Acta Oto-Laryngologica

ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20

Auditory processing abilities in children with chronic otitis media with effusion Bahare Khavarghazalani, Farhad Farahani, Maryam Emadi & Zahra Hosseni Dastgerdi To cite this article: Bahare Khavarghazalani, Farhad Farahani, Maryam Emadi & Zahra Hosseni Dastgerdi (2016): Auditory processing abilities in children with chronic otitis media with effusion, Acta Oto-Laryngologica, DOI: 10.3109/00016489.2015.1129552 To link to this article: http://dx.doi.org/10.3109/00016489.2015.1129552

Published online: 16 Feb 2016.

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Date: 21 February 2016, At: 12:36

ACTA OTO-LARYNGOLOGICA, 2016 http://dx.doi.org/10.3109/00016489.2015.1129552

ORIGINAL ARTICLE

Auditory processing abilities in children with chronic otitis media with effusion Bahare Khavarghazalania, Farhad Farahanib, Maryam Emadia and Zahra Hosseni Dastgerdic

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a Department of Audiology, Faculty of Rehabilitation Science, Hamadan University of Medical Sciences, Hamadan, Iran; bFaculty of Otolaryngology, School of Medicine, Hamadan University of Medical Sciences & Health Services, Hamadan, Iran; cDepartment of Audiology, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran

ABSTRACT

ARTICLE HISTORY

Conclusion The study results indicate that children with a history of otitis media with effusion (OME) suffer from auditory processing disorder to some degree. The findings support the hypothesis that fluctuating hearing loss may affect central auditory processing during critical periods. Objectives Evidence suggests that prolonged OME in children can result in an auditory processing disorder, presumably because hearing has been disrupted during an important developmental period. A lack of auditory stimulation leads to the abnormal development of the hearing pathways in the brain. The aim of the present study was to determine the effects of OME on binaural auditory function and auditory temporal processing. Method In the present study, the dichotic digit test (DDT) was used for binaural hearing, and the gap in noise (GIN) test was used to evaluate temporal hearing processing. Results The average values of GIN differed significantly between children with a history of OME and normal controls (p50.001). The mean values of the DDT score were significantly different between the two groups (p ¼ 0.002).

Received 30 October 2015 Revised 26 November 2015 Accepted 30 November 2015 Published online 12 February 2016

Introduction Central auditory processing (CAP) refers to how the central nervous system uses auditory information. Subjects with CAP disorders (CAPD) report difficulties with listening skills, despite normal peripheral auditory function. CAPD appears to be the result of perceptual auditory processing dysfunction. Subjects with CAPD report various symptoms and complaints, such as difficulty in sound localization and lateralization, auditory discrimination, auditory pattern recognition, auditory temporal processing, and poor auditory performance with competing or degraded acoustic signals [1,2]. The primary cause of this disorder may be neural or developmental. Although APD may have a hereditary basis, there is long controversy research that auditory deprivation secondary to chronic otitis media with effusion (OME) impacts auditory processing [3]. OME can lead to mild-to-moderate fluctuating hearing loss in childhood. Chronic OME is a common condition in childhood. Amongst its causes are viral or bacterial infection, Eustachian tube malfunction, and upper respiratory tract infection [4]. OME occurs mainly in children and its prevalence decreases with age. Approximately two out of three children between 1–5 years of age have had OME at least once [5]. Studies show that active OME can cause hearing loss (40 dB), particularly at low frequencies and with transmission delays up to 300 ms [6]. Inappropriate sensory experiences during child development can cause long-term changes in neural function, CONTACT Farhad Farahani Hamadan, Iran ß 2016 Taylor & Francis

[email protected]

KEYWORDS

Auditory processing disorder; auditory temporal processing; binaural auditory function; children; otitis media with effusion

structure, and connectivity. Evidence from animal studies shows that chronic conductive hearing loss may alter auditory system structure and function. For example, unilateral conductive hearing loss can affect the relative size of dendrites in the superior olivary nucleus [7]. By occluding one ear and making a unilateral conductive hearing loss, the balance of input to higher levels of the brain is altered [8]. OME may, thus, alter brain function, and OME-related changes in the auditory nervous system are more long lasting than other types of conductive hearing losses [9]. Hearing fluctuation in OME occurs in one or both ears and may last a few days to several weeks. Although some studies have shown that, after OME treatment, binaural hearing disorders or other auditory deficits remain, OME sensory disorders seem to be reversible and auditory training may accelerate the recovery process. Chronic OME is accompanied by a set of sensory, cognitive, and social impairments; moreover, its effects on hearing may be acute and temporary or chronic and permanent. There is no consensus about OME-related disorders. The aim of the present study was to determine the effects of OME on binaural auditory function and auditory temporal processing.

Method Participants This cross-comparative study sampled 12 children with a history of OME (seven males, five females) between the ages of

Faculty of Otolaryngology, School of Medicine, Hamadan University of Medical Sciences & Health Services,

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B. KHAVARGHAZALANI ET AL.

8–10 years. Children with a history of OME were selected from available patients, based on inclusion criteria, from Hamedan Besaat Hospital during the period from 2008–2011. The control group subjects were selected according to their age and inclusion criteria. Inclusion criteria for all participants was as follows: 8– 10-year old age range, normal hearing levels (Air conduction and bone conduction thresholds was in normal limit, by Interacoustics AC33 clinical audiometer), normal otoscopy (by Heine mini 3000), and tympanometry (An tympanogram by GSI 39), right-handedness (by Edinburgh handedness inventory). Children in the OME group had history of recurrent OME in childhood and history of ventilation tube (VT) in both ears before the age of 5 years, and children in the control group had no history of recurrent OME. Air conduction and bone conduction thresholds were evaluated in 250–8000 HZ octave frequencies. The gap in noise test (GIN) and dichotic digit test (DDT) were performed at the most comfortable level of 50 dB sensation level (SL) by a CD player connected to the audiometer. Before testing, all parents were informed about the test procedures and the non-invasive nature of the tests. The participants were volunteers and signed a written consent form. Test materials Gin This test is sensitive to central auditory nervous system deficits and temporal lobe lesions. It consists of 6-s segments of broadband noise (white noise) containing three silent intervals. The silent gaps have random durations including 2, 3, 4, 5, 6, 8, 10, 12, 15, and 20 ms, and subjects must respond to silent gaps. Ten items were used before the actual test for practice and were intended to familiarize subjects with the task. Two indices of responses were analyzed: the GIN approximate threshold, which is determined as the shortest gap duration that a person can detect in at least four of six presentations, and the percentage of correct answers for each ear. The sensitivity and specificity of this test are 72% and 94%, respectively [10].

Results The participants were 12 children with a history of OME (mean age ¼ 9.4  0.5) and 14 normal children (mean age ¼ 9.5  0.5). GIN and DDT were performed in both groups.

GIN results The results of the GIN approximate threshold and the percentage of correct answers are presented in Table 1. Neither the difference between the right and left ear GIN approximate threshold nor the percentage of correct answers were significant, in either group (p ¼ 0.05 and 0.3, respectively; see Table 2). The differences in the total mean scores of both ears were compared for the two groups. The GIN approximate threshold means and the percentage of correct answers were significantly different between children with a history of OME and normal controls (p50.001). In children with a history of OME, the GIN approximate threshold was higher and the percentage of correct answers was lower than that in the normal controls (see Table 3). DDT results Descriptive information about the DDT test in both groups is presented in Table 1. The DDT mean scores differed significantly between the two groups (p ¼ 0.002) (see Table 3). The DDT and GIN performance of each child in both groups is illustrated in Figures 1 and 2. Table 1. Descriptive results (mean  SE). Variables DDa GIN (A.th.)b Right Left Total GIN (%)c Right Left Total

Normal

OME

Total

81.6 (0.4)

78.3 (0.8)

80.1 (0.5)

5.07 (0.07) 5.1 (0.09) 5.1 (0.05)

5.9 (0.3) 5.8 (0.3) 5.8 (0.2)

5.4 (0.1)

64.6 (0.7) 64.3 (0.5) 64.5 (0.4)

60.1 (1.4) 59.7 (1.6) 59.9 (1.08)

62.4 (0.6)

a

Dichotic Digit. Mean GIN approximate thresholds (A.th.). Mean percentage correct for the GIN test.

b c

Ddt This test evaluates the binaural integration at the brainstem and cerebral (via the corpus collusum) levels. Four different digits are presented simultaneously to both ears, and subjects must repeat all numbers, regardless of the ear or presentation order. Before the actual test, a three-digit series is presented for practice. The test consists of 20 dichotic pairs, yielding a total of 40 test items for each ear. Correct repetition of each number yields a score of 2.5%. The scores for each ear have been reported separately [11]. Descriptive statistics, including means and standard deviations, are illustrated in graphs. Based on the Kolmogorov– Smirnov test, data distributions were not normal; thus, the Mann–Whitney U-test with a 0.05 level of significance was used to compare the group results.

Table 2. Statistical Whitney test). Variables GIN (A.th.) Normal Left Right OME Left Right GIN (%) Normal Left Right OME Left Right

results

(Mann–

Mean Rank

Statistic

p

15 14

91

0.5

12.08 12.9

67

0.7

13.04 15.9

77.5

0.3

12.04

66.5

0.7

ACTA OTO-LARYNGOLOGICA

Discussion In the present study, DDT was used to evaluate binaural hearing, and GIN was used to evaluate temporal hearing processing evaluation. The experimental group consisted of children with recurrent OME who had undergone myringotomy surgery between the ages of 3–4-years old.

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OME and binaural hearing DDT scores differed significantly in children with a history of OME and normal controls. This finding is consistent with Borges et al. [12] and Pillsbury et al. [13]. Borges et al. suggested that various factors affect the persistence of OMErelated auditory processing disorders, reporting that children with a history of OME during their first 5 years who attended private kindergartens performed better on auditory tasks than children with a history of OME in state kindergartens. In Hall et al. [14], the Masking level difference (MLD) test was used for binaural hearing evaluation. Children with a history of OME had weaker binaural hearing abilities. Hall et al. showed that primary OME complications are reversible and decrease with age. They followed the binaural hearing function of children with OME over 4 years. Binaural hearing processing deficits were significant before treatment, but decreased afterwards. After 2 years, there were no significant differences between treated children and the control group; only a few children with a history of OME exhibited abnormal binaural processing [14]. In this study, the children had a long history of OME and VT surgery at the age of 4 or 5 years. The present study was conducted after at least 3 years of OME treatment. Most children with OME scored similarly on DDT as the control group; a few children performed worse than the normal controls (Figure 1). These findings demonstrate that lack of sufficient binaural stimulation during OME may lead to binaural processing deficits. Auditory deprivation enhancement may help them receive normal binaural cues, thus resolving binaural deficits. Binaural hearing studies indicate that long-lasting changes in the balance of the inputs from the two ears to the brain may alter CAP and create inappropriate brain circuitry. After treating hearing loss, the brain is capable of making effective connections, and the binaural hearing improves [9]. Moore et al. [15] demonstrated that chronic occlusion of one ear may temporarily change sound conduction pathways and lead to changes in binaural processing. These changes are reversible if ear occlusion is removed. Auditory function recovery may occur over time. Moore et al. suggested that children with OME and other conditions involving long lasting hearing loss develop a type of auditory neural learning. This process is akin to central changes after long-term auditory experiences and auditory training.

However, in both groups, there was no significant difference between the right and left ears. These findings are consistent with Borges et al. [12]. Borges et al. studied the effects of OME on auditory processing in children who had received VT before the age of 5. They used a series of tests, including GIN, and found that these children had a higher prevalence of temporal processing disorders than normal controls. Hall et al. [16] used co-modulation masking release (CMR) as an auditory temporal processing test. Hall et al. found that children with a history of OME had lower scores on this test than normal controls. In the present study, some children with a history of OME performed worse on the GIN test as compared to the normal controls (Figure 2). It appears that children with an early history of OME suffer from temporal processing disorders, owing to the lack of appropriate auditory development. After treating conductive hearing loss, temporal processing can recover to its pre-morbid level of function. These findings are consistent with those of Hartley and Moore [17]. It appears that only chronic OME causes OME-related auditory deprivation and auditory processing disorders. This situation is also true for children who do not have sufficient communication. Lack of communication is a type of auditory deprivation and can exacerbate OME-related auditory deprivation. Table 3. Statistical results (Mann–Whitney test). Variables Mean rank Statistic GIN (A.th.) Normal OME GIN (%) Normal OME DD Normal OME

p

21.07 32.3

184.0

50.001*

33.8 18.0

132.0

50.001*

17.5 8.7

27.0

0.002*

*Significant at 0.05.

OME and auditory temporal processing The GIN test in children with OME showed that the thresholds were significantly higher and the percentage of correct answers was significantly lower than that in the control group.

3

Figure 1. Individual DDT results for normal and OME groups.

4

B. KHAVARGHAZALANI ET AL.

Acknowledgements We are very grateful to the patients and individuals who participated in this study. The research was supported by Hamadan University of Medical Sciences and Health Services.

Disclosure statement The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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References

Figure 2. Individual GIN approximate thresholds (A.th.) for normal and OME groups.

This and similar studies demonstrate that recurrent OME and hearing loss is an obstacle to consistent, appropriate auditory input to the central auditory nervous system and may cause temporal encoding and deficits in temporal resolution. Auditory temporal resolution is a key factor in speech understanding and language acquisition. Identification of transient phonemes is dependent on this resolution. Haapala et al. [18] used event-related potentials including mismatch negativity in children with a history of OME to evaluate cortical speech processing. They demonstrated problems in the discrimination of fast speech elements, such as consonants. Thus, alterations to auditory temporal processing, even temporary and mild disorders, may interfere with speech understanding and, consequently, with the education and social development of children.

Conclusion OME may cause mild-to-moderate conductive hearing loss. During critical periods, this fluctuating hearing loss may alter central auditory processing and interfere with speech and language development. OME is mainly reversible, but may be chronic. Early interventions and the provision of rich speech and language stimuli after OME treatment can decrease the complications associated with auditory deprivation. It is recommended that children with a history of OME be evaluated using both temporal and dichotic hearing processing tests, as these represent two critical auditory abilities. Appropriate aural rehabilitation is essential to manage auditory processing problems. Rehabilitation plans should be tailored to the needs of the individual child.

[1] Dawes P, Bishop D. Auditory processing disorder in relation to developmental disorders of language, communication and attention: a review and critique. Int J Lang Commun Disord 2009;44:440–65. [2] Moore DR, Ferguson MA, Edmondson-Jones AM, Ratib S, Riley A. Nature of auditory processing disorder in children. Pediatrics 2010;126:e382–90. [3] Moore DR. Auditory processing disorders: acquisition and treatment. J Commun Disord 2007;40:295–304. [4] Roberts J, Hunter L, Gravel J, Rosenfeld R, Berman S, Haggard M, et al. Otitis media, hearing loss, and language learning: controversies and current research. J Dev Behav Pediatr 2004;25:110–22. [5] Chhetri SS. Acute otitis media: a simple diagnosis, a simple treatment. Nepal Med Coll J 2014;16:33–6. [6] Hartley DE, Moore DR. Effects of conductive hearing loss on temporal aspects of sound transmission through the ear. Hear Res. 2003;177:53–60. [7] Tucci DL, Rubel EW. Afferent influences on brain stem auditory nuclei of the chicken: effects of conductive and sensorineural hearing loss on n. magnocellularis. J Comp Neurol 1985;238:371–81. [8] Moore DR, Hutchings ME, King AJ, Kowalchuk NE. Auditory brain stem of the ferret: some effects of rearing with a unilateral ear plug on the cochlea, cochlear nucleus, and projections to the inferior colliculus. J Neurosci 1989;9:1213–22. [9] Moore DR, Hartley DE Hogan SC, editors. Effects of otitis media with effusion (OME) on central auditory function. Int J Pediatr Otorhinolaryngol. 2003;67 Suppl 1:S63–7. [10] Musiek FE, Shinn JB, Jirsa R, Bamiou D-E, Baran JA, Zaida E. GIN (Gaps-In-Noise) test performance in subjects with confirmed central auditory nervous system involvement. Ear Hear 2005;26:608–18. [11] Musiek FE. Assessment of central auditory dysfunction: the dichotic digit test revisited. Ear Hear 1983;4:79–83. [12] Borges LR, Paschoal JR, Colella-Santos MF. (Central) auditory processing: the impact of otitis media. Clinics (Sao Paulo) 2013;68:954–9. [13] Pillsbury HC, Grose JH, Hall JW. Otitis media with effusion in children. Binaural hearing before and after corrective surgery. Arch Otolaryngol Head Neck Surg 1991;117:718–23. [14] Hall JW III, Grose JH, Pillsbury HC. Long-term effects of chronic otitis media on binaural hearing in children. Arch Otolaryngol Head Neck Surg 1995;121:847–52. [15] Moore DR, Hine JE, Jiang ZD, Matsuda H, Parsons CH, King AJ. Conductive hearing loss produces a reversible binaural hearing impairment. J Neurosci 1999;19:8704–11. [16] Hall JW, Grose JH, Dev MB, Drake AF, Pillsbury HC. The effect of otitis media with effusion on complex masking tasks in children. Arch Otolaryngol Head Neck Surg 1998;124:892–6. [17] Hartley DE, Moore DR. Effects of otitis media with effusion on auditory temporal resolution. Int J Pediatr Otorhinolaryngol 2005;69:757–69. [18] Haapala S, Niemitalo-Haapola E, Raappana A, Kujala T, Suominen K, Kujala T, et al. Effects of recurrent acute otitis media on cortical speech-sound processing in 2-year old children. Ear Hear 2014;35:e75–83.

Auditory processing abilities in children with chronic otitis media with effusion.

The study results indicate that children with a history of otitis media with effusion (OME) suffer from auditory processing disorder to some degree. T...
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