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Artigo Original

Kátia de Freitas Alvarenga1 Eliene Silva Araújo1 Érika Ferraz1 Patrícia Abreu Pinheiro Crenitte1

Descritores

Potenciais evocados auditivos Audição Potencial evocado P300 Dislexia Leitura Aprendizagem

Keywords

Evoked potentials, auditory Hearing Event-related potentials, P300 Dyslexia

Reading Learning

Correspondence address: Kátia de Freitas Alvarenga Departamento de Fonoaudiologia Alameda Octávio Pinheiro Brisola, 9-75, Bauru (SP), Brasil, CEP: 17012-901. E-mail: katialv@fob.usp.br

Received: 09/12/2012

Study carried out at the Speech Therapy Department, Dentistry School of Bauru at Universidade de São Paulo – USP – Bauru (SP), Brazil.

(1) Universidade de São Paulo – USP – Bauru (SP), Brazil.

Financial support: São Paulo Research Foundation (FAPESP), process n. 2009/11114-1. Conlict of interests: nothing to declare.

indicator of therapeutical evolution in students with

developmental dyslexia

Potencial Cognitivo Auditivo - P300 como indicador de evolução

terapêutica em escolares com Dislexia do Desenvolvimento

ABSTRACT

Purpose: To verify the effectiveness of the Cognitive Auditory Evoked Potential-P300 (CAEP-P300) for monitoring the therapeutical evolution of students with developmental dyslexia. Methods: Twenty students diagnosed with developmental dyslexia, of both genders, aged between 8 and 14 years, divided into two randomized groups, one of them submitted to a phonological remediation program associated with reading and writing (GI), and the other one representing the control group (GII), participated in the study. The groups were paired up, and the individuals were submitted to two evaluations of the CAEP-P300 and the same interval was kept for both. Paired Student’s t-test, ANOVA test, and Pearson’s correlation coeficient were used, adopting 5% signiicance level. Results: The statistical comparison of the pre and post evaluations of each group demonstrated difference in the Phonological Awareness Test (p=0.000) and in the P300 latency (p=0.005) only for GI. Conclusion: CAEP-P300 use for monitoring the therapeutical evolution of children with developmental dyslexia is possible and represents a viable option for intervention programs.

RESUMO

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INTRODUCTION

Developmental dyslexia consists in a range of speciic symptoms that imply in sub-cortical and cortical dysfunctions, which frequently have a constitutional origin and may affect reading and writing learning processes(1). In order to compre-hend dyslexia manifestations, the literature focuses on the phonological deicit(2) hypothesis; however, there is still no con-sensus about it. One of the hypotheses is that the phonological deicit happens due to changes in the auditory processing, i.e. children with dyslexia present an altered sound discrimination ability, therefore the quick fusion of stimuli is compromised, resulting in the temporal processing alteration(3,4).

Taking into account this assumption, intervention programs have been focused on the maximization of phonological abili-ties, with satisfactory results(5-8). However, the eficacy verii-cation of such programs as well as the therapeutical evolution monitoring have been restricted to behavioral measures, with a limited quantity of studies in the national and international literatures that use methods aimed for this purpose.

Thus, auditory evoked potentials are well-recognized, since neurophysiological changes tend to happen before the behav-ioral ones(9). The Cognitive Auditory Evoked Potential-P300 (CAEP-P300) has been used to measure and monitor neuro-physiological modiications of the central auditory nervous system(10-12). Also known as a potential associated with events, it is an endogenous potential elicited by auditory discrimina-tion, when the subject reacts to rare stimuli randomly presented between frequent stimuli (Oddball paradigm)(13,14).

The P300 component happens when the subject consciously recognizes the presence of a change in the auditory stimulus, however the exact generators are unknown, but it includes reticular formation, lemniscus, inferior colliculus, thalamus, primary cortex, frontal cortex, centro-parietal cortex, temporal cortex, and hippocampus(13,15). On the other hand, the N200 component is associated with perception, discrimination, recognition, and classiication of an auditory stimulus and has multiple generators, among which is the supratemporal cor-tex(13,15). Thereby, its use can be investigated in students with developmental dyslexia, once they present alterations in their phonological aptitudes.

In the light of what has been exposed, the objective of this study was to verify the CAEP-P300 effectiveness for monitor-ing the therapeutical evolution of students with developmental dyslexia that were submitted to phonological remediation as-sociated with reading and writing.

METHODS

The study was approved by the Ethics Committee of Human Beings Research from Faculdade de Odontologia de Bauru at São Paulo University (FOB-USP), process number 008/2011. All participants and people in charge were aware of the pro-cedures, received the information letter, and signed the Free Informed Consent.

From 2008 to 2010, 350 children complaining about learning dificulties were sent to the Speech Therapy Clinic

of FOB-USP. Among them, only 20 were diagnosed with developmental dyslexia, forming the casuistry of this study. Diagnosis was carried out by an interdisciplinary team in the Speech Therapy Clinic of FOB-USP, following DSM-IV (2002) and ICD-10 criteria. As part of the protocol from the Speech Therapy Diagnostic Clinic of the institution, neuro-psychological, neurological, psychopedagogical, and speech therapy evaluations were performed. Furthermore, the school is contacted in order to obtain relevant data for the inal diagnosis.

The age range of these children varied from 8 to 14 years old, of both genders, and they were regularly enrolled in public and private schools. Regardless of age, all children presented the same level of reading dificulties, which was proved by previous diagnosis evaluation.

The inclusion factors included absence of recent or previ-ous complaints about visual and hearing acuity, normal cog-nitive performance, and absence of genetics or neurological syndromes. The casuistry was randomly divided into two groups: Group I (GI) included 10 students, who were submit-ted to a phonological remediation program associasubmit-ted with reading and writing, and Group II (GII) was composed of 10 students, who initially did not receive any intervention, they became the control group of the study in order to demonstrate the variation test–retest.

The program used for this study was based on Salgado(16) and structured in three different stages, with 24 cumulative sessions, twice a week, lasting around 45 minutes each. The original program proposed by Salgado(16) has 20 sessions; however, this study added other four sessions in order to better develop the abilities under work. The sessions were divided into three different stages, with eight each, being:

1. Phonological (eight sessions), which includes hearing discrimination; sum and subtraction of phonemes and syl-lables; syllabic and phonemic manipulation; rhyme and alliteration.

2. Phonological and Reading (eight sessions), which encloses hearing discrimination; sum and subtraction of phonemes and syllables; syllabic and phonemic manipulation; rhyme; alliteration; letters and phonemes identiication; fast nomi-nation: letters–digits; visual discrimination; silent story reading–oral comprehension; and oral story reading–oral comprehension.

3. Phonological, Reading, and Writing (eight sessions), which include hearing discrimination; sum and subtraction of pho-nemes and syllables; syllabic and phonemic manipulation; rhyme; alliteration; letters and phonemes identiication; fast nomination: letters–digits; visual discrimination; silent story reading–oral comprehension; oral story reading–oral comprehension; dictation of syllables, real words and pseudowords; dictations of sentences; dictation of texts; and written storytelling.

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The objective evaluation of Phonological Awareness (PA) was performed for this study through the Sequential Evaluation Instrument (Conias)(17), which has the aim of verifying the child’s PA level, at the syllabic and phonemic levels, using speciic tests. It is composed of two parts; the irst one corre-sponds to the syllabic awareness that has nine items: synthesis, segmentation, initial syllable identiication, rhyme identiica-tion, word production with the given syllable, medial syllable identiication, rhyme production, exclusion, and transposition. The second part corresponds to phonemes awareness with seven items: production of a word that begins with the given sound, initial phoneme identiication, inal phoneme identiication, exclusion, synthesis, segmentation, and transposition. The test is graded in a speciic protocol, and the correct answers score one point and the incorrect ones have no points. In the syllable part, the maximum grade is 40 points and in the phonemes part it is 30, together they sum 70 points, i.e. 100% correct ones.

The groups were paired up according to their chronological age and all the students were submitted to two evaluations for the CAEP-P300 research. For the GI, evaluations happened be-fore and after the phonological remediation program associated with reading and writing, with a 12-week interval; and for GII, although there was no intervention, the same interval was kept between the two evaluations. The same day in the week and time for the evaluation before and after the students’ program of GI was determined, since how the child is at the moment of the test may inluence the results. Following the same reason-ing, the times of GII evaluation were determined by their pair in the experimental group.

The CAEP-P300 test for speech stimulus was performed using the Biologic Evoked Potential System (EP) equipment, in a quiet room, with the student comfortably lay down on a stretcher, instructed to remain in alert state, paying attention to the rare stimulus, which was randomly presented to the frequent stimulus (Oddball paradigm). Also, when every dis-criminated rare stimulus was done, the patient was supposed to raise his index inger. The test parameters and electrodes positioning are described in Chart 1. Latency of N200 and P300 (ms) components and P300 (ΩV) amplitude, registered in Cz, were analyzed.

Data were submitted to descriptive and inferential statistics analysis through paired Student’s t-test, analysis of variance (ANOVA), and Pearson’s correlation coeficient. A 5% (0.05) level of signiicance was adopted.

RESULTS

In the PA Test, the GI presented improvement of the per-formance after the phonological remediation associated with reading and writing, with higher values of means in all items of the test, but with a more expressive one in the phonemic subtest. In GII, there was not quite a measure change of the scores, in any subtests, with absence of difference (Tables 1 and 2).

Table 3 presents the CAEP-P300 descriptive statistics analy-sis, of both groups, regarding the absolute latencies of N200 and P300 components in ms, and P300 amplitude, in mV, in the two evaluation moments (before and after).

Table 4 shows the statistic comparison of the two evalu-ations (before and after) of each group, through the paired Student’s t-test and ANOVA regarding absolute latencies of N200 and P300 components, in ms, and P300 amplitude, in mV. The absence of difference in GI, when analyzing the latency and amplitude measures of the considered components, dem-onstrates test–retest reliability of the procedure. In this table, there is also a comparison of the groups concerning N200 and P300 components, before and after the phonological remedia-tion associated with reading and writing.

Correlation measures of the CAEP-P300 and the PA Test, on both evaluation moments, are presented in Table 5.

DISCUSSION

The PA, i.e. the metalinguistic skill that allows analyzing and relecting consciously upon the phonological structure of the oral language, is settled as an important precursor for the development of reading and writing abilities(18,19), therefore it is the focus of phonological remediation programs.

Students from GI, who were submitted to the phonologi-cal remediation program associated with reading and writing,

Chart 1. Parameters used for the research about Cognitive Hearing Evoked Potential-P300

Parameters for the Cognitive Hearing Evoked Potential-P300 Stimulus type Speech (20% rare and 80% frequent) Stimulus syllables /da/ (rare); /ba/ (frequent)

Stimulus intensity 80 dBNA

Rate 1 stimulus per second

Electrodes positioning Fz and Cz (active); m1 and m2 (reference) Impedance ≤5 kΩ (individual); ≤2 kΩ (between electrodes)

Band-pass filter 1–30 Hz

Transducer Third insertion receivers, binaural stimulation

Table 1. Mean scores before and after testing in the Phonological Aware-ness proof

Caption: SD = standard deviation; GI, submitted to a phonological remediation program associated with reading and writing; GII, control group.

Syllable Phoneme Total

Mean SD Mean SD Mean SD

GI – Before 30.1 6.47 12.6 5.44 42.7 11.75

GI – After 34.4 6.47 20.8 7.36 55.2 12.96

GII – Before 29.9 6.14 12.9 4.87 42.8 10.37

GII – After 30.5 5.61 13.3 5.31 43.8 10.33

Table 2. Performance comparison in the Phonological Awareness proof, on both evaluation moments

*p≤0.05 – statistically significant. Paired Student’s t-test.

Caption: Confias = Sequential Evaluation Instrument; GI. submitted to a phonologi-cal remediation program associated with reading and writing; GII, control group.

Confias

Syllable Phoneme Total

GI – Before × After 0.000* 0.000* 0.000*

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demonstrated better performance in the PA test, both in the syl-lables and in the phonemes test. Increase in the average of hits on both tests was similar; however, in the phoneme test, students reached results that were closer to the test maximum scoring (Tables 1 and 2). Furthermore, it was possible to notice this improvement in a qualitative manner, which was evidenced by the increase of the student’s ability to deal with games about PA.

The results obtained after the test revealed that dificulties in PA were overcome, because, even if the standard deviations are considered, the GI students reached normality values.

Most researches about reading and writing have dem-onstrated the relationship between PA and progress in the reading and writing learning process, together with different factors that promote learning of spelling patterns associated with the pronunciation based on phonological aspects. Thus, with the continuous and progressive learning, the student reaches the orthographic stage in which recognition and reading of words happen via a direct lexical and semantic

access from certain graphic characteristics of the word,

which are orthographically stored(20).

Eficiency in the process of word decodiication promotes increase of reading speed, which creates positive inluences in reading comprehension. Increase of reading speed and ability is directly associated with PA skills, lexical access, and work memory. Therefore, as the remediation program associated with reading and writing provided an improvement in the phonological processing abilities, the impacts on reading speed became more perceptible.

Due to blood low alterations in some areas of the tempo-ral cortex, children with developmental dyslexia may pres-ent some laws on the information neurological processing, causing dificulty in the hearing perception of phonological information about reading learning in a writing system with alphabetical base. Studies carried out in Brazil evidenced these alterations in the neurological functioning of children

with such diagnosis(21,22).

Table 3. Descriptive statistics analysis of the Cognitive Hearing Evoked Potential-P300

Caption: SD = standard deviation; Lat., latency; GI, submitted to a phonological remediation program associated with reading and writing; Amp., amplitude; GII, control group.

Cognitive Hearing Evoked Potential-P300 (ms/ΩV)

Before After

Mean SD Minimum Maximum Mean SD Minimum Maximum

Lat. N200 GI 271.53 43.30 221.98 348.98 257.581 37.84 211.57 324

Lat. P300 GI 431.22 29.69 392.7 490.56 387.71 31.18 338.57 446.84

Amp. P300 GI 7.85 2.77 3.26 11.99 8.48 2.08 5.26 12.03

Lat. N200 GII 267.57 44.13 211.57 334.41 257.37 52.01 190.75 338.57

Lat. P300 GII 398.33 48.22 303.18 471.82 385.21 46.37 303.18 461.41

Amp. P300 GII 7.25 4.94 1.99 14.65 7.74 3.32 3.71 15.39

Table 4. Comparison of the Cognitive Hearing Evoked Potential-P300 in the two moments of evaluation for each group and comparison between the groups

*p≤0.05 – statistically significant.

Caption: Lat. = latency; Amp., amplitude; GI, submitted to a phonological remediation program associated with reading and writing; GII, control group; ANOVA, analysis of variance.

Cognitive Hearing Evoked Potential-P300

Lat. N200 Lat. P300 Amp. P300 Statistical test

GI – Before × After p=0.487 p=0.005* p=0.335 Paired t-test

p=0.453 p=0.005* p=0.569 ANOVA

GII – Before × After p=0.480 p=0.321 p=0.660 Paired t-test

p=0.642 p=0.543 p=0.799 ANOVA

Before – GI × GII p=0.842 p=0.083 p=0.744 Paired t-test

After – GI × GII p=0.992 p=0.889 p=0.556 Paired t-test

Table 5. Correlation measures of the Cognitive Hearing Evoked Potential-P300 and of the Phonological Awareness proof in both evaluation moments

Caption: Lat. = latency; Amp., amplitude.

Syllable Phoneme Total

Before After Before After Before After

Lat. N200 r=-0.703

Moderate negative

r=-0.824 Strong negative

r=-0.735 Moderate negative

r=-0.845 Strong negative

r=-0.564 Weak negative

r=-0.769 Strong negative

Lat. P300 r=-0.934

Strong negative

r=-0.844 Strong negative

r=-0.949 Strong negative

r=-0.872 Strong negative

r=-0.934 Strong negative

r=-0.582 Weak negative

Amp. P300 r=0.962

Strong positive

r=0.954 Strong positive

r=0.982 Strong positive

r=0.956 Strong positive

r=0.962 Strong positive

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Results from the study of Kujala et al.(23) indicated that

training causes a change in the cortical hearing plasticity, which is a result from the increase of neurophysiological activities and time of reaction to alteration of sounds, accom-panied by improvement in reading performance. A posterior study showed that there are changes in the brain activation of the posterior region of the middle temporal gyrus seen in the magnetoencephalography after the intervention through read-ing remediation(24).

CAEP-P300 relects the electrical activity of brain areas that happens before a speciic task that includes skills like at-tention, discrimination, integration and memory, which are also involved in the information phonological processing.

Thus, normal functionality of central hearing structures is fundamental in order that perceptual abilities are acquired in the expected pattern. According to literature of the area, neu-rophysiological changes are relected on the hearing evoked potentials, both in their latency or amplitude; therefore, it is possible to determine the relationship between these changes and the behavioral hearing abilities.

Taking into account that children with developmental

dyslexia present alterations in phonological abilities(3,4), the

investigation of CAEP-P300 in the therapeutical processes, focusing on these skills, may provide additional information to the behavioral observation.

In the literature, CAEP-P300 use to assess neurophysi-ological changes that happened after the hearing training was

seen in patients with hearing process disorder(10), in cases of

disluency(12), as well as a predictor of the results of chemical

dependence treatment(11).

In this study, CAEP-P300 was analyzed in two moments, before and after the phonological remediation, associated with reading and writing. Initially, a strong correlation between the CAEP-P300 characteristics, latency and ampli-tude, and the performance in PA tests (Table 5) was seen, which shows the pertinence of using CAEP-P300 to monitor the therapeutical evolution in a phonological remediation program associated with reading and writing.

Hence, another important datum is that there was no difference in the latency and amplitude of P300 component when the two moments of the GII evaluation were compared (Table 4), which demonstrates the test–retest reliability of the

procedure(13). Besides, the inexistence of difference between

the groups regarding latency of N200 and P300 components and amplitude of P300 before remediation reinforces the control of variables that could inluence on the obtained results.

On the other hand, if compared to the average of latency values of the P300 component, in the two evaluation moments of the group submitted to phonological remediation associ-ated with reading and writing (GI), a decrease was seen in the latency with a signiicant difference (Table 4). No signiicant differences were found both in the GI and in the GII, for P300 amplitude and N200 latency.

Therefore, decrease in the P300 component latency for the GI demonstrates that work with phonological abilities in-duced to changes in the central hearing nervous system, which could be monitored through CAEP-P300. These physiological

changes seen in the CAEP-P300 relected on the child’s behav-ioral performance, because the same difference was observed in the PA test, in which a better performance was seen after the intervention. These indings showed the therapeutical evolution of students with developmental dyslexia that were submitted to therapies focused on the maximization of phonological abilities,

which is in agreement with previous studies(5–8).

Based on the abovementioned results, P300 may provide pieces of information that help guiding the intervention process of students with developmental dyslexia, since the absence of changes in the P300 latency can be seen as a sign for the need to reassess the therapeutical approach that was used and if some appropriations are needed.

CONCLUSION

The use of CAEP-P300 for the aimed monitoring of the therapeutical evolution of developmental dyslexia children is possible and represents a viable option for intervention programs.

*KFA was in charge of outlining the study, she also monitored data collection and tabulation and collaborated on data analysis and manuscript elaboration; ESA was in charge of data collection and tabulation and collaborated on data analysis and manuscript elaboration; EF was in charge of data collection and tabulation and collaborated on data analysis and manuscript elaboration; PAPC was in charge of outlining the study, she also monitored data collection and tabulation, and collaborated on data analysis and manuscript elaboration.

REFERENCES

1. American Psychiatric Association. DSM IV: Manual de Diagnóstico e Estatística das Perturbações Mentais. Lisboa: Climepsi Editores; 1996. 2. Lyon R, Shaywitz SE. A deinition of dyslexia. Ann Dyslexia. 2003;53:1-14. 3. Rey V, De Martino S, Espesser R, Habib M. Temporal processing

and phonological impairment in dyslexia: effect of phoneme lengthening on order judgment of two consonants. Brain Lang. 2002;80(3):576-91.

4. Germano GD, Pinheiro FH, Capellini SA. Desempenho de escolares com dislexia do desenvolvimento em tarefas fonológicas e silábicas. Rev CEFAC. 2009;11(2):213-20.

5. Capellini SA, Padula NA, Ciasca SM. Desempenho de escolares com distúrbio especíico de leitura em programa de remediação. Pró-Fono R Atual Cient. 2004;16(3):261-74.

6. Salgado CA, Capellini SA. Programa de remediação fonológica em escolares com dislexia do desenvolvimento. Pró-Fono R Atual Cient. 2008;20(1):31-7.

7. Snowling MJ, Hulme C. Evidence-based interventions for reading and language dificulties: creating a virtuous circle. Br J Educ Psychol. 2011;81(Pt 1):1-23.

8. FadiniCC, Capellini SA. Treinamento de habilidades fonológicas em escolares de risco para dislexia. Rev Psicopedag. 2011;28(5):3-13. 9. Jirsa RE. Clinical efficacy of eletrophysiologic measures in APD

management programs. Semin Hear. 2002;23(4):349-55.

10. AlonsoR, Schochat E. A eficácia do treinamento auditivo formal em crianças com transtorno de processamento auditivo (central): avaliação comportamental e eletroisiológica. Braz J Otorhinolaryngol. 2009;75(5):726-32.

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12. Sassi FC, Matas CG, de Mendonça LI, de Andrade CR. Stuttering treatment control using P300 event-related potentials. J Fluency Disord. 2011;36(2):130-8.

13. Musiek FE, Lee WW. Potenciais auditivos de média e longa latência. In: Musiek FE, Rintelmann WF. Perspectivas atuais em avaliação auditiva. Barueri: Manole; 2001. p. 239-267.

14. Cone-Wesson B, Wunderlich J. Auditory Evoked Potentials from the cortex: audiology applications. Curr Opin Otolaryngol Head Neck Surg. 2003;11(5):372-7.

15. McPherson DL. Late potentials of the auditory system. San Diego: Singular Publishing Group, Inc.; 1996.

16. Salgado CA. Programa de remediação fonológica, de leitura e escrita em crianças com dislexia do desenvolvimento [Tese]. Campinas: Faculdade de Ciências Médicas, Universidade Estadual de Campinas; 2010. 17. Moojen S, Lamprecht R, Santos RM, Freitas GM, Brodacz R, Siqueira

M, et al. Consciência fonológica: instrumento de avaliação seqüencial. São Paulo: Casa do Psicólogo; 2003.

18. Paula GR, Mota HB, Keske-Soares M. A terapia em consciência fonológica no processo de alfabetização. Pró-Fono R Atual Cient. 2005;17(2):175-84.

19. Barrera SD, Maluf MR. Consciência metalinguística e alfabetização: um estudo com crianças da primeira série do ensino fundamental. Psicol Relex Crit. 2003;16(3):491-502.

20. Salles JF, Mota HB, Cechella C, Parente MAMP. Desenvolvimento da consciência fonológica de crianças de primeira e segunda séries. Pró-Fono. 1999;11(2):68-76.

21. Sauer LO, Pereira LD, Ciasca SM, Pestun M, Guerreiro MM. Processamento auditivo e SPECT em crianças com dislexia. Arq Neuropsiquiatr. 2006; 64(1):108-11.

22. Arduini R, Capellini SA, Ciasca SM. Comparative study of the neuropsychological and neuroimaging evaluations in children with dyslexia. Arq Neuropsiquiatr. 2006;64(2B):369-75.

23. Kujala T, Lovio R, Lepistö T, Laasonen M, Näätänen R. Evaluation of multi-attribute auditory discrimination in dyslexia with the mismatch negativity. Clin Neurophysiol. 2006;117(4):885-93.

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Table 1. Mean scores before and after testing in the Phonological Aware- Aware-ness proof
Table 5.  Correlation measures of the Cognitive Hearing Evoked Potential-P300 and of the Phonological Awareness proof in both evaluation moments

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