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Brazilian Journal of Otorhinolaryngology

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Review article • Braz. j. otorhinolaryngol. 88 (Suppl 3) • Nov-Dec 2022 • https://doi.org/10.1016/j.bjorl.2021.10.006 copy

Ocular findings from otoneurological examinations in children with and without dyslexia: a systematic review with meta-analysis

Authorship SCIMAGO INSTITUTIONS RANKINGS

Highlights

Vestibular evaluation of children with dyslexia.

Ocular evidence of otoneurology in dyslexia.

The measurements of ocular tests in children with dyslexia.

Vectoelectro-nystagmography and videonystagmography exams in children with dyslexia.

Abstract

Objective:

To investigate ocular movements measures of vectoelectro-nystagmography and video-nystagmography in dyslexic children and compare with measures of typical children.

Methods:

A systematic review of observational studies comparing the ocular movements differences between dyslexic and typical children with no publication date or language restriction. The literature survey included the bibliographic databases MEDLINE, ScienceDirect, Scopus, Web of Science, SciELO, Lilacs and CENTRAL. Gray literature databases were also searched, including: OpenGrey.eu, DissOnline.de, The New York Academy of Medicine and WorldCat. The meta-analysis was performed using software RevMan 5.3 (Cochran Collaboration).

Results:

A total of 2375 articles were found of which 113 fell within the inclusion criteria. Among these, 52 were duplicates (found in more than one research source), and 45 articles were selected for reading in full. Thirteen (13) articles were included for analysis and discussion. Meta-analysis showed statistical differences between the two groups for the total number of saccades and duration of fixation.

Conclusion:

The study revealed that children with dyslexia have longer duration of fixation and fewer saccades during ocular movements on vectoelectro-nystagmography and videonystagmography when compared to children without dyslexia.

Keywords
Dyslexia; Disorder of language; Videonystagmography; Vectoelectronystagmography; Eye tests

Name	Location	Year	Reason	Name	Location	Year	Reason
Benfatto et al.	Sweden	2016	Did not analyze saccades	Bucci et al.²⁷27 Bucci MP, Nassibi N, Gerard CL, Bui-Quoc E, Seassau M. Immaturity of the oculomotor saccade and vergence interaction in dyslexic children: evidence from a reading and visual search study. PLoS One. 2012;7:e33458.,^a a Articles excluded only from meta-analysis but included in the qualitative evaluation.	France	2008	Insufficient data for meta-analysis
Krieber et al.	Austria	2016	Age group	Huang et al.	China	2008	Reviewed abstract only
Lukasova et al.²⁴24 Bucci MP, Brémond-Gignac D, Kapoula Z. Latency of saccades and vergence eye movements in dyslexic children. Exp Brain Res. 2008;188:1–12.,^a a Articles excluded only from meta-analysis but included in the qualitative evaluation.	Brazil	2016	Insufficient data for meta-analysis	Kirkby et al.	UK	2008	Review article
Huettig e Brouwer	UK	2015	Age group	Judge et al.	England	2007	Age group
Kunert e Sheepers	Scotland	2015	Did not analyze saccades	Wright	Australia	2007	Visual training
Kim	China	2014	Reviewed abstract only	Judge et al.	England	2006	Age group
Pan	China	2014	Did not analyze saccades	Santos et al.¹³13 Sales R, Colafêmina JF. A influência da oculomotricidade e do reflexo-vestíbulo-ocular na leitura e escrita. Rev CEFAC. 2014;16:1791–7.,^a a Articles excluded only from meta-analysis but included in the qualitative evaluation.	Brazil	1995	Insufficient data for meta-analysis
Bucci et al.²⁵25 Jainta S, Kapoula Z. Dyslexic children are confronted with unstable binocular fixation while reading. PLoS One. 2011;6:e18694.,^a a Articles excluded only from meta-analysis but included in the qualitative evaluation.	France	2014	Insufficient data for meta-analysis	Rodger	Australia	1985	Review article
Xiu et al.	China	2013	Unsupported method	Brown et al.	USA	1983	Visual Evaluation
Pensiero et al.	Italy	2013	Age group	Olson et al.	Germany	1983	Unsupported method
Bellocchi e al.	France	2013	Review article	Romero et al.	USA	1982	Unsupported method
Oliveira et al.	Brazil	2013	Age group	Pavlidis	USA	1981	Visual Training
Kraljevic e Palmovic²⁶26 Kraljevic JK, Palmovic M. Spatial and temporal measurements of eye movement in children with dyslexia. Coll Antropol. 2011;35:191–8.,^a a Articles excluded only from meta-analysis but included in the qualitative evaluation.	Croatia	2011	Insufficient data for meta-analysis	Gabersek et al.	France	1981	Unsupported method
Quercia	France	2010	Review article	Elterman et al.	Canada	1980	Reviewed abstract only
Hawelka et al.	Germany	2010	Unsupported method	Leisman e Schwartz	USA	1978	Unsupported method
Medland et al.	UK	2010	Visual Evaluation	Adler-Grinberg e Stark	USA	1978	Visual training
Thaler et al.	Germany	2009	Population with comorbidity	Bogacz et al.	USA	1974	Age group
Kapoula et al.	France	2009	Reviewed abstract only	Zangwill e Blakemore	USA	1972	Unsupported method
Kirk	UK	2009	Visual Training

Authors	Year	Local	Apparatus/Method	N of the dyslexic group	N of the control group
Tiadi et al.²⁴24 Bucci MP, Brémond-Gignac D, Kapoula Z. Latency of saccades and vergence eye movements in dyslexic children. Exp Brain Res. 2008;188:1–12.	2016	France	Video-oculografia (EyeBrainr T2).	55 (IM= 10.2)	55 (AA = 8.34)^a a Group paired for school age. e 55 (AA= 10.5)^b b Group paired by chronological age.
Vagge et al.²⁵25 Jainta S, Kapoula Z. Dyslexic children are confronted with unstable binocular fixation while reading. PLoS One. 2011;6:e18694.	2015	Switzerland	Video-oculografia infravermelha (OBER 2 System)	11 (IM = 9.4)	11 (AA = 9.2)^b b Group paired by chronological age.
Seassau et al.²⁶26 Kraljevic JK, Palmovic M. Spatial and temporal measurements of eye movement in children with dyslexia. Coll Antropol. 2011;35:191–8.	2014	France	Video-oculografia	43 (IM= 10.6)	42 (AA= 10.7)^a a Group paired for school age.
Tiadi et al.²⁷27 Bucci MP, Nassibi N, Gerard CL, Bui-Quoc E, Seassau M. Immaturity of the oculomotor saccade and vergence interaction in dyslexic children: evidence from a reading and visual search study. PLoS One. 2012;7:e33458.	2014	France	Video-oculografia infravervelha (mobileEBT®, e(ye)BRAIN)	56 (IM= 10.5)	56 (AA= 10.6)^b b Group paired by chronological age.
Pan et al.²⁸28 Pan J, Yan M, Laubrock J, Shu H, Kliegl R. Eye-voice span during rapid automatized naming of digits and dice in Chinese normal and dyslexic children. Dev Sci. 2013;16:967–79.	2013	China	Video-oculografia (EyeLink II -Eye Tracker de alta velocidade)	30 (IM= 10.7)	26 (AA= 10.6)^b b Group paired by chronological age.
Bucci et al.²⁹29 Bucci MP, Mélithe D, Ajrezo L, Bui-Quoc E, Gérard CL. The influence of oculomotor tasks on postural control in dyslexic children. Front Hum Neurosci. 2014;8:981.	2012	USA	Video-oculografia infravervelha (mobileEBTH, e(ye)BRAIN).	12 (IM= 11)	10 (AA = 8.3)^a a Group paired for school age. e 9 (AA= 11)^b b Group paired by chronological age.
Jainta e Kapoula³⁰30 Seassau M, Gérard CL, Bui-Quoc E, Bucci MP. Binocular saccade coordination in reading and visual search: a developmental study in typical reader and dyslexic children. Front Hum Neurosci. 2014;8:85.	2011	USA	Video-oculografia (Chronos Eye-tracking).	13 (IM= 11.7)	7 (AA= 12.7)^b b Group paired by chronological age.
Bucci et al.³¹31 Tiadi A, Seassau M, Bui-Quoc E, Gerard CL, Bucci MP. Vertical saccades in dyslexic children. Res Dev Disabil. 2014;35:3175 –81.	2007	France	Video-oculografia fotoelétrica (Oculomotor-Bouis).	18 (IM= 11.4)	13 (AA= 11.1)^b b Group paired by chronological age.

Authors	Average amplitude of saccades (±SD)
Authors	Dyslexic group	Control group
Bucci et al.³¹31 Tiadi A, Seassau M, Bui-Quoc E, Gerard CL, Bucci MP. Vertical saccades in dyslexic children. Res Dev Disabil. 2014;35:3175 –81.	27.1 ±1	35 ±0.8
Bucci et al.²⁶26 Kraljevic JK, Palmovic M. Spatial and temporal measurements of eye movement in children with dyslexia. Coll Antropol. 2011;35:191–8.	29.1 ± 1.8	36.9 ± 1.8
Jainta e Kapoula³⁰30 Seassau M, Gérard CL, Bui-Quoc E, Bucci MP. Binocular saccade coordination in reading and visual search: a developmental study in typical reader and dyslexic children. Front Hum Neurosci. 2014;8:85.	2.42 ±0.99	2.09±0.52
Tiadi et al.²⁴24 Bucci MP, Brémond-Gignac D, Kapoula Z. Latency of saccades and vergence eye movements in dyslexic children. Exp Brain Res. 2008;188:1–12.	8.6± 1.3	9.7± 1.2

Authors	Average length of saccades fixation (±SD) ms
Authors	Dyslexic group	Control group
Bucci et al.³¹31 Tiadi A, Seassau M, Bui-Quoc E, Gerard CL, Bucci MP. Vertical saccades in dyslexic children. Res Dev Disabil. 2014;35:3175 –81.	1497 ±107	337 ±29
Jainta e Kapoula³⁰30 Seassau M, Gérard CL, Bui-Quoc E, Bucci MP. Binocular saccade coordination in reading and visual search: a developmental study in typical reader and dyslexic children. Front Hum Neurosci. 2014;8:85.	351 ± 118.4	280.1 ±85.1
Pan et al.²⁸28 Pan J, Yan M, Laubrock J, Shu H, Kliegl R. Eye-voice span during rapid automatized naming of digits and dice in Chinese normal and dyslexic children. Dev Sci. 2013;16:967–79.	322 ±42	283 ±30
Tiadi et al.²⁷27 Bucci MP, Nassibi N, Gerard CL, Bui-Quoc E, Seassau M. Immaturity of the oculomotor saccade and vergence interaction in dyslexic children: evidence from a reading and visual search study. PLoS One. 2012;7:e33458.	291.2±36.4	235.5 ±34.3

Authors	Average number of total saccades (±SD)
Authors	Dyslexic group	Control group
Bucci et al.²⁹29 Bucci MP, Mélithe D, Ajrezo L, Bui-Quoc E, Gérard CL. The influence of oculomotor tasks on postural control in dyslexic children. Front Hum Neurosci. 2014;8:981.	95 ±9	36±3
Vagge et al.²⁵25 Jainta S, Kapoula Z. Dyslexic children are confronted with unstable binocular fixation while reading. PLoS One. 2011;6:e18694.	170.8 ±77.7	101.9±32.7

Authors	Representativeness of the sample	Justified sample size	Rate of non-answers	Exposure calculation	Comparability	Evaluation of results	Appropriate statistical testing	Final evaluation
Tiadi, Gérard, Peyre et al. (2016)²⁴24 Bucci MP, Brémond-Gignac D, Kapoula Z. Latency of saccades and vergence eye movements in dyslexic children. Exp Brain Res. 2008;188:1–12.	Not representative	Yes	0	Validated tool	Yes	Own report	Yes	7/10
Lukasova, Silva and Macedo (2016)²⁰20 Sterne JAC, Egger M, Moher D. Addressing reporting biases. In: Higgins JPT, Chichester GS, editors. Cochran handbook for systematic reviews of interventions. UK: Wiley; 2008. p. 297 –325.	Not representative	Yes	0	Validated tool	Yes	Own report	Yes	7/10
Vagge, Cavanna, Traverso et al. (2015)²⁵25 Jainta S, Kapoula Z. Dyslexic children are confronted with unstable binocular fixation while reading. PLoS One. 2011;6:e18694.	Not representative	No	0	Validated tool	Yes	Own report	Yes	6/10
Bucci, Mélithe, Ajrezo et al.(2014)²¹21 Higgins JPT, Altman DG, Sterne JAC. Assessing risk of bias in included studies. In: Higgins JPT, Green S, editors. Cochran handbook for systematic reviews of interventions. UK: Wiley; 2016. p. 8–73.	Not representative	Yes	0	Validated tool	Yes	Own report	Yes	7/10
Seassau, Gérard, Bui-Quoc et al. (2014)²⁶26 Kraljevic JK, Palmovic M. Spatial and temporal measurements of eye movement in children with dyslexia. Coll Antropol. 2011;35:191–8.	Not representative	Yes	0	Validated tool	Yes	Own report	Yes	7/10
Tiadi, Seassau, Bui-Quoc et al. (2014)²⁷27 Bucci MP, Nassibi N, Gerard CL, Bui-Quoc E, Seassau M. Immaturity of the oculomotor saccade and vergence interaction in dyslexic children: evidence from a reading and visual search study. PLoS One. 2012;7:e33458.	Not representative	Yes	0	Validated tool	Yes	Own report	Yes	7/10
Pan, Yan, Laubrock, Hua Shu et al. (2013)²⁸28 Pan J, Yan M, Laubrock J, Shu H, Kliegl R. Eye-voice span during rapid automatized naming of digits and dice in Chinese normal and dyslexic children. Dev Sci. 2013;16:967–79.	Not representative	Yes	0	Validated tool	Yes	Own report	Yes	7/10
Bucci, Nassibi, Gerard et al. (2012)²⁹29 Bucci MP, Mélithe D, Ajrezo L, Bui-Quoc E, Gérard CL. The influence of oculomotor tasks on postural control in dyslexic children. Front Hum Neurosci. 2014;8:981.	Not representative	No	0	Validated tool	Yes	Own report	Yes	6/10
Kraljevic and Palmovic (2011)²²22 Santos MTM, Behlau MS, Caovilla HH. Crianças com distúrbios de leitura e escrita: movimentos oculares na leitura à nistagmografia computadorizada. Rev Bras Med Otorrinolaringol. 1995;2:100–8.	Not representative	No	0	Validated tool	Yes	Own report	Yes	5/10
Jainta and Kapoula (2011)³⁰30 Seassau M, Gérard CL, Bui-Quoc E, Bucci MP. Binocular saccade coordination in reading and visual search: a developmental study in typical reader and dyslexic children. Front Hum Neurosci. 2014;8:85.	Not representative	No	0	Validated tool	Yes	Own report	Yes	6/10
Bucci, Gignac and Kapoula (2008)²³23 Bucci MP, Brémond-Gignac D, Kapoula Z. Poor binocular coordination of saccades in dyslexic children. Graefe’s Arch Clin Exp Ophthalmol. 2008;246:417–28.	Not representative	No	0	Validated tool	Yes	Own report	Yes	6/10
Bucci, Gignac and Kapoula (2007)³¹31 Tiadi A, Seassau M, Bui-Quoc E, Gerard CL, Bucci MP. Vertical saccades in dyslexic children. Res Dev Disabil. 2014;35:3175 –81.	Not representativa	No	0	Validated tool	Yes	Own report	Yes	6/10
Santos, Behlau and Caovilla (1995)¹²12 Hutzler F, Wimmer H. Eye movements of dyslexic children when reading in a regular orthography. Brain Lang. 2004;89:235–42.	Not representative	No	0	Validated tool	Yes	Own report	Yes	6/10

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