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Visual profile of children with handwriting difficulties in Hong Kong Chinese
Research in Developmental Disabilities 35 (2014) 144–152
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Research in Developmental Disabilities
Visual profile of children with handwriting difficulties in Hong Kong Chinese Mabel M.P. Leung a,*, Carly S.Y. Lam a, Sutie S.T. Lam b, Natalie W.Y. Pao b, Cecilia W.P. Li-Tsang b a b
School of Optometry, The Hong Kong Polytechnic University, Hung Hom, Hong Kong, China Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Hong Kong, China
A R T I C L E I N F O
A B S T R A C T
Article history: Received 5 June 2013 Received in revised form 7 October 2013 Accepted 8 October 2013 Available online 29 October 2013
The purpose of this study was to find out the visual profiles of children with handwriting difficulties (HWD) in Hong Kong Chinese. Forty-nine children with HWD (mean age 8.4 1.1 years) and 27 controls (mean age 7.7 0.7 years) were recruited. All subjects received eye examination and vision assessment included ocular health, refraction, accommodative functions, binocularity, visual perception (by Gardner reversal frequency test: recognition subtest; Test of visual perceptual skills (non-motor)-revised) and motor skills (by The BeeryBuktenica developmental test of visual motor integration; Detroit test of motor speed and precision). Higher percentages of tropia and phoria (of magnitude >6 prism dioptres) were found in children with HWD of 6.1% and 14.3% respectively. After adjusted for the effect of age, children with HWD showed significantly worse accommodative facility, directionality, visual discrimination, visual spatial relation, visual form constancy, visual sequential memory, visual figure ground, visual closure and visual motor integration. Studies reported the visual functions of children with HWD were mostly concerned with alphabetic languages, while studies concerning Chinese HWD were relatively less. This study provided the visual profiles of children with Chinese HWD. Based on the visual profile, further study is indicated to investigate the effect of optometric interventions on the assessment and remediation for children with HWD. ß 2013 Elsevier Ltd. All rights reserved.
Keywords: Visual function Handwriting difficulties Chinese
1. Introduction Handwriting is an important medium for expressing, communicating and recording ideas (Erhardt & Meade, 2005; Reisman, 1993). For school-aged children, good handwriting skill is a prerequisite of learning. Children from kindergartens and primary schools spend 30 to 60% of their school time on fine motor activities, predominately on writing (Marr, Cermak, Cohn, & Henderson, 2003; McHale & Cermak, 1992). It was reported that 10–27% children showed handwriting problems of various degrees (Hammerschmidt & Sudsawad, 2004; Karlsdottir & Stefansson, 2002; Maeland, 1992). Children who are slow in handwriting may have difficulty to cope with the volume of school work and to finish within time constraint. Impaired handwriting can affect children’s academic performance as well as psychological well-being (Bonney, 1992; Erhardt & Meade, 2005; Feder & Majnemer, 2007; Graham & Weintraub, 1996; Hammerschmidt & Sudsawad, 2004; Markham, 1976; Rosenblum, Weiss, & Parush, 2003). Poor handwriting not only frustrated children’s learning, but also influenced teacher’s evaluation of written work (Karlsdottir & Stefansson, 2002; Markham, 1976). Papers with poor handwriting were
* Corresponding author. Tel.: +852 27665225. E-mail addresses: [email protected] (Mabel M.P. Leung), [email protected] (Carly S.Y. Lam), [email protected] (Sutie S.T. Lam), [email protected] (Natalie W.Y. Pao), [email protected] (Cecilia W.P. Li-Tsang). 0891-4222/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ridd.2013.10.013
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consistently marked lower regardless of the contents (Markham, 1976). Illegible handwriting further hindered the accomplishment of higher-orders skills including spelling or story composition (Feder & Majnemer, 2007). In a word reading task, children with HWD showed slower reading speed and larger number of errors compared with controls (Dusek, Pierscionek, & McClelland, 2010). In addition, character copying skills were found related to the development of Chinese literacy skills (McBride-Chang, Chung, & Tong, 2011). Since good handwriting skill is so important for children, early and appropriate intervention is highly indicated. Investigation on the visual profiles of children with HWD, which may aid in the design of appropriate assessment tools and remediation programs, is of particular interest. 1.1. Relationship between handwriting and vision Handwriting is not a simple fine motor task. It involves complex visual perceptual-motor integration. Good Handwriting requires the integration among visual perception, motor planning, cognitive, tactile and kinesthetic functions, gross and fine motor skills, as well as sustained attention (Bonney, 1992; Erhardt & Meade, 2005; Feder & Majnemer, 2007; Maeland, 1992; Reisman, 1993; Rosenblum et al., 2003). Various evidences suggested for the important role of vision in handwriting (Daly, Kelley, & Krauss, 2003; Smyth & Silvers, 1987; Tseng & Chow, 2000; Van Doorn & Keuss, 1992, 1993). The absence of vision during handwriting affected the spatial orientation of written words and caused an increase in errors produced, increase in stroke size and decrease in writing speed (Smyth & Silvers, 1987; Van Doorn & Keuss, 1992, 1993). Further support can be obtained from brain imaging study in which both dorsal and ventral visual streams were found involved at the initial learning stage of Chinese handwriting (Swett, Contreras-Vidal, Birn, & Braun, 2010). Although vision and handwriting are closely related functions, limited studies reported the visual functions of children with HWD. Children with problem in handwriting showed weakness in visual memory, visual sequential memory, visual spatial relation, form constancy, figure ground and visual motor integration (Markham, 1976; Tseng & Chow, 2000; Volman, Schendel, & Jongmans, 2006). However, information about the binocular vision and accommodative functions of children with HWD were scarce. Only one study reported the increased binocular vision and accommodation anomalies including exophoria, convergence insufficiency, accommodation insufficiency and lower accommodative convergence in children with both handwriting and reading difficulties (Dusek et al., 2010). 1.2. Language difference Unlike alphabetic scripts that compose left-to-right languages, Chinese characters are characterized by the spatial organization of strokes making visual-spatial perception important for the orthographic processing and writing of Chinese characters (Kao, Leong, & Gao, 2002). Neuroimaging evidences suggested different neural networks involved in the processing of Chinese characters and alphabetic languages (Sun, Yang, Desroches, Liu, & Peng, 2011; Wu, Ho, & Chen, 2012). Therefore, the complex orthography of Chinese characters as opposed to the phonologic alphabetic languages may lead to differences in visual motor demand. 1.3. Aim of study Vision is an integral part of handwriting. The visual motor demand in handwriting may vary between languages. However, little studies reported the deficient visual functions in children with HWD and mostly were in alphabetic languages (Dusek et al., 2010; Markham, 1976; Volman et al., 2006). Investigation on the visual profiles of Chinese children with HWD may help to identify some possible handwriting performance components, which in turn, aid in the design of appropriate assessment tools and remediation programs (Feder & Majnemer, 2007). This study aimed to find out the visual profiles, from basic visual functions to higher order visual perceptual and visual motor integration skills, of children with HWD particularly in Chinese. 2. Methodology 2.1. Subjects recruitment Seventy-six children, 49 with HWD and 27 controls, were recruited from different Hong Kong mainstream primary schools. All recruited subjects were studying primary 1 or 2 and using Chinese and Cantonese as their primary written and spoken language. By using a validated handwriting ability checklist (Tam, 2008), children were rated by their parents in the aspect of handwriting legibility, speed, physical and emotional responses. Completed checklists were assessed and compared against the suggested cut-off scores (Tam, 2008). Subjects scored 31 or above were classified as HWD and were recruited into the group with HWD, whilst subjects scored 30 or below were recruited into the control group. Children with physical impairments, learning disabilities, attention and behavior problems, neuromuscular disabilities and/or history of any previous intervention on handwriting were excluded from the study. All research procedures adhered to the tenets of the Declaration of Helsinki and were approved by the Ethics Committee of The Hong Kong Polytechnic University. The parents of the children were fully informed and written consent was obtained before all experimental measurements.
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2.2. Visual functions assessment All subjects received eye examination and vision function assessments, including ocular health assessment (biomicroscopy and direct ophthalmoscopy), subjective refraction, accommodative functions (accommodative amplitude by push-up method binocularly and accommodative facility by a lens flipper of 2.00D binocularly) and binocularity (heterophoria by cover test and prism neutralization, convergence by near point of convergence method, fusional vergence by step vergence method, vergence facility by facility prism of 3 prism dioptre base-in/12 prism dioptre base-out and stereoacuity by Randot stereotest). The instructions and procedures for each test on accommodative functions and binocularity were adopted from Scheiman and Wick (Scheiman & Wick, 2002). The patient then received various visual perceptual and motor skills assessments including Gardner reversal frequency test: recognition subtest; The seven subtests of Test of visual perceptual skills (non-motor)-revised (TVPS-R): visual discrimination, visual memory, visual spatial-relationship, visual form-constancy, visual sequential-memory, visual figureground and visual closure; The Beery-Buktenica developmental test of visual motor integration (VMI); Developmental eye movement test (DEM) and Detroit test of motor speed and precision. The procedures and instructions for all assessments were straight away followed according to the examiner’s manuals. 2.3. Data analysis IBM SPSS 16 (SPSS inc., Chicago USA) was used for data analysis. After checking for normality using Shapiro–Wilk test, normal distribution of data in both groups was found in part of the data (Vergence facility, accommodative facility, visual memory, visual closure, VMI, vertical time in DEM and Detroit test of motor speed and precision). The mean age of HWD group was older than that of the control group. Since increase in age could improve motor and most vision functions (Feder & Majnemer, 2007; Scheiman & Wick, 2002; Schneck & Henderson, 1990), the age difference between groups may influence results analysis. To adjust for the effect of age, ANCOVA (with age as a covariate) was used to compare the difference in all visual functions (except ocular deviation) between the HWD and control groups. As stable ocular alignment is expected by the age of 3 months (Mills, 1999), ocular alignment should be independent on age in the studied age group of 7 to 8 years old. One-way ANOVA was used to compare the difference in magnitude of ocular deviation between the HWD and control groups. Chi-square Cramer’s V test was used to analysis the relationship between the direction of ocular deviation and grouping. 3. Results 3.1. Subjects demographic data Table 1 shows the demographic data of the 2 groups of subjects. A total of 76 subjects were recruited. Forty-nine children with HWD of mean age 8.4 1.1 years were recruited into the HWD group. Twenty-seven children without HWD of mean age 7.7 0.7 years were recruited into the control group. There were 67% and 52% males in the HWD and control group respectively. 3.2. Refractive error The refractive error measured by subjective refraction was converted into a spherical equivalent value (Spherical equivalent = Spherical error + Cylindrical error/2) for statistical analysis. The spherical equivalent of the refractive error in the right and left eyes were shown in Table 2. Statistical analysis showed no significant differences in the mean spherical equivalent between the control and HWD groups in both the right and left eye. 3.3. Binocularity and accommodation The percentages of children with tropia were 6.1% and 0% in the HWD and control group respectively. The percentages of children with major phoria (of magnitude greater than 6 prism dioptres) were 14.3% and 7.4% in the HWD and control group respectively. The mean ocular deviation magnitude of HWD group was 1.5 3.7 and 3.9 4.8 prism dioptres at distance and near respectively, while that of control group was 0.5 1.5 and 2.3 3.3 prism dioptres at distance and near respectively. There was no statistically significant difference between the two groups in the magnitude of ocular deviation at both distance (One-Way
Table 1 Demographic data of HWD and controls groups.
Number (n) Mean Age + SD (years) Age range (years) Gender
Control
HWD
27 8.4 + 1.1 6.3 to 9.1 14 Males; 13 Females
49 7.7 + 0.7 6.7 to 10.9 33 Males; 16 Females
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Table 2 Comparison of spherical equivalent of refractive errors between HWD and control groups.
Number (n) Mean + SD
Left eye Right eye
Range
Right eye Left eye
Control
HWD
27
49
0.11 + 1.06 0.16 + 1.14 +1.50 to +1.50 to
3.00 3.63
Statistical calculation (one-way ANOVA)
0.28 + 1.48 0.37 + 1.40 +2.50 to +1.50 to
NO F = 0.29; p = 0.59
5.00 5.00
NO F = 0.44; p = 0.51
ANOVA: F = 1.63, p = 0.21) and near (One-Way ANOVA: F = 2.34, p = 0.13). Statistical calculation also showed no significant difference in the direction of ocular deviation between the two groups at both distance (Cramer’s V = 0.105, p = 0.41) and at near (Cramer’s V = 0.19, p = 0.24). Figs. 1 and 2 shows the percentage of orthophoria, exophoria and esophoria at distance and near respectively in both groups of subjects. After adjusted for the effect of age, no statistically significant difference was found between the two groups in the near point of convergence (ANCOVA: F = 0.05, p = 0.83) and vergence facility (ANCOVA: F = 0.00; p = 0.99). For fusional vergence, all three values of blur, break and recovery points were measured during the study. However, since some of the patients were unable to report the blur point, the recovery point was used instead for statistical calculation. There was also no statistically significant difference in the fusional vergence values between the two groups at both distance and near. The statistical calculation results were summarized in Table 3. According to Sheard’s criterion, the fusional vergence should be at least twice that of the demand for comfortable binocular vision (Scheiman & Wick, 2002). We analyzed the subject’s binocular vision status by checking their tropia or 100
Percentage of subjects (%)
90
HWD
80
Control
70 60 50 40 30 20 10 0
ORTHO
EXO
ESO
Fig. 1. Direction of ocular deviation at distance for both groups. Histogram shows the percentage of orthophoria (ORTHO), exophoria (EXO) and esophoria (ESO) for both HWD and control group when fixating at distance.
100
Percentage of subjects (%)
90
HWD
80
Control
70 60 50 40 30 20 10 0
ORTHO
EXO
ESO
Fig. 2. Direction of ocular deviation at near for both groups. Histogram shows the percentage of orthophoria (ORTHO), exophoria (EXO) and esophoria (ESO) for both HWD and control group when fixating at near.
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Table 3 Comparison of binocularity and accommodative skills between HWD and control groups.
Near point of convergence (cm) Fusional vergence (DD) Distant positive fusional vergence Distant negative fusional vergence Near positive fusional vergence Near negative fusional vergence
Control
HWD
Statistical calculation
(Mean + SD)
(Mean + SD)
ANCOVA (adjusted for age)
5.3 + 1.0
5.3 + 1.3
12.7 + 8.1 7.2 + 3.2 22.1 + 7.6 11.4 + 5.1
13.1 + 8.4 6.2 + 3.0 26.4 + 11.1 10.0 + 3.6
F = 0.05, p = 0.83
F = 2.84, F = 0.02, F = 0.68, F = 2.99,
p = 0.10 p = 0.90 p = 0.41 p = 0.09
Vergence facility (cycles/min.) 3 DD Base In/12 DD Base Out
9.3 + 5.9
9.4 + 5.1
F = 0.00, p = 0.99
Amplitude of accommodation
16.2 + 1.8
15.9 + 2.4
F = 0.12, p = 0.73
7.2 + 2.9
5.2 + 3.4
F = 5.98, p = 0.02
Accommodation facility (cycles/min.)
The bold in the first left column is to separate main categories from sub-categories. The bold in the right column (statistical calculation) is for indicating statistically significant difference.
phoria magnitude against their fusional vergence values. Among those subjects with tropia or phoria, 40.7% of the children with HWD and 27.3% of the controls failed to fulfill the Sheard’s criterion. From our results, children with HWD showed deficient accommodative function. The mean amplitude of accommodation of HWD children was 15.9 2.4 Dioptres which is lower than that of the controls with mean amplitude of accommodation of 16.2 1.8 Dioptres. However, the difference was not statistically significant (ANCOVA: F = 0.12, p = 0.73). The mean accommodation facility of children with and without HWD was 5.2 3.4 and 7.2 2.9 cycles/min respectively. After adjusted for the effect of age, the accommodation facility of HWD children was significantly worse than the controls (ANCOVA: F = 4.09, p < 0.05). 3.4. Visual perceptual skills Table 4 shows the comparison of various visual perceptual skills between children with HWD and the controls. Children with HWD made significantly more errors in the Gardner reversal frequency test: recognition subtest (ANCOVA: F = 4.07, p = 0.047). After adjusted for the effect of age, children with HWD showed consistently poorer performance in visual discrimination (ANCOVA: F = 9.28, p = 0.003), visual spatial relation (ANCOVA: F = 4.29, p = 0.04), visual form constancy (ANCOVA: F = 5.60, p = 0.02), visual sequential memory (ANCOVA: F = 7.95, p = 0.006), visual figure ground (ANCOVA: F = 6.84, p = 0.01), visual closure (ANCOVA: F = 5.20, p = 0.03). Table 4 Comparison of visual perceptual and motor skills between HWD and control groups. Control
HWD
Statistical Calculation
(Mean + SD)
(Mean + SD)
ANCOVA (adjusted for age)a
Gardner reversal frequency test: Recognition subtest
5.2 + 6.3
6.9 + 6.0
F = 4.07, p = 0.047
TVPR-Rb Subtests Visual discrimination Visual memory Visual spatial relations Visual form constancy Visual sequential memory Visual figure ground Visual closure
13. 4 + 1.4 12.4 + 2.0 14.1 + 1.8 11.2 + 1.9 12.3 + 2.1 11.3 + 2.5 9.9 + 3.3
12.3 + 2.6 12.0 + 2.1 13.4 + 2.4 10.2 + 2.8 11.1 + 2.9 10.5 + 3.4 9.0 + 3.6
F = 9.28, F = 3.42, F = 4.29, F = 5.60, F = 7.95, F = 6.84, F = 5.20,
VMIc
18.7 + 3.4
18.0 + 2.5
F = 6.06, p = 0.02
Detroit test of motor speed and precision
75.9 + 17.2
78.6 + 23.3
F = 1.82, p = 0.18
50.0 + 12.5 68.6 + 17.0 4.4 + 6.5 1.4 + 0.2
56.1 + 15.9 79.5 + 35.1 6.3 + 7.7 1.4 + 0.4
F = 12.57, p = 0.001 F = 10.33, p = 0.002 F = 5.50, p = 0.02 F = 1.31, p = 0.26
p = 0.003 p = 0.07 p = 0.04 p = 0.02 p = 0.01 p = 0.01 p = 0.03
d
DEM Vertical time Horizontal time Error score Horizontal ratio a b c d
Statistically significant difference were bolded. Test of visual perceptual skills (non-motor)-revised. The Beery-Buktenia developmental test of visual motor integration: Beery. Developmental eye movement test.
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3.5. Motor skills Children with HWD showed significantly worse performance in VMI (ANCOVA: F = 4.29, p = 0.04). In DEM test, statistically significant difference was found in vertical time (ANCOVA: F = 12.57, p = 0.001), horizontal time (ANCOVA: F = 10.33, p = 0.002) and error score (ANCOVA: F = 5.50, p = 0.02), while no significant difference was found in vertical to horizontal ratio (ANCOVA: F = 1.31, p = 0.26). No significant difference was found in Detroit test of motor speed and precision results between children with or without HWD (ANCOVA: F = 1.82, p = 0.18). 4. Discussion 4.1. Gender bias From our study, more males than females were found in the group with HWD. There was 76% of male in the HWD group and 52% in the control group. Similar gender bias, with 64% in the referred group and 59% in the control group, was reported in a study involving children with reading and handwriting difficulties (Dusek et al., 2010). Besides, males also showed comparatively lower handwriting speed and poorer legibility than females (Feder et al., 2005; Karlsdottir & Stefansson, 2002; Rosenblum et al., 2003). 4.2. Visual functions of children with HWD Our results showed that children with HWD showed weakness in binocularity, accommodative facility, higher order visual perceptual skills and visual motor integration. 4.2.1. Binocularity and accommodation Compared with the controls, the HWD group showed a higher percentage of tropia or significant phoria (magnitude >6 prism dioptres). In the HWD group, percentages of children with tropia and significant phoria were 6.1% and 14.3% respectively, which is much higher than that in the control group. No significant difference in the fusional vergence values between the two groups were found, however the percentage of children who failed to reach the Sheard’s criterion was higher in the HWD group (40.7%) than in the control group (27.3%). According to the Sheard’s criterion, if the fusional vergence is lower than twice that of the demand, it is more likely to have discomfort related to binocular vision (Scheiman & Wick, 2002). Our findings suggested that children with HWD were more likely to have discomfort in binocular vision due to the higher percentage of tropia, phoria and limited fusional vergence that failed to cope with the demand (ocular deviation). In addition, children with HWD showed significantly reduced accommodative facility, while the amplitude of accommodation, convergence and vergence facility were all relatively normal. The higher percentage of ocular deviation in children with HWD was not reported elsewhere before. In addition to the reduced accommodative facility, previous study reported that children with reading and writing difficulties showed reduction in amplitude of accommodation, vergence facility, convergence insufficiency and lower accommodative convergence to accommodation ratio (Dusek et al., 2010). Besides, children with reading and writing difficulties were more likely to report visual related complaints, included burning or stinging eyes, tiredness after reading, eye strain when looking at a near target, blurred vision and diplopia (Dusek et al., 2010). The differences in basic visual functions, including ocular deviation, accommodation and binocularity, between our study and a previous study (Dusek et al., 2010), could be due to the different methodology, exclusion criteria (our study excluded children with learning disabilities) or language systems (alphabetic versus Orthographic). Nevertheless, the poorer basic visual functions and increased likelihood of visual discomfort found in subjects with HWD indicated for optometric intervention. 4.2.2. Visual perceptual skills From our results, children with HWD showed impaired performance in 6 out of the 7 subtests of TVPS-R, including visual discrimination, visual spatial relation, visual form constancy, visual sequential memory, visual figure ground and visual closure compared with those without HWD. The difference in the mean TVPS-R subtest score between children with and without HWD was the greatest in visual sequential memory, followed by visual discrimination and visual closure. Similarly, a study on Taiwan children found that slow handwriters showed significantly worse performance in 5 subtests of TVPS, including visual spatial relation, visual memory, visual sequential memory, visual figure ground and visual closure, of which, visual sequential memory was the best predictor of their handwriting speed (Tseng & Chow, 2000). In addition, our results showed that children with HWD showed impaired visual spatial skills as revealed by their significantly more errors made in the Gardner reversal test: recognition subtest. These findings suggested that both visual spatial and visual perceptual skills could be one of the performance components in Chinese handwriting. On the other hand, HWD in alphabetic languages was also reported to relate closely with visual perception, visual closure, visual memory and position in space (Feder & Majnemer, 2007; Volman et al., 2006). However, the various differences in methodology affect direct comparison between studies. Further study with standardized methodology is needed to confirm whether or not the visual perceptual deficits reported have any language specific pattern.
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Although children with HWD showed less proficient visual perceptual and visual spatial skills, relation between the two was not clearly understood. Neuroscientific studies demonstrated that the analysis, processing and writing of Chinese characters required both sequential knowledge and spatial feature analysis skills (Kao et al., 2002; Qiu & Zhou, 2010). The recognition of Chinese characters was found more dependent on visual-spatial processing than the recognition of English word (Sun et al., 2011; Wu et al., 2012). Poor visual sequential memory can affect sequential knowledge buildup. Some authors suggested that the demand on various visual perceptual skills, particularly spatial features analysis, in the writing of Chinese was due to the inherent orthographic nature of Chinese characters (Kao et al., 2002). However, statistical correlation analysis regarding the relationship between handwriting and visual perceptual skills were inconsistent (Tseng & Cermak, 1993; Tseng & Chow, 2000; Volman et al., 2006). Visual perceptual skills could be one of the performance components of handwriting, but correlation does not necessarily mean causation (Feder & Majnemer, 2007; Tseng & Chow, 2000). Further research is indicated to examine the actual relationship. 4.2.3. Motor skills VMI tests evaluate a child’s ability to integrate visual perception and motor control, whereas Detroit test of motor speed and accuracy evaluates predominantly a child’s fine motor skills. Our subjects with HWD showed weakness in visual motor integration. This finding agreed well with previous studies (Daly, Kelley, & Krauss, 2003; Tseng & Chow, 2000; Volman et al., 2006). In addition, visual motor integration was found closely associated with both handwriting legibility and speed (Daly et al., 2003; Tseng & Chow, 2000; Volman et al., 2006). However, unlike previous studies in which children with HWD showed problem in fine motor control (Tseng & Chow, 2000; Volman et al., 2006), subjects with HWD in present study showed relatively normal fine motor skills. Several studies suggested different mechanisms underlying the quality and speed of handwriting in children with and without HWD. The handwriting mechanism in children with HWD was more dependent on visual motor integration, while that in normal children was more dependent on fine motor control (Tseng & Chow, 2000; Volman et al., 2006). The suggestion of a more visual dependent mechanism in children with HWD may somehow explain our opposing findings in visual motor integration and fine motor skills. From our results in DEM, children with HWD showed significantly lower score in the vertical test, horizontal test and error score, while no significant difference were found in the ratio score. According to the examiner booklet of DEM (Richman & Garzia, 1987), the vertical test involves less pursuit and saccadic eye movement, which is more a measure of one’s ability in visualizing, recognizing and verbalizing visually presented materials. The horizontal test involves more pursuit and saccadic eye movement, which is a measure of one’s ability in visualizing, recognizing and verbalizing visually presented materials as well as eye movement skills. The horizontal to vertical ratio score is invented to show rather the subject performance is affected more by his or her ability in visualizing, recognizing and verbalizing visually presented materials or by eye movement skills. Based on our results, we can speculate that children with HWD may have slower reading speed. Besides, the slower reading speed in children with HWD may be affected more by the deficiency in visualizing, recognizing and verbalizing visually presented materials, but affected to a lesser extent by the deficiency in pursuit and saccadic eye movement. This speculation was supported by another study, which found that children with HWD showed slower reading speed and larger number of errors compared with controls (Dusek et al., 2010). 4.3. Coexisting problems in visual functions and handwriting Both previous studies (Dusek et al., 2010; Tseng & Chow, 2000; Volman et al., 2006) and our findings showed that children with HWD had coexisting problems in a number of visual functions. Some individual visual functions associated strongly with handwriting performance (Tseng & Chow, 2000; Volman et al., 2006). However, the exact relationship was not clearly understood. Brain imaging study found that learning of Chinese handwriting involved multiple interacting neural regions, which included a visual component (dorsal and ventral visual streams) and a motor component (basal ganglia and cerebellum) (Swett et al., 2010). The dorsal stream provides information on spatial location and movement while ventral stream provides information on physical properties, shape, size and color (Donkelaar & Brabec, 2011). They were important for the cortical processing and internal mapping of the movement sequences during handwriting (Swett et al., 2010). The basal ganglia are important for posture and movement control and the automatic execution of learned motor plans while cerebellum is important in the modulation of motor activity originating from other brain centers and regulation of equilibrium (Kimura, 1993). The basal ganglia and cerebellum network together helped in the encoding and refining stages as handwriting performance improved (Swett et al., 2010). Learning to write involves this complex neural interaction. Problems at a particular point along this neurological processing may lead to poor visual motor skill and handwriting performance. Some anatomical and functional imaging studies attributed the coexisting difficulties in reading and writing to the deficit in cerebellum function (Mather, 2003; Nicolson & Fawcett, 2011; Rapcsak et al., 2009). On the other hand, a recent research suggested that organization ability (one of the components of executive functions) constitutes a major underlying mechanism for handwriting performance (Rosenblum, Aloni, & Josman, 2010). Intact organization in space and time is important for the simultaneous activation of both sensory-motor and cognitive skills necessary for handwriting. Children
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with dysgraphia showed poor performance in both handwriting and organization skills with moderate correlation (Rosenblum et al., 2010). The deficient organization ability was reflected as extensive problems in other daily functioning as well as learning (Rosenblum et al., 2010). Children with learning disabilities showed significantly poorer executive function (Mattison & Mayes, 2012) as well as visual processing deficits (Kevan & Pammer, 2008, 2009; Nandkumar & Leat, 2008; Vidyasagar & Pammer, 2010). Therefore, whether the coexisting vision and handwriting problems are causally related to each other or they are the result of a common underlying deficit require further investigation. 4.4. Limitation It should be noted that children with HWD were reported to have poorer sustained attention (Rosenblum et al., 2010; Tseng & Chow, 2000). In our study, subject exclusion was based on self-report of previous diagnosis. Therefore, one limitation of the current study is that we cannot eliminate the possibility where undiagnosed attention problem of children with HWD during visual assessment, particularly those requires long administration time, may obscure their true performance. Besides, the mean age of HWD group was older than that of control group. Since motor and vision functions could improve with age (Feder & Majnemer, 2007; Scheiman & Wick, 2002; Schneck & Henderson, 1990), direct comparison may mask the true differences between groups. Therefore, age adjustment was made in statistical analysis. 5. Conclusion Children with HWD not only showed problem in visual motor integration, but also showed deficient binocularity, accommodation and visual perceptual ability. Based on their visual profile, we would suggest further study to investigate the effect of optometric interventions in the assessment and remediation for children with HWD. Notifications of ethical adherence All research procedures adhered to the tenets of the Declaration of Helsinki and were approved by the Ethics Committee of the Hong Kong Polytechnic University. Conflicts of interest None. Acknowledgement This study was supported by grants from the PolyU Central Research Grant (Account no. G-YF14 G-YF92). References Bonney, M.-A. (1992). Understanding and assessing handwriting difficulty: Perspectives from the literature. Australian Occupational Therapy Journal, 39, 7–15. Daly, C. J., Kelley, G. T., & Krauss, A. (2003). Relationship between visual-motor integration and handwriting skills of children in kindergarten: A modified replication study. American Journal of Occupational Therapy, 57, 459–462. Donkelaar, T. H. J., & Brabec, J. i. (2011). Clinical neuroanatomy brain circuitry and its disorders:. Springer. Dusek, W., Pierscionek, B. K., & McClelland, J. F. (2010). 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American Journal of Occupational Therapy, 58, 185–192. Kao, H. S. R., Leong, C. K., & Gao, D.-G. (2002). Cognitive neuroscience studies of the Chinese language. Hong Kong: Hong Kong University Press. Karlsdottir, R., & Stefansson, T. (2002). Problems in developing functional handwriting. Perceptual and Motor Skills, 94, 623–662. Kevan, A., & Pammer, K. (2008). Visual deficits in pre-readers at familiar risk for dyslexia. Vision Research, 48, 2835–2839. Kevan, A., & Pammer, K. (2009). Predicting early reading skills from pre-reading measures of dorsal stream functioning. Neuropsychologia, 47, 3174–3181. Kimura, D. (1993). Neuromotor mechanisms in human communication:. Oxford University Press. Maeland, A. F. (1992). Handwriting and perceptual-motor skills in clumsy, dysgraphic and ‘normal’ children. Perceptual and Motor Skills, 72, 1207–1217. Markham, L. R. (1976). Influences of handwriting quality on teacher evaluation of written work. American Educational Research Journal, 13, 277–283. Marr, D., Cermak, S., Cohn, E. S., & Henderson, A. (2003). Fine motor activities in head start and kindergarten classrooms. American Journal of Occupational Therapy, 57, 550–557. Mather, D. S. (2003). Dyslexia and dysgraphia: More than written language difficulties in common. Journal of Learning Disabilities, 36, 307–317. Mattison, R. E., & Mayes, S. D. (2012). Relationships between learning disability, executive function, and psychopathology in children with ADHD. Journal of Attention Disorder, 16, 138–146. McBride-Chang, C., Chung, K. K. H., & Tong, X. (2011). Copying skills in relation to word reading and writing in Chinese children with and without dyslexia. Journal of Experimental Child Psychology, 110, 422–433. McHale, K., & Cermak, S. A. (1992). Fine motor activities in elementary school: Preliminary findings and provisional implications for children with fine motor problems. 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Mills, M. D. (1999). The eye in childhood. American Family Physician, 60, 907–916. Nandkumar, K., & Leat, S. J. (2008). Dyslexia: A review of two theories. Clinical and Experimental Optometry, 91, 333–340. Nicolson, R. I., & Fawcett, A. J. (2011). Dyslexia, dysgraphia, procedural learning and the cerebellum. Cortex, 47, 117–127. Qiu, Y., & Zhou, X. (2010). Perceiving the writing sequence of Chinese characters: An ERP investigation. NeuroImage, 50, 782–795. Rapcsak, S. Z., Beeson, P. M., Henry, M. L., Leyden, A., Kim, E., Rising, K., et al. (2009). Phonological dyslexia and dysgraphia: Cognitive mechanisms and neural substrates. Cortex, 45, 575–591. Reisman, J. E. (1993). Development and reliability of research version of the Minnesota handwriting test. Physical and Occupational Therapy in Pediatrics, 13, 41–55. Richman, J. E., & Garzia, R. P. (1987). Developmental eye movement test (DEM) examiner’s booklet. Rosenblum, S., Aloni, T., & Josman, N. (2010). Relationships between handwriting performance and organizational abilities among children with and without dysgraphia: A preliminary study. Research in Developmental Disabilities, 31, 502–509. Rosenblum, S., Weiss, P. L., & Parush, S. (2003). Product and process evaluation of handwriting difficulties: A review. Educational Psychology Review, 15, 41–81. Scheiman, M., & Wick, B. (2002). Clinical management of binocular vision: Heterophoric accommodative and eye movement disorders (2nd ed.). Lippincott Williams & Wilkins. Schneck, C. M., & Henderson, A. (1990). Descriptive analysis of the developmental progression of grip position for pencil and crayon control in nondysfunctional children. American Journal of Occupational Therapy, 44, 893–900. Smyth, M. M., & Silvers, G. (1987). Functions of vision in the control of handwriting. Acta Psychologica, 65, 47–64. Sun, Y., Yang, Y., Desroches, A. S., Liu, L., & Peng, D. (2011). The role of the ventral and dorsal pathways in reading Chinese characters and english words. Brain & Language, 119, 80–88. Swett, B. A., Contreras-Vidal, J. L., Birn, R., & Braun, A. (2010). Neural substrates of graphomotor sequence learning: A combined fMRI and kinematic study. Journal of Neurophysiology, 103, 3366–3377. Tam, H. Y. T. (2008). A validation study on handwriting ability checklist (HAC). The Hong Kong Polytechnic University: Hong Kong. Tseng, M. H., & Cermak, S. A. (1993). The influence of ergonomic factors and perceptual-motor abilities on handwriting performance. American Journal of Occupational Therapy, 47, 919–926. Tseng, M. H., & Chow, S. M. K. (2000). Perceptual-motor function of school-age children with slow handwriting speed. American Journal of Occupational Therapy, 54, 83–88. Van Doorn, R. R. A., & Keuss, P. J. G. (1992). The role of vision in the temporal and spatial control of handwriting. Acta Psychologica, 81, 269–286. Van Doorn, R. R. A., & Keuss, P. J. G. (1993). Does the production of letter strokes in handwriting benefit from vision? Acta Psychologica, 82, 275–290. Vidyasagar, T. R., & Pammer, K. (2010). Dyslexia: A deficit in visuo-spatial attention, not in phonological processing. Trends in Cognitive Sciences, 14, 57–63. Volman, M. J. M., Schendel, B. M. V., & Jongmans, M. J. (2006). Handwriting difficulties in primary school children: A search for underlying mechanisms. American Journal of Occupational Therapy, 60, 451–460. Wu, C.-Y., Ho, M.-H.R., & Chen, S.-H.A. (2012). A meta-analysis of fMRI studies on Chinese orthogrpahic, phonological and semantic processing. NeuroImage, 63, 381–391.
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Visual profile of children with handwriting difficulties in Hong Kong Chinese Mabel M.P. Leung a,*, Carly S.Y. Lam a, Sutie S.T. Lam b, Natalie W.Y. Pao b, Cecilia W.P. Li-Tsang b a b
School of Optometry, The Hong Kong Polytechnic University, Hung Hom, Hong Kong, China Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Hong Kong, China
A R T I C L E I N F O
A B S T R A C T
Article history: Received 5 June 2013 Received in revised form 7 October 2013 Accepted 8 October 2013 Available online 29 October 2013
The purpose of this study was to find out the visual profiles of children with handwriting difficulties (HWD) in Hong Kong Chinese. Forty-nine children with HWD (mean age 8.4 1.1 years) and 27 controls (mean age 7.7 0.7 years) were recruited. All subjects received eye examination and vision assessment included ocular health, refraction, accommodative functions, binocularity, visual perception (by Gardner reversal frequency test: recognition subtest; Test of visual perceptual skills (non-motor)-revised) and motor skills (by The BeeryBuktenica developmental test of visual motor integration; Detroit test of motor speed and precision). Higher percentages of tropia and phoria (of magnitude >6 prism dioptres) were found in children with HWD of 6.1% and 14.3% respectively. After adjusted for the effect of age, children with HWD showed significantly worse accommodative facility, directionality, visual discrimination, visual spatial relation, visual form constancy, visual sequential memory, visual figure ground, visual closure and visual motor integration. Studies reported the visual functions of children with HWD were mostly concerned with alphabetic languages, while studies concerning Chinese HWD were relatively less. This study provided the visual profiles of children with Chinese HWD. Based on the visual profile, further study is indicated to investigate the effect of optometric interventions on the assessment and remediation for children with HWD. ß 2013 Elsevier Ltd. All rights reserved.
Keywords: Visual function Handwriting difficulties Chinese
1. Introduction Handwriting is an important medium for expressing, communicating and recording ideas (Erhardt & Meade, 2005; Reisman, 1993). For school-aged children, good handwriting skill is a prerequisite of learning. Children from kindergartens and primary schools spend 30 to 60% of their school time on fine motor activities, predominately on writing (Marr, Cermak, Cohn, & Henderson, 2003; McHale & Cermak, 1992). It was reported that 10–27% children showed handwriting problems of various degrees (Hammerschmidt & Sudsawad, 2004; Karlsdottir & Stefansson, 2002; Maeland, 1992). Children who are slow in handwriting may have difficulty to cope with the volume of school work and to finish within time constraint. Impaired handwriting can affect children’s academic performance as well as psychological well-being (Bonney, 1992; Erhardt & Meade, 2005; Feder & Majnemer, 2007; Graham & Weintraub, 1996; Hammerschmidt & Sudsawad, 2004; Markham, 1976; Rosenblum, Weiss, & Parush, 2003). Poor handwriting not only frustrated children’s learning, but also influenced teacher’s evaluation of written work (Karlsdottir & Stefansson, 2002; Markham, 1976). Papers with poor handwriting were
* Corresponding author. Tel.: +852 27665225. E-mail addresses: [email protected] (Mabel M.P. Leung), [email protected] (Carly S.Y. Lam), [email protected] (Sutie S.T. Lam), [email protected] (Natalie W.Y. Pao), [email protected] (Cecilia W.P. Li-Tsang). 0891-4222/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ridd.2013.10.013
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consistently marked lower regardless of the contents (Markham, 1976). Illegible handwriting further hindered the accomplishment of higher-orders skills including spelling or story composition (Feder & Majnemer, 2007). In a word reading task, children with HWD showed slower reading speed and larger number of errors compared with controls (Dusek, Pierscionek, & McClelland, 2010). In addition, character copying skills were found related to the development of Chinese literacy skills (McBride-Chang, Chung, & Tong, 2011). Since good handwriting skill is so important for children, early and appropriate intervention is highly indicated. Investigation on the visual profiles of children with HWD, which may aid in the design of appropriate assessment tools and remediation programs, is of particular interest. 1.1. Relationship between handwriting and vision Handwriting is not a simple fine motor task. It involves complex visual perceptual-motor integration. Good Handwriting requires the integration among visual perception, motor planning, cognitive, tactile and kinesthetic functions, gross and fine motor skills, as well as sustained attention (Bonney, 1992; Erhardt & Meade, 2005; Feder & Majnemer, 2007; Maeland, 1992; Reisman, 1993; Rosenblum et al., 2003). Various evidences suggested for the important role of vision in handwriting (Daly, Kelley, & Krauss, 2003; Smyth & Silvers, 1987; Tseng & Chow, 2000; Van Doorn & Keuss, 1992, 1993). The absence of vision during handwriting affected the spatial orientation of written words and caused an increase in errors produced, increase in stroke size and decrease in writing speed (Smyth & Silvers, 1987; Van Doorn & Keuss, 1992, 1993). Further support can be obtained from brain imaging study in which both dorsal and ventral visual streams were found involved at the initial learning stage of Chinese handwriting (Swett, Contreras-Vidal, Birn, & Braun, 2010). Although vision and handwriting are closely related functions, limited studies reported the visual functions of children with HWD. Children with problem in handwriting showed weakness in visual memory, visual sequential memory, visual spatial relation, form constancy, figure ground and visual motor integration (Markham, 1976; Tseng & Chow, 2000; Volman, Schendel, & Jongmans, 2006). However, information about the binocular vision and accommodative functions of children with HWD were scarce. Only one study reported the increased binocular vision and accommodation anomalies including exophoria, convergence insufficiency, accommodation insufficiency and lower accommodative convergence in children with both handwriting and reading difficulties (Dusek et al., 2010). 1.2. Language difference Unlike alphabetic scripts that compose left-to-right languages, Chinese characters are characterized by the spatial organization of strokes making visual-spatial perception important for the orthographic processing and writing of Chinese characters (Kao, Leong, & Gao, 2002). Neuroimaging evidences suggested different neural networks involved in the processing of Chinese characters and alphabetic languages (Sun, Yang, Desroches, Liu, & Peng, 2011; Wu, Ho, & Chen, 2012). Therefore, the complex orthography of Chinese characters as opposed to the phonologic alphabetic languages may lead to differences in visual motor demand. 1.3. Aim of study Vision is an integral part of handwriting. The visual motor demand in handwriting may vary between languages. However, little studies reported the deficient visual functions in children with HWD and mostly were in alphabetic languages (Dusek et al., 2010; Markham, 1976; Volman et al., 2006). Investigation on the visual profiles of Chinese children with HWD may help to identify some possible handwriting performance components, which in turn, aid in the design of appropriate assessment tools and remediation programs (Feder & Majnemer, 2007). This study aimed to find out the visual profiles, from basic visual functions to higher order visual perceptual and visual motor integration skills, of children with HWD particularly in Chinese. 2. Methodology 2.1. Subjects recruitment Seventy-six children, 49 with HWD and 27 controls, were recruited from different Hong Kong mainstream primary schools. All recruited subjects were studying primary 1 or 2 and using Chinese and Cantonese as their primary written and spoken language. By using a validated handwriting ability checklist (Tam, 2008), children were rated by their parents in the aspect of handwriting legibility, speed, physical and emotional responses. Completed checklists were assessed and compared against the suggested cut-off scores (Tam, 2008). Subjects scored 31 or above were classified as HWD and were recruited into the group with HWD, whilst subjects scored 30 or below were recruited into the control group. Children with physical impairments, learning disabilities, attention and behavior problems, neuromuscular disabilities and/or history of any previous intervention on handwriting were excluded from the study. All research procedures adhered to the tenets of the Declaration of Helsinki and were approved by the Ethics Committee of The Hong Kong Polytechnic University. The parents of the children were fully informed and written consent was obtained before all experimental measurements.
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2.2. Visual functions assessment All subjects received eye examination and vision function assessments, including ocular health assessment (biomicroscopy and direct ophthalmoscopy), subjective refraction, accommodative functions (accommodative amplitude by push-up method binocularly and accommodative facility by a lens flipper of 2.00D binocularly) and binocularity (heterophoria by cover test and prism neutralization, convergence by near point of convergence method, fusional vergence by step vergence method, vergence facility by facility prism of 3 prism dioptre base-in/12 prism dioptre base-out and stereoacuity by Randot stereotest). The instructions and procedures for each test on accommodative functions and binocularity were adopted from Scheiman and Wick (Scheiman & Wick, 2002). The patient then received various visual perceptual and motor skills assessments including Gardner reversal frequency test: recognition subtest; The seven subtests of Test of visual perceptual skills (non-motor)-revised (TVPS-R): visual discrimination, visual memory, visual spatial-relationship, visual form-constancy, visual sequential-memory, visual figureground and visual closure; The Beery-Buktenica developmental test of visual motor integration (VMI); Developmental eye movement test (DEM) and Detroit test of motor speed and precision. The procedures and instructions for all assessments were straight away followed according to the examiner’s manuals. 2.3. Data analysis IBM SPSS 16 (SPSS inc., Chicago USA) was used for data analysis. After checking for normality using Shapiro–Wilk test, normal distribution of data in both groups was found in part of the data (Vergence facility, accommodative facility, visual memory, visual closure, VMI, vertical time in DEM and Detroit test of motor speed and precision). The mean age of HWD group was older than that of the control group. Since increase in age could improve motor and most vision functions (Feder & Majnemer, 2007; Scheiman & Wick, 2002; Schneck & Henderson, 1990), the age difference between groups may influence results analysis. To adjust for the effect of age, ANCOVA (with age as a covariate) was used to compare the difference in all visual functions (except ocular deviation) between the HWD and control groups. As stable ocular alignment is expected by the age of 3 months (Mills, 1999), ocular alignment should be independent on age in the studied age group of 7 to 8 years old. One-way ANOVA was used to compare the difference in magnitude of ocular deviation between the HWD and control groups. Chi-square Cramer’s V test was used to analysis the relationship between the direction of ocular deviation and grouping. 3. Results 3.1. Subjects demographic data Table 1 shows the demographic data of the 2 groups of subjects. A total of 76 subjects were recruited. Forty-nine children with HWD of mean age 8.4 1.1 years were recruited into the HWD group. Twenty-seven children without HWD of mean age 7.7 0.7 years were recruited into the control group. There were 67% and 52% males in the HWD and control group respectively. 3.2. Refractive error The refractive error measured by subjective refraction was converted into a spherical equivalent value (Spherical equivalent = Spherical error + Cylindrical error/2) for statistical analysis. The spherical equivalent of the refractive error in the right and left eyes were shown in Table 2. Statistical analysis showed no significant differences in the mean spherical equivalent between the control and HWD groups in both the right and left eye. 3.3. Binocularity and accommodation The percentages of children with tropia were 6.1% and 0% in the HWD and control group respectively. The percentages of children with major phoria (of magnitude greater than 6 prism dioptres) were 14.3% and 7.4% in the HWD and control group respectively. The mean ocular deviation magnitude of HWD group was 1.5 3.7 and 3.9 4.8 prism dioptres at distance and near respectively, while that of control group was 0.5 1.5 and 2.3 3.3 prism dioptres at distance and near respectively. There was no statistically significant difference between the two groups in the magnitude of ocular deviation at both distance (One-Way
Table 1 Demographic data of HWD and controls groups.
Number (n) Mean Age + SD (years) Age range (years) Gender
Control
HWD
27 8.4 + 1.1 6.3 to 9.1 14 Males; 13 Females
49 7.7 + 0.7 6.7 to 10.9 33 Males; 16 Females
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Table 2 Comparison of spherical equivalent of refractive errors between HWD and control groups.
Number (n) Mean + SD
Left eye Right eye
Range
Right eye Left eye
Control
HWD
27
49
0.11 + 1.06 0.16 + 1.14 +1.50 to +1.50 to
3.00 3.63
Statistical calculation (one-way ANOVA)
0.28 + 1.48 0.37 + 1.40 +2.50 to +1.50 to
NO F = 0.29; p = 0.59
5.00 5.00
NO F = 0.44; p = 0.51
ANOVA: F = 1.63, p = 0.21) and near (One-Way ANOVA: F = 2.34, p = 0.13). Statistical calculation also showed no significant difference in the direction of ocular deviation between the two groups at both distance (Cramer’s V = 0.105, p = 0.41) and at near (Cramer’s V = 0.19, p = 0.24). Figs. 1 and 2 shows the percentage of orthophoria, exophoria and esophoria at distance and near respectively in both groups of subjects. After adjusted for the effect of age, no statistically significant difference was found between the two groups in the near point of convergence (ANCOVA: F = 0.05, p = 0.83) and vergence facility (ANCOVA: F = 0.00; p = 0.99). For fusional vergence, all three values of blur, break and recovery points were measured during the study. However, since some of the patients were unable to report the blur point, the recovery point was used instead for statistical calculation. There was also no statistically significant difference in the fusional vergence values between the two groups at both distance and near. The statistical calculation results were summarized in Table 3. According to Sheard’s criterion, the fusional vergence should be at least twice that of the demand for comfortable binocular vision (Scheiman & Wick, 2002). We analyzed the subject’s binocular vision status by checking their tropia or 100
Percentage of subjects (%)
90
HWD
80
Control
70 60 50 40 30 20 10 0
ORTHO
EXO
ESO
Fig. 1. Direction of ocular deviation at distance for both groups. Histogram shows the percentage of orthophoria (ORTHO), exophoria (EXO) and esophoria (ESO) for both HWD and control group when fixating at distance.
100
Percentage of subjects (%)
90
HWD
80
Control
70 60 50 40 30 20 10 0
ORTHO
EXO
ESO
Fig. 2. Direction of ocular deviation at near for both groups. Histogram shows the percentage of orthophoria (ORTHO), exophoria (EXO) and esophoria (ESO) for both HWD and control group when fixating at near.
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Table 3 Comparison of binocularity and accommodative skills between HWD and control groups.
Near point of convergence (cm) Fusional vergence (DD) Distant positive fusional vergence Distant negative fusional vergence Near positive fusional vergence Near negative fusional vergence
Control
HWD
Statistical calculation
(Mean + SD)
(Mean + SD)
ANCOVA (adjusted for age)
5.3 + 1.0
5.3 + 1.3
12.7 + 8.1 7.2 + 3.2 22.1 + 7.6 11.4 + 5.1
13.1 + 8.4 6.2 + 3.0 26.4 + 11.1 10.0 + 3.6
F = 0.05, p = 0.83
F = 2.84, F = 0.02, F = 0.68, F = 2.99,
p = 0.10 p = 0.90 p = 0.41 p = 0.09
Vergence facility (cycles/min.) 3 DD Base In/12 DD Base Out
9.3 + 5.9
9.4 + 5.1
F = 0.00, p = 0.99
Amplitude of accommodation
16.2 + 1.8
15.9 + 2.4
F = 0.12, p = 0.73
7.2 + 2.9
5.2 + 3.4
F = 5.98, p = 0.02
Accommodation facility (cycles/min.)
The bold in the first left column is to separate main categories from sub-categories. The bold in the right column (statistical calculation) is for indicating statistically significant difference.
phoria magnitude against their fusional vergence values. Among those subjects with tropia or phoria, 40.7% of the children with HWD and 27.3% of the controls failed to fulfill the Sheard’s criterion. From our results, children with HWD showed deficient accommodative function. The mean amplitude of accommodation of HWD children was 15.9 2.4 Dioptres which is lower than that of the controls with mean amplitude of accommodation of 16.2 1.8 Dioptres. However, the difference was not statistically significant (ANCOVA: F = 0.12, p = 0.73). The mean accommodation facility of children with and without HWD was 5.2 3.4 and 7.2 2.9 cycles/min respectively. After adjusted for the effect of age, the accommodation facility of HWD children was significantly worse than the controls (ANCOVA: F = 4.09, p < 0.05). 3.4. Visual perceptual skills Table 4 shows the comparison of various visual perceptual skills between children with HWD and the controls. Children with HWD made significantly more errors in the Gardner reversal frequency test: recognition subtest (ANCOVA: F = 4.07, p = 0.047). After adjusted for the effect of age, children with HWD showed consistently poorer performance in visual discrimination (ANCOVA: F = 9.28, p = 0.003), visual spatial relation (ANCOVA: F = 4.29, p = 0.04), visual form constancy (ANCOVA: F = 5.60, p = 0.02), visual sequential memory (ANCOVA: F = 7.95, p = 0.006), visual figure ground (ANCOVA: F = 6.84, p = 0.01), visual closure (ANCOVA: F = 5.20, p = 0.03). Table 4 Comparison of visual perceptual and motor skills between HWD and control groups. Control
HWD
Statistical Calculation
(Mean + SD)
(Mean + SD)
ANCOVA (adjusted for age)a
Gardner reversal frequency test: Recognition subtest
5.2 + 6.3
6.9 + 6.0
F = 4.07, p = 0.047
TVPR-Rb Subtests Visual discrimination Visual memory Visual spatial relations Visual form constancy Visual sequential memory Visual figure ground Visual closure
13. 4 + 1.4 12.4 + 2.0 14.1 + 1.8 11.2 + 1.9 12.3 + 2.1 11.3 + 2.5 9.9 + 3.3
12.3 + 2.6 12.0 + 2.1 13.4 + 2.4 10.2 + 2.8 11.1 + 2.9 10.5 + 3.4 9.0 + 3.6
F = 9.28, F = 3.42, F = 4.29, F = 5.60, F = 7.95, F = 6.84, F = 5.20,
VMIc
18.7 + 3.4
18.0 + 2.5
F = 6.06, p = 0.02
Detroit test of motor speed and precision
75.9 + 17.2
78.6 + 23.3
F = 1.82, p = 0.18
50.0 + 12.5 68.6 + 17.0 4.4 + 6.5 1.4 + 0.2
56.1 + 15.9 79.5 + 35.1 6.3 + 7.7 1.4 + 0.4
F = 12.57, p = 0.001 F = 10.33, p = 0.002 F = 5.50, p = 0.02 F = 1.31, p = 0.26
p = 0.003 p = 0.07 p = 0.04 p = 0.02 p = 0.01 p = 0.01 p = 0.03
d
DEM Vertical time Horizontal time Error score Horizontal ratio a b c d
Statistically significant difference were bolded. Test of visual perceptual skills (non-motor)-revised. The Beery-Buktenia developmental test of visual motor integration: Beery. Developmental eye movement test.
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3.5. Motor skills Children with HWD showed significantly worse performance in VMI (ANCOVA: F = 4.29, p = 0.04). In DEM test, statistically significant difference was found in vertical time (ANCOVA: F = 12.57, p = 0.001), horizontal time (ANCOVA: F = 10.33, p = 0.002) and error score (ANCOVA: F = 5.50, p = 0.02), while no significant difference was found in vertical to horizontal ratio (ANCOVA: F = 1.31, p = 0.26). No significant difference was found in Detroit test of motor speed and precision results between children with or without HWD (ANCOVA: F = 1.82, p = 0.18). 4. Discussion 4.1. Gender bias From our study, more males than females were found in the group with HWD. There was 76% of male in the HWD group and 52% in the control group. Similar gender bias, with 64% in the referred group and 59% in the control group, was reported in a study involving children with reading and handwriting difficulties (Dusek et al., 2010). Besides, males also showed comparatively lower handwriting speed and poorer legibility than females (Feder et al., 2005; Karlsdottir & Stefansson, 2002; Rosenblum et al., 2003). 4.2. Visual functions of children with HWD Our results showed that children with HWD showed weakness in binocularity, accommodative facility, higher order visual perceptual skills and visual motor integration. 4.2.1. Binocularity and accommodation Compared with the controls, the HWD group showed a higher percentage of tropia or significant phoria (magnitude >6 prism dioptres). In the HWD group, percentages of children with tropia and significant phoria were 6.1% and 14.3% respectively, which is much higher than that in the control group. No significant difference in the fusional vergence values between the two groups were found, however the percentage of children who failed to reach the Sheard’s criterion was higher in the HWD group (40.7%) than in the control group (27.3%). According to the Sheard’s criterion, if the fusional vergence is lower than twice that of the demand, it is more likely to have discomfort related to binocular vision (Scheiman & Wick, 2002). Our findings suggested that children with HWD were more likely to have discomfort in binocular vision due to the higher percentage of tropia, phoria and limited fusional vergence that failed to cope with the demand (ocular deviation). In addition, children with HWD showed significantly reduced accommodative facility, while the amplitude of accommodation, convergence and vergence facility were all relatively normal. The higher percentage of ocular deviation in children with HWD was not reported elsewhere before. In addition to the reduced accommodative facility, previous study reported that children with reading and writing difficulties showed reduction in amplitude of accommodation, vergence facility, convergence insufficiency and lower accommodative convergence to accommodation ratio (Dusek et al., 2010). Besides, children with reading and writing difficulties were more likely to report visual related complaints, included burning or stinging eyes, tiredness after reading, eye strain when looking at a near target, blurred vision and diplopia (Dusek et al., 2010). The differences in basic visual functions, including ocular deviation, accommodation and binocularity, between our study and a previous study (Dusek et al., 2010), could be due to the different methodology, exclusion criteria (our study excluded children with learning disabilities) or language systems (alphabetic versus Orthographic). Nevertheless, the poorer basic visual functions and increased likelihood of visual discomfort found in subjects with HWD indicated for optometric intervention. 4.2.2. Visual perceptual skills From our results, children with HWD showed impaired performance in 6 out of the 7 subtests of TVPS-R, including visual discrimination, visual spatial relation, visual form constancy, visual sequential memory, visual figure ground and visual closure compared with those without HWD. The difference in the mean TVPS-R subtest score between children with and without HWD was the greatest in visual sequential memory, followed by visual discrimination and visual closure. Similarly, a study on Taiwan children found that slow handwriters showed significantly worse performance in 5 subtests of TVPS, including visual spatial relation, visual memory, visual sequential memory, visual figure ground and visual closure, of which, visual sequential memory was the best predictor of their handwriting speed (Tseng & Chow, 2000). In addition, our results showed that children with HWD showed impaired visual spatial skills as revealed by their significantly more errors made in the Gardner reversal test: recognition subtest. These findings suggested that both visual spatial and visual perceptual skills could be one of the performance components in Chinese handwriting. On the other hand, HWD in alphabetic languages was also reported to relate closely with visual perception, visual closure, visual memory and position in space (Feder & Majnemer, 2007; Volman et al., 2006). However, the various differences in methodology affect direct comparison between studies. Further study with standardized methodology is needed to confirm whether or not the visual perceptual deficits reported have any language specific pattern.
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Although children with HWD showed less proficient visual perceptual and visual spatial skills, relation between the two was not clearly understood. Neuroscientific studies demonstrated that the analysis, processing and writing of Chinese characters required both sequential knowledge and spatial feature analysis skills (Kao et al., 2002; Qiu & Zhou, 2010). The recognition of Chinese characters was found more dependent on visual-spatial processing than the recognition of English word (Sun et al., 2011; Wu et al., 2012). Poor visual sequential memory can affect sequential knowledge buildup. Some authors suggested that the demand on various visual perceptual skills, particularly spatial features analysis, in the writing of Chinese was due to the inherent orthographic nature of Chinese characters (Kao et al., 2002). However, statistical correlation analysis regarding the relationship between handwriting and visual perceptual skills were inconsistent (Tseng & Cermak, 1993; Tseng & Chow, 2000; Volman et al., 2006). Visual perceptual skills could be one of the performance components of handwriting, but correlation does not necessarily mean causation (Feder & Majnemer, 2007; Tseng & Chow, 2000). Further research is indicated to examine the actual relationship. 4.2.3. Motor skills VMI tests evaluate a child’s ability to integrate visual perception and motor control, whereas Detroit test of motor speed and accuracy evaluates predominantly a child’s fine motor skills. Our subjects with HWD showed weakness in visual motor integration. This finding agreed well with previous studies (Daly, Kelley, & Krauss, 2003; Tseng & Chow, 2000; Volman et al., 2006). In addition, visual motor integration was found closely associated with both handwriting legibility and speed (Daly et al., 2003; Tseng & Chow, 2000; Volman et al., 2006). However, unlike previous studies in which children with HWD showed problem in fine motor control (Tseng & Chow, 2000; Volman et al., 2006), subjects with HWD in present study showed relatively normal fine motor skills. Several studies suggested different mechanisms underlying the quality and speed of handwriting in children with and without HWD. The handwriting mechanism in children with HWD was more dependent on visual motor integration, while that in normal children was more dependent on fine motor control (Tseng & Chow, 2000; Volman et al., 2006). The suggestion of a more visual dependent mechanism in children with HWD may somehow explain our opposing findings in visual motor integration and fine motor skills. From our results in DEM, children with HWD showed significantly lower score in the vertical test, horizontal test and error score, while no significant difference were found in the ratio score. According to the examiner booklet of DEM (Richman & Garzia, 1987), the vertical test involves less pursuit and saccadic eye movement, which is more a measure of one’s ability in visualizing, recognizing and verbalizing visually presented materials. The horizontal test involves more pursuit and saccadic eye movement, which is a measure of one’s ability in visualizing, recognizing and verbalizing visually presented materials as well as eye movement skills. The horizontal to vertical ratio score is invented to show rather the subject performance is affected more by his or her ability in visualizing, recognizing and verbalizing visually presented materials or by eye movement skills. Based on our results, we can speculate that children with HWD may have slower reading speed. Besides, the slower reading speed in children with HWD may be affected more by the deficiency in visualizing, recognizing and verbalizing visually presented materials, but affected to a lesser extent by the deficiency in pursuit and saccadic eye movement. This speculation was supported by another study, which found that children with HWD showed slower reading speed and larger number of errors compared with controls (Dusek et al., 2010). 4.3. Coexisting problems in visual functions and handwriting Both previous studies (Dusek et al., 2010; Tseng & Chow, 2000; Volman et al., 2006) and our findings showed that children with HWD had coexisting problems in a number of visual functions. Some individual visual functions associated strongly with handwriting performance (Tseng & Chow, 2000; Volman et al., 2006). However, the exact relationship was not clearly understood. Brain imaging study found that learning of Chinese handwriting involved multiple interacting neural regions, which included a visual component (dorsal and ventral visual streams) and a motor component (basal ganglia and cerebellum) (Swett et al., 2010). The dorsal stream provides information on spatial location and movement while ventral stream provides information on physical properties, shape, size and color (Donkelaar & Brabec, 2011). They were important for the cortical processing and internal mapping of the movement sequences during handwriting (Swett et al., 2010). The basal ganglia are important for posture and movement control and the automatic execution of learned motor plans while cerebellum is important in the modulation of motor activity originating from other brain centers and regulation of equilibrium (Kimura, 1993). The basal ganglia and cerebellum network together helped in the encoding and refining stages as handwriting performance improved (Swett et al., 2010). Learning to write involves this complex neural interaction. Problems at a particular point along this neurological processing may lead to poor visual motor skill and handwriting performance. Some anatomical and functional imaging studies attributed the coexisting difficulties in reading and writing to the deficit in cerebellum function (Mather, 2003; Nicolson & Fawcett, 2011; Rapcsak et al., 2009). On the other hand, a recent research suggested that organization ability (one of the components of executive functions) constitutes a major underlying mechanism for handwriting performance (Rosenblum, Aloni, & Josman, 2010). Intact organization in space and time is important for the simultaneous activation of both sensory-motor and cognitive skills necessary for handwriting. Children
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with dysgraphia showed poor performance in both handwriting and organization skills with moderate correlation (Rosenblum et al., 2010). The deficient organization ability was reflected as extensive problems in other daily functioning as well as learning (Rosenblum et al., 2010). Children with learning disabilities showed significantly poorer executive function (Mattison & Mayes, 2012) as well as visual processing deficits (Kevan & Pammer, 2008, 2009; Nandkumar & Leat, 2008; Vidyasagar & Pammer, 2010). Therefore, whether the coexisting vision and handwriting problems are causally related to each other or they are the result of a common underlying deficit require further investigation. 4.4. Limitation It should be noted that children with HWD were reported to have poorer sustained attention (Rosenblum et al., 2010; Tseng & Chow, 2000). In our study, subject exclusion was based on self-report of previous diagnosis. Therefore, one limitation of the current study is that we cannot eliminate the possibility where undiagnosed attention problem of children with HWD during visual assessment, particularly those requires long administration time, may obscure their true performance. Besides, the mean age of HWD group was older than that of control group. Since motor and vision functions could improve with age (Feder & Majnemer, 2007; Scheiman & Wick, 2002; Schneck & Henderson, 1990), direct comparison may mask the true differences between groups. Therefore, age adjustment was made in statistical analysis. 5. Conclusion Children with HWD not only showed problem in visual motor integration, but also showed deficient binocularity, accommodation and visual perceptual ability. Based on their visual profile, we would suggest further study to investigate the effect of optometric interventions in the assessment and remediation for children with HWD. Notifications of ethical adherence All research procedures adhered to the tenets of the Declaration of Helsinki and were approved by the Ethics Committee of the Hong Kong Polytechnic University. Conflicts of interest None. Acknowledgement This study was supported by grants from the PolyU Central Research Grant (Account no. G-YF14 G-YF92). References Bonney, M.-A. (1992). Understanding and assessing handwriting difficulty: Perspectives from the literature. Australian Occupational Therapy Journal, 39, 7–15. Daly, C. J., Kelley, G. T., & Krauss, A. (2003). Relationship between visual-motor integration and handwriting skills of children in kindergarten: A modified replication study. American Journal of Occupational Therapy, 57, 459–462. Donkelaar, T. H. J., & Brabec, J. i. (2011). Clinical neuroanatomy brain circuitry and its disorders:. Springer. Dusek, W., Pierscionek, B. K., & McClelland, J. F. (2010). 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