CoDAS vol.25 número4

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Artigo Original

Bianca Simone Zeigelboim1 Hélio Afonso Ghizoni Teive2 Rosane Sampaio Santos1 Walter Oleschko Arruda2 Ari Leon Jurkiewicz1 Heidi Mengelberg1 Denise França3 Jair Mendes Marques1

Descritores

Degenerações espinocerebelares Ataxias espinocerebelares Ataxia Audição Transtornos da audição Audiometria de resposta evocada Audiometria Potenciais evocados auditivos

Keywords

Spinocerebellar degenerations Spinocerebellar ataxias Ataxia Hearing Hearing disorders Audiometry, evoked response Audiometry Evoked potentials, auditory

Correspondence address: Bianca Simone Zeigelboim

R. Gutenberg, 99, 9º andar, Curitiba (PR), Brasil, CEP: 80420-030.

E-mail: [email protected] Received: 05/03/2012

Study carried out at the Universidade Tuiuti do Paraná – UTP – Curitiba (PR), Brazil. (1) Universidade Tuiuti do Paraná – UTP – Curitiba (PR), Brazil.

(2) Universidade Federal do Paraná – UFPR – Curitiba (PR), Brazil.

(3) Universidade do Centro-Oeste do Paraná – UNICENTRO – Irati (PR), Brazil. Conlict of interest: nothing to declare.

Avaliação audiológica na ataxia espinocerebelar

ABSTRACT

Purpose: To describe the audiological and electrophysiological results in patients with spinocerebellar ataxia (SCA). Methods: Retrospective and cross-sectional studies were performed. Forty-three patients were assessed using the following procedures: anamnesis and otolaryngologic exam, pure tone audiometry, acoustic immittance measures and brainstem auditory evoked potential (BAEP). Results: Patients showed gait abnormality (83.7%), speech disorder (48.8%), dizziness (41.8%) and dysphagia (39.5%). Hearing loss was referred in 27.9% of the cases; in the audiometric exams, 14 patients (32.5%) presented disorders; in SCA 3, 33.3%; in SCA 2, 12.5%; in SCA 4, 100.0%; in SCA 6, 100.0%; in SCA 7, 100.0%; in SCA 10, 50.0%; and in undetermined SCA, 21.4%. In BAEP, 20 patients (46.5%) were abnormal, being 58.3% in SCA 3, 62.5% in SCA 2, 100.0% in SCA 6, 100.0% in SCA 7, 66.7% in SCA 10 and 14.2% in undetermined SCA. While in acoustic immittance, 19 patients (44.1%) presented disorders, being 50.0% in SCA 3, 50.0% in SCA 2, 100.0% in SCA 4, 100.0% in SCA 6, 100.0% in SCA 7, 33.3% in SCA 10 and 28.5% in undetermined SCA. Conclusion: The most evident abnormalities in the audiological evaluation were the predominance of the down-sloping audiometric coniguration beginning at 4 kHz bilaterally and the bilateral absence of acoustic relex at the frequencies of 3 and 4 kHz. In the electrophysiological evaluation, 50% of the patients showed abnormalities with prevalence of an increase of the latency of waves I, II and V and of the interval in the interpeaks I-III, I-V and III-V.

RESUMO

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INTRODUCTION

Spinocerebellar ataxia (SCA) is a disease that belongs to a heterogeneous group of neurodegenerative disorders that are characterized by the presence of progressive cerebellar ataxia(1)_{. It can be classiied as sensitive, frontal, vestibular, and}

cerebellar, with the latter being the object of this study(1)_{. Out}

of the 30 types of identiied SCAs, Types 2 and 3 are among the most prevalent(1,2)_.

There are about 3.0 to 4.2 cases of SCAs per 100,000,0 inhabitants(3)_{, and the most common clinical manifestations are}

gait and appendicular ataxia (dysmetria, dysdiadochokinesia, and intention tremor), dysarthria, nystagmus, ophthalmople-gia, dysphaophthalmople-gia, hearing loss (in some cases), pyramidal signs, lower motor neuron syndrome, cognitive dysfunction, epilepsy, visual disorders (retinitis pigmentosa), peripheral neuropathy, dementia, and movement disorders (including Parkinson’s, dystonia, myoclonus, and chorea)(1,3-5)_.

SCAs can be divided according to genetic inheritance: (a) autosomal recessive hereditary ataxia, (b) autosomal dominant hereditary ataxia, (c) hereditary ataxia related to the x chromo-some, and (d) mitochondrial hereditary ataxia(6)_.

Studies describe differences in the severity of clinical manifestations and the age of onset of symptoms, depending on which parent the expanded gene is inherited from. In the case of SCAs transmitted from the father, an increasing trend was observed in the number of repetitions in children, which is different when SCAs are transmitted from the mother. Therefore, when an SCA is transmitted from the father, it means more severe clinical manifestations in the children, who can even present the irst symptoms of ataxia before the father(7)_.

In Brazil, especially in the South region, a great number of families have been detected to carry SCAs(3,6)_{. The}

Machado-Joseph disease (MJD), also known as SCA 3, is the most com-mon form of autosomal dominant hereditary ataxia found in a number of epidemiological studies(3,6-8)_.

The exploration of peripheral and central auditory system is conducted by using behavioral, electroacoustic, and electro-physiological assessment methods.

Many authors(9-11)_{report that in neurodegenerative diseases,}

the most common auditory dysfunctions are observed in the brainstem auditory-evoked potential (BAEP) test and occur in the inferior colliculus, lateral lemniscus, and cochlear nuclei.

SCAs are part of a group of diseases that present important changes in the speech-language ield. Such research is a key contributor in building knowledge as a substitute for cumber-some and elongated assessment and therapeutic procedures focusing on this disease.

The objective of this study was to assess the results of au-diological and electrophysiological evaluations in SCA patients.

METHODS

This study was approved by the Institutional Ethics Committee (Number: 058/2008) and authorized by the

patients who conirmed their acceptance by signing the in-formed consent form.

A retrospective cross-sectional study was conducted. A total of 43 patients were evaluated (17 female and 26 male) and referred to the clinical department of Hospital das Clínicas, who were also assisted at the otoneurology department of a teaching institution in the same city. The study participants were diagnosed with SCA (twelve with SCA 3, eight with SCA 2, one with SCA 4, one with SCA 6, one with SCA 7, and six with SCA 10).

The diagnosis of ataxia was performed by a genetic test, us-ing the polymerase chain reaction (PCR)(12-14)_{. Fourteen patients}

were genetically analyzed to discover the type of SCA, who were also part of the group of people with undetermined SCA.

The age of patients ranged from 18.0 to 70.0 years (mean age: 41.6 years, SD=13.0 years). Duration of disease was 1.0 to 15.0 years (mean duration: 7.9 years, SD=3.9 years; Table 1).

Patients with alterations that prevented their participation in examinations were excluded from the study.

The following procedures were performed:

• Anamnesis: A questionnaire with emphasis on otoneuro -logical signs and symptoms was applied.

• Otolaryngologic evaluation: Evaluation was carried out

with the objective of excluding any alteration that could interfere with the examination.

• Audiological evaluation: Patients were submitted to

pure-tone air conduction audiometry at frequencies ranging from 250 to 8 kHz, bone conduction at frequencies ranging from 500 to 4 kHz, and tests of speech recognition threshold (SRT) as well as the percentage index of speech recogni-tion (PISR). For these tests, the equipment used was Itera Madsen-GN Otometrics, TDH-39 headphones, from GN-ReSound, with thresholds expressed in dBNA and calibrated according to the ISO 8253 standard(15,16)_.

• BAEP: Two channels with 90-dBnHL click stimuli, polarity

alternated with presentation frequency of 21.1 c/s, 15-ms window, 30- to 3-kHz ilter, and at least 2,000 stimuli and two reproduction registers were used. Electrodes from Kendall Medtrace 2000 were placed in the right and left mastoid positions as well as in Fz (10-20 system), and the earth electrode was placed on the forehead. Clicks were presented with 3A insert earphones. The latency of Waves I, III, and V and the Interpeak intervals I-III, III-V, and I-V were analyzed. The equipment used was the Bio-logic’s Evoked Potential System, and the analysis criterion was proposed by the author(17)_.

• Acoustic immittance measures: This procedure was per -formed to assess the integrity of the tympanic ossicles, and the equipment used for this purpose was the Otolex middle-ear analyzer, TDH 39P headphones, from Gn-ReSound, and the author’s criteria were applied(18)_.

Statistical analysis

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acoustic immittance measure, by analyzing results indicating normalcy and abnormalcy. Rejection level in the null hypothesis was ixated at 0.05 or 5%.

RESULTS

The most frequently mentioned complaints in anamnesis (Table 2) were as follows: gait imbalance (83.7%), trouble speaking (48.8%), dizziness (41.8%), dysphagia (39.5%), dysphonia (34.8%), and hearing loss (27.9%).

During the audiological evaluation, 14 patients (32.5%) presented changes in the examination – 2.3% in the right ear

(RE), 4.6% in the left ear (LE), and 25.6% bilaterally (B) –

which translated to 33.3% in SCA 3, 12.5% in SCA 2, 100.0% in SCA 4, 100.0% in SCA 6, 100.0% in SCA 7, 50.0% in SCA 10, and 21.4% in undetermined SCA (Table 3).

The application of the difference-in-proportions test proved there was signiicant difference between normal and abnormal

cases – RE (p<0.05), LE (p<0.05), and B (p=0.0001*). The

results of SRT and PISR were compatible with tone thresholds.

Table 1. Genetic aspects of spinocerebellar ataxias

Patient Age

(years) Gender

Spinocerebellar ataxias

Duration of

disease (years) Chromosome Gene Mutation Protein

1 42 M SCA 3 12 14q32.1 ATAXIN3 CAG Ataxin3

2 48 F SCA 3 15 14q32.1 ATAXIN3 CAG Ataxin3

21 43 M SCA 4 5 16q24.qter SCA4 PLEKHG4? —

22 57 F SCA 6 5 19q13.1 CACNA1A CAG CACNA1A

23 47 F SCA 7 10 3p14.1 ATAXIN7 CAG Ataxin7

24 49 F SCA 10 6 22q13.3 ATAXIN10 ATTCT Ataxin10

25 46 M SCA 10 10 22q13.3 ATAXIN10 ATTCT Ataxin10

30 24 M Und. 2 — — — —

31 27 M Und. 7 — — — —

32 20 M Und. 1 — — — —

33 32 M Und. 5 — — — —

34 22 M Und. 8 — — — —

35 22 M Und. 7 — — — —

36 62 M Und. 3 — — — —

37 66 M Und. 12 — — — —

38 18 F Und. 4 — — — —

39 23 M Und. 1 — — — —

40 37 F Und. 9 — — — —

41 48 F Und. 8 — — — —

42 48 F Und. 8 — — — —

43 51 F Und. 7 — — — —

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In BAEP, 20 patients (46.5%) presented changes in the

examinations (11.6% in the LE and 34.9% in B), which

translated to 58.3% in SCA 3, 62.5 in SCA 2, 100.0% in SCA 6, 100.0% in SCA 7, 66.7% in SCA 10, and 14.2% in undetermined SCA (Table 3).

The application of the difference-in-proportions test proved there was a signiicant difference between the

pro-portions of normal and abnormal cases – LE (p<0.05) and B (p=0.0063*).

In the acoustic immittance measure, 19 patients (44.1%) registered changes in the examinations, especially bilaterally, which translated to 50.0% in SCA 3, 50.0% in SCA 2, 100.0% in SCA 4, 100.0% in SCA 6, 100.0% in SCA 7, 33.3% in SCA 10, and 28.5% in undetermined SCA (Table 4).

The application of the difference-in-proportions test further proved there was no signiicant difference between the propor-tions of normal and abnormal cases – B (p=0.2843).

The results of audiological evaluation, BAEP, and acoustic immittance measure in relation to the proportions of normal and abnormal cases in SCAs 2, 3, and 10 are presented in Table 5.

The application of the difference-in-proportions test proved there was signiicant difference only in the audiological

evalu-ation and in SCA 2 (p=0.0096*).

DISCUSSION

Anamnesis revealed the predominance of gait disorders, which was expected in terms of SCA. Changes in speech, diz-ziness, dysphagia, dysphonia, and hearing loss are the most frequent symptoms as described in many past studies(1-4)_.

Changes in audiological evaluation were present in 30% of the patients with ataxia, especially those in the category of SCA 3 and SCA 10. The authors(19)_{assessed 18 patients with SCA and}

observed normal hearing in all of them but found hearing changes using the BAEP test, with a 71% occurrence in Friedreich’s ataxia, in which only Wave I was found, and 71% in olivopontocerebellar atrophy, which does not refer to the type of alteration found. The authors pointed out to important abnormalities in the brainstem auditory pathways of patients with this disease.

In this study, 46.5% of patients presented alterations in BAEP, with increased Wave I latency only in SCA 3. An in-crease in Wave V latency was observed in SCAs 3, 6, 7, 10, and undetermined SCA; an increase in Wave III latency was observed in SCAs 2, 6, and 7; and an increase in Interpeak intervals I-III, I-V, and III-V occurred in SCAs 2, 3, 6, 7, 10, and the undetermined SCA. The authors(19-22)_{reported frequent}

abnormalities in this examination. The prevalence of changes in SCAs 2 and 3 are in accordance with the authors(20,21)_{, which is}

due to higher prevalence of these types of SCA. Some studies(21)

have evaluated the BAEP test in 36 patients (eight with SCA 1, twelve with SCA 2, and sixteen with SCA 3) and observed re-sults indicating abnormalities in 50% of those with SCA 1, 42% with SCA 2, and 63% with SCA 3. Another group of research-ers(23)_{assessed 30 patients with spinocerebellar degeneration}

and observed abnormalities in 30% of these patients after the BAEP test, with prolonged latencies and Interpeaks of waves I-III and I-V, which is in accordance with this study.

Some authors(24) _{conducted an anatomopathological}

inves-tigation of brain in 12 patients with SCA (three with SCA 2, seven with SCA 3, and two with SCA 7), considering tissue cuts of auditory nuclei; they reported substantial damage to the central auditory system.

The study showed neural loss of the dorsal and ventral nuclei of the lateral lemniscus in two patients with SCA 2, in all of those with SCA 3, and in one patient with SCA 7. The superior olivary nucleus proved to be the most severely affected by degeneration, and the loss of myelinated ibers in brainstem pathways restricted to the lateral lemniscus was found in a patient with SCA 2, in ive patients with SCA 3, and in all of those with SCA 7. The trapezoid body was altered in a patient with SCA 2 and in two patients with SCAs 3 and 7. The involvement of these structures offered plausible explanations for the hearing damage observed in these patients.

Acoustic immittance measures were altered in 44.1% of these patients, and literature has no reference about this inding, so the results cannot be reconirmed. It is known that ibers leave from the anterior cochlear nuclei, via trapezoid body, and move toward the nuclei of the contralateral facial nerve and the superior olivary nucleus, which in turn forms synapses with the facial nerve nucleus. There are also homo-lateral ibers coming from the anterior cochlear nuclei, which establish such communications, and, in addition, axons inner-vate the stapedius muscle or the stapes. However, when there are multiple neurodegenerative diseases, the anterior cochlear nuclei are affected, which in turn renders impossible the task of making interferences in the acoustic relex mechanism(25,26)_.

Table 2. Frequency of symptoms in 43 patients with spinocerebellar ataxia

Symptoms Number of

patients

Frequency (%)

Gait imbalance 36 83.7

Trouble speaking 21 48.8

Dizziness 18 41.8

Dysphagia 17 39.5

Dysphonia 15 34.8

Hearing loss 12 27.9

Headache 11 25.5

Falling 11 25.5

Diplopia 10 23.2

Paresthesia in the extremities 7 16.2

Anxiety 6 13.9

Double vision 5 11.6

Tremor 5 11.6

Pain irradiated to the shoulder and arm 5 11.6

Insomnia 5 11.6

Depression 5 11.6

Pain and difficulty moving the neck 4 9.3

Migraine 4 9.3

Tinnitus 4 9.3

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In the present study, a higher prevalence of alterations observed in the BAEP examination proved there were severe changes in the integrity of the brainstem auditory pathway. This inding is in accordance with many other research works(19-24)_{, where the authors have observed}

al-terations in many structures of the central auditory pathway,

demonstrating the greater sensitivity of this examination to detect changes in the path of acoustic impulse throughout the central auditory pathway.

The importance of studying the auditory system is empha-sized, especially in the context of electrophysiological control, together with clinical and genetic follow-ups.

Table 3. Results of audiological and brainstem auditory-evoked potential evaluations in 43 patients with spinocerebellar ataxia

Patient Audiological evaluation BAEP SCA

RE LE RE LE

1 Normal Normal Altered Altered SCA 3

2 Normal Normal Normal Normal SCA 3

3 Normal Normal Normal Altered SCA 3

4 Descending from the 4-kHz frequency Normal Altered Altered SCA 3

6 SNHL – Mild SNHL – mild Normal Normal SCA 3

7 Normal SNHL – severe Normal Absent SCA 3

10 SNHL – severe SNHL – mild Altered Altered SCA 3

15 Descending from the 2-kHz frequency Descending from the 2-kHz frequency Altered Altered SCA 2

21 Descending from the 4-kHz frequency Descending from the 4-kHz frequency Normal Normal SCA 4

22 Descending from the 4-kHz frequency SNHL – moderate Normal Altered SCA 6

23 Descending from the 4-kHz frequency Descending from the 4-kHz frequency Altered Altered SCA 7 24 With notch at the 6-kHz frequency With notch at the 6-kHz frequency Altered Altered SCA 10

26 Descending from the 2-kHz frequency Descending from the 2-kHz frequency Altered Altered SCA 10

28 Normal SNHL – severe Altered Altered SCA 10

30 Normal Normal Normal Normal Und.

33 Normal Normal Altered Altered Und.

36 Descending from the 3-kHz frequency Descending from the 3-kHz frequency Normal Normal Und. 37 Descending from the 2-kHz frequency Descending from the 2-kHz frequency Altered Altered Und.

42 Descending from the 4-kHz frequency Descending from the 4-kHz frequency Normal Normal Und.

Legend: BAEP = brainstem auditory-evoked potential; SCA = spinocerebellar ataxia; RE = right ear; LE = left ear; SNHL = sensorineural hearing loss; Und = undetermined. The application of the difference-in-proportions test in audiological evaluation proves there was a significant difference between the proportion of normal and abnormal cases: RE (p<0.05), LE (p<0.05), and B (p=0.0001*)

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CONCLUSION

The alterations that mostly appeared in the audiological evaluation include the prevalence of descending audiometric coniguration from the 4-kHz frequency, bilaterally, and the

absence of acoustic relex in 3- and 4-kHz frequencies, again bilaterally.

In the electrophysiological evaluation, 50% of the patients presented with changes, especially increased latencies in Waves I, III, and V and Interpeak intervals I-III, I-V, and III-V.

Table 4. Results of the immittance test in 43 patients with spinocerebellar ataxia

Patient

Acoustic immittance measure

SCA

RE LE

Tympanometric

curve Acoustic reflex

Tympanometric

curve Acoustic reflex

1 Type A Present Type A Present SCA 3

3 Type A Absent in the 4-kHz frequency Type A Absent SCA 3

4 Type A Absent in the 4-kHz frequency Type A Absent in the 4-kHz frequency SCA 3

5 Type A Absent in the 3- and 4-kHz frequencies Type A Absent in the 3- and 4-kHz frequencies SCA 3 6 Type A Absent in the 3- and 4-kHz frequencies Type A Absent in the 3- and 4-kHz frequencies SCA 3

7 Type A Absent in the 3- and 4-kHz frequencies Type A Absent SCA 3

10 Type A Absent Type A Absent in the 3- and 4-kHz frequencies SCA 3

14 Type As Absent Type As Absent SCA 2

15 Type A Absent in the 2-, 3-, and 4-kHz frequencies Type A Absent in the 2-, 3- and 4-kHz frequencies SCA 2 16 Type A Absent in the 3- and 4-kHz frequencies Type A Absent in the 3- and 4-kHz frequencies SCA 2 17 Type A Absent in the 3- and 4-kHz frequencies Type A Absent in the 3- and 4-kHz frequencies SCA 2

21 Type A Absent in the 4-kHz frequency Type A Absent in the 4-kHz frequency SCA 4

22 Type A Absent in the 4-kHz frequency Type A Absent SCA 6

23 Type A Absent in the 4-kHz frequency Type Ad Absent SCA 7

26 Type As Absent in the 3- and 4-kHz frequencies Type As Absent in the 3- and 4-kHz frequencies SCA 10

28 Type A Absent in the 3- and 4-kHz frequencies Type As Absent SCA 10

30 Type A Present Type A Present Und.

33 Type A Absent in the 3- and 4-kHz frequencies Type A Absent in the 3- and 4-kHz frequencies Und.

36 Type A Absent in the 3- and 4-kHz frequencies Type A Absent in the 3- and 4-kHz frequencies Und. 37 Type A Absent in the 3- and 4-kHz frequencies Type A Absent in the 3- and 4-kHz frequencies Und.

42 Type A Absent in the 4-kHz frequency Type A Absent in the 4-kHz frequency Und.

Legend: RE = right ear; LE = left ear; SCA = spinocerebellar ataxia; Und. = Undetermined.

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ACKNOWLEDGEMENT

National Council for Scientific and Technological Development (CNPQ), Report n. 309965/2009-8.

*WOA collaborated with data collection and formatting; RSS collaborated with collection and bibliography; DF collaborated with collection and bibliography; HM collaborated with collection and bibliography; JMM collaborated with data analysis; HGAT was in charge of writing and inal review; ALI participated in the writing and inal review; BSZ was in charge of the project and study design as well as general orientation of the stages of execution and elaboration of the manuscript.

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Table 5. Distribution of the results of the audiological, brainstem auditory evoked potential and acoustic immittance evaluations in spinocerebellar ataxias 2, e, and 10

Audiological evaluation SCA 2 n (%)

SCA 3 n (%)

SCA 10 n (%)

Normal 7 (87.5) 8 (66.7) 3 (50.0)

Altered 1 (12.5) 4 (33.3) 3 (50.0)

Total 8 (100.0) 12 (100.0) 6 (100.0)

p-value 0.0096* 0.1160 1.0000

BAEP

Normal 3 (37.5) 5 (41.7) 2 (33.3)

Altered 5 (62.5) 7 (58.3) 4 (66.7)

Total 8 (100.0) 12 (100.0) 6 (100.0)

p-value 0.3343 0.4248 0.2742