Brain & Development xxx (2016) xxx–xxx
www.elsevier.com/locate/braindev

Original article

Reading diﬃculty in school-aged very low birth weight infantsin JapanAkihito Takeuchi a,⇑, Tatsuya Koeda b,c, Toshimitsu Takayanagi d, Kazuo Sato e,
Noriko Sugino f, Motoki Bonno f, Akiko Kada g, Makoto Nakamura a,
Misao Kageyama abaDepartment of Neonatology, Okayama Medical Center, National Hospital Organization, Okayama, Japan
Child Development and Learning Research Center, Faculty of Regional Sciences, Tottori University, Tottori, Japanc
Department of Clinical Research, Tottori Medical Center, National Hospital Organization, Tottori, Japand
Department of Pediatrics, Saga Hospital, National Hospital Organization, Saga, Japane
Department of Pediatrics, Kyushu Medical Center, National Hospital Organization, Fukuoka, Japanf
Department of Neonatology, Mie Chuo Medical Center, National Hospital Organization, Tsu, Japang
Center for Clinical Research, Nagoya Medical Center, National Hospital Organization, Nagoya, Japan

Received 19 February 2016; received in revised form 29 March 2016; accepted 22 April 2016

Abstract
Objective: To investigate the prevalence of and the perinatal risk factors related to reading diﬃculty in school-aged very low birthweight infants (VLBWI) with normal intelligence.
Methods: Subjects were 79 Japanese children in the second to fourth grade of elementary school who had been born at very low
birth weight and who regularly visited a follow-up clinic at one of four hospitals. All members had a full-scale IQ score of 80 or
higher. Perinatal information was obtained retrospectively from medical records. Each subject underwent four reading tasks, testing
monomoratic syllable reading, word reading, non-word reading and short sentence reading. Subjects with an SD reading time score
greater than 2.0 in two or more tasks were considered to have reading diﬃculty (RD). Furthermore we investigated the relations
between RD and perinatal factors using logistic regression analysis adjusted for potential confounding factors.
Results: Twenty-ﬁve (31.6%) out of 79 subjects had RD. We discovered that treated retinopathy of prematurity (tRoP) was asigniﬁcant risk factor (adjusted OR = 5.80, 95% conﬁdence interval = 1.51–22.33).
Conclusion: The rate of RD in school-aged VLBWI was higher than the estimated prevalence of dyslexia in Japan. Even in children with normal intelligence, long-term developmental follow-up including support for reading skills is necessary for VLBWI.
Further investigation is desired to elucidate the relations between visual problems and RD in school-aged children.
Ó 2016 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.

Keywords: Very low birth weight infant; Premature; Reading diﬃculty; Dyslexia

1. Introduction⇑ Corresponding author at: Department of Neonatology, Okayama
Medical Center, National Hospital Organization, 1711-1 Tamasu,
Kita-ku, Okayama 701-1192, Japan. Tel.: +81 86 294 9911; fax: +81 86
294 9255.
E-mail address: gmd18025@s.okayama-u.ac.jp (A. Takeuchi).

A recent study showed that the survival rate of very
low birth weight infants (VLBWI, less than 1500 g) inJapan has improved to more than 90% in the past
10 years [1]. Yet about 15% of VLBWI discharged fromhttp://dx.doi.org/10.1016/j.braindev.2016.04.013
0387-7604/Ó 2016 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.

Please cite this article in press as: Takeuchi A et al. Reading diﬃculty in school-aged very low birth weight infants in Japan. Brain Dev (2016),
http://dx.doi.org/10.1016/j.braindev.2016.04.013

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A. Takeuchi et al. / Brain & Development xxx (2016) xxx–xxx

Japanese Neonatal Intensive Care Units (NICUs) exhibited developmental delay at 3 years of age [2]. Previous
studies from abroad have shown that many schoolaged preterm children without mental retardation havelearning diﬃculties in reading, writing or mathematics[3]. Reading diﬃculty in school-aged preterm children
has been particularly well studied in many countries,
and a recent meta-analysis of English-speaking schoolaged children showed that preterm children perform
worse than peers born at term at both decoding andreading comprehension [4].
In Japan, however, there have been few studies about
learning problems including reading diﬃculty in schoolaged preterm children. More than 10 years ago, Haraet al. reported that 6 (14%) out of 44 children withoutmajor neurodevelopmental sequelae but with extremely
low birth weight (less than 1000 g) had learning disabilities in the third grade (approximate age 8–9) [5]. Also,
Koeda et al. reported that 3 (25%) out of 12 children
born at very low birth weight (VLBW) had typical learning disabilities [6]. Because the methods of evaluating
learning problems in those two studies were subjective,
however, the authors of both studies noted the needfor established methods for the objective assessment oflearning problems in Japanese children.
Recently, a new set of Japanese guidelines for the
diagnosis and treatment of speciﬁc developmental disorders [7] was published. In these guidelines, standardized
objective tests for evaluating subjects’ ability to readhiragana script were proposed. In the present study,
using these objective evaluations, we aimed to estimate
the prevalence of reading diﬃculty in school-aged children born at VLBW and to elucidate the perinatal risk
factors for reading diﬃculty in children born at VLBW.
2. Methods
2.1. Subjects
Japanese children with normal intelligence in the second to fourth grades of elementary school (approximate
age range 7–10) who had been born at VLBW and who
regularly visited a follow-up clinic at one of the participating hospitals (Okayama Medical Center, Kyushu
Medical Center, Saga Hospital and Mie Chuo Medical
Center) were eligible for the study and were recruited
prospectively between April 2013 and March 2015. Subjects had been scored according to the Wechsler Intelligence Scale for Children (WISC)-III or IV during
preschool or later, and all participants had full-scale
IQ scores of 80 or higher. Children with hearing diﬃculties, impaired visual acuity in spite of using eyeglasses,
or articulatory disorders were excluded. Also, children
in inappropriate educational settings were excluded.
Written informed consent was obtained from all participants and/or their parents at the time of this study. This

study was approved by the Ethical Committee of the
National Hospital Organization (H25-0213005).
2.2. Reading tests
Each subject underwent all four of the reading tasks
described below, in accordance with the methods previously reported by Ogino et al. [8]. All subjects were
examined by experts on neuropsychology in quiet
rooms. During each of the four tasks, we recorded thesubjects’ voices with an IC recorder.
2.2.1. Monomoratic syllable reading task [7–9]
We deﬁned ‘mora’ as the smallest rhythmic element
into which a word can be divided. Subjects were
instructed to read aloud 50 monomoratic syllables,
including 20 contracted sounds, as quickly and as accurately as possible. Syllables were printed in hiragana on
210  297 mm white cards, arranged into ﬁve rows and
10 columns of syllables on each card. Before trial, subjects practiced with sample cards. The amount of timeeach subject required to read all 50 syllables wasrecorded.
2.2.2. Word reading tasks [7,8,10]
Subjects were instructed to read aloud 30 Japanesewords of three to four moras each (e.g., ‘‘”[genkan] (entrance)) as quickly and as accurately as possible. Words were printed in hiragana on 210  297 mm
white cards, arranged into three columns and 10 rows ofwords on each card. Before trial, subjects practiced withsample cards. The amount of time each subject required
to read all 30 words was recorded.
2.2.3. Non-word reading tasks [7,8,10]
Subjects were instructed to read aloud 30 non-wordsof three to four moras each (e.g., ‘‘” [shitebou](no meaning)) as quickly and as accurately as possible.
These non-words were printed in hiragana on
210  297 mm white cards, arranged into three columns
and 10 rows of non-words on each card. Before trial,
subjects practiced with sample cards. The amount oftime each subject required to read all 30 non-words
was recorded.
2.2.4. Short sentence reading task [8,11]
Subjects were instructed to read aloud three short
sentences of 23–27 moras each. Each sentence wasprinted in mixed hiragana and kanji on a
210  297 mm white card. Above the kanji letters, there
were hiragana indicating the correct pronunciation of
the kanji letters. Subjects were shown three cards in succession, and were instructed to read the short sentences
aloud as quickly and as accurately as possible. The
amount of time each subject required to read all of thesentences was recorded.

Please cite this article in press as: Takeuchi A et al. Reading diﬃculty in school-aged very low birth weight infants in Japan. Brain Dev (2016),
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A. Takeuchi et al. / Brain & Development xxx (2016) xxx–xxx

Reading times were measured using DigiOnSound 5
Express (DigiOn, Inc., Fukuoka, Japan) voice analyzing
software on a personal computer by a single researcher.
Based on gender-segregated, grade-speciﬁc normative
times required for comparable reading tasks [7], we calculated the Z scores of reading times of each readingtask. Because the Japanese school year starts in April
and the normative data was recorded in October, subjects who were tested on our reading tasks between April
and September were scored relative to the normative
data from the grade below [7]. According to the Japanese guidelines for the diagnosis and treatment of speciﬁc developmental disorder [7], we identiﬁed subjects
with Z scores greater than 2.0 in two or more tasks ashaving reading diﬃculty (RD).
2.3. Perinatal information
Subjects’ gestational age (GA), birth weight (BW),height at birth (HT), head circumference at birth(HC), and Apgar scores at 1 min (Aps1) and 5 min(Aps5) were collected retrospectively from their medical records. Also, presence or absence of intraventricular hemorrhage (IVH), symptomatic patentductus arteriosus (sPDA), necrotizing enterocolitis(NEC), intestinal perforation, late circulatory collapse(LCC), treated retinopathy of prematurity (tRoP) andsevere chronic lung disease (CLD36) was noted
retrospectively from medical records. We deﬁned
CLD36 as oxygen dependence after 36 weeks of postconception age.
2.4. Data analysis
First, we analyzed the results of the reading tasks andcalculated the prevalence of RD among our subjects.
Then, to elucidate the perinatal risk factors for RD in
school-age children born at VLBW, we performed logistic regression analysis adjusted for potential confounding factors to estimate the odds ratios (ORs) for RD.

3Here, we showed two representative cases with RD.
Case 1 was a boy born at 24 weeks of GA. His BW
and HT were appropriate for GA. He was mechanicallyventilated for 35 days due to prematurity. He had a mild
(grade I) IVH. LCC occurred when he was 20 days oldand dexamethasone was administered intravenously
for several days. He did not have sPDA, NEC, intestinal
perforation or CLD36 during his clinical course. Laser
retinal photocoagulation was done bilaterally for treatment of RoP. After discharge from the NICU, his developmental milestones were not delayed. He used
eyeglasses because of myopia of the left eye. At school,
he was not good at taking notes or learning Japanese
kanji, although he had no signiﬁcant diﬃculties understanding his studies. In the third grade of elementary
school (8 years of age) WISC-III and kana reading tests
was done. His full-scale intelligence quotient (FIQ), performance intelligence quotient (PIQ) and verbal intelligence quotient (VIQ) were 98, 93 and 103,
respectively. His verbal comprehension (VC), perceptualorganization (PO), freedom from distractibility (FD)and processing speed (PS) were 103, 95, 97 and 106,
respectively. On kana reading tests, he scoredbelow 2.0 SD in three of four reading tasks, and was
judged to have RD.
Case 2 was a girl born at 30 weeks of GA. She was a
SGA infant. She did not have IVH, sPDA, NEC, intestinal perforation, LCC or CLD36 during her clinicalcourse. Although she had mild RoP, treatment was
not needed. After discharge from the NICU, her developmental milestones were not delayed. At school, she
did not like reading long text, and she was not goodat reading Japanese kanji, although she had no signiﬁcant diﬃculties with understanding her studies. In the
fourth grade of elementary school (9 years of age)
WISC-III and kana reading tests were done. Her FIQ,
PIQ and VIQ were 87, 87 and 89 respectively. Her
VC, PO, FD and PS were 86, 85, 94 and 103, respectively. On kana reading tests, she scored below 2.0
SD in two of four reading tasks, and was judged to haveRD.

3. Results
3.2. Perinatal risk factors for RD
3.1. Prevalence of RD among school-aged children born at
VLBW
The subjects were 79 Japanese children, speciﬁcally,
31 boys and 48 girls. Medians of GA and BW were
29 weeks 0 days (range: 23 weeks 3 days – 36 weeks
3 days) and 959 g (425–1498 g), respectively. Medianage at the time of the reading test was 8 years 11 months(7 years 4 months – 9 years 11 months). The Z scores foreach reading task are shown in Fig. 1. Twenty-ﬁve outof 79 subjects (31.6%) were judged to have RD. Detailed
characteristics of subjects stratiﬁed by birth weight are
shown in Table 1.

Signiﬁcant diﬀerences were seen in the morbidity of
tRoP (OR = 4.52, 95% CI = 1.30–15.72 p = 0.018)
between the RD group (n = 25) and the non-RD group(n = 54) (Table 2). Aps5 was mildly related to the morbidity of both tRoP and RD, and was adopted as a confounding factor. Adjusted OR of tRoP for RD was 5.80
(95% C.I., 1.51–22.33). Although GA had no relation to
RD, GA was signiﬁcantly related to the morbidity of
tRoP. Accordingly, we divided subjects into two subgroups according to GA, with the cutoﬀ point set as
the median GA for the entire subject population(29 weeks 0 days). In the low-GA group (less than

Please cite this article in press as: Takeuchi A et al. Reading diﬃculty in school-aged very low birth weight infants in Japan. Brain Dev (2016),
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A. Takeuchi et al. / Brain & Development xxx (2016) xxx–xxx

Fig. 1. Distributions of Z scores for each reading task. Based on gender-segregated, grade-speciﬁc normative times required for comparable readingtasks, we calculated the Z scores of the reading times of each reading task. Subjects judged to have RD (scored 2.0 SD or higher in two or more
reading tasks) were shown as ﬁlled circle (group RD), and subjects without RD was shown as open circle (group non-RD). The horizontal line wasdrawn at 2.0 SD.

Table 1
Detailed characteristics of the subjects stratiﬁed by birth weight.
Birth weightaGestational age
Birth weighta
Male
Apgar score 1 min
Apgar score 5 min
Small for gestational age
Intraventricle hemorrhage
Necrotizing enterocolitis
Intestinal perforation
Symptomatic PDA
Late circulatory collapse
Severe CLD
Treated RoP
Reading diﬃculty<750 g (n = 17)

750–999 g (n = 25)

1000–1249 g (n = 17)

1250–1499 g (n = 20)

27w1d (23w3d–31w4d)
674 g (425–738)
7 (41.2%)
4 (1–6)
7 (1–9)b
8 (47.1%)
2 (11.8%)
00
11 (64.7%)
3 (17.6%)
3 (17.6%)
5 (29.4%)
6 (35.3%)

27w6d (24w5d–34w2d)
891 g (750–990)
10 (40.0%)
4.5 (1–9)c
7 (1–10)
11 (44.0%)
3 (12.0%)0
1 (4.0%)13 (52.0%)
8 (32.0%)
4 (16.0%)
5 (20.0%)8 (32.0%)29w3d (26w5d–33w6d)
1108 g (1004–1224)
6 (35.3%)
5 (1–9)8 (4–9)6 (37.5%)b
1 (6.3%)b0b0b6 (37.5%)b
2 (12.5%)b
2 (12.5%)b
3 (18.8%)b
5 (29.4%)

32w1d (29w0d–36w3d)
1393 g (1250–1498)
8 (40.0%)
8 (2–9)9 (6–10)6 (30.0%)
1 (5.0%)002 (10.0%)01 (5.0%)0
6 (30.0%)

PDA, patent ductus arteriosus; CLD, chronic lung disease; RoP, retinopathy of prematurity.
aMedian (min–max).
bn = 16.
cn = 24.

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5

Table 2
Diﬀerences of patient characteristics between group RD and group non-RD.
Logistic regression
Gestational agea
Birth weighta
Male
Apgar score at 1 min
Apgar score at 5 min
Small for gestational age
Intraventricle hemorrhage
Necrotizing enterocolitis
Intestinal perforation
Symptomatic PDA
Late circulatory collapse
Severe CLD
Treated RoPGroup RD (n = 25)

Group non-RD (n = 54)

29w3d (24w0d–36w3d)
959 g (425–1498 g)
7 (28.0%)
6 (1–9)8 (1–10)12 (48.0%)
2 (8.0%)0 (0%)
1 (4.0%)10 (41.5%)
4 (16.0%)
4 (16.0%)8 (32.0%)

28w6d (23w3d–34w2d)
961.5 g (573–1492 g)
24 (44.4%)
5 (1–9)b
8 (1–10)b19 (35.8%)b
5 (0.4%)b
0 (0%)b0 (0%)b22 (40.0%)b
8 (15.1%)b
6 (11.3%)b
5 (9.4%)b

OR (95% CI)

p value

0.99 (0.99–1.00)
0.49 (0.17–1.36)
1.12 (0.93–1.35)
1.21 (0.92–1.59)
1.65 (0.63–4.34)
0.84 (0.15–4.63)––
0.94 (0.36–2.48)
1.07 (0.29–3.96)
1.49 (0.38–5.85)
4.52 (1.30–15.72)

0.483
0.557
0.168
0.229
0.165
0.308
0.836
–
1.000
0.899
0.918
0.566
0.018

PDA, patent ductus arteriosus; CLD, chronic lung disease; RoP, retinopathy of prematurity; RD, reading diﬃculty.
aMedian (min–max).
bn = 53.

Table 3Adjusted odds ratios of treated RoP for RD in two subgroups stratiﬁed by gestational age.
Logistic regression

Gestational age >= 29w0d
Treated RoP
Gestational age < 29w0d
Treated RoPGroup RD (n = 15)
2 (13.3%)
Group RD (n = 10)
6 (60.0%)Group non-RD (n = 25)
1 (4.0%)Group non-RD (n = 28)
4 (14.8%)

OR (95% CI)ap value

3.81 (0.31–46.10)

0.294

8.93 (1.51–52.64)

0.016

RoP, retinopathy of prematurity; RD, reading diﬃculty.
aAdjusted for Apgar score at 5 min.

29 weeks 0 days), adjustedOR of tRoP for RD was 8.30
(95% C.I., 1.51, 52.64). In the high-GA group (morethan 29 weeks 0 days), on the other hand, adjustedORof tRoP for RD was 3.81 (95% C.I., 0.31, 46.10,
p = 0.294) (Table 3).
4. Discussion
According to the results of our Japanese kana reading tests, we judged that 25 (31.6%) out of 79 study participants had RD. In contrast, a previous large study inJapan estimated that the prevalence of dyslexia, including suspected cases, in the general population of Japanwas 0.7–2.2% [7]. Though it is diﬃcult to compare
directly the results of the present study with those of
the previous dyslexia study, it seems clear that the rateof RD is higher in school-aged Japanese VLBWI thanin the general population of Japan. In Sweden, Samuelsson et al. previously reported that 31% of school-aged
VLBWI had low reading skill scores in reading comprehension tests [12]. The rate of poor reading skills in
Samuelsson’s study in Sweden are comparable with thatin the present study in Japan.

In the present study, we found that treated RoP wasthe most signiﬁcant risk factor for RD in school-aged
VLBWI. No signiﬁcant relation between CLD36 andRD was shown in the present study, though a relation
between co-morbid chronic lung disease (CLD) and
low academic achievement among children born with
ELBW has been reported previously [13].
The relation between RoP and reading problems in
VLBWI has not been reported previously as far as weknow. The negative impacts of RoP on visual function
in childhood, such as strabismus, abnormal refraction
and abnormal contrast sensitivity, have been previously
reported, however [14]. Similarly, Larsson et al. reported
that the peripheral visual ﬁeld is constricted in children
who have undergone cryotreatment [15]. Therefore it ispossible that tRoP has a direct negative impact on visualfunction despite the exclusion of subjects with impaired
visual acuity from the present study.
In many languages, including Japanese, the primarycause of dyslexia is thought to be a problem in decoding
function [16,17]. Yet Samuelsson has reported that
weaknesses in orthographic (spelling-based) reading
skills were more prominent relative to weaknesses in

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A. Takeuchi et al. / Brain & Development xxx (2016) xxx–xxx

phonological (sound-based) skills in the VLBW groupthan in the normal-birth-weight controls [18,19].
Recently, the crowding phenomenon attracted attention
as a basis of reading disorders [20]. Crowding refers to
the interference of ﬂanking letters in the recognition oftarget letters [20]. Larsson et al. showed that prematurely born children, especially those with severe
untreated RoP or cryotreated RoP, had poor crowding
acuity compared with full-term children [21]. The
crowding phenomenon might contribute to the relation
between treated RoP and RD discovered in the present
study.
Also, the increased risk of reading diﬃculty in children with very low birth weight is reportedly associatedwith periventricular white matter injury [22]. The portion of periventricular white matter that is sometimes
injured in premature infants is part of the visual cognition pathway [23]. Therefore the mechanism by whichreading diﬃculty occurs might diﬀer between VLBWIand children born at full term. Problems with visual cognition, in addition to phonological weakness, might play
an important role in reading diﬃculty in school-aged
VLBWI.
Among the subjects of the present study, four children received special-needs education a few hours each
week, and three of these had RD. Though we did notinvestigate the reasons why these children were receiving
special-needs education, it is likely that they exhibitedlearning problems or behavioral problems such as attention deﬁcit hyperactivity disorder (ADHD) or autism
spectrum disorder (ASD). A high prevalence of RD inpatients with ADHD or ASD in Japan has been shownin a previous study [24].
The present study had two major strengths. First, thiswas a multicenter study, reducing the possibility that thetherapeutic characteristics of any particular hospitalaﬀected our results. Second, we adopted an objective
reading evaluation; this was the ﬁrst report on reading
diﬃculty in school-aged VLBWI in Japan in which thedata was collected using an objective test. On the other
hand, this study had some limitations. First, we could
not eliminate the possibility of selection bias because
the follow-up rates at two of the four participating hospitals were too low. Moreover, we could not recruit all
potential subjects followed in the developmental outpatient clinics at each hospital. Second, tests of precise
visual acuity, detailed visual ﬁeld tests and refraction
tests at the time of the reading test were not available,
because not all of the patients received ophthalmologic
examinations after admission into elementary school.
Further large prospective studies, including brain
imaging, detailed ophthalmologic examinations at
school age, tests for phonological processing, neuropsychological evaluations for visual cognition such as the
Frostig developmental test of visual perception [25] or

Rey–Osterrieth Complex Figure [26] and behavioral
evaluations able to detect ADHD and ASD are desired.
Although Samuelsson et al. reported that the reading
skills of school-aged VLBWI improved over time until,by the age of 15 years [19], there was no signiﬁcant difference between VLBWI and normal control subjects, itis thought that reading diﬃculty in the lower grades of
elementary school might have a negative impact on academic achievement throughout a child’s school career.
Accordingly, it is important to diagnose reading diﬃculties and provide appropriate educational environments
as early as possible. Long-term developmental followup for VLBWI including support for reading skills isnecessary even for VLBWI of normal intelligence, andcooperation with schools and specialized institutions
for educational and behavioral problems is very
important.
5. Conclusions
About 30% of school-aged VLBWI with normal
intelligence and no signiﬁcant visual problems had apossible reading disorder. This rate is higher than theestimated prevalence (0.7–2.2%) of dyslexia in the Japanese general population. In spite of normal intelligence,long-term developmental follow-up for VLBWI including support for reading skills is needed. Moreover, we
discovered that treated RoP was a signiﬁcant risk factor
for reading diﬃculties among school-aged VLBWI. Further investigation is desired to elucidate the relations
between visual problems and RD in school-aged
VLBWI.

Acknowledgements
This research was funded by a grant from the
National Hospital Organization (H24 Seiiku-03). We
appreciate the valuable comments provided by Dr.
Akiko Saito, Dr. Keizo Horibe and the attendees of
the NHO Child Health and Development Research
Meeting. We also appreciate the valuable support of
Tomoko Sakashita, Hitomi Hanada, Mizuko Hashimoto, Ryoko Matsuda, and Naomi Abe.
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Please cite this article in press as: Takeuchi A et al. Reading diﬃculty in school-aged very low birth weight infants in Japan. Brain Dev (2016),
http://dx.doi.org/10.1016/j.braindev.2016.04.013