School-age hearing screening : identification of hearing impairments in first grade students

Purpose: to characterize the audiological profile of students in the first year of municipal elementary schools in Caxias do Sul-RS, investigating and identifying the occurrence of hearing impairment in this population, by electroacoustic measurements. Methods: cross-sectional, prospective, descriptive and quantitative study of 391 students from first year of municipal elementary schools in Caxias do Sul-RS. Students were submitted to four audiological procedures in School Hearing Screening: Meatoscopy, Transient Evoked Otoacustic Emissions, Otoacoustic Emissions Distortion Product and Tympanometry. Furthermore, those responsible for the children answered a questionnaire relating to development and the otological history of each child. The students who had some hearing impairment in hearing screening were referred for evaluation otorhinolaryngological and/or complete audiological evaluation at a reference center in the same city. Results: of the 782 ears evaluated, 85,4% in the examinations were normal and 14,6% shown some kind of change. In Meatoscopy, it was found that 6,3% of the ears showed alterations. 94,8% ears have passed the Transient Evoked Otoacustic Emissions and 95,8% the Otoacoustic Emissions Distortion Product. In Tympanometry, the curve predominant was type A, followed by type C. Referrals were made to 14,6% of students. Conclusion: the population of this study was composed mostly by male schoolchildren, with six years of age. Of the 782 ears evaluated, 85,4% had normal test findings and 14,6% showed some kind of change.

an important instrument for early identification of hearing impairments 15 .It provides the possibility to offer greater attention to children's auditory health and, especially, to the diagnosis of hearing loss and early intervention in this population.The detection of hearing loss in school-age children is essential.The later the hearing loss is detected, the greater will be the difficulties.Early diagnosis allows the referral to specialists, who will act to provide rehabilitation and prevention of children's cognitive, social, emotional and communicative alterations.
Therefore, this study had the aim to characterize the audiological profile of first grade students from municipal elementary schools in Caxias do Sul-RS, Brazil, by using electroacoustic measures to investigate and identify the occurrence of hearing impairments in this population.

METHODS
This study was approved by the Research Ethics Committee of the Associação Cultural e Científica Virvi Ramos (Cultural and Scientific Association Virvi Ramos), under protocol number 183.613.The study was conducted after approval of the Municipal Department of Education of Caxias do Sul -RS, Brazil (document number 728/2012).
Three hundred and ninety one school-age children were screened in this prospective descriptive quantitative cross-sectional study.The subjects were male and female students with ages between six and nine years, enrolled in the first grade of nine municipal elementary schools in Caxias do Sul-RS, which were randomly selected to include all four regions of the city and different socioeconomic levels.
The following inclusion criteria were considered: to be attending the first grade of elementary school in one of the municipal schools selected for this study, and to have the Free and Informed Consent signed by the student's legal guardian.Subjects that had presented a previous otologic alteration referred to in the questionnaire and/or those who had been diagnosed with permanent hearing loss were excluded from the sample.
The Free and Informed Consent was sent to the family through the students' agenda book, along with a questionnaire specially adapted for this study 3,16 (Figure 1).The questionnaire included 11 multiple choice questions, which were objective and easy to understand.The questions regarded each child's development and otologic history.tested function.Failing this test, the individual should be referred to more complex diagnostic procedures.In short, the hearing screening has the aim to identify individuals with hearing impairments in order to refer them for otorhinolaryngological assessment and a complete audiological evaluation 7,8 .The Hearing Screening Programs have been demonstrating their relevance as the primary means for early detection of hearing loss in children.Up until now, the Programs performed in schools have been offered mainly as local initiatives in places such as the United States, Australia, China and a few European countries 9 .In Brazil, they are not yet part of the routine in most schools.
Public Health Policies recommend, in addition to the Neonatal Hearing Screening Program, the School-age Hearing Screening, in order to early diagnose hearing loss and perform the necessary interventions as early as possible 1 .Among the tests used in different screening programs, the hearing assessment can be performed by using objective tests, such as the Otoacoustic Emissions (OAE) and the Tympanometry, which are both fast, non-invasive and reliable tests, thus representing an ideal test profile 10,11 .
The OAE were first observed and described by Kemp 12 , who defined them as the release of sound energy originated in the cochlea, which propagates through the middle ear until it reaches the external auditory canal (EAC).He proved that they are present in all normally functioning ears and are not detected when the pure-tone thresholds are above 20-30 dB.According to the author, the measurement of OAEs is an objective, non-invasive and fast procedure, applicable in non-soundproofed facilities and possible to be performed with all age groups.Its use is recommended for hearing screening in school-age children, since it is proved to be an objective test that allows the evaluation of cochlear function 3 .
The tympanometry is an electroacoustic test that contributes to the identification of middle ear alterations by investigating the integrity of the tympanicossicular system.This low-cost, fast and simple procedure is the method of choice for differentiating among the middle ear conditions that may affect individuals in all age groups, especially in school age, when most hearing impairments are due to middle ear alterations 13,14 .
Due to the fact that many children have no access to any sort of hearing evaluation before school age, the School-age Hearing Screening is Unit) (CSCM -UA) -a reference center for medium complexity otorhinolaryngological and audiological care of the Unified Health System (SUS) in Caxias do Sul-RS, Brazil -on a different day from the hearing screening, and unlike the usual flow.Students were reassessed on the same date and place, after the otorhinolaryngological evaluation and conduct.
After the EAC inspection, the students without alterations were submitted to the TEOAE and DPOAE tests, as well as the tympanometry.The Maico ERO-SCAN™ portable automatic equipment was used for the TEOAE and DPOAE , and the Interacoustics MT-10 portable immitance meter, for the tympanometry, the.All equipments were calibrated according to the standards and guidelines recommended by the manufacturers.
For the TEOAE, the results that presented amplitude values equal or superior to -12 dB and signal-to-noise ratio equal or superior to 4 dB The hearing screening was performed in quiet rooms, where students were submitted to four audiological procedures: meatoscopy, Transient Evoked Otoacustic Emissions (TEOAE), Distortion Product Otoacoustic Emissions (DPOAE), and tympanometry.
The HEINE MINI 3000 diagnostic otoscope was used for the meatoscopy, which was the first procedure performed.This procedure had the aim to evaluate whether the students' EAC presented suitable conditions for the other tests, as well as to verify the presence of excessive cerumen or foreign body.The students that presented no alterations in the EAC were submitted to the other procedures of the School-age Hearing Screening.When alterations were observed, the student was referred to a prescheduled otorhinolaryngological evaluation at the Centro de Saúde Clélia Manfro -Unidade Auditiva (Health Center Clélia Manfro -Auditory Adapted from Guerra-Silva 3 and Lacerda 16 .

Figure 1 -Pre-hearing screening questionnaire
The test for equality of two proportions and the chi-square test were used to analyze the results.For some results, it was necessary to use the Yates' Correction, since the chi-square test presented significant results, but with a frequency below or equal to five cases.A significance level of 0.05 (5%) was adopted, with 95% confidence intervals.

RESULTS
A total of 391 school-age children were screened for hearing impairments, 208 male (53.2%) and 183 female (46.8%).From these subjects, 288 (73.7%) were six, 101 (25.8%) were seven, and two (0.5%) were nine years old.All of them were submitted to four audiological procedures in both ears, hence 782 ears were assessed.
From the 782 ears, 85.4% presented normal results on the audiological procedures (meatoscopy, TEOAE, DPOAE, and tympanometry), and 14.6% presented some kind of deficit.The results obtained in each procedure are described next.It is worth mentioning that, for this, all ears were considered (both right and left).
All students with alterations in the meatoscopy were referred to the otorhinolaryngologist (Figure 2) and submitted to the hearing screening after medical conduct.Table 1 presents the pass/fail results on the TEOAE and DPOAE by ear, considering those that did not present alterations in the meatoscopy and those that were assessed after medical conduct regarding EAC alterations.
in at least three of the tested frequencies were considered normal ("pass" criteria).For the DPOAE, it was considered normal ("pass") the results that presented amplitude equal or superior to 6 dB in at least three of the frequencies tested.These criteria were used according to the manufacturer's suggestion.
The classification proposed by Jerger 17 was used to analyze the values of tympanometric curves.Students who presented types A, C, Ad and As curves and satisfactory results on the TEOAE and DPOAE were considered "pass".Those who presented type B curve in at least one ear were considered "fail", and referred for complete audiological evaluation, in order to confirm the presence of middle ear alterations.
Students who presented no alterations in the meatoscopy but failed the OAE and/or the tympanometry were referred for audiological diagnosis at the CSCM -UA using Pure-Tone Air-and Bone-Conduction Audiometry, speech audiometry (using the Maico MA 41 audiometer), immittance measures (using the Interacoustics AT 235 automatic immittance meter), TEOAE and DPOAE (using the ERO-SCAN™).
For better elucidation, a flowchart of the performed procedures from the school-age hearing screening to the students' final audiological conduct is presented in Figure 2.
Immediately after getting the audiological diagnosis, the caregivers of the students that presented alterations in the audiological evaluation received a referral for otorhinolaryngological evaluation.-or 49 ears -were referred for otorhinolaryngological assessment, and 21 (5.4%) for audiological diagnosis.From these, conductive hearing loss was detected in 14 (66.7%), while three (14.3%)presented normal hearing, as shown in Table 2.
The results obtained on the tympanometry are presented in Figure 3. Type A were the most common curve type found in this test, followed by type C.
From the students who presented alterations in any of the hearing screening procedures, 37 (9.5%)

Figure 3 -Distribution of the types of tympanometric curves
Table 3 shows the values regarding the conduct adopted after all assessments.Fifteen (3.8%) students presented alterations in the audiological diagnosis and were referred to otorhinolaryngological assessment.
Caregivers' responses to the questionnaire applied before the hearing screening are presented in Table 4.
found on the EAC inspection and the child passed the TEOAE, the DPOAE and the tympanometry.In the cases where the caregiver declared to suspect that the child did not hear well, 23% had alterations on the meatoscopy, 27% failed the TEOAE and the DPOAE, and 32% failed the tympanometry.
When the questionnaire results were compared to the outcome on the four procedures included in the hearing screening, there were significant associations between the question "Do you think your child hears well?" and all the hearing screening tests.In 92% of the cases where the caregiver declared that the child had good hearing no alterations were  your child hears well?" and "Did your child ever have ear infections of other ear problems?".
Table 5 shows that the TEOAE was also significantly associated with the questions "Do you think

DISCUSSION
Four distinct procedures were selected for this study in order to provide a full evaluation in the school-age hearing screening, examining from the EAC to the integrity and functionality of the outer hair cells in the cochlea, and considering that the early detection of hearing losses that may interfere in the process of learning, reading and writing of school-age children is indispensable.The early identification and rehabilitation of hearing impairments provide great benefits for the child 18 , besides reducing the linguistic, educational and psychosocial consequences.Hence, it is consensus that the hearing assessment and monitoring should not be carried out only in newborns, but also during the first years of school life.
The cerumen is a natural event, normally expelled from the EAC and, usually, asymptomatic.However, if excessive, it may cause complications such as the hearing loss 19 .In the present study, the most observed alteration in the meatoscopy was excessive cerumen, which is reported in literature as one of the most frequent causes of alterations in preschool and school-age children 1 .Recent studies have found that the presence of excessive cerumen in the EAC was the most common alteration found in students [20][21][22] , which complies with the results in this study.However, in other researches 10,11,23,24 , there the prevalence of excessive cerumen was a higher than in this study.
the types of hearing loss (conductive and mixed) found in the school-age children referred for audiological diagnosis.
Any alteration found in the school-age hearing screening requires an appropriate referral for full audiological evaluation, in order to provide more complete and definitive tests.The hearing screening will only bring benefits for the student if the results that are outside the normal range are confirmed and the appropriate intervention is performed after that 35 .
Conductive hearing loss, which is more frequent in the months of fall and winter due to the weather, may be considered the most common cause of fail results in the school-age hearing screening 32,35 .It is worth emphasizing that the data collection for the present study was performed in these seasons.This type of hearing impairment is the most reported fail in the school-age hearing screening, both in national and international literature 10,22,32,38 .
The combination of procedures to identify children with hearing impairments is recommended because children often fail only one of them 6 .Performing the TEOAE along with the DPOAE 3 , as well as the tympanometry and the full audiological evaluation after the school-age hearing screening, in cases where referral is needed, is important to avoid false positive results, since some students referred for audiological diagnosis in this study presented normal hearing.
The significant relationship between some of the answers from caregivers and the procedures performed in the school-age hearing screening demonstrates it is possible to associate the use questionnaires along with other tests in hearing screenings.The authors from a study that had the aim to analyze the effectiveness of a low-cost screening instrument concluded that questionnaires may be used to classify children as having normal hearing or hearing loss.Furthermore, they pointed out that developing low-cost strategies can help in caring for children with hearing impairments in developing countries.Therefore, it is necessary to establish and adopt procedures with lower expenses, such as screenings and/or questionnaires, which are accessible to needy areas and allow the identification of groups of children at risk for hearing loss 39 .
It has been reported in literature that hearing loss can be noticed by some of the students' behavior, such as: frequently asking to repeat sentences, turning the head towards the speaker, higher or lower intensity in speech, demonstrating effort in trying to listen, looking at and concentrating on the teacher's lips, being inattentive in classroom debates, preferring social isolation, being passive or tense, easily getting tired, no effort in demonstrating capacity, presenting learning difficulties 1 .
The OAE has been revealing an important applicability to perform hearing screenings, as it is a quick, effective and viable method 25 .Nevertheless, the results of these screenings are frequently influenced by the presence of middle ear abnormalities.The OAE have been shown as effective measures to identify these alterations, as well as moderate or more severe degrees of cochlear hearing loss 26 .
The frequency of fail results in the OAE found in literature diverges from the observed in the present study.Performing the screening with 744 preschool students using the TEOAE, authors found a failure rate of 5.5% 25 .Another study performed the TEOAE in 93 school-age students, finding a failure rate of 25.8% 27 .Authors who performed the DPOAE in 105 children found that 5.37% presented alterations 28 .DPOAE was also performed in 846 children from another study, in which 96% of the subjects passed the hearing screening 29 , similar to the data found in the present study.
In a research that used similar methods to the present study, analyzing the tests by ear, it was found 818 (90.6%) pass and 84 (9.4%) fail results in the TEOAE.The DPOAE was performed in the same ears, and obtained 849 (94.0%) pass and 53 (6.0%) fail results 10 .These data corroborate the present study, once it was found a greater number of pass in the DPOAE than in the TEOAE.This may be due to the fact that the TEOAE are registered in nearly 98% of people with hearing thresholds of up to 25 dBHL, while the DPOAE can be detected in practically 100% of the individuals with normal hearing thresholds or better than 45 dBHL.Hence, the DPOAE does not detect mild cochlear hearing losses 30,31 .
Furthermore, the literature reports variations between 11.6 and 37.8% of hearing impairments found in the school-age hearing screening 11,32,33 .Authors recommend that the TEOAE are always used along with the tympanometry, thus providing a more significant interpretation and allowing the detection of hearing impairments with middle ear alterations 26,27,34,35 .
The tympanometry is a quick and objective test designed to evaluate the functional integrity of the tympanic-ossicular system 7,36 , and that has been broadly used in hearing screening programs for precisely identifying conductive alterations.Like in this study, other authors have also observed the predominance of type A curves 37,38 , followed by type C, when performing the tympanometry in the school-age hearing screening 2,7,22,27 .The occurrence of 26.5% of types B, C, As and Ad tympanometric curves in this study's population, which may be related to middle ear and/or auditory tube alterations, infers that the findings were compatible with Therefore, the regular hearing screening of children during their school years would guarantee that they were affected by hearing loss or other preventable alterations.Information in this study demonstrate the importance of prioritizing the identification and early treatment of hearing impairments.

CONCLUSION
The sample of this study was composed mostly by male school-age children with six years of age.From the 782 ears evaluated, 85.4% had normal results on the hearing screening and 14.6% showed alterations.From these, 5.8% had absence of responses in the TEOAE, and 4.2% in the DPOAE.The predominant tympanometric curve was type A, followed by type C. The most common alteration found in the students referred for audiological diagnose was the conductive hearing loss.
Caregivers often do not notice the hearing difficulty of the child.It is not uncommon to detect the hearing loss only in school, through the schoolage hearing screening and the observation of the student's behavior.Many children that get to schoolage without a hearing loss diagnose are wrongly classified as inattentive, hyperactive, with poor academic performance, difficult to adjust to school, among other things, while the actual problem is an undiagnosed hearing loss 24 .
The prevalence of 14.6% of hearing alterations found in this sample evidences the need to intensify the implementation of programs for prevention and early diagnosis of hearing impairments.The schoolage hearing screening has been shown as an effective and accessible mean of identifying impairments that were not diagnosed until school-age, as well as those developed during this period, fulfilling its objective to minimize the difficulties and losses due to hearing deficits.

1 . 2 . 3 . 4 . 5 .
Date:____/____/____ Age:_____________ DOB____/____/____ Phone number: (__) _________________ School:__________________________________________________ Class:________ Did your child ever have a hearing evaluation? ( ) Yes ( ) No Do you think your child hears well?( ) Yes ( ) No Does your child seem to hear better on some days rather than others?( ) Yes ( ) No Does anyone in the family present hearing impairments?( ) Yes ( ) No Was there any complication during pregnancy or birth?( ) Yes ( ) No If yes, which one?_____________________________________________________ 6. Did your child ever have ear infections of any other ear problems?( ) Yes ( ) No If yes, which one?_____________________________________________________ 7. Did your child ever have any ear surgery?( ) Yes ( ) No 8. Does your child use cotton swabs to clean his/her ears? ( ) Yes ( ) No 9. Does your child have any health problem? ( ) Yes ( ) No If yes, which one?_____________________________________________________ 10.Does your child present learning difficulties in school?( ) Yes ( ) No 11.Does your child present language or speech problems?( ) Yes ( ) No Note -SAHS: School-age Hearing Screening; EAC: External Auditory Canal; ORL: Otorhinolaryngologist; TEOAE: Transient-Evoked Otoacoustic Emissions; DPOAE: Distortion Product Otoacoustic Emissions.

Figure 2 -
Figure 2 -Flowchart of the procedures, from the school-age hearing screening to the final audiological conduct

Table 2 -Distribution of audiological diagnosis Audiological diagnosis N % P-value
Note -SAHS: School-age Hearing Screening.Test for Equality of Two Proportions; P-value <0.05.

Table 5 -Association between transient-evoked otoacoustic emissions and the pre-screening questionnaire
Note -N: Number of subjects.Chi-Square test and Yates' Correction.P-value <0.05.