Child Neuropsychology

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The Impact of Periventricular Brain Injury on Reading and Spelling Abilities in the Late Elementary and Adolescent Years

Andrea L. S. Downie a; Virginia Frisk b; Lorna S. Jakobson c a Department of Psychology, Children's Hospital of Western Ontario; London Health Sciences Centre, London, Ontario, Canada b Department of Psychology, The Hospital for Sick Children, Toronto, Ontario, Canada c Department of Psychology, University of Manitoba, Winnipeg, Manitoba, Canada Online Publication Date: 01 December 2005 To cite this Article: Downie, Andrea L. S., Frisk, Virginia and Jakobson, Lorna S. (2005) 'The Impact of Periventricular Brain Injury on Reading and Spelling Abilities in the Late Elementary and Adolescent Years', Child Neuropsychology, 11:6, 479 - 495 To link to this article: DOI: 10.1080/09297040591001085 URL: http://dx.doi.org/10.1080/09297040591001085

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Child Neuropsychology, 11: 479–495, 2005 Copyright © Taylor & Francis Inc. ISSN: 0929-7049 print / 1744-4136 online DOI: 10.1080/09297040591001085

THE IMPACT OF PERIVENTRICULAR BRAIN INJURY ON READING AND SPELLING ABILITIES IN THE LATE ELEMENTARY AND ADOLESCENT YEARS Andrea L. S. Downie,1 Virginia Frisk,2 and Lorna S. Jakobson3 1

Department of Psychology, Children’s Hospital of Western Ontario; London Health Sciences Centre, London, Ontario, Canada, 2Department of Psychology, The Hospital for Sick Children, Toronto, Ontario, Canada, and 3Department of Psychology, University of Manitoba, Winnipeg, Manitoba, Canada The present study was designed: (1) to investigate the long-term consequences of both the presence and the severity of periventricular brain injury (PVBI) on intellectual, academic, and cognitive outcome in extremely-low-birthweight (ELBW: < 1,000 grams) children at a mean age of 11 years; and (2) to determine the nature of the underlying difficulties associated with academic problems in these children. The results indicated that ELBW children without PVBI performed as well as full-term children on intelligence, academic, and cognitive ability tests. In contrast, ELBW children with mild and severe PVBI achieved significantly lower scores than either ELBW children without PVBI or children who were born at term. A second analysis indicated that, after accounting for Full Scale IQ, working memory and phonological processing were significant predictors of reading and spelling performance in ELBW children. These findings suggest that the presence and severity of PVBI, and not ELBW status alone, is associated with performance on tests of intelligence, and academic and cognitive functioning, and that some of the same factors known to be associated with learning disabilities in full-term children contribute to learning disabilities in ELBW children. Keywords: low birth weight, premature, periventricular, outcome, reading disability

INTRODUCTION Within the last three decades significant advances in medical technology have greatly improved obstetric and neonatal care. Despite these improvements, relative to children born at term who were appropriate in size for their gestational age, full-term and preterm children born at low-birthweight (LBW, < 2,500 gm) continue to be at an elevated risk for language disorders and for problems with academic and intellectual functioning that affect, among other things, the acquisition of reading and spelling skills (Aylward, This research was supported by a grant from the Natural Sciences and Engineering Research Council of Canada to L. Jakobson. We are indebted to all of the families who participated in this study. We are grateful to Dr. Hilary Whyte for coding of patient head ultrasound scans, Dr. Kevin Munhall for helpful comments regarding this manuscript, Dr. Warren Eaton for statistical advice, and to Miriam Beauchamp for her help in doublescoring participant files. Address correspondence to Dr. Lorna Jakobson, Department of Psychology, University of Manitoba, Winnipeg, Manitoba, R3T 2N2, Fax: (204) 474-7599. E-mail: [email protected] 479


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2002; Daniel, Lim, & Clarke, 2003; Fletcher et al., 1997; Klebanov, Brooks-Gunn, & McCormick, 1994; Ross, Evelyn, & Auld, 1996; Taylor, Klein, Minich, & Hack, 2000). The fact that a significant number of LBW children repeat a grade by age 8 (approximately 40%) or require special education assistance (between 27% to 38%; Calame et al., 1986; Hall, McLeod, Counsell, Thomson, & Mutch, 1995; Klein, Hack, & Breslau, 1989; Ross, Lipper, & Auld, 1991; Vohr & Coll, 1985) strengthens the conclusion that LBW status has a significant, negative impact on academic and cognitive outcome. It is important to note that a number of factors other than LBW status could affect outcome in this population. For example, many LBW children who were also born prematurely suffer from a particular form of brain injury that occurs in and around the periventricular region (periventricular brain injury, or PVBI). The incidence of PVBI increases with decreasing birthweight (Allen, Donohue, & Dusman, 1993; Volpe, 1995), with children being born at extremely-low-birthweight (ELBW; < 1,000 gm) being at particularly high risk. The two most common forms of PVBI, germinal matrix/ intraventricular hemorrhage (GM/IVH) and hypoxic/ischemic injury (H/I), often destroy glial precursor cells, and this is thought to interfere with early neurodevelopmental processes such as myelination and cortical organization (Evrard, Gressens, & Volpe, 1992; Gressens, Richelme, Kadhim, Gadisseux, & Evrard, 1992; Inder et al., 1999; Maalouf et al.,1999; Van de Bor, Guit, Schreuder, Wondengrem, & Vielroye, 1989). Recent findings suggest that the resultant brain abnormalities persist into adolescence, with individuals who were born very preterm showing significantly smaller brain volumes and enlarged lateral ventricular volumes than full-term controls (Nosarti et al., 2002). Some progress has been made toward understanding the functional significance of PVBI in infants and young children (8 years of age or younger) who were born prematurely. Numerous researchers have reported a link between the presence (Fletcher et al., 1997; Schatz, Craft, Koby, & Park, 1997; Vohr, Coll, Flanagan, & Oh, 1992; WeisglasKuperus, Baerts, Fetter, & Sauer, 1992) and severity (de Vries et al., 1998; Frisk & Whyte, 1994; Peterson et al., 2000, 2003; Skranes et al., 1993) of PVBI and poor performance on tests of language, memory, general cognitive ability, and neurodevelopmental outcome in such children. Studies involving adolescents born very prematurely are less common and, as such, the long-term consequences of PVBI are still not well understood. Some findings suggest remarkable plasticity. Rushe et al. (2001), for example, recently reported that their sample of 14–15-year-old, very premature participants performed normally on tests of attention, memory, perceptual processing, visuomotor skill, and executive function, whether or not they had a history of PVBI. Indeed, the only measure the preterm children in this study were impaired on was word production. This result is surprising given that a number of other investigators have reported a substantially elevated risk of academic and cognitive difficulties in ELBW children during the late elementary and early high school years (Agarwal & Lim, 2003; Saigal, 2000; Saigal, Hoult, Streiner, Stoskopf, & Rosenbaum, 2000; Taylor, Klein, & Hack, 2000). Even when problems in these areas have been documented, however, the impact of PVBI has been difficult to establish. Thus, some investigators have reported no association between conventional markers of perinatal brain injury and learning disabilities, attention deficit, or dyspraxia in adolescence (Abernethy, Palaniappan & Cooke, 2002), while others do find a higher incidence of difficulties in these areas in adolescents with a history of PVBI, compared to those without such a history (Allin et al., 2001; Stewart & Kirkbride, 1996).


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Given the lack of consensus in the extant literature, the first goal of the present study was to assess the impact of the presence and severity of PVBI on the intellectual, academic, and cognitive outcomes of ELBW children in late childhood and early adolescence. To isolate (to the extent possible) effects due to PVBI, we excluded from our sample children born small for gestational age, those with major sensory impairments (blindness, deafness), and those with other forms of neurological insult (meningitis, seizures, shunted hydrocephalus), genetic abnormalities, or major psychiatric illness or developmental disability in a parent. We also had to exclude several children with mental retardation (Full Scale IQ < 70) who were unable to complete all of the tests in the battery. This left a group that was representative of the majority of ELBW survivors who, although frequently scoring within the normal range on tests of intelligence in later childhood (e.g., Forslund & Bjerre, 1990; Ornstein, Ohlsson, Edmonds, & Asztalos, 1991), frequently exhibit “minor” developmental disabilities that nonetheless have a significant impact on functioning in multiple domains (e.g., Aylward, 2002; Ross et al., 1996; Taylor et al., 2000). It is important for researchers and clinicians to understand the bases of these difficulties in order to optimize the design of interventions for this high-risk population. It was hypothesised that ELBW children with PVBI would perform more poorly on tests of reading, spelling, phonological processing, working memory, and intellectual ability than ELBW children who showed no signs of PVBI, or full-term controls. Moreover, the severity of PVBI was expected to be negatively associated with performance in these same domains. Support for a link between PVBI and reading difficulties comes from several recent studies. First, there are a series of studies linking PVBI with altered development of posterior white matter (Back et al., 2001; Goto, Ota, lai, Sugita, & Tanabe, 1994; Peterson et al., 2003). Second, it has been suggested that, in children with developmental dyslexia, white matter disruptions in this region could explain reading impairments if they resulted in a disconnection between anterior and posterior language areas (Paulesu et al., 1996; Temple, 2002). We also sought to assess the impact of specific sociodemographic variables (maternal education level and family income) and cognitive abilities (phonological processing and working memory) on reading and spelling performance in our preterm sample. Our interest in sociodemographics was prompted by the fact that a number of studies involving younger samples of LBW (Hack & Breslau, 1986; Vohr, Coll, & Oh, 1988) or ELBW (Saigal et al., 2000) children have reported that cognitive outcomes are associated with such variables. We expected that this relationship would also hold in early adolescence. Our interest in examining phonological processing and working memory in our preterm sample stemmed from the well-established facts that, in full-term children, these abilities (1) play a crucial role in the early development of reading and spelling skills (e.g., Bradley & Bryant, 1985; Hatcher, Hulme, & Ellis, 1994; Stanovich, Cunningham, & Cramer, 1984; Swanson, 1992, 1994; Wagner & Torgesen, 1987); and (2) continue to be correlated with reading and spelling abilities in the late elementary years (Scarborough, 1998). These findings suggest that the development of fluent reading skills (which play an increasingly important role in determining academic success as one progresses through school) is partly dependent upon the ability to identify the phonological components of words and to store these components in working memory while blending them to form words (Beech, 1997; Swanson, 1994; Wagner & Torgesen, 1987). On this basis, we predicted that the reading and spelling abilities of ELBW children, like full-term children, would be influenced by their phonological processing and working memory abilities.


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METHOD Participants Fifty-four children with a mean age of 11 years, 7 months (range 8 years, 10 months to 14 years, 5 months) participated in this study with informed consent from their parents. Thirty-nine of these children were followed by the Integrated Perinatal Follow-Up Program at The Hospital for Sick Children and at Mount Sinai Hospital, Toronto, Ontario, Canada, for extreme prematurity (M = 26 weeks of gestation, range 23–30 weeks), and extremelylow-birth-weight status (M = 814 gm, range 560–1000 gm). The remaining 15 children were born full-term (M = 40.6 weeks of gestation, range 38–42 weeks) and had normal developmental histories; they were recruited to participate in this study from the community. In both samples, gestational age was based on the mother’s expected due date. Preterm children were recruited from the cohort of ELBW children born between January 1984 and January 1987 (n = 221). To qualify for the study, ELBW children had to meet the following inclusion criteria: (1) appropriate in size for gestational age (birthweight falling within 2 standard deviations of the mean birthweight for gestational age, using the Usher & MacLean, 1969, norms); (2) absence of severe sensory impairment (blindness, deafness) or mental retardation (Full Scale IQ < 70); (3) no history of seizures, meningitis, or ventriculo-peritoneal shunting for posthemorrhagic hydrocephalus; (4) no known genetic abnormality, and no history of major psychiatric or developmental disorder in parent; (5) English-speaking or fluently bilingual, having attended school in English for a minimum of 3 years before testing. Eighty-one children were excluded for one or more of these reasons. Of the remaining group, 43 children were excluded because they did not have the minimum number of cranial ultrasound scans needed to document the presence and severity of PVBI (see below). One more child had died, bringing the potential subject pool to 96 cases. Of these, 57 were lost to follow-up or refused to participate. We verified that this group of eligible, but nonparticipating, children did not differ from our final sample (n = 39) in terms of their cranial ultrasound results. Thus, there were equivalent proportions of children with no history of PVBI, with mild lesions, and with severe lesions in the two groups, χ2 (2) = 1.97, p = .37. To assess the presence and severity of GM/IVH and H/I injuries, all participating ELBW children had received at least three head ultrasound scans during the first 6 weeks of life as part of their routine care. These ultrasound scans were retrospectively reviewed by two independent physicians to determine the presence, type, and severity of PVBI. Inconsistencies between raters regarding the presence or severity of PVBI were resolved through joint consultation. Physicians were unaware of the children’s medical and developmental history or test results when rating the scans. The extent and nature of GM/IVH and H/I injuries were determined using the Papile (Papile, Burstein, Burstein, & Koffler, 1978) and Frisk and Whyte (1994) classification systems, respectively. Both of these systems utilize a 4-point scale to indicate lesion severity. Based upon these classification systems, ELBW children were placed into the following three groups: (1) ELBW children with normal head ultrasound scans (No PVBI, n = 11); (2) ELBW children with mild (Grades I or II) GM/IVH or H/I injury (Mild PVBI, n = 18); and (3) ELBW children with severe (Grades III or IV) GM/IVH or H/I injury (Severe PVBI, n = 10). Within the Mild PVBI group, there were 14 children with GM/IVH only, 2 with H/I injury only, and 2 with combined GM/IVH and H/I injuries. Within the Severe PVBI group, there were 4 children with GM/IVH, 6 with both GM/IVH and H/I injuries, and no children with isolated H/I injuries.



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Materials and Procedure Demographic variables were collected through the use of a questionnaire that was completed by a parent. Medical variables associated with the ELBW children (e.g., birthweight, weeks of gestation) were collected from the hospital medical charts. Standardized tests of intelligence, academic achievement (reading and spelling), and auditory memory were administered individually to each participant in a quiet testing room, along with experimental tests of phonological processing. These tests are described in brief below, according to each skill area assessed. Each child underwent 4 hours of testing, with breaks after each hour to prevent fatigue. Throughout the testing, the examiner was blind to the neurological status of the ELBW children. To reduce the possibility of subjective bias in scoring, all files were scored twice: once by the first author (A.L.S.D.) and then again by a research assistant who was unaware of the child’s group membership. When scoring discrepancies were found, scores were changed to those determined by the research assistant. Intelligence. A short form of The Wechsler Intelligence Scale for Children–Third Edition (WISC–III; Wechsler, 1991) was administered to each child. Verbal and Performance IQ scores were derived from prorated scaled scores (see Wechsler, 1991, pp. 54) on the following subtests: Information, Similarities, Arithmetic and Vocabulary from the Verbal Scale; and Picture Completion, Coding, Picture Arrangement, and Block Design from the Performance Scale. This short form has been validated in several recent studies (Connery, Katz, Kaufman & Kaufman, 1996; Donders, 2001). Academic Achievement. The Word Identification and Word Attack subtests of the Woodcock Reading Mastery Test–Revised (WRMT–R) were administered to assess the ability to read real English words and nonsense words, respectively (Woodcock, 1987). The Spelling subtest of the Wide Range Achievement Test–3 (WRAT–3) was also administered to assess the ability to spell English words (Wilkinson, 1993). Raw scores on these tests were converted to standard scores according to age. Auditory Working Memory. Auditory short-term memory was measured by asking children to recall a string of numbers and letters in the order given (Numbers and Letters subtest, Wide Range Assessment of Memory and Learning, WRAML, Sheslow & Adams, 1990). Auditory working memory was assessed by asking children to recall a string of numbers in the reverse order to that given by the examiner (Numbers Reversed subtest, Woodcock Johnson Tests of Cognitive Ability, Woodcock & Johnson, 1989). Raw scores on the Letters and Numbers subtest were converted to scaled scores (M = 10, SD = 3) and then transformed to standard scores (M = 100, SD = 15) using appropriate age norms. Raw scores on the Numbers Reversed subtest were converted to standard scores using appropriate age norms. The standard scores on the two auditory working memory tests were then averaged to produce an auditory working memory composite score. Phonological Processing. Three experimental measures were used to assess phonological processing skills. During the Strip Initial Consonant Test (adapted from Stanovich et al., 1984), each child was instructed to say the English word that remained after the removal of the first sound of a nonsense word (e.g., /r/eat = eat, /s/air = air). A total of five practice trials were administered, followed by 20 test words. During the Delete Initial Sound Test (adapted from Wagner, Torgesen & Rashotte, 1994), each child was instructed to say aloud the nonsense word that remained after the first sound of a nonsense word was removed (e.g., /b/ool = ool). Similarly, during the Delete Final Sound Task (adapted from Wagner et al., 1994), the child was instructed to say aloud the


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nonsense word that remained after the final sound of a nonsense word was removed (e.g., zear/d/ = zear). These latter two tasks were each preceded by two practice trials followed by 15 test words. All test items were administered orally. Raw scores on each of the phonological processing tests were converted to percent correct scores, and from these values a phonological processing composite score was computed for each participant (mean percent correct). Although these composite scores were derived from raw scores, rather than standard scores, they did not correlate with age, r = .17, p > .20. RESULTS To address the two major aims of the present study, two separate sets of analyses were carried out. The first set of analyses examined the association between the presence and severity of PVBI and intellectual, academic, and cognitive abilities. In the second set of analyses, hierarchical multiple regressions were used to evaluate the contributions of Full Scale IQ, maternal education, annual household income, auditory working memory and phonological processing to the performance of ELBW children on the three academic measures (English word reading, nonsense word reading, and spelling). Analysis 1: The Impact of Periventricular Brain Injury on Intellectual, Academic, and Cognitive Ability in the Late Elementary and Early High School Period As a first step in this analysis, we sought to establish how comparable our four subgroups of children (Full-term, No PVBI, Mild PVBI and Severe PVBI) were on a variety of demographic variables. Separate Kruskal-Wallis tests indicated that there were no significant group differences in maternal education level or annual household income, and Chi-square tests revealed no group differences in the gender distribution or racial composition of the groups (all p values >.05). A one-way analysis of variance (ANOVA) test confirmed that the groups did not differ significantly in age, F(3,50) = 1.835, p > .15, and a one-way multivariate analysis of variance (MANOVA) test confirmed that the three subgroups of preterm children did not differ from one another in terms of either birthweight or gestational age, F(4,70) = 0.88, p > .45 (Wilks’ Lambda criterion). Information about demographic variables is summarized in Table 1. It is important to note that, although the groups were well-matched on the demographic variables, participants in this study were not representative of the general population. Participants were from predominantly white, middle-class families (modal annual household income $51,000–$75,000 CAD) and had relatively well-educated mothers, many of whom had completed high school or obtained a postsecondary degree. Nonetheless, the full range of educational and income scores were represented. To test the hypothesis that the presence and the severity of PVBI would be associated with intellectual, academic and cognitive abilities in ELBW children, we first conducted a one-way MANOVA on the following measures: Verbal and Performance IQ scores, standard scores on the tests of academic achievement (Word Attack, Word Identification, and Spelling), and the auditory working memory composite score. Group membership was the between subjects factor. The use of this conservative, multivariate approach allowed us to minimize the chance of Type 1 error. The phonological processing composite scores could not be included in the MANOVA as, unlike the other variables, these scores were not normally distributed (see below). Maternal education and annual



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Table 1 Demographic information on each group. Mean values (standard deviations) are shown for age, birthweight, and weeks’ gestation. Modal values for are indicated for income and maternal education level.

Variable Age (years) Birthweight (grams) Weeks of gestation Income* Maternal education** Gender (M/F) Race (White/non-White)

Full Term (n= 15)

No PVBI (n= 11)

Mild PVBI (n= 18)

Severe PVBI (n= 10)

12.1 (1.3) 3842 (697) 40.6 (1.4) 7 5 4/11 11/4

11.4 (1.0) 844 (124) 26.3 (1.2) 7 4 4/7 10/1

11.8 (1.2) 776 (146) 25.5 (1.3) 7 5 7/11 11/7

11.1 (1.3) 853 (184) 25.9 (1.7) 6 4 5/5 6/4

*1 = Under CAD $11,000; 2 = CAD $11,000 – CAD $20,999; 3 = CAD $21,000 – CAD $30,999; 4 = CAD $31,000 – CAD $40,999; 5 = CAD $41,000 – CAD $50,999; 6 = CAD $51,000 – CAD $75,000; 7 = Over CAD $75,000. **1 = Some elementary school, 2 = Completed elementary school, 3 = Some high school, 4 = Completed high school, 5 = Completed postsecondary degree/diploma.

family income were not entered as covariates in this analysis as: (1) the groups did not differ on these variables (see above); and (2) neither of these demographic variables was found to be significantly correlated with any of the dependent measures ( p > .05 in all cases). The omnibus test was significant (Wilks’ Lambda criterion), F(18,128) = 3.62, p < .001, ηp2 = .322, and follow-up univariate tests revealed significant group differences on all measures (see Table 2 for univariate statistics and the results of pairwise comparisons). Following each of the significant univariate tests, pairwise comparisons (Tukey tests) were evaluated at α = .05/6 = .008. These tests revealed that full-term controls and preterm children with no evidence of PVBI performed at comparable levels on all measures. In contrast, full-term children showed a trend to outperform preterm children with mild PVBI on four of the six measures: Performance IQ, Word Identification, WRAT-R Spelling, and the auditory working memory composite ( p < .05 in all cases). In addition, full-term controls scored significantly better than preterm children with severe PVBI on all measures except Verbal IQ (which showed only a trend in this direction, p < .05). Among preterm children, a history of PVBI increased risk for problems on all three tests of academic achievement; thus, preterm children with no history of PVBI outperformed those with mild or severe PVBI. There was also a trend for those with mild PVBI to outperform those with severe PVBI on both of the reading tests ( p < .05). Finally, preterm children with no history of PVBI outperformed those with severe lesions in terms of auditory working memory. Removing the two IQ measures from the MANOVA and repeating the analysis with Verbal IQ entered as a covariate produced no change in the pattern of significant results for the remaining measures. Similarly, repeating the MANOVA adding Gender as a second grouping factor did not change the pattern of significant results, and no significant main effect or interaction involving Gender was observed. The number of children in each group who experienced clinically significant difficulties on each test of reading and spelling ability (i.e., obtained a standard score one standard deviation or more below the mean for each test) was also examined. None of the children in the Full-term or No PVBI groups obtained scores within this range. In contrast, many of the children in the Mild and Severe PVBI groups obtained scores within this range. This was true for both reading, [Word Attack: Mild PVBI 17% (n = 3), Severe


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Table 2 Mean scores and statistics for the Group main effect in univariate tests conducted on tests of intelligence, academic achievement, auditory working memory, and phonological processing. Standard deviations are indicated in parentheses. (ηp2: partial eta squared.) Skill Domain and Variable Intelligence Quotients Verbal IQa, c, e

Performance IQa, b, c, e

Full Term (n= 15)

No PVBI (n= 11)

Mild PVBI (n= 18)

Severe PVBI (n= 10)

102.9 (9.8)

104.0 (16.2)

92.4 (13.0)

87.6 (14.2)

112.3 (13.1)

104.0 (9.5)

98.1 (13.1)

87.3 (15.9)

108.1 (8.9)

94.1 (11.0)

83.3 (12.1)

Academic Achievement (standard scores) Word Identificationa, b, c, d, e, f 104.0 (7.3)

Statistic

F(3,50) = 4.44 p < .01 ηp2 = .210 F(3,50) = 7.96 p < .001 ηp2 = .323 F(3,50) = 13.83 p < .001 ηp2 = .454 F(3,50) = 14.06 p < .001 ηp2 = .458 F(3,50) = 10.59 p < .001 ηp2 = .389

Word Attacka, c, d, e, f

101.0 (9.4)

106.6 (9.2)

93.1 (9.6)

82.9 (7.1)

Spellinga, b, c, d, e

107.6 (7.4)

109.5 (10.8)

95.8 (11.0)

88.4 (12.9)

106.5 (13.2)

105.7 (11.3)

94.0 (12.4)

87.5 (9.6)

F(3,50) = 7.28 p < .001 ηp2 = .304

94.5 (5.2)

91.8 (5.3)

86.6 (9.3)

67.9 (29.7)

χ2 (3) = 14.24 p < .005

Auditory Working Memory Composite scorea, b, c, e

Phonological Processing Composite scorea, b, c a

Full-term and No PVBI groups do not differ, p > .05 (not significant). Full-term > Mild PVBI, p < .05 (trend) in all cases but phonological processing, where p < .008. c Full-term > Severe PVBI, p < .008 in all cases but Verbal IQ, where p < .05 (trend). d No PVBI > Mild PVBI, p < .008 in all cases but auditory working memory. e No PVBI > Severe PVBI, p < .008 in all cases but Verbal and Performance IQ, where p < .05 (trend). f Mild PVBI > Severe PVBI, p < .05 (trend). b

PVBI 40% (n = 4); [Word Identification: Mild PVBI 22% (n = 4), Severe PVBI 60% (n = 6)], and spelling [WRAT-3 Spelling: Mild PVBI 17% (n = 3), Severe PVBI 40% (n = 4)]. Through the use of logistic regression, we verified that the odds of a child obtaining an abnormal outcome on each of the tests did vary with group membership: χ2(1) = 18.26, p < 0.0001 for Word Identification, and χ2(1) = 10.94, p < 0.001 for both Word Attack and WRAT–3 Spelling. Children with severe lesions were 2.8 times more likely than controls to have an abnormal result on the Word Identification test; for both Word Attack and WRAT–3 Spelling, they were 1.8 times more likely than controls to have an abnormal result. Because the composite scores on the phonological processing tests were negatively skewed, a nonparametric approach was adopted to examine possible group differences on this measure. A significant Kruskal-Wallis test indicated that the groups differed on this measure, χ2 (3) = 14.243, p < .005 and follow-up tests revealed that full-term controls and preterm children with no history of PVBI did not differ from one another, but that both outperformed children with severe PVBI. Full-term controls also outperformed preterm children with mild PVBI. (See Table 2.)



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Analysis 2: Contributions of Intelligence, Annual Household Income, Maternal Education Level, Working Memory, and Phonological Processing to Reading and Spelling Performance in ELBW Children. Variables were entered into each hierarchical regression equation first to control for their influence on other variables, and second according to their assumed causal relation to the dependent variable, from most distal cause to most proximal cause (Cohen & Cohen, 1983). Thus, Full Scale IQ was entered into the regression equation first, in order to control for any association between lowered intellectual ability and both working memory skills (Kyllonen & Christal, 1990) and poor reading and spelling ability (see Hoskyn & Swanson, 2000, for a recent review of this issue). Full Scale IQ was used because, of the three IQ scores, it was the most strongly correlated with scores on the tests of academic achievement. The sociodemographic measures (maternal education level and annual household income) were entered in the second step because these variables are expected to have an impact upon both working memory and phonological processing and, as described above, both of these cognitive measures play an important role in reading ability. In the final step, working memory and phonological processing composite scores were entered. Because the phonological processing composite scores were negatively skewed, they were first normalized using a reflect and log transformation. The two cognitive measures were entered simultaneously because (1) they were significantly correlated with each other (see below), and (2) successful completion of the phonological processing tasks included in our battery required the use of a working memory store. Significant bivariate correlations (p < .005 in all cases) were observed between Full Scale IQ, auditory working memory, and phonological processing and (a) Word Identification (r = .685, r = .503, and r = .456, respectively); (b) Word Attack (r = .520, r = .484, and r = .420, respectively); and (c) Spelling (r = .551, r = .469, and r = .467, respectively). In addition, auditory working memory and phonological processing were correlated significantly with one another (r = .559, p < .001). On the other hand, neither maternal education level nor annual household income was correlated with any of the academic measures. Table 3 shows the significant R2 change for the hierarchical regression equations predicting Spelling, Word Identification, and Word Attack scores, and the adjusted cumulative R2 for each of these equations. After the variance accounted for by Full Scale IQ on reading and spelling was removed, maternal education level and annual household income did not significantly change the overall variance accounted for on Word Identification, Word Attack, or Spelling scores. However, the variables entered into each equation next, namely the composite scores on auditory working memory and phonological processing, significantly increased the proportion of variance accounted for in each model, accounting for 14.5% of the variance in Word Identification scores, 13.6% of the variance in Word Attack scores, and 10.8% of the variance in Spelling scores. Overall, these models accounted for 62.4% of the variance in Word Identification scores, 42.9% of the variance in Word Attack scores, and 46.4% of the variance in Spelling scores. DISCUSSION The first aim of the present study was to determine the relationship between the presence and severity of PVBI and intellectual, academic, and cognitive outcomes during the late elementary and early high school period. Because of our interest in PVBI, we focused our investigation on a group of ELBW children who had not suffered other significant


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Table 3 Adjusted cumulative R2, significant R2 changes, unstandardized (B) and standardized (beta) coefficients for each predictor variable in each of the hierarchical regression analyses. (ME: maternal education; Inc: annual family income; AMC: auditory working memory composite; PPC: phonological processing composite; SE: standard error, indicated in parentheses). Adjusted R2 Word Identification FSIQ Sociodemographic variables Cognitive variables Word Attack FSIQ Sociodemographic variables Cognitive variables Spelling FSIQ Sociodemographic variables Cognitive variables

R2 Change

B coefficient (SE)

Beta coefficient

.455 .434

.470** .009

.501 ME .135 Inc .069

.566

.145**

.494 (.124) ME 1.984 (1.877) Inc .549 (.912) AMC .258 (.146) PPC 4.389 (2.268)

.250 .232

.270** .023

.342

.136*

.285 .301

.304** .052

.383

.108*

.308 (.135) ME .777 (2.052) Inc .666 (.997) AMC .252 (.160) PPC 3.313 (2.480) .439 (.145) ME -1.159 (2.198) Inc .555 (1.068) AMC .169 (.171) PPC 4.435 (2.657)

AMC .255 PPC .242

.351 ME .059 Inc .095 AMC .266 PPC .217

.453 ME -.080 Inc .071 AMC .161 PPC .262

*Indicates a significant R2 change, p < .05. **Indicates a significant R2 change, p < .01.

complications that could have compromised neurodevelopment (i.e., intrauterine growth restriction, neurological complications other than PVBI). For practical purposes, we also had to exclude children with severe sensory and cognitive disabilities. Although this removed some children with more significant disabilities from investigation, we were still able to demonstrate that children in our clinical sample, who are quite representative of the majority of ELBW survivors, continue to experience considerable academic difficulties at a mean age of 11 years. Importantly, however, we were also able to demonstrate that those who showed no evidence of PVBI in neonatal ultrasound scans achieved equivalent scores to children who were born full-term on all measures. In contrast, the presence of PVBI was associated with lowered Verbal and Performance IQ ratings, as well as lowered scores on a variety of reading and spelling measures, and on cognitive measures that are believed to be important for the acquisition of these academic skills. Performance on the tests of reading ability followed a pattern of decline as the severity of PVBI increased; thus, children who had suffered from severe PVBI tended to have worse decoding skills than those who had suffered from mild PVBI. The group differences described above cannot be attributed to degree of prematurity or to sociodemographic factors, as all ELBW groups were matched for birthweight and gestational age at birth, and all groups (including controls) were matched for maternal education level and annual household income, and had comparable racial compositions and gender distributions. It is also unlikely that IQ differences between the subgroups of children can fully account for the significant differences in performance noted on the academic and cognitive measures, since covarying out Verbal IQ did not affect the pattern of significant pairwise comparisons on these measures. Moreover, in the preterm sample, auditory working memory and phonological processing ability continued to explain a



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significant amount of the variance in reading and spelling scores after controlling for Full Scale IQ. We conclude on this basis that the reading and spelling difficulties seen in our sample of ELBW children were due, in part, to specific effects of early brain damage on the development of auditory working memory and phonological processing abilities. The results of this study contribute to the literature suggesting that the presence of PVBI may be one of the critical determinants of adverse long-term outcome in appropriately grown preterm ELBW children who escaped severe disability. We suggest that the academic and cognitive differences observed in other studies between “neurologically normal” preterm children and full-term children (e.g., Grunau, Whitfield, & Davis, 2002) might be accounted for by inclusion of preterm children with “clinically silent” PVBI in preterm samples, and/or by reliance on the results of a single head ultrasound scan to document the presence and severity of PVBI. The groupings made in the present study were based upon a minimum of three cranial ultrasound examinations carried out at specified intervals over a 4- to 6-week period, allowing for more accurate documentation of PVBI. A second aim of the present study was to determine if sociodemographic factors (maternal education and annual household income) and cognitive factors (phonological processing and working memory) known to be strongly associated with reading and spelling ability in full-term children would predict performance on tests of reading and spelling ability in ELBW children. Surprisingly, in the present sample of ELBW children, maternal education level and annual household income were not significant predictors of academic ability. It is possible that this null result reflects reduced variability within this particular sample, as the children participating in this study were from predominantly white, middleclass families (modal annual household income $51,000–$75,000 CAD) with relatively well-educated mothers (many of whom had completed high school or obtained a postsecondary degree). One must also consider the possibility that although sociodemographic variables may play an important role in the development of academic skills in younger children (Hack et al., 1994; Koller, Lawson, Rose, Wallace, & McCarton, 1997; Ross et al., 1991, 1996; Sansavini, Rizzardi, Alessandroni, & Giovanelli, 1996), the direct impact of these particular factors may be attenuated as preterm children get older. It is also possible that other, more proximal, environmental factors (not examined in this study)—such as the quality of stimulation the children received, the amount of support available to them in the home, and the amount of remedial support they obtained at school—played an important role in determining long-term outcome in this sample. The relationship of these variables to long-term outcome should be evaluated in future studies, given the considerable evidence in support of the notion that brain structure is partly mediated through experience (see Greenough & Black, 1992; Kolb & Whishaw, 1998, for reviews) and evidence that measures of family and social environment moderate outcome in children with closed-head injury (Taylor et al., 1999;Yeates et al., 1997). Overall, the results of the hierarchical regression analyses presented here provide support for the notion that reading and spelling difficulties among premature children are partly affected by deficits in two of the underlying cognitive abilities that are thought to play a role in learning disabilities among full-term children (i.e., phonological processing and working memory). In a previous study, we have also documented evidence for auditory temporal processing deficits in ELBW children who experienced PVBI (Downie, Jakobson, Frisk, & Ushycky, 2002). A deficit in this area is thought to contribute to the difficulties dyslexic readers experience in discriminating rapidly presented auditory patterns, such as speech sounds (Tallal, 1976; Watson & Miller, 1993). A biological basis for phonological processing and auditory temporal processing deficits has been documented


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using functioning imaging techniques in children and adults with dyslexia (see Temple, 2002, for review). Among dyslexic readers, reduced neural activity is observed in temporoparietal areas during phonological processing tasks (Shaywitz et al., 1998), and in prefrontal areas during auditory temporal processing tasks (Temple et al., 2000). These findings have led to the suggestion that reading impairments may arise from white matter disruptions between anterior and posterior language areas, resulting in a “disconnection syndrome” (Paulesu et al., 1996, Temple, 2002). The presence of phonological processing and auditory temporal processing deficits in ELBW children who experience white matter injury as a result of PVBI may provide an opportunity to test this disconnection hypothesis using functional imaging techniques such as diffusion tensor imaging, in which the microstructure of the white matter can be measured. Reading difficulties in ELBW children may also be tied to additional deficits that are not characteristic of full-term children with specific reading disability. Recent evidence indicates that children with closed-head injury are slower at naming words than control children who were matched to the clinical sample on the basis of age, grade, and word decoding accuracy (Barnes, Dennis, & Wilkinson, 1999). In addition, although reading speed is associated with reading comprehension in children with closed-head injury, this association is not seen in control children who are equally accurate readers. These findings suggest that reading difficulties in head-injured children may be the result of specific effects associated with the brain injury. It remains to be seen whether additional deficits also characterize the reading and spelling difficulties experienced by ELBW children. Conclusion It is largely unknown to what extent the human brain is able to “recover” from injuries experienced perinatally through behavioural compensation, salvaging of damaged circuits, or active reorganization of brain-behavior relations. Although it has been assumed that the young brain is more plastic and therefore more likely to recover from brain injury than the adult brain (Lenneberg, 1967), recent theories suggest that the extent and nature of recovery depends upon the particular stage of brain development at the time of injury, the age at which a follow-up assessment is made (Kolb, 1995), and the specific neural structures that are damaged (Stiles, 1995). The present finding that our “No PVBI” group performed in a manner that was indistinguishable from full-term controls on every measure is important in this regard. We relied on serial, cranial ultrasound scans to document the presence and severity of PVBI and may, therefore, have failed to detect subtle structural abnormalities that might have been visible with MRI (cf. Arzoumanian et al., 2003; Inder, Anderson, Spencer, Wells, & Volpe, 2003; Miller et al., 2003). If subtle lesions were, in fact, missed in our “No PVBI” group, the present findings suggest that the preterm brain can compensate quite well for such damage, probably through behavioral compensation and/or functional reorganization—although we caution that the present data only speak to compensation in the domains of intellectual functioning, and reading and spelling outcomes. This conclusion is consistent with other recent reports that: (1) the presence of subtle white matter abnormalities, visible in a high percentage of MRI scans from teenagers born preterm (but likely to be missed by neonatal cranial sonography) does not correlate well with outcome (Ment, Schneider, Ainley, & Allan, 2000); and (2) MRI does not provide better prediction of outcome in infancy (Van Wezel-Meijler et al., 1999) or early childhood (Guit, Van de Bor, den Ouden, & Wondergem, 1990; Van der Bor, den Ouden, & Guit, 1992) than cranial sonography.



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