Evidence that vestibular hypofunction affects reading acuity in children

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1 International Journal of Pediatric Otorhinolaryngology (2006) 70, Evidence that vestibular hypofunction affects reading acuity in children Jennifer Braswell a, *, Rose Marie Rine b,1 a Department of Physical Therapy, The University of Alabama at Birmingham, RMSB 389, rd Avenue South, Birmingham, AL 35222, United States b University of North Florida, College of Health, Department of Physical Therapy, 4567 St. Johns Bluff Road, South Jacksonville, FL , United States Received 22 April 2006; received in revised form 13 July 2006; accepted 14 July 2006 KEYWORDS Dynamic visual acuity; Development; Reading acuity; Vestibular hypofunction; Children Summary Objective: Despite reported gaze stability deficits in children with hearing impairment and concurrent vestibular hypofunction, the reading difficulties reported in this population have not been linked to the gaze instability. The purpose of this study was to develop a modified version of the MNREAD chart that enabled responses orally or using sign language. Methods: Seventy-two typically developing children and 14 children with sensorineural hearing loss with and without vestibular hypofunction participated. We examined: (1) reliability and age related changes in reading acuity scores, (2) the effect of vestibular hypofunction on reading acuity scores, and (3) the relationship between these scores and a test of dynamic visual acuity. Results: The test was reliable (ICC (3,2) 0.86). Reading acuity scores were significantly worse in children with vestibular hypofunction ( p 0.002). Furthermore, reading acuity scores correlated with dynamic not static visual acuity scores (r = 0.55, p < 0.001). Conclusions: These results imply that the gaze instability due to vestibular hypofunction affects reading ability in young children. # 2006 Elsevier Ireland Ltd. All rights reserved. 1. Introduction * Corresponding author. Tel.: ; fax: addresses: Jbraswel@uab.edu (J. Braswell), rrine@gowebway.com (R.M. Rine). 1 Tel.: Reading acuity is dependent upon visual acuity and ocular motor control, both of which may be deficient in individuals with vestibular hypofunction resulting in an aberrant vestibular-ocular reflex (VOR) [1 3]. The VOR typically enables the eyes /$ see front matter # 2006 Elsevier Ireland Ltd. All rights reserved. doi: /j.ijporl

2 1958 J. Braswell, R.M. Rine to fixate on a target of interest when the head is moving at a velocity greater than or equal to 1008 s 1, the limits of the smooth pursuit system [4,5]. Therefore, although oculomotor mechanisms are not directly affected by a peripheral vestibular lesion [6], it is possible that the VOR deficit disrupts the coupling of eye and head movement [7] that is used for reading, thus contributing to gaze instability during reading. This concept is supported by reports that adults with peripheral vestibular hypofunction complain of difficulty reading, particularly when upright and moving [1]. Demer and Viirre [8] and others [1,2] tested visual acuity with head movement (i.e. visual acuity when walking), and reported oscillopsia or a disruption of gaze stability and difficulty reading in adults with vestibular hypofunction (VH). Herdman et al. [9] reported improved gaze stability, based on measures of dynamic visual acuity, following exercise intervention in a similar group of adults. Based on these reports, it is tempting to conclude that as a consequence of VH, reading acuity is impaired but can be improved with intervention. However, reports of these changes are anecdotal. The effect of VH on reading is particularly relevant for young children who have VH since or shortly after birth since it may interfere with learning to read. Despite reports that bilateral VH is common in children with sensorineural hearing loss [10 18], and that many of these children have oculomotor [19,20] and reading impairments [21 23] the relationship of VH and reading problems in this group has not been examined. The reading impairment in this group has been solely attributed to a deficit in language acquisition [21]. RineandBraswell[10] have demonstrated that children with SNHL and bilateral VH have deficits in gaze stability or dynamic visual acuity. However, there are no reports of the effect of intervention on gaze stability, or whether the disruption in gaze stability affects reading acuity in children with VH. Because of the increased incidence of visual and reading problems in children with hearing loss, investigation of the impact of VH on these problems is important. This type of investigation has been limited, in part, by limitations of available tests of reading acuity. The MNREAD test [24] was developed as an outcome measure for reading acuity and speed in adults so that improvement due to intervention (e.g. glasses, magnification) could be assessed. Based on examination of the psychophysics of reading [24 26] and the effect of print characteristics on reading ability, the following have been identified as critical parameters of a chart to test reading acuity [24]: (1) print size should be based on the height of the lower case x or o, smaller than the acuity of people with typical vision, large enough to accommodate all subjects, and should follow a logarithmic progression, (2) font should be that used in everyday reading materials with no special symbols, (3) each line of words must have the same number of characters, including spaces, should fit into a box of fixed aspect ratio and be printed in three or more lines of text that are left and right justified, (4) words should be those used with high frequency, avoiding words with regional spelling and punctuation, (5) two versions of the chart should be created to avoid memorization, (6) high contrast text should be used, and (7) testing should be done with uniform lighting and no shadows. Based on these criteria, the MNREAD chart [24] was developed. It uses a series of sentences printed at sizes ranging from 1.3 to 0.4 logmar in 0.1 logmar steps, and Mansfield et al. [24] demonstrated that acuity measured with this chart correlated highly with acuity measured with the Sloan M Cards (r = 0.94). The MNREAD test yields three measures of reading performance: (1) reading acuity, or the smallest print size that can be read, (2) maximum reading speed or the speed at which print size is not a limiting factor and (3) critical print size, the smallest print that can be read with minimal errors and maximum speed (considered effortless reading). However, the test was designed for use with adults, and the lack of control for lexical cueing limits validity of its use with individuals with language deficits. The use of sign language by adults or children with hearing loss limits the use of the MNREAD test because the sentences on the test do not clearly interpret into sign (e.g. articles), and similar words are used that have the same sign (e.g. small and little). Additionally, reading level is set at the third grade level and the use of complete sentences enables lexical cueing/interference. Individuals use lexical cues, the recognition of a word based on context cues and seeing only a few letters, when words are outside of the visual span. Visual span is the number of letters recognizable in a glance. Legge et al. [27] measured reading time as a function of word length. These investigators found that the visual span in central vision is 10 letters, and is reduced to 1.7 letters in peripheral vision. Individuals with language deficits or poor understanding of reading may not be able to take advantage of lexical cueing resulting in a reduction in score. This would place those with language difficulties at a disadvantage and confound results: are lower scores due to acuity or an inability to use lexical cueing that is used by those without language difficulties? Clearly, to test reading acuity in young children and

3 Evidence that vestibular hypofunction affects reading acuity in children 1959 adults, a test of reading acuity must minimize cognitive demands, enable testing of individuals who use sign language, and use groups of unrelated words rather than sentences to control for lexical cueing/interference. In summary, VH has been shown to cause gaze stability deficits in children with SNHL and a concurrent VH. Determination of the effect of this impairment on reading is critical to the development of appropriate interventions to address this problem. To do this requires testing of VH, gaze stability and reading acuity. A test of reading acuity for children and adults should include the parameters as described for the MNREAD chart to measure critical print size and reading acuity in logmar [24]. In addition, the chart should: (1) use groups of unrelated words, rather than sentences, to prevent lexical interference and to control for cognitive effects (i.e. children who do not understand the language but are able to read the words), (2) have more words per line, thus mimicking real life situations (e.g. books with large pages, copying from the blackboard), and (3) contain words that are able to be signed using American Sign Language so that children or adults can either read out loud or sign the words. The purpose of this study was threefold: (1) to develop a modification of the MNREAD test for use with young children (second grade level) using sign or verbal responses, and in which the effect of lexical cueing is minimized (study 1), (2) to examine the effect of VH on reading acuity (study 2) and (3) to examine the relationship of gaze stability scores to reading acuity scores in children with SNHL (study 2). 2. Study 1: development of the pediatric reading acuity test: reliability and age related changes Two reading acuity charts were developed to test children and adults with or without SNHL. The first chart was developed using first and second grade level Dolch words (i.e. the 220 most commonly used words in the written English language) [28]. The second chart was a signing chart, developed with identical properties but with words at the first and second grade level, each having a unique sign. Both charts contained 17 word strings (Fig. 1A). Each word string consisted of three lines of seven words with 21 words per string. The words were chosen from the word lists in a random-blocked manner so that each line contained three 3-letter words (nine in each group), one 4-letter word (three in each group), two 5-letter words (six in each group) and one 6-letter word (three in each group). This provided 35 characters per line (counting spaces) and enough character spaces to exceed the visual span of 10 letters [27] at the smaller font sizes. For example, the word group printed in 11.5 font (log- MAR 0.50) spanned 9.4 cm and exceeded 18 of arc. A total of 17 word strings were used, with words repeated every third string (each word was repeated a total of six times on the chart). A total of 63 different words were used per chart, minimizing memorization. The word strings were printed at sizes from 1.3 to 0.30 logmar with successive strings differing in size by 0.10 logmar (Table 1). To convert font size to acuity in logmar, the formula as described by Mansfield et al. was used: logmar value = log 10 (angle subtended by lowercase Fig. 1 The Pediatric Reading Acuity chart includes groups of Dolch words in successively smaller sizes (A). Only the group being read was visible during testing (B).

4 1960 J. Braswell, R.M. Rine Table 1 Dolch words used in the development of the oral chart 1.3 logmar: around two find ran could sit funny her where 1.2 logmar: before off very may drink you found myself are kind saw after him help green out little hot which always let keep its white yes want see every laugh red yellow use sleep 1.1 logmar: too hold who small for round got eight please and show ask under big take brown 10 better eat black 0.9 logmar: around for very and laugh eat green hot funny pretty yes show ran where her hold found ask yellow let drink 0.7 logmar: yellow are kind who drink red funny ran under please yes find use which hot hold every big little her where 0.5 logmar: around him keep ask could out black too brown pretty saw very its laugh may help found eat better for eight 0.3 logmar: myself its take saw round big eight out after pretty too show eat where ran help funny see please for under 0.1 logmar: always two very sit where big under ran laugh before who hold yes found too help green its myself for eight 0.1 logmar: little 10 want may funny got sleep see drink yellow you kind use every off show black and better hot small 0.3 logmar: always too very off after who brown 10 round pretty sit want yes funny eat find eight you around let could 1.0 logmar: better red help off under see round got which little 10 find use after him take sleep out myself you brown 0.8 logmar: please too want big every its small are eight before sit kind may black two keep could who always saw white 0.6 logmar: myself off want you white let small got sleep always and show see green 10 take after two before sit round 0.4 logmar: before off hold yes drink use small 10 green better sit find and brown are kind laugh may little him found 0.2 logmar: always you keep let black two which red white around who very ask sleep hot want could got yellow her every 0 logmar: please ask find let brown red could him which around her keep eat after out take round saw pretty are white 0.2 logmar: better its show big small out where saw laugh little two help ran white are take under ask before got green x height)/5 min of arc) [24]. A Vernier caliper, accurate to mm, was used to determine that one point in Times Roman font is equal to 0.16 mm. Due to limitations of commercially available printing equipment, the smallest size on the reading charts was 0.3 logmar, which corresponds to a font size of two point. The charts were printed at a resolution of 1400 dots per inch, allowing resolution of 0.3 logmar. Because word processing programs are only able to print whole and half point sizes, each size was rounded to the nearest half point. Scoring was similar to that used in the MNREAD test. Reading speed, in words per minute, was calculated for each word string using the formula: (21 words per group) (60 s)/time in seconds = 1260/ time in seconds [24]. Critical print size (CPS, in logmar) was determined based on the relative speed. Relative speed was calculated using the following equation: relative speed = speed of the word string read with only one incorrect word divided by the mean reading speed of all word strings through the smallest string read with one incorrect word. The logmar of the smallest string read with one or no word missed, that had a relative speed of at least 80%, was identified as the critical print size. Reading acuity (RA, in logmar) was calculated using the following formula: 1.4 (word groups attempted 0.1) + (errors 0.005). Because maximum reading speed depends on how quickly the subject speaks or signs, differences cannot be attributed to reading performance. Therefore, when testing those using sign, only CPS and RA should be used Methods Subjects Seventy-two healthy subjects were recruited from the Miami community to examine age related changes in reading acuity. Subjects included adults (n = 29, mean age = years; range = ) and children (n = 43, mean age = years; range = 7 17) with no known vestibular, orthopedic, visual or neurological disorder. Subjects were grouped to enable examination of the effect of age on scores: (1) 7 8 years and older (n = 11); (2) years and older (n = 10); (3) years and older (n = 10); (4) years and older (n = 12); (6) 18.1 years and older (n = 29). In addition, a group of 14 children with bilateral SNHL (mean age =

5 Evidence that vestibular hypofunction affects reading acuity in children years; range = 8 14) were recruited to assure that those who sign could complete the test without difficulty. Exclusion criteria included any neurologic (other than SNHL or vestibular lesion in this group), orthopedic, cognitive, ocular-motor dysfunction or inability to read the words on the chart. Informed consent was obtained from all subjects 18 years and older, and from the parents of all subjects under the age of 18 years. Assent was obtained from all children 7 to 18 years, per the protocol approved by the Medical Sciences Review Committee of the University of Miami School of Medicine Instrumentation All subjects completed a health questionnaire concerning previous and present health status to include history of hearing loss or vestibular dysfunction. An oculomotor screen was performed that included examination of smooth pursuit, saccades, convergence and optokinetic nystagmus Reading acuity testing To assure that each subject knew the words, a pretest was done. Healthy subjects were presented with 20 words randomly selected from the chart. Each word was presented one at a time on three by five inch cards at 72 point font. Testing on the acuity chart was completed only if all words on the pre-test were read correctly. The children with SNHL who used American Sign Language were required to sign all of the words used on the signing chart, presented as above, before reading acuity testing was done. For this group, a teacher or interpreter fluent in sign language gave the instructions. The investigator was familiar with the signs for words on the chart to score during testing. In addition, testing of the children with SNHL was videotaped for reference and to assure accuracy of scoring. To complete the Pediatric Reading Acuity Test, subjects sat with the chart placed 40 cm from the eyes, which was monitored to assure this distance was maintained. The chart was on a stand that enabled height adjustment so that the group of words being read was at eye level throughout testing. Only the group of words being read was visible (Fig. 1B). Subjects were instructed to begin reading the words out loud at a comfortable pace as accurately as possible as soon as the group was uncovered. Words unable to be read were to be skipped so that the entire group of words could be completed. Testing was stopped when subjects were unable to read all words in a group. The examiner marked the words missed, and recorded the time in seconds, to the hundredths of a second, to complete each group. Two trials were completed. The first trial began at 1.3 logmar (the largest group). The second trial began five groups above the smallest word group that was read correctly on the first trial. Scores were averaged for analysis. To examine test retest reliability, 48 of the 72 healthy subjects (adults n = 28, children n = 20) and 10 of the 14 children with SNHL participated in repeat testing (mean time between tests = 10.3 days). To assure that the signing and oral charts were similar, five healthy children (mean age = years) and five healthy adults (mean age = years) were tested using both charts, with chart sequence done in a random-blocked design Analysis Descriptive statistics were used to examine trends in the data. Intra-class correlation coefficient model three was used to examine intra-rater reliability [29]. Paired samples t-test was used to compare results of the oral chart versus signing chart. ANOVA with Tukey HSD post hoc tests were used to determine whether differences existed between the age groups on reading acuity and critical print size in the normative sample. In the event that the data did not meet the assumptions for parametric statistics, nonparametric statistics were used. The differences between reading acuity scores in children with SNHL were analyzed in study # Results All children with SNHL were able to complete the reading acuity test using either sign (n = 9) or oral reading (n = 5). Test retest reliability was excellent for CPS (ICC (3,2) = 0.86) and reading acuity (ICC (3,2) = 0.88). The mean difference between tests one and two was logmar for reading acuity and for critical print size. When scores of the ten subjects with SNHL who completed reliability testing were analyzed separately, reliability was lower for CPS (ICC (3,2) = 0.76), but the mean difference between test one and two was only logmar. This was less than the mean difference of all subjects. Reliability for RA was excellent (ICC (3,2) = 0.91) for the subjects with SNHL. The lower ICC value for CPS is attributed to the smaller number of subjects in the SNHL group Comparison of oral chart versus signing chart The results of paired t-test revealed that CPS scores achieved on the two charts were different (t = 3.161, p = 0.012), but differences were not clinically significant. Scores were within one line of each other (difference = logmar), which is similar to test retest differences on the same

6 1962 J. Braswell, R.M. Rine Table 2 Critical print size and reading acuity mean scores by age group Groups N CPS a, mean S.D. (logmar) RA b, mean S.D. (logmar) 7 8 years and older years and older years and older years and older Adult (>18 years and older, 52 years and older) Total a Critical print size. b Reading acuity. chart, and the better score was on the second test, indicating a learning effect. RA scores achieved on the two charts did not differ Age related changes Kruskall Wallis was used to examine the age related changes in CPS of the normative sample due to violation of assumption of homogeneity of variances. Although a step-wise change is evident, differences were not significant (X 2 = 4.082, p = 0.395, Z 2 = 0.068). One-way ANOVA results revealed differences of RA scores between at least two of the groups (F(4,67) = 4.859, p=0.002, Z 2 = 0.225). Tukey HSD post hoc analysis revealed that RA scores achieved by the 7 8 year and year old groups were significantly higher (larger print size) than those of the year old group. Only the 7 8 year old group scores differed significantly from adults. No other groups differed on RA (Tables 2 and 3) Summary The Pediatric Reading Acuity Test provides reliable measures of RA and CPS that can be used with children as young as 7 years with or without a hearing impairment. Furthermore, use of a chart designed for use with sign language yields results similar to those when using the second chart and speaking the words aloud. 3. Study 2: Gaze stability and reading acuity in children with SNHL and VH 3.1. Methods Subjects The 14 children with bilateral severe or profound SNHL who participated in the initial study also participated in this study. The children were grouped by vestibular function, based on rotary testing with electro-oculography: (1) SNHL and hypofunction, (2) SNHL and normal vestibular function. Rotary testing with electro-oculography (sinusoidal harmonic acceleration and trapezoidal) test was completed as described by Wall [30]. Three of the subjects had bilateral VH (BVH; 21.43%), two had rotary chair results consistent with a compensated unilateral loss (14.29%) (a total of five with VH). Nine (64.28%) were either normal (n = 7) or had a gain that was greater than the normative sample (hyperfunction, n = 2). These nine subjects were considered to have normal vestibular function for analysis (Table 4) Instrumentation Gaze stability: dynamic visual acuity was also tested for 23 of the healthy children (mean age = years, range = 7 13) and for the 14 children with SNHL using the protocol described in a previous Table 3 Reading acuity post hoc analysis of group comparisons with effect size measures Groups compared Mean difference S.E. p g Effect size Adults and 7 8 years and older Large Adults and years and older Large Adults and years and older <Small Adults and years and older Medium and years and older Medium and years and older Large and 7 8 years and older Large and years and older Large and 7 8 years and older Large and 7 8 years and older <Small

7 Evidence that vestibular hypofunction affects reading acuity in children 1963 Table 4 Frequencies and age ranges of subjects with SNHL by vestibular function N Mean S.D. (range) in years Bilateral vestibular hypofunction (8 14) Compensated unilateral vestibular hypofunction ( ) Normal vestibular function (8 14) All children with SNHL (8 14) report [10]. Visual acuity was tested with the head still, and again with the head passively moved by the examiner in a 308 arc (158 to the left and right of straight ahead) at 2 Hz. Two trials were completed under each condition, with scores averaged. Dynamic visual acuity score was calculated as the difference (in logmar) in scores attained on static and dynamic testing Reading acuity Scores attained in study 1 were used Analysis ANOVA was used to determine if differences existed between: children with SNHL and hypofunction (n = 5), children with SNHL and normal vestibular function (n = 9) and healthy children (n = 43). Independent samples t-test was used to examine differences between children with SNHL and normal vestibular function (n = 9) and age matched healthy subjects (30 healthy subjects were in the age range of 8 14 years). To examine the relationship of RA and DVA in the children who completed both RA and DVA testing (n = 37), data was analyzed using the Pearson Product Moment Correlation Results Results support the idea that children with VH, particularly those with BVH, have poorer reading acuity scores than peers without VH regardless of hearing status. Specifically, results of one-way Fig. 2 Critical print size (CPS) and reading acuity (RA) scores were significantly higher in children with SNHI and VH, as compared to peers without VH regardless of hearing status. Hypofunction = vestibular hypofunction (n = 5), SNHL NVF = sensorineural hearing loss and normal vestibular function (n = 9), healthy = normal hearing and vestibular function (n = 43). ANOVA revealed differences between at least two of the groups in CPS (F(2,54) = 6.740, p = 0.002, Z 2 = 0.200) and RA (F(2,54) = , p < 0.001, Z 2 = 0.354) (Table 5). The large effect size indicated that VH (VH versus normal vestibular function with and without SNHL) explains 20 and 35% of the variability in CPS and RA, respectively. Tukey HSD post hoc analysis revealed that subjects with SNHL and VH had CPS and RA scores that were significantly larger than subjects with SNHL and normal vestibular function ( p = 0.02) and subjects without SNHL ( p = 0.002). The RA (t = 2.53; p = 0.016), but not the CPS (t = 0.569; p = 0.573) scores achieved by children with SNHL without VH (n = 9) differed from that achieved by age matched peers without hearing impairment (Fig. 2). Table 5 CPS and RA mean scores for subjects with and without SNHL Groups N Mean CPS S.D. (logmar) Corresponding font size (from 40 cm) Mean RA S.D. (logmar) Corresponding font size (from 40 cm) SNHL hypo a point point BVH b point point UVH c point point SNHL NVF d point point Healthy point point Total a SNHL hypo = sensorineural hearing impairment and vestibular hypofunction. b BVH = bilateral vestibular hypofunction. c UVH = unilateral vestibular hypofunction. d SNHL NVF = sensorineural hearing impairment and normal vestibular function.

8 1964 J. Braswell, R.M. Rine A significant positive correlation was found between dynamic visual acuity and CPS (r = 0.55; p < 0.001) and dynamic visual acuity and RA (r = 0.66; p < 0.001). Static visual acuity scores did not correlate with CPS. 4. Discussion The results of this study reveal that the Pediatric Reading Acuity Test is a reliable measure of critical print size and reading acuity for children, adults and children with SNHL. Furthermore, test results distinguish reading ability between subjects with and without VH, regardless of hearing status. The oral and signing charts were designed with identical parameters, and scores between the two did not differ by more than one line in subjects who completed both. Therefore, scores obtained from the oral or the signing chart can be considered equivalent. Interestingly, critical print size, but not reading acuity, was found to be adult-like by the age of 7 years. This differs from results by Virgili et al. [31] who report a linear increase in CPS with grade level, which may be attributed to a difference in methods, charts used for testing and statistical analysis. The higher reading acuity score (larger size required) achieved by children under the age of 9 years suggests that even if time is not limited, children under the age of 9 years require a larger print size. The finding that reading acuity is adult-like at 9 years of age implies that binocular stereo-acuity needed for reading is not mature until this age. Children with SNHL, a group that reportedly has reading difficulty due to language impairments, were able to reliably complete the test using sign or reading orally. Although the study included a very small number of children with SNHL, several important trends emerged. The lack of difference on CPS between those with and without SNHL without VH implies that this reading acuity test was able to eliminate the effects of language impairments in the identification of the size font that is required for efficient reading. Although the RA score achieved by children with SNHL without VH was higher than typical peers, the range of RA values in this group was 0.11 to 0.17 logmar. This corresponds to a font size of point, which is much smaller than font sizes used in everyday reading material. The ability of this group to read (verbally aloud or sign) effortlessly at a very small font size indicates that differences in RA due to hearing alone is not clinically significant. Conversely children with SNHL with VH had CPS and RA scores that were significantly lower than subjects without hypofunction, regardless of hearing status (6 7.5 point font). This implies that the VH contributes to the reading difficulties reported in children with hearing loss. The correlation of DVA with CPS & RA implies that the disruption of gaze stability due to VH would be evident only with DVA testing and that VH contributes to the reading difficulties reported in children with hearing loss. 5. Conclusion In summary, the Pediatric Reading Acuity Test provides reliable measures of reading ability of young children and adults who may use sign language. Data presented here demonstrate that dynamic visual acuity scores correlate with CPS (effortless reading score), and that VH affects reading ability in children. This finding supports the importance of testing vestibular function in children with SNHL, and the testing of reading acuity for all children with VH, so that appropriate intervention can be provided to minimize reading difficulty. Future studies should examine critical print size related to measures of reading achievement to determine optimal print to be used and to determine whether rehabilitation aimed at improving gaze stability might improve reading acuity scores in this group. References [1] G. Grossman, R. Leigh, Instability of gaze during locomotion in patients with deficient vestibular function, Ann. Neurol. 27 (1990) [2] E.J. Hillman, J.J. Bloomberg, P. McDonald, H.S. Cohen, Dynamic visual acuity while walking in normals and labyrinthine-deficient patients, J. Vestibular Res. 9 (1999) [3] M.C. Schubert, S.J. Herdman, R.J. Tusa, Vertical dynamic visual acuity in normal subjects and patients with vestibular hypofunction, Otol. Neurol. 23 (2002) [4] S.J. Herdman, R.J. Tusa, P. Blatt, A. Suzuki, P.J. Venuto, D. Roberts, Computerized dynamic visual acuity test in the assessment of vestibular deficits, Am. J. Otol. 19 (1998) [5] R.J. Leigh, D.S. Zee, Smooth pursuit and visual fixation, in: R.J. Leigh, D.S. Zee (Eds.), The Neurology of Eye Movements, FA Davis, Philadelphia, [6] M.A. Gresty, K. Hess, J. Leech, Disorders of the vestibuloocular reflex producing oscillopsia and mechanisms compensating for loss of labyrinthine function, Brain 100 (1977) [7] C. Lee, Eye and head coordination in reading: roles of head movement and cognitive control, Vision Res. 39 (1999) [8] J.L. Demer, E.S. Viirre, Visual-vestibular interaction during standing, walking, and running, J. Vestibular Res. 6 (4) (1996) [9] S.J. Herdman, M.C. Schubert, V.E. Das, R.J. Tusa, Recovery of dynamic visual acuity in unilateral vestibular hypofunction, Otolaryngol. Head Neck Surg. 129 (2003)

9 Evidence that vestibular hypofunction affects reading acuity in children 1965 [10] R.M. Rine, J. Braswell, A clinical test of dynamic visual acuity for children, Int. J. Pediatric Otorhinolaryngol. 67 (11) (2003) [11] R.M. Rine, G. Cornwall, K. Gan, C. LoCascio, T. O Hare, E. Robinson, et al., Evidence of progressive delay of motor development in children with sensorineural hearing loss and concurrent vestibular dysfunction, Perceptual Motor Skills 90 (2000) [12] P.E. Brookhouser, D.G. Cyr, K.A. Beauchaine, Vestibular findings in the deaf and hard of hearing, Otolaryngol. Head Neck Surg. 90 (1982) [13] P.L. Huygen, J.B. Hinderink, P. van den Brock, S. van den Borne, J.P. Brokx, L.H. Mens, et al., The risk of vestibular function loss after intracochlear implantation, Acta Otolaryngol. Suppl. 520 (2) (1995) [14] P.L. Huygen, P.M. van Rijn, C.W. Cremers, E.J. Theunissen, The vestibulo-ocular reflex in pupils at a Dutch school for the hearing impaired; findings relating to acquired causes, Int. J. Pediatric Otorhinolaryngol. 25 (1993) [15] P.A. Selz, M. Girardi, H.R. Konrad, L.F. Hughes, Vestibular deficits in deaf children, Otolaryngol. Head Neck Surg. 115 (1) (1996) [16] A. Tribukait, K. Brantberg, J. Bergenius, Function of semicircular canals, utricles and saccules in deaf children, Acta Otolaryngol. 124 (2004) [17] F.O. Black, D.J. Lilly, R.J. Peterka, M.A. Fowler, F.B. Simmons, Vestibulo-ocular and vestibulospinal function before and after cochlear implant surgery., Ann. Otol. Rhinol. Laryngol. Suppl. 96 (1987) [18] K. Kaga, J. Suzuki, R. Marsh, Y. Tanaka, Influence of labyrinthine hypoactivity on gross motor development of infants, Ann. New York Acad. Sci. 374 (1981) [19] I.M. Armitage, J.P. Burke, J.T. Buffin, Visual impairment in severe and profound sensorineural deafness, Arch. Dis. Childhood 73 (1995) [20] R.M. Siatkowski, J.T. Flynn, A.V. Hodges, T.J. Balkany, Visual function in children with congenital sensorineural deafness, Trans. Am. Ophthalmol. Soc. 91 (1993) [21] I. Fusfield, The academic program of schools for the deaf, Volta Rev. 57 (1955) [22] C. Goetzinger, C. Rousey, Educational achievement of deaf children, Am. Ann. Deaf 104 (1959) [23] A. Limbrick, S. McNaughton, M. Clay, Time engaged in reading: a critical factor in reading achievement, Am. Ann. Deaf 137 (4) (1992) [24] J. Mansfield, S.J. Ahn, G. Legge, A. Luebker, A new readingacuity chart for normal and low vision, Ophthalmic Visual Optics/Noninvasive Assess. Visual Syst. Tech. Digest 3 (1993) [25] G. Legge, J. Ross, A. Luebker, J. LaMay, Psychophysics of reading VIII. The Minnesota low-vision reading test, Optom. Vis. Sci. 66 (1989) [26] J. Mansfield, G. Legge, M. Bane, Psychophysics of reading XV: font effects in normal and low vision, Invest. Ophthalmol. Vis. Sci. 37 (8) (1996) [27] G. Legge, J. Mansfield, S. Chung, Psychophysics of reading XX. Linking letter recognition to reading speed in central and peripheral vision, Vis. Res. 41 (2001) [28] E. Fry, J. Kress, D. Fountoukidis, The Reading Teacher s Book of Lists, Prentice Hall, Paramus, New Jersey, [29] P.E.F.J. Shrout, Intraclass correlation: uses in assessing rater reliability, Psychol. Bull. 86 (1979) [30] C. Wall, The sinusoidal harmonic acceleration rotary chair test: theoretical and clinical basis, Neurol. Clin. 8 (2) (1990) [31] G. Virgili, C. Cordaro, A. Bigoni, S. Crovato, P. Cecchini, U. Menchini, Reading acuity in children: evaluation and reliability using MNREAD charts, Invest. Ophthalmol. Vis. Sci. 45 (9) (2004)