Abstracts
Purpose
This study sought to characterize the peripheral auditory system of individuals with Down syndrome (DS) using conventional and high-frequency audiometry.
Methods
We performed a cross-sectional and observational study. Fifteen individuals with DS, who were of both genders and between 7 and 15 years of age, participated in this study. The following procedures were performed: otoscopy, tympanometry with ipsilateral and contralateral acoustic reflex, pure-tone audiometry, vocal audiometry and high-frequency audiometry.
Results
There was a predominance of mild conductive hearing loss in one or both ears. The mean hearing thresholds for conventional audiometry were below 20 dB HL and between 20 and 40 dB HL for high-frequency audiometry. The Pearson correlation coefficient indicated a moderate positive correlation between the 9-14 kHz thresholds and age.
Conclusion
Overall, no significant differences were observed when comparing the right and left ears of individuals with DS, in regards to pure-tone audiometry, immittance testing and speech audiometry. Most children showed middle ear abnormalities and conductive hearing loss. Moreover, high-frequency audiometry suggested the onset of impaired cochlear function, which may be associated with frequent otitis media episodes and/or early cochlear degeneration.
Hearing; Audiometry; Down syndrome; Auditory threshold; Hearing loss; high-frequency
Objetivo
Caracterizar o sistema auditivo periférico de indivíduos com síndrome de Down, por meio da audiometria convencional e de altas frequências.
Métodos
Estudo do tipo transversal e observacional. Participaram 15 indivíduos com síndrome de Down, de ambos os gêneros, entre 7 e 15 anos de idade. Foram realizados os seguintes procedimentos: Meatoscopia, Timpanometria com pesquisa do reflexo acústico ipsilateral e contralateral, Audiometria Tonal, Audiometria Vocal e Audiometria de Altas Frequências.
Resultados
Houve predomínio de perda auditiva condutiva de grau leve, em uma ou ambas as orelhas. As médias dos limiares auditivos para a audiometria convencional ficaram abaixo de 20 dBNA e, para a audiometria de altas frequências, ficaram entre 20 e 40 dBNA. O coeficiente de correlação de Pearson revelou correlação moderada positiva, entre os limiares de 9 a 14 kHz e a idade.
Conclusão
De forma geral, não foram observadas diferenças significativas, quando comparadas as orelhas direita e esquerda de indivíduos com síndrome de Down, na audiometria tonal, imitanciometria e logoaudiometria. A maioria das crianças apresentou alteração de orelha média e perda auditiva condutiva. A audiometria de altas frequências sugere o início de prejuízo da função coclear, que pode estar associado às otites médias frequentes e/ou à degeneração coclear precoce.
Audição; Audiometria; Síndrome de Down; Limiar auditivo; Perda auditiva de alta frequência
INTRODUCTION
Hearing loss can be caused by environmental or genetic factors. For instance, some genetic disorders demonstrate isolated hearing loss, whereas others show hearing loss associated with abnormalities of other organs due to a variety of syndromes(11 . Ginsberg IA, White TP. Considerações otológicas em audiologia. In: Katz J. Tratado de audiologia clínica. São Paulo: Manole; 1999. p. 6-23.).
Down syndrome (DS) is a genetic disorder characterized by the presence of an
extra copy of chromosome 21 or excess genetic material present on this
chromosome(22 . Limongi SCO. Linguagem na síndrome de Down. In: Ferreira LP,
Befi-Lopes DM, Limongi SCO. Tratado de Fonoaudiologia. São Paulo: Rocca; 2004.
p. 954-66.).
Diagnosis is based on a series of signs and symptoms, and confirmation is
established by chromosome analysis. Because not all affected individuals show
the same characteristics, cytogenetic analysis is necessary(33 . Oliveira ACB, Jorge ML, Paiva SM. Aspectos relevantes à abordagem
odontológica da criança com síndrome de Down. Rev CROMG.
2001;7(1):36-42.,44 . Sommer CA, Henrique-Silva F. Trisomy 21 and Down syndrome: a short
review. Braz J Biol. 2008;68(2):447-52.
http://dx.doi.org/10.1590/S1519-69842008000200031
https://doi.org/10.1590/S1519-6984200800...
).
Studies have demonstrated that this syndrome occurs in 1 in every 1,000 live births. The most common clinical characteristics include intellectual disability, muscular hypotonia, oblique palpebral fissures, increased vascularity, microcephaly and flat occiput. Additional characteristics include a small and flat nose, low nasal bridge, cardiovascular malformations and respiratory infections due to obstruction of the upper airways(55 . Mustacchi Z. Síndrome de Down. In: Mustacchi Z, Peres S. Genética baseada em evidências: sídromes e heranças. São Paulo: CID; 2000. p. 817-94.).
Muscular hypotonia affects the muscles of the bronchial tree, impairing the
elimination of secretions. The accumulation of mucus can lead to infections of
the upper airways and a consequent increase in the incidence of otitis
media(55 . Mustacchi Z. Síndrome de Down. In: Mustacchi Z, Peres S. Genética
baseada em evidências: sídromes e heranças. São Paulo: CID; 2000. p.
817-94.). Another
factor that may contribute to the increased incidence of ear infections in DS
patients is the dysfunction or impairment of the middle ear, which is frequently
observed in this population. This factor is related to anatomical defects such
as an abnormal Eustachian tube, persistent mesenchymal tissue in the tympanic
cavity, external auditory canal stenosis and hypoplasia of the
mastoid(66 . Balkany TJ, Downs MP, Jafer BW, Krajicek MJ. Hearing loss in
Down’s syndrome: a treatable handicap more common than generally recognized.
Clin Pediatr (Phila). 1979;18:116-8.
http://dx.doi.org/10.1177/000992287901800207
https://doi.org/10.1177/0009922879018002...
).
Hearing loss occurs in approximately two-thirds of children with DS and may
present as conductive, sensorineural or mixed hearing loss(77 . Roizen NJ. Down syndrome. In: Batshaw ML. Children with
disabilities. 5th ed. Baltimore: Brookes; 2002. p. 361–76.,88 . Han F, Yu H, Zhang J, Tian C, Schmidt C, Nava C, et al. Otitis
media in a mouse model for Down syndrome. Int J Exp Pathol. 2009;90(5):480-8.
http://dx.doi.org/10.1111/j.1365-2613.2009.00677.x
https://doi.org/10.1111/j.1365-2613.2009...
). However, the prevalence of conductive hearing loss is
greater, occurring in approximately 60-80% of individuals with DS(99 . Werner LA, Mancl LR, Folsom RC. Preliminary observations on the
development of auditory sensitivity in infants with Down syndrome. Ear Hear.
1996;17(6):455-68.
10 . Tomé DC, Sanchez TG, Bento RF. Síndrome de Down e o
otorrinolaringologista: características gerais e aspectos otológicos (Parte I).
Arq Int Otorrinolaringol. 1999;3(3):93-8.-1111 . Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion
products otoacoustic emissions in diagnosis of hearing loss in Down syndrome.
Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206.
http://dx.doi.org/10.1016/S0165-5876(98)00106-2
https://doi.org/10.1016/S0165-5876(98)00...
).
Histopathological studies have shown that in cases of secretory otitis media,
there may be diffusion of bacterial toxins and cytokines from the middle ear to
the cochlea by way of the round window membrane. These events can cause
structural injury to the inner ear, such as rupture of cochlear membranes,
resulting in sensorineural hearing loss(1212 . Winter AJ, Comis SD, Osborne MP, Tarlow MJ, Stephen J, Andrew PW,
et al. A role for pneumolysin but not neuraminidase in the hearing loss and
cochlear damage induced by experimental pneumococcal meningitis in guinea pigs.
Infect Immun. 1997;65(11):4411-8.
13 . Cauwenbege P, Watelet JB, Dhooge I. Uncommon and unusual
complications of otitis media with effusion. Int J Pediatr Otorhinolaryngol.
1999;49 Suppl 1:S119-25.
http://dx.doi.org/10.1016/S0165-5876(99)00214-1
https://doi.org/10.1016/S0165-5876(99)00...
-1414 . Tuomanen EI. Pathogenesis of pneumococcal inflammation: otitis
media. Vaccine. 2000;19 Suppl 1:38-40.
http://dx.doi.org/10.1016/S0264-410X(00)00276-0
https://doi.org/10.1016/S0264-410X(00)00...
).
Congenital abnormalities of the inner ear are not frequent, although individuals
with DS present with anatomically smaller cochlea than typically developing
children(1515 . Harada T, Sando I. Temporal bone histopathologic findings in
Down´s syndrome. Arch Otolaryngol. 1981;107(2):96-103.).
Moreover, beginning in the second decade of life, individuals with DS present a
decline in hearing thresholds with a progressive “presbycusis” type
pattern(1010 . Tomé DC, Sanchez TG, Bento RF. Síndrome de Down e o
otorrinolaringologista: características gerais e aspectos otológicos (Parte I).
Arq Int Otorrinolaringol. 1999;3(3):93-8.,1111 . Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion
products otoacoustic emissions in diagnosis of hearing loss in Down syndrome.
Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206.
http://dx.doi.org/10.1016/S0165-5876(98)00106-2
https://doi.org/10.1016/S0165-5876(98)00...
,1616 . Marcell MM. Relationships between hearing and auditory cognition
in Down’s syndrome youth. Downs Syndr Res Pract. 1995;3(3):75-91.
http://dx.doi.org/10.3104/reports.54
https://doi.org/10.3104/reports.54...
).
Few studies have performed peripheral auditory system evaluations in subjects with DS. Because hearing loss can impair language development and oral expression, complete audiological evaluation of these individuals is crucial for differential diagnosis and treatment guidance. This study therefore aimed to characterize the peripheral auditory system of individuals with DS, using both conventional and high-frequency audiometry.
METHODS
This was a prospective observational study approved by the Ethics Committee for Analysis of Research Projects, School of Medicine, Universidade de São Paulo (USP) (No. 138/11). In addition, parents or guardians signed informed consent forms prior to enrollment in the study.
A total of 15 individuals with DS were studied; these patients were of both genders, between the ages of 7 and 15 years (mean 10 years and 9 months ± 1 year and 6 months) and included 8 females and 7 males. The presence of other associated impairments, such as neurological and psychiatric disorders that could impede the application of audiological procedures, was considered exclusion criteria. It should be noted that subjects’ handedness was not considered in the present study.
First, an interview was conducted with parents or guardians in which information about medical and otologic history was collected. The external auditory canal and tympanic membrane were then examined to determine the existence of problems that could interfere with the evaluation, such as the presence of cerumen, foreign bodies, etc. A Heine® otoscope was used for this examination.
To investigate the ipsilateral and contralateral acoustic reflexes and mobility
of the tympanic-ossicular chain, immittance testing was performed using an
Interacoustics® AT 235 analyzer. A type A tympanogram with the presence of
acoustic reflex was considered a normal result, whereas a type B or C
tympanogram and/or the absence of acoustic reflex was considered an abnormal
result(1717 . Jerger J. Clinical experience with impedance audiometry. Arch
Otolaryngol.1970;92(4):311-24
http://dx.doi.org/10.1001/archotol.1970.04310040005002
https://doi.org/10.1001/archotol.1970.04...
).
Conventional pure-tone audiometry and high-frequency audiometry were performed in
a soundproof booth using a GSI-61 audiometer (Grason-Stadler®) and model TDH-50
and HDA 200 supra-aural headphones(1818 . Ferreira MS, Almeida K, Atherino CCT. Limiares de audibilidade em
altas frequências em crianças com história de otite média secretora bilateral.
Rev Bras Otorrinolaringol. 2007;73(2):231-8.
http://dx.doi.org/10.1590/S0034-72992007000200014
https://doi.org/10.1590/S0034-7299200700...
).
Hearing thresholds with air conduction were obtained at frequencies ranging from
250-8,000 Hz and with bone conduction at frequencies from 500-4,000 Hz whenever
air conduction thresholds exceeded 15 dB HL. Air conduction thresholds above 15
dB HL were defined as the presence of hearing loss. Hearing losses were
classified according to type, either as conductive hearing loss or sensorineural
hearing loss, and according to degree, using the mean of the 500-4,000 Hz
frequencies(1919 . Russo ICP, Pereira LD, Carvallo RMM, Anastásio ART.
Encaminhamentos sobre a classificação do grau de perda auditiva em nossa
realidade. Rev Soc Bras Fonoaudiol. 2009;14(2):287-8.
http://dx.doi.org/10.1590/S1516-80342009000200023
https://doi.org/10.1590/S1516-8034200900...
). It is
important to note that classification according to degree was not performed in
cases of hearing loss at an isolated frequency.
Next, speech audiometry was performed to obtain the speech reception threshold (SRT) and speech discrimination index (SDI)(2020 . Santos TMM, Russo ICP. Logoaudiometria. In: Santos TMM, Russo ICP. A prática da audiologia clínica. 3a ed. São Paulo: Cortez; 1991.p. 73-88.).
High-frequency audiometry was also carried out at the following frequencies: 9,000, 10,000, 12,500, 14,000, 16,000, 18,000 and 20,000 Hz (investigated in this order). All thresholds (obtained in dB HL) were determined using the descending method in steps of 10 dB and the ascending method in steps of 5 dB. The hearing thresholds at high frequencies were classified as normal according to the mean standards for high-frequency thresholds (10, 12.5, 14 and 16 kHz) proposed by a previous study(2121 . Pedalini MEB, Sanchez TG, D’Antonio A, D’Antonio W, Balbani A, Hachiya A, et al. Média dos limiares tonais na audiometria de alta frequência em indivíduos normais de 4 a 60 anos. Pró Fono. 2000;12(2):17-20.) for each age group. The result was classified as abnormal if one or more frequencies in one or both ears was higher than the previously proposed standard(2121 . Pedalini MEB, Sanchez TG, D’Antonio A, D’Antonio W, Balbani A, Hachiya A, et al. Média dos limiares tonais na audiometria de alta frequência em indivíduos normais de 4 a 60 anos. Pró Fono. 2000;12(2):17-20.).
All subjects were evaluated in a maximum of two sessions, performed on sequential days, and acoustic impedance measurements were always performed at the beginning of the evaluation.
Data analysis
For data analysis, a quantitative and qualitative description of the audiological profile of individuals with DS was made. The Wilcoxon test, equality of two proportions, ANOVA and the Pearson correlation coefficient were used for statistical analysis. The results were analyzed with a significance level of 5% (0.05).
RESULTS
With regard to the otological history of the 15 children, 10 had a history of otitis media, and the number of episodes in these 10 individuals ranged from 2 to 8 (average 5.3 episodes).
There was a higher percentage of subjects with abnormal immittance testing results (tympanometry and acoustic reflexes) bilaterally. However, this difference was not significant (Table 1).
There was no difference between the right and left ears for audiometric thresholds between 250 and 8,000 Hz. However, for high frequencies, differences were observed between right and left ears at frequencies of 9,000 Hz and 11,200 Hz, with worse thresholds for the left ear. Qualitative analysis by individual revealed the following results:
-
- Five subjects (33.3%) had mild conductive hearing loss, considering the mean of the 500-4,000 Hz frequencies in one or both ears (accompanied by changes in immittance testing, type B or C tympanograms and/or the absence of acoustic reflexes);
-
- Three subjects (20.0%) had hearing loss at the 8,000 Hz frequency alone, in one or both ears (with or without a change in immittance testing);
-
- Four subjects (26.7%) had hearing thresholds within normal limits in both ears (accompanied by changes in immittance testing, type C tympanograms and the absence of acoustic reflexes);
-
- Three subjects (20.0%) had hearing thresholds within normal limits in both ears (accompanied by normal results on immittance testing).
In the classification of hearing thresholds at high frequencies, only 2 individuals (13.33%) presented normal results for the frequencies tested, whereas 13 children (86.67%) showed altered hearing thresholds.
Comparisons between right and left ears in pure-tone air conduction audiometry are presented in Table 2.
Comparisons between right and left ears using the SRT and SDI tests revealed differences that were not considered significant (Table 3).
The Pearson correlation coefficient indicated a moderate positive correlation between age and the 9-14 kHz thresholds and a weak positive correlation for the other hearing thresholds evaluated. These results indicated that increased age was associated with a deterioration of hearing thresholds, mainly at the frequencies that demonstrated a moderately positive correlation (Table 4).
DISCUSSION
One of the characteristics observed in DS is the high prevalence of hearing loss
due to middle ear infections(77 . Roizen NJ. Down syndrome. In: Batshaw ML. Children with
disabilities. 5th ed. Baltimore: Brookes; 2002. p. 361–76.
8 . Han F, Yu H, Zhang J, Tian C, Schmidt C, Nava C, et al. Otitis
media in a mouse model for Down syndrome. Int J Exp Pathol. 2009;90(5):480-8.
http://dx.doi.org/10.1111/j.1365-2613.2009.00677.x
https://doi.org/10.1111/j.1365-2613.2009...
9 . Werner LA, Mancl LR, Folsom RC. Preliminary observations on the
development of auditory sensitivity in infants with Down syndrome. Ear Hear.
1996;17(6):455-68.
10 . Tomé DC, Sanchez TG, Bento RF. Síndrome de Down e o
otorrinolaringologista: características gerais e aspectos otológicos (Parte I).
Arq Int Otorrinolaringol. 1999;3(3):93-8.-1111 . Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion
products otoacoustic emissions in diagnosis of hearing loss in Down syndrome.
Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206.
http://dx.doi.org/10.1016/S0165-5876(98)00106-2
https://doi.org/10.1016/S0165-5876(98)00...
). Abnormal immittance testing
results were obtained for 66.6% of subjects in this study, which agrees with the
prevalence observed in previous studies.
In addition, 33.3% of subjects showed mild conductive hearing loss in one or both
ears, and 26.7% had hearing thresholds within normal limits in both ears, but
with abnormalities in immittance testing. These results suggest that these
children may have been entering or leaving an episode of otitis media, although
hearing thresholds were not compromised, confirming other findings reported in
the literature(1111 . Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion
products otoacoustic emissions in diagnosis of hearing loss in Down syndrome.
Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206.
http://dx.doi.org/10.1016/S0165-5876(98)00106-2
https://doi.org/10.1016/S0165-5876(98)00...
,1616 . Marcell MM. Relationships between hearing and auditory cognition
in Down’s syndrome youth. Downs Syndr Res Pract. 1995;3(3):75-91.
http://dx.doi.org/10.3104/reports.54
https://doi.org/10.3104/reports.54...
).
The prevalence of otitis media episodes, as evidenced by the otologic history of
the study participants, also agrees with the literature(77 . Roizen NJ. Down syndrome. In: Batshaw ML. Children with
disabilities. 5th ed. Baltimore: Brookes; 2002. p. 361–76.
8 . Han F, Yu H, Zhang J, Tian C, Schmidt C, Nava C, et al. Otitis
media in a mouse model for Down syndrome. Int J Exp Pathol. 2009;90(5):480-8.
http://dx.doi.org/10.1111/j.1365-2613.2009.00677.x
https://doi.org/10.1111/j.1365-2613.2009...
9 . Werner LA, Mancl LR, Folsom RC. Preliminary observations on the
development of auditory sensitivity in infants with Down syndrome. Ear Hear.
1996;17(6):455-68.
10 . Tomé DC, Sanchez TG, Bento RF. Síndrome de Down e o
otorrinolaringologista: características gerais e aspectos otológicos (Parte I).
Arq Int Otorrinolaringol. 1999;3(3):93-8.-1111 . Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion
products otoacoustic emissions in diagnosis of hearing loss in Down syndrome.
Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206.
http://dx.doi.org/10.1016/S0165-5876(98)00106-2
https://doi.org/10.1016/S0165-5876(98)00...
); we found that 66% of DS subjects had a history of
otitis, with a mean of 5.3 episodes.
The literature also reports that abnormalities of the inner ear are not common in
individuals with DS(1515 . Harada T, Sando I. Temporal bone histopathologic findings in
Down´s syndrome. Arch Otolaryngol. 1981;107(2):96-103.), which
is in agreement with the findings of this study, which did not detect
sensorineural hearing loss in any case. It is important to note that there is a
tendency toward increased sensorineural hearing loss in the second decade of
life in individuals with DS(1111 . Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion
products otoacoustic emissions in diagnosis of hearing loss in Down syndrome.
Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206.
http://dx.doi.org/10.1016/S0165-5876(98)00106-2
https://doi.org/10.1016/S0165-5876(98)00...
), although this was not the case for participants in the
present study.
Regarding conventional audiometry hearing thresholds, there was no difference
between left and right ears or for the SRT and SDI speech tests, which is in
agreement with a previous study(2222 . Oliveira DCCM, Lima MAMT. Da audiometria tonal limiar em baixa e
alta frequência: comparação dos limiares auditivos entre tabagistas e
não-tabagistas. Braz J Otorhinolaryngol. 2009;75(5):738-44.
http://dx.doi.org/10.1590/S1808-86942009000500021
https://doi.org/10.1590/S1808-8694200900...
).
Differences were observed between the right and left ears for high frequencies at
9,000 Hz and 11,200 Hz. In addition, left ears presented air conduction
thresholds at high frequencies higher than right ears, and this finding was also
reported in another study for frequencies of 9 kHz and 11.2 kHz(2323 . Kotzias SA. Influência na fala das altas frequências em portadores
de hipoacusia neurossensorial severa e profunda bilateral pré-lingual [tese de
doutorado]. São Paulo: Faculdade de Medicina da Universidade de São Paulo;
2004.). However, most studies
demonstrate concordance of results in regard to the absence of differences
between the high-frequency thresholds obtained in the left and right
ear(2121 . Pedalini MEB, Sanchez TG, D’Antonio A, D’Antonio W, Balbani A,
Hachiya A, et al. Média dos limiares tonais na audiometria de alta frequência em
indivíduos normais de 4 a 60 anos. Pró Fono. 2000;12(2):17-20.,2424 . Zeigelboim BS, Mangabeira-Albernaz PL, Fukuda Y. High frequency
audiometry and chronic renal failure. Acta Otolaryngol. 2001;121(2):245-8.
http://dx.doi.org/10.1080/000164801300043686
https://doi.org/10.1080/0001648013000436...
25 . Retamal MCR, Marochi R, Zeigelboim BS, Marques JM. Estudo dos
limiares de audibilidade nas altas frequências em indivíduos monitoramento
normo-ouvintes de 12 a 19 anos. Distúrb Comun.
2004;16(1):35-42.
26 . Figueredo RBS, Corona AP. Influência do zumbido nos limiares
auditivos de altas frequências. Rev Soc Bras Fonoaudiol. 2007;12(1):29-33.
http://dx.doi.org/10.1590/S1516-80342007000100007
https://doi.org/10.1590/S1516-8034200700...
-2727 . Carvallo RMM, Koga MC, Carvalho M, Ishida IM. Limiares auditivos
para altas frequências em adultos sem queixa auditiva. Acta AWHO.
2002;21(1):62-6.).
High-frequency audiometry (above 8 kHz) has been shown to be sensitive for
measuring cochlear function and can diagnose sensory dysfunction earlier than
conventional audiometry(2828 . Wiley TL, Torre III P, Cruickshanks KJ, Nondahl DM, Tweed TS.
Hearing sensitivity in adults screened for selected risk factors. J Am Acad
Audiol. 2001;12(7):337-47.).
However, there is no standard of normality for high frequencies, and thus, it is
recommended that hearing thresholds should be compared among groups, while
controlling for the “age” variable and defining similar patterns among groups
for conventional pure-tone thresholds(2929 . Klagenberg KF, Oliva FC, Gonçalves CGO, Lacerda ABM, Garofani VG,
Zeigelboim BS. Audiometria de altas frequências no diagnóstico complementar em
audiologia: uma revisão da literatura nacional. Rev Soc Bras Fonoaudiol.
2011;16(1):109-14.
http://dx.doi.org/10.1590/S1516-80342011000100020
https://doi.org/10.1590/S1516-8034201100...
).
One previous study on this theme(2121 . Pedalini MEB, Sanchez TG, D’Antonio A, D’Antonio W, Balbani A, Hachiya A, et al. Média dos limiares tonais na audiometria de alta frequência em indivíduos normais de 4 a 60 anos. Pró Fono. 2000;12(2):17-20.) determined a mean standard for high-frequency thresholds in individuals without otological disorders between 4 and 60 years of age, distributed according to age group. Comparing the thresholds obtained in this study with those proposed in the previous study, 86.67% of children with DS showed abnormal hearing thresholds.
In another study on this topic, 31 children aged 7 to 12 years were evaluated,
with hearing thresholds below 20 dB HL, for conventional audiometry frequencies.
The children were divided into 2 groups: one group with up to 3 episodes of
otitis and the other with 4 or more episodes of otitis media. The second group
showed higher hearing thresholds at high frequencies at all frequencies
evaluated. The mean 9-18 kHz thresholds did not exceed 15 dB HL for the first
group but were between 13 and 26 dB HL for the second group, suggesting that 4
episodes of otitis media are sufficient to determine differences in hearing
thresholds at high frequencies(1818 . Ferreira MS, Almeida K, Atherino CCT. Limiares de audibilidade em
altas frequências em crianças com história de otite média secretora bilateral.
Rev Bras Otorrinolaringol. 2007;73(2):231-8.
http://dx.doi.org/10.1590/S0034-72992007000200014
https://doi.org/10.1590/S0034-7299200700...
).
According to the results of the above-cited study(1818 . Ferreira MS, Almeida K, Atherino CCT. Limiares de audibilidade em
altas frequências em crianças com história de otite média secretora bilateral.
Rev Bras Otorrinolaringol. 2007;73(2):231-8.
http://dx.doi.org/10.1590/S0034-72992007000200014
https://doi.org/10.1590/S0034-7299200700...
), which was performed with children of a
similar age to those in the present study as well as a history of frequent
otitis media, it can be concluded that the thresholds obtained in the present
study were worse for all high frequencies evaluated, suggesting that cochlear
function in these children can be affected even in the absence of sensorineural
hearing loss in conventional audiometry. It can also be inferred that the
presence of hearing loss only at 8,000 Hz, observed in this study in 20% of
cases, suggests that cochlear impairment was the result of frequent otitis media
in individuals with DS.
It has also been reported that high-frequency audiometry is more sensitive to the effects of otitis media on cochlear function, most likely due to the proximity of the region responsible for the high frequencies in the cochlea to the round window membrane and the middle ear space. In addition, recurrent episodes of otitis media may damage high-frequency thresholds in the long term, even after complete resolution of the condition(2727 . Carvallo RMM, Koga MC, Carvalho M, Ishida IM. Limiares auditivos para altas frequências em adultos sem queixa auditiva. Acta AWHO. 2002;21(1):62-6.).
It is important to note that individuals with DS may present early cochlear
degeneration, which is referred to as “early presbycusis” by some
authors(1111 . Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion
products otoacoustic emissions in diagnosis of hearing loss in Down syndrome.
Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206.
http://dx.doi.org/10.1016/S0165-5876(98)00106-2
https://doi.org/10.1016/S0165-5876(98)00...
.1616 . Marcell MM. Relationships between hearing and auditory cognition
in Down’s syndrome youth. Downs Syndr Res Pract. 1995;3(3):75-91.
http://dx.doi.org/10.3104/reports.54
https://doi.org/10.3104/reports.54...
). It is therefore believed
that this factor may contribute to reduced hearing thresholds at high
frequencies at an earlier stage. In the present study, the Pearson correlation
coefficient revealed a moderate positive correlation for 9-14 kHz thresholds and
a weak positive correlation for the other hearing thresholds evaluated,
indicating a trend for worsening hearing thresholds with increasing age, even in
very young study subjects.
It is important to mention that the variable “age” is a factor that must be
considered in studies of hearing thresholds at high frequencies, as it has been
shown that small children do not perform well in this evaluation. However, in
the case of the participants in this study, the mean age was approximately 11
years, an age range described as appropriate for investigating hearing
thresholds at high frequencies(2929 . Klagenberg KF, Oliva FC, Gonçalves CGO, Lacerda ABM, Garofani VG,
Zeigelboim BS. Audiometria de altas frequências no diagnóstico complementar em
audiologia: uma revisão da literatura nacional. Rev Soc Bras Fonoaudiol.
2011;16(1):109-14.
http://dx.doi.org/10.1590/S1516-80342011000100020
https://doi.org/10.1590/S1516-8034201100...
).
Although cognitive development in individuals with DS can affect hearing
thresholds, especially with regard to higher frequencies, auditory responses
cannot be disregarded because hearing loss can contribute to the worsening of
cognitive skills in individuals with DS(1616 . Marcell MM. Relationships between hearing and auditory cognition
in Down’s syndrome youth. Downs Syndr Res Pract. 1995;3(3):75-91.
http://dx.doi.org/10.3104/reports.54
https://doi.org/10.3104/reports.54...
). The need for greater care in behavioral hearing
evaluations in this population should therefore be stressed.
Despite these limitations, the present study demonstrated the importance of using high-frequency audiometry to evaluate individuals with DS while monitoring cochlear function. Indeed, frequent episodes of otitis media and the trend toward early cochlear degeneration may contribute to the development of sensorineural hearing loss, which is not initially evident through conventional audiometry alone.
CONCLUSION
Overall, no significant differences were observed when comparing the right and left ears of individuals with DS, in regards to pure-tone audiometry, immittance testing and speech audiometry. Most children presented middle ear abnormalities and conductive hearing loss, and the high-frequency audiometry results suggest the onset of impaired cochlear function, which may be associated with frequent otitis media episodes and/or early cochlear degeneration.
ACKNOWLEDGEMENTS
The authors would like to acknowledge the Foundation for Research Support of the State of São Paulo (Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP) for its support in carrying out this study, case number 2010/18650-3.
REFERÊNCIAS
-
1Ginsberg IA, White TP. Considerações otológicas em audiologia. In: Katz J. Tratado de audiologia clínica. São Paulo: Manole; 1999. p. 6-23.
-
2Limongi SCO. Linguagem na síndrome de Down. In: Ferreira LP, Befi-Lopes DM, Limongi SCO. Tratado de Fonoaudiologia. São Paulo: Rocca; 2004. p. 954-66.
-
3Oliveira ACB, Jorge ML, Paiva SM. Aspectos relevantes à abordagem odontológica da criança com síndrome de Down. Rev CROMG. 2001;7(1):36-42.
-
4Sommer CA, Henrique-Silva F. Trisomy 21 and Down syndrome: a short review. Braz J Biol. 2008;68(2):447-52. http://dx.doi.org/10.1590/S1519-69842008000200031
» https://doi.org/10.1590/S1519-69842008000200031 -
5Mustacchi Z. Síndrome de Down. In: Mustacchi Z, Peres S. Genética baseada em evidências: sídromes e heranças. São Paulo: CID; 2000. p. 817-94.
-
6Balkany TJ, Downs MP, Jafer BW, Krajicek MJ. Hearing loss in Down’s syndrome: a treatable handicap more common than generally recognized. Clin Pediatr (Phila). 1979;18:116-8. http://dx.doi.org/10.1177/000992287901800207
» https://doi.org/10.1177/000992287901800207 -
7Roizen NJ. Down syndrome. In: Batshaw ML. Children with disabilities. 5th ed. Baltimore: Brookes; 2002. p. 361–76.
-
8Han F, Yu H, Zhang J, Tian C, Schmidt C, Nava C, et al. Otitis media in a mouse model for Down syndrome. Int J Exp Pathol. 2009;90(5):480-8. http://dx.doi.org/10.1111/j.1365-2613.2009.00677.x
» https://doi.org/10.1111/j.1365-2613.2009.00677.x -
9Werner LA, Mancl LR, Folsom RC. Preliminary observations on the development of auditory sensitivity in infants with Down syndrome. Ear Hear. 1996;17(6):455-68.
-
10Tomé DC, Sanchez TG, Bento RF. Síndrome de Down e o otorrinolaringologista: características gerais e aspectos otológicos (Parte I). Arq Int Otorrinolaringol. 1999;3(3):93-8.
-
11Hassmann E, Skotnicka B, Midro AT, Musiatowicz M. Distortion products otoacoustic emissions in diagnosis of hearing loss in Down syndrome. Int J Pediatr Otorhinolaryngol. 1998;45(3):199-206. http://dx.doi.org/10.1016/S0165-5876(98)00106-2
» https://doi.org/10.1016/S0165-5876(98)00106-2 -
12Winter AJ, Comis SD, Osborne MP, Tarlow MJ, Stephen J, Andrew PW, et al. A role for pneumolysin but not neuraminidase in the hearing loss and cochlear damage induced by experimental pneumococcal meningitis in guinea pigs. Infect Immun. 1997;65(11):4411-8.
-
13Cauwenbege P, Watelet JB, Dhooge I. Uncommon and unusual complications of otitis media with effusion. Int J Pediatr Otorhinolaryngol. 1999;49 Suppl 1:S119-25. http://dx.doi.org/10.1016/S0165-5876(99)00214-1
» https://doi.org/10.1016/S0165-5876(99)00214-1 -
14Tuomanen EI. Pathogenesis of pneumococcal inflammation: otitis media. Vaccine. 2000;19 Suppl 1:38-40. http://dx.doi.org/10.1016/S0264-410X(00)00276-0
» https://doi.org/10.1016/S0264-410X(00)00276-0 -
15Harada T, Sando I. Temporal bone histopathologic findings in Down´s syndrome. Arch Otolaryngol. 1981;107(2):96-103.
-
16Marcell MM. Relationships between hearing and auditory cognition in Down’s syndrome youth. Downs Syndr Res Pract. 1995;3(3):75-91. http://dx.doi.org/10.3104/reports.54
» https://doi.org/10.3104/reports.54 -
17Jerger J. Clinical experience with impedance audiometry. Arch Otolaryngol.1970;92(4):311-24 http://dx.doi.org/10.1001/archotol.1970.04310040005002
» https://doi.org/10.1001/archotol.1970.04310040005002 -
18Ferreira MS, Almeida K, Atherino CCT. Limiares de audibilidade em altas frequências em crianças com história de otite média secretora bilateral. Rev Bras Otorrinolaringol. 2007;73(2):231-8. http://dx.doi.org/10.1590/S0034-72992007000200014
» https://doi.org/10.1590/S0034-72992007000200014 -
19Russo ICP, Pereira LD, Carvallo RMM, Anastásio ART. Encaminhamentos sobre a classificação do grau de perda auditiva em nossa realidade. Rev Soc Bras Fonoaudiol. 2009;14(2):287-8. http://dx.doi.org/10.1590/S1516-80342009000200023
» https://doi.org/10.1590/S1516-80342009000200023 -
20Santos TMM, Russo ICP. Logoaudiometria. In: Santos TMM, Russo ICP. A prática da audiologia clínica. 3a ed. São Paulo: Cortez; 1991.p. 73-88.
-
21Pedalini MEB, Sanchez TG, D’Antonio A, D’Antonio W, Balbani A, Hachiya A, et al. Média dos limiares tonais na audiometria de alta frequência em indivíduos normais de 4 a 60 anos. Pró Fono. 2000;12(2):17-20.
-
22Oliveira DCCM, Lima MAMT. Da audiometria tonal limiar em baixa e alta frequência: comparação dos limiares auditivos entre tabagistas e não-tabagistas. Braz J Otorhinolaryngol. 2009;75(5):738-44. http://dx.doi.org/10.1590/S1808-86942009000500021
» https://doi.org/10.1590/S1808-86942009000500021 -
23Kotzias SA. Influência na fala das altas frequências em portadores de hipoacusia neurossensorial severa e profunda bilateral pré-lingual [tese de doutorado]. São Paulo: Faculdade de Medicina da Universidade de São Paulo; 2004.
-
24Zeigelboim BS, Mangabeira-Albernaz PL, Fukuda Y. High frequency audiometry and chronic renal failure. Acta Otolaryngol. 2001;121(2):245-8. http://dx.doi.org/10.1080/000164801300043686
» https://doi.org/10.1080/000164801300043686 -
25Retamal MCR, Marochi R, Zeigelboim BS, Marques JM. Estudo dos limiares de audibilidade nas altas frequências em indivíduos monitoramento normo-ouvintes de 12 a 19 anos. Distúrb Comun. 2004;16(1):35-42.
-
26Figueredo RBS, Corona AP. Influência do zumbido nos limiares auditivos de altas frequências. Rev Soc Bras Fonoaudiol. 2007;12(1):29-33. http://dx.doi.org/10.1590/S1516-80342007000100007
» https://doi.org/10.1590/S1516-80342007000100007 -
27Carvallo RMM, Koga MC, Carvalho M, Ishida IM. Limiares auditivos para altas frequências em adultos sem queixa auditiva. Acta AWHO. 2002;21(1):62-6.
-
28Wiley TL, Torre III P, Cruickshanks KJ, Nondahl DM, Tweed TS. Hearing sensitivity in adults screened for selected risk factors. J Am Acad Audiol. 2001;12(7):337-47.
-
29Klagenberg KF, Oliva FC, Gonçalves CGO, Lacerda ABM, Garofani VG, Zeigelboim BS. Audiometria de altas frequências no diagnóstico complementar em audiologia: uma revisão da literatura nacional. Rev Soc Bras Fonoaudiol. 2011;16(1):109-14. http://dx.doi.org/10.1590/S1516-80342011000100020
» https://doi.org/10.1590/S1516-80342011000100020
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Study conducted at the Laboratory of Speech Therapy Research in Primary Care in Audiology, Department of Physical, Speech and Occupational Therapy, School of Medicine, Universidade de São Paulo – USP – São Paulo (SP), Brazil.
Publication Dates
-
Publication in this collection
Sept 2014
History
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Received
29 Aug 2013 -
Accepted
29 July 2014