed worse performance in auditory abilities, and children from public
schools had worse results on auditory processing tests compared with students from private schools.

KEYWORDS: Ear Diseases, Otitis Media, Otitis Media With Effusion.

Borges LR, Paschoal JR, Colella-Santos MF. (Central) Auditory Processing: the impact of otitis media. Clinics. 2013;68(7):954-959.
Received for publication on March 14, 2013; First review completed on March 14, 2013; Accepted for publication on March 14, 2013
E-mail: [email protected]
Tel.: 55 19 3521-8936

& INTRODUCTION and effectiveness with which the central nervous system
uses auditory information (2).
The auditory system consists of a set of structures that Conversely, (Central) Auditory Processing Disorder,
enables a person to receive and analyze sounds, and this (C)APD, refers to difficulties in the perceptual processing
system includes the sensory organ, the nervous system of auditory information in the central nervous system and
auditory pathways and the brain structures that are the neurobiologic activity that gives rise to the electro-
responsible for sound reception. While the peripheral physiologic auditory potentials that are not related to
auditory system receives and analyzes the acoustic waves changes in cognitive speech or other associated factors (2).
emitted by vibrations in the environment, the central A previous study has shown that there is a correlation
auditory system and the brain analyze the internal response between otitis media events that occur during childhood
for the acoustic stimulus, and a reaction is elicited (1). and auditory perceptual changes, with increased risks of
The American Speech Hearing Association defined the future speech deficits in children who experience otitis
term (Central) Auditory Processing, (C)AP, as the efficiency media events (1, 3).
Otitis media is defined as inflammation of the middle ear
and is often associated with an increase in the volume of
infected fluid. This disease has several etiologic factors, such
Copyright ß 2013 CLINICS – This is an Open Access article distributed under as infection (viral or bacterial), Eustachian tube dysfunction,
the terms of the Creative Commons Attribution Non-Commercial License (http://
creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non- immune status depression, upper respiratory tract infections,
commercial use, distribution, and reproduction in any medium, provided the environmental problems and, in some cases, social problems
original work is properly cited.
(4). Inflammation is mostly seen in early childhood and
No potential conflict of interest was reported. decreases with age. About two-thirds of children have at least
DOI: 10.6061/clinics/2013(07)11 one episode of secretory otitis media (SOM) between 1 and 5

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Borges LR et al.

years of age. This condition is very common in young Therefore, the objectives of this study were to analyze
children due to the flattening of the Eustachian tube, which (C)AP test results in children who suffer from otitis media
promotes recurring episodes of otitis media (5). and underwent surgery for insertion of bilateral ventilation
If medical intervention is not performed early enough, tubes considering gender and ear side (right ear (RE) and
otitis media can cause hearing loss due to the accumulation left ear (LE)) and to classify the (C)AP test findings as
of fluid in the middle ear, which makes the transmission of auditory abilities.
sound vibrations through the ossicular chain more difficult
due to dissipation of sound energy. As a result, the child & MATERIALS AND METHODS
experiences mild or moderate conductive hearing loss,
which is usually classified as fluctuating character (6). This experimental study was approved by the Faculty of
In otitis media, even though periods of normal hearing Medical Sciences Ethics Committee at the University of
may occur, its fluctuating character leads to inconsistent Campinas (UNICAMP) under protocol number 682/2010.
sound stimulation of the auditory central nervous system, Data were collected at the Audiology Study Center and
thereby distorting sound perception. Speech discrimination, Research in Rehabilitation under Professor Gabriel Porto
(CEPRE).
especially in noisy environments, and phonological aware-
ness skills can also be affected and consequently negatively
affect school performance (7,8). Subjects
Several studies have reported significant differences in The study included 109 elementary school students from
phonological disorders in children with and without a public and private schools, consisting of 53 females and 56
history of otitis media. In general, children who suffer from males with ages between 8 and 12.
otitis media had worse performance on tests of perception The subjects were divided into three groups: the control
and auditory processing compared with children without group (CG) comprised 40 students without a history of otitis
otitis media and had a high incidence of academic problems, media or school complaints, experimental group I (EGI)
especially due to changes in reading and writing (9,10). consisted of 39 students from public schools who suffered
from SOM in their first 5 years and who underwent surgery
The standards for ear, nose and throat elective surgery
for placement of bilateral ventilation tubes, and experi-
were modified to consider the consequences of otitis media
mental group II (EGII) consisted of 30 students from private
in childhood, especially in relation to the acquisition and
schools who suffered from SOM in their first 5 years and
development of speech skills. Surgery for ventilation tube
who underwent surgery for placement of bilateral ventila-
placement, known as myringotomy, has become the most
tion tubes.
common procedure in small children, and in 1994 more than
The criteria for inclusion in the CG were as follows: age
500,000 children underwent surgery in the USA. This between 8 and 12 years; acceptable results for otoscopy,
method is used to drain fluid from the middle ear and audiometry and tympanometry tests; and no school
restore hearing (11,12). complaints.
However, a single surgical intervention for SOM is not Inclusion criteria for EGI and EGII were as follows: age
sufficient to ensure adequate central auditory system between 8 and 12 years; normal otoscopy, audiometry and
stimulation. In addition to genetic factors, social factors, tympanometry test results; history of SOM with surgical
such as interactions between children and their parents, intervention for placement of bilateral ventilation tubes in
family and school, and behavioral factors, such as reading, the first 5 years of age; and absence of middle ear infection
listening to songs and attending theaters and parks, are for 12 months prior to the date of assessment.
needed to ensure cognitive and lingual development (13). Children who had mental disorders, neurological dis-
Several studies have shown that, compared with children orders and/or genetic syndromes; were using psychoactive
who live in high-income households, children who live in medications; attended phonotherapy; or did not fulfill the
low-income households have less cognitive development inclusion criteria were excluded from the sample.
and lower school performance due to a deficiency of
educational materials, appropriate role models and lack of Procedures
parental help in perceptual, verbal and reading develop- CG subjects were selected by the school’s pedagogical
ment (14,15). coordinator, who analyzed the academic performance of
Curi and Menezes-Filho (16) recognized that the choice of children, and later by the researcher, who considered their
school depends on the family’s income and the parents’ otologic complaints.
educational level, as measured by the public’s ability to EGI and EGII subjects who underwent surgery for
send their children to a desired school. The authors found a placement of bilateral ventilation tubes at the State
correlation between parental education and school choice. Hospital of Sumare and private clinics, respectively, were
In Brazil, 55% of private school students’ parents have selected by the researcher through analyzing the medical
completed at least high school, compared with less than records.
20% of parents whose children attend public schools. All selected subjects were invited to participate via
Consequently, the socioeconomic status of children in telephone contact with their guardians, who also signed
private schools is higher compared with public schools. consent forms allowing their children to participate in the
In this context, socioeconomic status and family educa- study.
tional status are factors that can contribute to delays in the The following procedures were performed: anamnesis
overall development of a child. These effects can be (survey of the child’s auditory history); basic hearing
exacerbated, especially in children who have had multiple evaluation by pure tone audiometry and speech audiometry
episodes of sensory deprivation hearing due to middle ear (speech recognition threshold (SRT) and phonemically
effusion (17). balanced monosyllabic words (PB words)); immittance

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Borges LR et al.

(tympanometry and acoustic reflexes) and evaluation of the For the (C)AP tests, a CD player was linked to the
(C)AP; dichotic digits test (DD); pediatric speech intellig- audiometer to allow stimuli to be presented through the CD.
ibility/synthetic sentence identification with ipsilateral The CDs were used according to the instructions on the
competing message (PSI/SSI); pitch pattern sequence test Central Auditory Processing book - Evaluation Manual,
(PPS); and gaps-in-noise (GIN). Volume 1 and 2 for the DD tests and PSI/SSI (21-23). For the
The basic hearing evaluation was the first test to be PPS and GIN tests, the CDs that were used were the
performed. The criteria for normality were as follows: versions proposed by Musiek (24,26).
hearing thresholds up to 20 dB according to the classifica- Statistical analysis was performed using nonparametric
tion of Davis and Silverman (18) and percentage of correct methods; tables show average values, standard deviations
answers between 88 and 100% of PB words (1). and p-values. The significance level was 5% (p,0.05), and
Tympanometry was considered at its maximum peak significant data are highlighted in bold.
compliance at an atmospheric pressure of 0 dPa, an To analyze student performance on (C)AP tests with
equivalent volume between 0.3 and 1.3 ml and an acoustic respect to the RE and LE, the Wilcoxon signed-rank test was
reflex between 70 and 100 dB above the hearing threshold utilized. When p,0.05, the subsequent statistical analysis
for pure tone, according to Jerger (19) and Carvalho (20). continued independently for each ear.
After basic hearing evaluations, the subjects were sub- Regarding student performance on the (C)AP test, the
mitted to the (C)AP. Kruskal-Wallis test was used to analyze significance. When
The DD test allows us to evaluate the figure-ground p,0.05, the Mann-Whitney test was utilized to compare
ability for verbal sounds through a binaural integration task. groups in pairs.
The test performance and reference values were adopted To verify student performance in regard to hearing skills,
according to the criteria proposed by Colella-Santos and a Chi-squared test was used to determine significance.
Pereira (21). Hearing abilities were classified as normal or altered
The figure-ground ability was assessed by the PSI/SSI. according to the benchmarks for each test. When p,0.05,
The reference values and evaluation procedures were based the odds ratio comparing groups was used to analyze
on the Ziliotto (22) and Kalil (23) protocols. The tests that differences.
were applied varied depending on the children’s age; the
PSI test was used for children aged 8 to 11, and the SSI test & RESULTS
was used for children aged 12.
Figure 1 shows the pre-surgical evaluations of tympanot-
Auditory temporal processing can be divided into four omy tube placement for EGI and EGII.
categories: ordination, integration, masking and temporal Student performance on the (C)AP tests, for both the RE
resolution. Temporal ordering and resolution were evalu- and the LE, is shown in Table 1. The results of (C)AP tests in
ated in this study. regard to groups are shown in Table 2. The results of (C)AP
The temporal ordering ability was assessed using the PPS tests of paired groups are shown in Table 3. Tables 4 and 5
described by Musiek (24) and adopting the values of show the comparisons between group performances, con-
normality published by Schochat and Rabelo (25). sidering altered auditory skills.
The GIN test proposed by Musiek (26) was performed to
evaluate temporal resolution ability by adopting the values
& DISCUSSION
of normality published by Perez (27) and Amaral and
Colella-Santos (28). The temporary alteration in the peripheral auditory
The basic hearing evaluation and (C)AP were performed system due to otitis media changes the quality of sound
in a 60-minute session in a soundproof booth. An AC40 perception once the acoustic signal can be observed in
audiometer and earphones (model: TDH 39P) were incomplete form (29).
used. Impedance was performed using 235 h immittance Most subjects went through preoperative audiometric
audiometry. All equipment was calibrated according to evaluation (Figure 1). For some subjects, only tympanome-
ISO-389 and IEC-645. try was performed due to their age. In EGI, most of the

Figure 1 - Percentage of presurgical hearing evaluations performed on students from EGI and EGII.

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Borges LR et al.

Table 1 - Student performance on the (C)AP tests for the Table 3 - Student performance on the (C)AP tests
RE and LE. between pairs of groups.
Right ear (n = 109) Left ear (n = 109) p-value p-value p-value

Tests Average SD Median Average SD Median p-value Tests CG x EGI CG x EGII EGI x EGII

DD 95.0 7.1 97.5 92.3 10.6 95.0 0.0001 DD

PPS 61.6 24.6 63.3 58.7 25.6 57.0 0.0251 RE 0.0004 0.0567 0.0687
GIN 5.5 2.5 5.0 5.4 2.0 5.0 0.5453 LE ,0.0001 0.0060 0.0177
GINP 70.8 14.2 73.3 70.6 12.8 72.0 0.7371 GIN ,0.0001 0.1611 0.0068
PSI/SSI 743.7 23.1 80.0 73.9 22.9 70.0 0.5473 GINP ,0.0001 0.7123 ,0.0001

n - number of subjects; SD - standard deviation; DD - dichotic digits; DD - dichotic digits; RE - right ear; LE - left ear; GIN – gaps-in-noise;
PPS – pitch pattern sequence test; GIN – gaps-in-noise; GINP – gaps-in- GINP – gaps-in-noise/percent.
noise/percent; PSI/SSI - pediatric speech intelligibility/synthetic sentence
identification with ipsilateral competing message. The p-value was This difference between experimental groups can be
calculated using the Wilcoxon paired test.
explained by the fact that public schools in Brazil may be
located in an environment that is susceptible to social
children showed conductive hearing loss and type B violence and has few recreational areas, low social cultural
tympanometric curves, while in EGII, most subjects showed education, a lack of books and little access to health
bilateral type B tympanometric curves. The data corroborate resources; that is, this environment does not favor language
the findings of Oliveira et al. (30), who identified the
development and adequate stimulation. However, the
presence of conductive hearing loss by pre-surgical audio-
group of private school children who have a higher
metry for subjects who had implanted ventilation tubes.
socioeconomic status and therefore more accessible lan-
Franche et al. (31) analyzed tympanometry results in 98
guage stimulation also showed alterations in DD test
subjects (196 ears) who were subjected to myringotomy
answers. These results are directly related to physiological
surgery and found types B and C tympanometry in 150 ears.
changes caused by otitis media and not to socioeconomic
The pre-surgical audiometric evaluation findings in this
factors.
study demonstrated alterations in all subjects, similar to the
literature cited above (11,32,1), which showed that SOM Colella-Santos (33) studied the DD test responses of 140
causes significant auditory deprivation characterized by right-handed subjects between the ages of 5 and 25 years
conductive hearing loss and changes based on tympano- during binaural integration and directed attention to the left
metry results. and right. She concluded that children between 5 and 6
In the analysis of the (C)AP tests, broken down by years had significantly better performance in the RE when
individual ears (Table 1), there was a significant difference compared with subjects aged 6 years, showing that test
between the RE and the LE. The RE performed better than performance improves as children become older.
the LE in DD and PPS across the three groups. Better performance in the RE is explained by the
In the analysis of the (C)AP tests, significant results for structural Kimura theory because all the children in this
the DD and GIN tests were found between groups based on study are right-handed (34). On the DD test, the better
the threshold of gap detection and percentage of correct performance in the RE compared with the LE in EGI
answers. In other tests, PSI/SSI and PPS differences were students is no longer expected because the asymmetry
not significant, but EGI performances were worse than CG between the ears for this test occurs up to 6 years of age.
and EGII in regard to the PPS test, while EGII showed worse However, in EGI, there were also lower average responses
PSI/SSI results compared with EGI and CG. for the LE in the DD test based on CG values. Thus, these
In a pairwise comparison of groups regarding the DD test, differences between the averages can be explained as a
EGI and EGII had worse performances compared to CG, but result of a maturational delay, which was most likely caused
EGI had changes in both ears, while EGII only had changes by stimulation inconsistency that aggravated the conductive
in the LE. hearing loss due to otitis media.

Table 2 - Student performance on (C)AP tests based on group.

CG EGI EGII

Test n Average SD Median n Average SD Median n Average SD Median p-value

DD
RE 40 97.9 3.3 100.0 39 91.3 9.5 95.0 30 95.8 4.9 97.5 0.0007
LE 40 96.7 5.5 100.0 39 86.6 14.4 90.0 30 93.9 5.6 95.0 ,0.0001
PPS
RE 40 66.7 22.4 70.0 39 56.8 26.1 56.7 30 60.9 24.9 64.8 0.1742
LE 40 64.4 24.5 80.0 39 53.9 27.3 47.0 30 57.2 24.1 63.0 0.1732
GIN 80* 5.1 2.6 5.0 78* 6.1 2.0 6.0 60* 5.2 1.8 5.0 ,0.0001
GINP 80* 74.7 11.4 75.5 78* 63.3 13.4 65.0 60* 75.1 12.1 78.0 ,0.0001
PSI/SSI 80* 78.4 19.9 80.0 78* 73.6 23.5 70.0 60* 69.8 25.4 75.0 0.1425

n - number of subjects/* number of ears; SD - standard deviation; DD - dichotic digits; RE - right ear; LE - left ear; PPS – pitch pattern sequence test;
GIN – gaps-in-noise; GINP – gaps-in-noise/percent; PSI/SSI - pediatric speech intelligibility/synthetic sentence identification with ipsilateral competing
message. The p-value was calculated by the Mann-Whitney test.

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Borges LR et al.

To have good performance on the figure-ground test and

Table 4 - CG and EG performance based on the hearing
a binaural integration task, the child needs to process
skills that were evaluated.
different information that is simultaneously presented to
CG EGI EGII p-value
both ears. Changes in this ability can be exposed by hearing
difficulties in situations of background noise or in the
Hearing Skills n % n % n %
presence of more than one person talking at the same time.
Figure-ground These difficulties can compromise performance in school,
Normal 35 87.5 19 48.7 15 50.0 0.0003 where there are frequently situations that require the
Altered 5 12.5 20 51.3 15 50.0 listener to ignore linguistic information from one source to
Temporal Ordering
Normal 28 70.0 16 41.0 17 56.7 0.0345
concentrate on a main message.
Altered 12 30.0 23 59.0 13 43.3 These data suggest that EGI and EGII students were
Temporal resolution influenced by otitis media on the auditory skills that were
Normal 34 85.0 13 33.3 20 66.7 ,0.0001 evaluated; therefore, these children would have fewer
Altered 6 15.0 26 66.7 10 33.3 chances (0.1) of having normal hearing abilities when
All normal 24 60.0 5 12.8 10 33.3 ,0.0001
compared with children without otitis media.
n - number of subjects; % - percent. The p-value was calculated by the chi- Studies that were conducted with children and adoles-
squared test. cents suffering from SOM in their first 5 years of age and
that considered (C)AP performance concluded that these

Table 5 - Statistical analysis comparing student performance based on hearing skills.

OR (CI 95%)

Hearing Skills EGI x CG EGII x CG EGI x EGII

Figure-ground ref 7.37 (2.39 to 22.76) ref 7.00 (2.15 to 22.76) ref 1.05 (0.41 to 2.73)
Temporal Ordering ref 3.35 (1.32 to 8.50) ref 1.78 (0.66 to 4.80) ref 1.88 (0.72 to 4.93)
Temporal Resolution ref 11.33 (3.80 to 33.83) ref 2.83 (0.89 to 8.98) ref 4.00 (1.46 to 10.98)
All normal ref 0.1 (0.03 to 0.30) ref 0.33 (0.12 to 0.90) ref 0.29 (0.09 to 0.98)

OR - Odds Ratio; CI - confidence interval; ref. – Reference.

In this study, to evaluate temporal resolution, the GIN test subjects had greater difficulty in hearing auditory closure,
was used. The EGI had a significant difference in relation to figure-ground and binaural integration and had deficits in
the gap detection threshold and percentage of correct attention and learning difficulties in class (36-38).
answers when compared with the CG and EGII. The data in this study suggest the importance of early
Several other studies have applied the GIN test in intervention in terms of minimizing the effects caused by
children and found values between 4.2 ms and 5 ms for otitis media in the development of auditory skills, especially
the gap detection threshold and values between 73.6% and considering the (C)AP evaluation in children who suffered
78.27% for the percentage of correct answers (27,35,28). from otitis media in early life to better understand the
These results are similar to our results when the GIN was changes in auditory function development in this popula-
applied to the CG. tion and to develop appropriate therapies.
The low GIN scores in the group of children who From the results, we conclude the following:
underwent bilateral ventilation tube insertion suggests that - Considering the (C)AP test, there were no significant
episodes of SOM during the early years can preclude the differences between males and females.
proper input of auditory information responsible for - There are significant differences between the RE and the
temporal information sensory encoding. These factors are LE in regard to DD and PPS tests.
essential for enhancing temporal resolution because this - Children who underwent surgery to insert ventilation
skill develops at approximately 6 to 7 years and depends on tubes bilaterally in their first 5 years and attended public
the segregation of different auditory stimuli. schools showed much worse performance when compared
Among the auditory skills evaluated, temporal proces- with children who had the same surgical procedure and
sing, which includes solving skills and temporal ordering, attended private schools when considering the LE DD test
was the most changed in EGI (Table 4). Thus, EGI children and GIN.
have an 11.33 times higher likelihood of having impaired - Temporal processing and figure-ground skills were the
temporal resolution compared with CG subjects (Table 5). most altered.
The temporal resolution auditory ability is an important
factor in speech perception because it contributes to the & ACKNOWLEDGMENTS
identification of small phonetic elements that are present in
speech, and alterations in this ability suggest a lack of This work was supported by the State of São Paulo Research Foundation
perception of normal speech and phoneme recognition. (FAPESP).
In the figure-ground evaluation, EGI students had poorer
hearing abilities; furthermore, children who underwent & AUTHOR CONTRIBUTIONS
bilateral ventilation tube insertion had a 7.37-fold higher Borges LT and Colella-Santos MF participated in the planning, research
likelihood of presenting changes in this ability when and writing of the manuscript. Paschoal JR provided advice and
compared with the CG. participated in the planning of the manuscript.

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20. Carvalho MMR. Fonoaudiologia: Informação para formação.

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