# School-entry age and academic difficulties at 7 years of age in children born very preterm: A call for age-corrected schooling

Jean-Christophe Roze, Geraldine Apprioual, Andrei Scott Morgan,

Jean-Baptiste Muller, Stephane Marret, Valerie Rouger, Ghislain Leduc, Nail

Benallegue, Mickael Dinonais, Charlote Bouvard, et al.

► To cite this version:

Jean-Christophe Roze, Geraldine Apprioual, Andrei Scott Morgan, Jean-Baptiste Muller, Stephane Marret, et al. School-entry age and academic difficulties at 7 years of age in children born very preterm: A call for age-corrected schooling. Archives de Pédiatrie, 2024, 10.1016/j.arcped.2024.10.007. hal-04903354

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Research paper

# School-entry age and academic difficulties at 7 years of age in children born very preterm: A call for age-corrected schooling

## School-entry age and academic difficulties at 7 years of age in children born very preterm

Jean-Christophe Roze<sup>a,b,*</sup>, Geraldine Apprioual<sup>a,†</sup>, Andrei Scott Morgan<sup>c,‡</sup>, Jean-Baptiste Muller<sup>a,b</sup>, Stephane Marret<sup>d</sup>, Valerie Rouger<sup>b</sup>, Ghislain Leduc<sup>b</sup>, Nail Benallegue<sup>b,e †</sup>, Mickael Dinonais<sup>b,f</sup>, Charlote Bouvard<sup>g</sup>, Pierre-Yves Ancel<sup>c</sup>, Cyril Flamant<sup>a,b</sup>

ARTICLE INFO

Keywords:

Very preterm infants

School age

Academic difficulties

ABSTRACT

**Background:** Very preterm children are at greater risk of academic difficulties (AD). Some of them start school a year earlier than anticipated during pregnancy due to being born preterm. The aim of this study was to analyze the relationship between neurodevelopment, school-entry age, and AD at age seven.

**Method:** AD were assessed at age seven in children born before 33 weeks of gestation between January 1st, 2007 and December 31, 2014 and enrolled in LIFT cohort. To analyze the relationship between school-entry age and AD, we used generalized equations with adjustment for perinatal, socio-economic factors, and neurodevelopment assessed by Age Stages Questionnaire (ASQ) at 5 years. Moreover, we used Global Scholar Adaptation (GSA) score to evaluate the school adaptation.

**Results:** 2599 children were in routine schooling. Entering school a year earlier was observed in 597 (23.0 %). AD was known for 1943/2599 (74.8 %). Starting school a year earlier was associated with an increased rate of AD: 35.4 % in the exposed group versus 20.2 % in the non-exposed group, with a relative risk of 1.76 (95 % CI: 1.48; 2.08). Both starting school a year earlier and ASQ at 5 years old were independently associated with the GSA score at age 7: standardized $\beta$ = -0.15 (95 % CI:-0.10;-0.20) and 0.40 (95 % CI: 0.35; 0.45) respectively.

**Conclusion:** Starting school a year earlier than anticipated during pregnancy was associated with an increased rate of AD at age 7 in children born very preterm, independently of their neurodevelopment at age 5 assessed by ASQ. Basing school entry age on corrected age seems appropriate to mitigate this risk.

# 1. Introduction

Rates of neurodevelopmental disorders remain high in very preterm infants (born at <33 weeks of gestational age), even though survival of preterm infants has improved in recent decades [1,2]. These children need regular follow-up after hospital discharge to monitor their development. Neurological assessment at two years of age is critical to

diagnose severe disability but is insufficient for finer prediction of outcomes [3]. More regular follow-up is required to identify problems such as cognitive disorders, learning disabilities and behavioral problems [4] which can lead to academic difficulties (AD).

AD among children born very preterm are frequent, with two meta-analyses highlighting difficulties in reading, spelling and arithmetic [5, 6]. This observation is stable over time, implying that deficits apparent

<footnote><sup>a</sup> Department of Neonatology, University Hospital of Nantes, Nantes, France</footnote>

<footnote><sup>b</sup> LIFT Network, University Hospital of Nantes, Nantes, France</footnote>

<footnote><sup>c</sup> INSERM U1153, Epidemiology and Biostatistics Sorbonne, Paris, France</footnote>

<footnote><sup>d</sup> Department of Neonatal and Pediatrics, Intensive Care, and Neuropediatrics, Rouen University Hospital, Normandy University, Rouen, France</footnote>

<footnote><sup>e</sup> Department of Pediatric Neurology, University hospital of Angers, Angers, France</footnote>

<footnote><sup>f</sup> Departement de médecine physique et réadaptation, University hospital of Angers, Angers, France</footnote>

<footnote><sup>g</sup> SOS Préma, association for the support of parents, Neuilly, France</footnote>

<footnote>* Corresponding author at: Department of Neonatology, University Hospital of Nantes, Nantes University, 38 Boulevard Jean Monnet, 44000 Nantes, France
E-mail address: jean-christophe.roze@inserm.fr (J.-C. Roze).</footnote>
in the first years of primary school neither improve nor worsen with progression through school [7]. Academic difficulties are also associated with multiple factors, including gestational age, birth weight Z-score, neonatal morbidities and socio-economic status of the family [8–10].

Age at school entry plays a role in academic performance. In two large studies in two different countries, enrolling more than 10,000 term-born children each, academic performances were higher in children who were older at school entry based on school admission laws exclusively using birth date [11,12]. In preterm infants, age of entry based on their actual birthday rather than their expected date of birth may therefore increase their risk of learning difficulties with corresponding school failure [11]. This modifiable effect of going to school a year earlier than otherwise expected by their due date appears to have measurable consequences for ex-preterm infants in adolescence and is likely to limit adulthood opportunities [13].

The LIFT (Loire Infant Follow-up Team) cohort [14], a regional, population-based prospective cohort, following very preterm infants up to seven years of age, provides an opportunity to explore the association between starting school a year earlier than expected (based upon pregnancy due date) and longitudinal neurodevelopment from 18 month to 5 years, school behaviour at age of 5 and academic difficulties at age of 7 among children born before 33 weeks of gestation.

## 2. Methods

### 2.1. Participants and data collections

This study included all children born between 1st January 2007 and 31st December 2014 with a gestational age of less than 33 weeks followed in the LIFT cohort [14], and enrolled in the general school system at age 7. Birth and perinatal data were collected at hospital discharge along with family socio-economic status. Perinatal data used in this study were gestational age at birth (completed weeks of gestation), birth weight z-score and sex (male/female). Neonatal morbidities were bronchopulmonary disease (defined as need for oxygen or assisted ventilation at 36 weeks corrected gestational age) and severe cerebral lesions (defined as the presence of intraventricular hemorrhage stage III or IV according to the Papile classification or periventricular leucomalacia at any stage during the neonatal hospitalisation). The socio-economic situation of the family was assessed on the basis of the nature of the parents' employment and eligibility for social security benefits for people on low incomes. If eligible, the socio-economic level was considered to be 'low'. Each parent's employment was assessed according to the official classification drawn up by the INSEE institute. If the job of one of the parents was rated highly, his or her socio-economic level was considered 'high'; if not, it was considered 'intermediate'.

### 2.2. Neurodevelopment

A network of about 180 trained physicians from the region monitored the children in a standardized manner at 3, 9, 12, and 24 months of corrected age, as well as 48, 60 and 84 months of chronological age. Furthermore, the second version of the parental Age and Stages Questionnaires (ASQ), composed of age-specific questions covering ages 4 to 60 months [15], was completed by parents at 18, 24, 36, 48 and 60 months before each medical visit. Each questionnaire includes 30 developmental items divided into five domains: communication abilities, gross motor skills, fine motor skills, problem solving abilities and personal-social skills. For each item, three responses are possible depending upon whether the child performs the task (10 points for "yes", 5 points for "sometimes" and 0 points for "not yet"). An overall ASQ score was established with a maximum global ASQ score for 300 points.

### 2.3. Exposure

School-entry in the academic year prior to that anticipated during

pregnancy was the exposure. In France, school admission laws are based on calendar year of birth. The year of school entry anticipated during pregnancy was based on the estimated due date. Hence, for children born at the end of the calendar year (November, December - and for some extremely preterm born children October and even September), the anticipated year is the year following the year of the birth – thus meaning school-entry occurs a year earlier than otherwise expected.

### 2.4. Outcomes

Academic difficulties and school behaviour at age 7 were the primary and secondary outcomes, respectively. Academic difficulties were reported by the parents and/or teacher at age 7, and were defined as either: regular schooling requiring additional academic support (e.g. from an assistant or special education team); regular support from the school psychologist or physician, or the need for therapeutic services at age 7 (one or more appointments with a speech-language therapist, physiotherapist, occupational therapist, orthoptist, or support at a child development center); or, needing to repeat a year of schooling [16].

School behaviour was assessed by the teacher using the global school adaption score (GSA) which is an evaluation tool, designed to assess academic and behavioral skills. The evaluation is composed of 20 questions: six questions about linguistic competence, five questions about nonverbal abilities, eight questions about children's behaviour in the classroom, and the 20th question is about the teacher's prognosis for future school life (adaptation to upcoming classes). Every question gives 1 to 3 points. The child is compared to his/her classmates for each question [17].

### 2.5. Ethics

The LIFT cohort is funded by the Health Regional Agency of Pays de la Loire and registered with the French Data Protection Authority for clinical research (Commission Nationale de l'Informatique et des Libertés or CNIL, No. 851,117). The study received a favorable assessment from the relevant ethics committee (GNEDS, Groupe Nantais d'Ethique dans le Domaine de la Santé). Written consent was obtained from parents before children were included in the cohort.

### 2.6. Statistical analysis

First, we compared characteristics and outcome between children born very preterm entering school during the year anticipated in pregnancy with those who entered a year early. Secondly, we calculate correlation between ASQ scores at 18, 24, 36, 48 and 60 months, and GSA scores at 5 and 7 years. Thirdly, we analysed the discriminating accuracy for predicting academic difficulties of the ASQ at 18, 24, 36, 48 and 60 months and the GSA score at 5 years of age by tracing the receiver operating characteristic (ROC) curve and estimating the area under the curve (AUC). Fourthly, to analyse the relationship between school-entry age and academic difficulties, we used generalized estimating equations with a log-Poisson model, adjusted for perinatal and socio-economic factors, and for neurodevelopment as assessed by the ASQ at the ages where the ASQ was the most discriminating. Finally, we conducted path analysis to investigate whether the association between school-entry age and GSA at age seven was mediated through neurodevelopment or adaptation to schooling at age 5 using the GSA.

Sensitivity analyses were performed using multiple imputation for missing ASQ at 18, 24, 48 and 60 months, and GSA at 5 and 7 years, using a linear regression model that included gestational age, sex, birth weight z-score, bronchopulmonary dysplasia at 36 weeks, cerebral lesions, socio-economic status and known ASQ and GSA scores. The level of statistical significance was set at $p < 0.05$ for all analyses performed with two-tailed tests. Analyses were performed with SPSS (version 28.0).
3. Results

Among 3501 preterm infants enrolled in the LIFT Cohort between
January 1st 2007 and December 31th 2014, 2882 were followed-up at 7
years (82.3 %) (Fig. 1). Among these 2882 chidren, 2599 were in

standard schools. School entry a year earlier than expected during
pregnancy was observed in 597/2599 (22.3 %). These children repre-
sented 100 %, 100 %, 50.9 % and 5.4 % of those born in, respectively,
December, November, October and September. Children who started
school a year earlier than otherwise expected were born more preterm (p

<figure><img src="image_3.png" /><figcaption>**Fig. 1.** Flow chart.
ASQ: Age and Stages Questionnaires; GSA/ Global Scholar Adaptation score; LIFT: Loire Infant Follow-up Team</figcaption></figure>
<caption>**Table 1**</caption>

Perinatal characteristics, Age and Stages Questionnaires (ASQ) score from 18 months to 60 months, Global Scholar Adaptation score (GSA) at 5 and 7-year and academic performance at 7-year in children exposed or not to enter a year earlier than expected during pregnancy.

<table><thead><tr><th>Characteristics</th><th>Not-Exposed</th><th>Exposed</th><th>p</th></tr></thead><tbody><tr><td>Socio-economic status</td><td>N = 2002</td><td>N = 597</td><td>0.19</td></tr><tr><td>- Favorable</td><td>483 (24.1)</td><td>134 (22.1)</td><td></td></tr><tr><td>- intermediate</td><td>1180 (58.9)</td><td>343 (57.5)</td><td></td></tr><tr><td>- low</td><td>289 (14.4)</td><td>97 (16.2)</td><td></td></tr><tr><td>- Unknown</td><td>50 (2.5)</td><td>23 (3.9)</td><td></td></tr><tr><td>Male</td><td>1029 (51.4)</td><td>332 (55.6)</td><td>0.07</td></tr><tr><td>Gestational age</td><td></td><td></td><td>&lt;0.001</td></tr><tr><td>- 24-26 weeks</td><td>140 (7.0)</td><td>69 (11.6)</td><td></td></tr><tr><td>- 27-28 weeks</td><td>301 (15.0)</td><td>127 (21.3)</td><td></td></tr><tr><td>- 29-30 weeks</td><td>519 (25.9)</td><td>158 (26.5)</td><td></td></tr><tr><td>- 30-31 weeks</td><td>1042 (52.0)</td><td>243 (40.7)</td><td></td></tr><tr><td>Birth weight (g)</td><td>1390 (390)</td><td>1325 (395)</td><td>&lt;0.001</td></tr><tr><td>Birth weight score</td><td>-0.22 (1.02)</td><td>-0.11 (1.01)</td><td>0.022</td></tr><tr><td>Multiple pregnancy</td><td>706 (35.3)</td><td>205 (34.3)</td><td>0.68</td></tr><tr><td>Bronchopulmonary dysplasia</td><td>124 (6.2)</td><td>43 (7.2)</td><td>0.38</td></tr><tr><td>Severe cerebral lesions</td><td>56 (2.8)</td><td>20 (3.4)</td><td>0.48</td></tr><tr><td>Breastfeeding at discharge</td><td>423 (22.6)</td><td>116 (20.5)</td><td>0.29</td></tr><tr><td>ASQ at 18 months, corrected age</td><td>n = 950, 224 (43)</td><td>n = 239, 219 (49)</td><td>0.13</td></tr><tr><td>ASQ at 24 months, corrected age</td><td>n = 1665, 246 (36)</td><td>n = 491, 242 (38)</td><td>0.03</td></tr><tr><td>ASQ at 36 months</td><td>n = 926, 252 (40)</td><td>n = 286, 249 (48)</td><td>0.33</td></tr><tr><td>ASQ at 48 months</td><td>n = 1563, 258 (38)</td><td>n = 452, 257 (37)</td><td>0.51</td></tr><tr><td>ASQ at 60months</td><td>n = 1505, 272 (32)</td><td>n = 408, 272 (27)</td><td>0.83</td></tr><tr><td>GSA at 5-year</td><td>n = 1607, 50 (8)</td><td>n = 411, 47 (8)</td><td>&lt;0.001</td></tr><tr><td>GSA at 7-year</td><td>n = 1258, 51 (8)</td><td>n = 370, 48 (8)</td><td>&lt;0.001</td></tr><tr><td>Academic performance at 7 year</td><td></td><td></td><td>&lt;0.001</td></tr><tr><td>- unknown</td><td>494 (24.7)</td><td>162 (27.1)</td><td></td></tr><tr><td>- No difficulties</td><td>1204 (60.1)</td><td>281 (47.1)</td><td></td></tr><tr><td>- Academic difficulties</td><td>304 (15.2)</td><td>154 (25.8)</td><td></td></tr></tbody></table>

< 0.001) and with a lower birth weight Z-score (p = 0.022) (Table 1).

School behaviour at age 7 was known for 1943 of the 2599 children in standard schools. The 656 children without information about academic difficulties were more often from lower socioeconomic status families (p < 0.001), less frequently breastfeed at discharge (p < 0.001), more likely to have severe cerebral lesions (p = 0.009), and had a lower ASQ scores at 18 (p = 0.005) and 24 months (p = 0.008), and lower GSA

score at age 5 (p < 0.001) (Supplemental Table S1). At age 7, academic difficulties were observed in 458/1943 (23.6 %) children. Lower gestational age (p < 0.001), lower birth weight Z-score (p < 0.001), male sex (p < 0.001), survival with severe neonatal morbidities (severe cerebral lesions (p < 0.001), bronchodysplasia at 36 weeks of post-menstrual age (p < 0.001)) were all strongly associated with academic difficulties (Table 2). ASQ scores between 18 months and 60 months

<caption>**Table 2**</caption>

Perinatal characteristics, Age and Stages Questionnaires (ASQ) score from 18 months to 60 months, and Global Scholar Adaptation score (GSA) at 5 in children with or without academic difficulties at age 7.

<table><thead><tr><th>Characteristics</th><th>Without academic<br>Difficulties at 7-year</th><th>With academic<br>Difficulties at 7-year</th><th>p</th></tr></thead><tbody><tr><td>Recognition of disability by MDPH</td><td>N = 1485</td><td>N = 458</td><td></td></tr><tr><td>Socio-economic status</td><td>19 (1.2)</td><td>68 (14.8)</td><td>&lt;0.001</td></tr><tr><td>- Favorable</td><td>401 (27.0)</td><td>90 (19.7)</td><td>0.015</td></tr><tr><td>- intermediate</td><td>863 (58.1)</td><td>288 (62.9)</td><td></td></tr><tr><td>- low</td><td>188 (12.7)</td><td>69 (15.1)</td><td></td></tr><tr><td>- Unknown</td><td>33 (2.2)</td><td>11 (2.4)</td><td></td></tr><tr><td>Male</td><td>752 (50.6)</td><td>271 (59.2)</td><td>0.001</td></tr><tr><td>Gestational age</td><td></td><td></td><td>&lt;0.001</td></tr><tr><td>- 24-26 weeks</td><td>112 (7.5)</td><td>53 (11.6)</td><td></td></tr><tr><td>- 27-28 weeks</td><td>228 (15.4)</td><td>97 (21.2)</td><td></td></tr><tr><td>- 29-30 weeks</td><td>376 (25.3)</td><td>130 (28.4)</td><td></td></tr><tr><td>- 30-31 weeks</td><td>769 (51.8)</td><td>178 (38.9)</td><td></td></tr><tr><td>Birth weight (g)</td><td>1385 (385)</td><td>1270 (460)</td><td>&lt;0.001</td></tr><tr><td>Birth weight score</td><td>-0.18 (1.00)</td><td>-0.37 (1.07)</td><td>&lt;0.001</td></tr><tr><td>Multiple pregnancy</td><td>512 (34.5)</td><td>154 (33.6)</td><td>0.74</td></tr><tr><td>Bronchopulmonary dysplasia</td><td>80 (5.4)</td><td>53 (11.6)</td><td>&lt;0.001</td></tr><tr><td>Severe cerebral lesions</td><td>25 (1.7)</td><td>22 (4.8)</td><td>&lt;0.001</td></tr><tr><td>Breastfeeding at discharge</td><td>104 (20.1)</td><td>343 (23.1)</td><td>&lt;0.03</td></tr><tr><td>ASQ at 18 months, corrected age</td><td>n = 761, 229 (39)</td><td>n = 188, 206 (48)</td><td>&lt;0.001</td></tr><tr><td>ASQ at 24 months, corrected age</td><td>n = 1281, 251 (32)</td><td>n = 394, 229 (39)</td><td>&lt;0.001</td></tr><tr><td>ASQ at 36 months</td><td>n = 737, 258 (37)</td><td>n = 206, 230 (48)</td><td>&lt;0.001</td></tr><tr><td>ASQ at 48 months</td><td>n = 1276, 266 (31)</td><td>n = 367, 234 (45)</td><td>&lt;0.001</td></tr><tr><td>ASQ at 60months</td><td>n = 1230, 279 (22)</td><td>n = 342, 251 (41)</td><td>&lt;0.001</td></tr><tr><td>GSA at 5-year</td><td>n = 1280, 51 (7)</td><td>n = 363, 44 (9)</td><td>&lt;0.001</td></tr></tbody></table>

MDPH: Maison Départementale pour les Personnes Handicapées
<caption>**Table 3**</caption>

Relationship between Age Stage Questionnaire (ASQ) at 18, 24 months of corrected age, 3, 4,5 years, Global School Adaptation score (GSA) at 5 years and Academic difficulties or Global School Adaptation score at age 7-year.

<table><thead><tr><th rowspan="2">Risk factors</th><th colspan="3">Correlation<br>with Global School Adaptation score at 7-year</th><th colspan="4">Receiver operating characteristic curves<br>to predict academic difficulties at 7-year</th></tr><tr><th>n</th><th>Rho de Spearman (95 %CI)</th><th>p</th><th>n</th><th>Area under the curve (95 % CI)</th><th>n</th><th>Difference of AUC with the previous curve</th><th>p</th></tr></thead><tbody><tr><td colspan="9"><strong>Among complete cases</strong></td></tr><tr><td>ASQ 18 months</td><td>848</td><td>0.265 (0.200-0.329)</td><td>&lt;0.001</td><td><strong>949</strong></td><td><strong>0.64 (0.60, 0.69)</strong></td><td></td><td></td><td></td></tr><tr><td>AS 24 months</td><td>1417</td><td>0.281 (0.231, 0.329)</td><td>&lt;0.001</td><td>1575</td><td>0.67 (0.64, 0.70)</td><td>949</td><td>0.04 (0.00, 0.08)</td><td>0.079</td></tr><tr><td>ASQ 3-year</td><td>776</td><td>0.258 (0.189, 0.324)</td><td>&lt;0.001</td><td>943</td><td>0.69 (0.65, 0.73)</td><td>815</td><td>0.00 (-0.04, 0.05)</td><td>0.910</td></tr><tr><td>ASQ 4-year</td><td>1407</td><td>0.385 (0.338, 0.430)</td><td>&lt;0.001</td><td>1643</td><td>0.73 (0.70-0.76)</td><td>837</td><td>0.05 (0.01, 0.09)</td><td>0.011</td></tr><tr><td>ASQ 5-year</td><td>1356</td><td>0.393 (0.346, 0.439)</td><td>&lt;0.001</td><td>1572</td><td>0.74 (0.71-0.77)</td><td>1387</td><td>0.03 (0.00, 0.06)</td><td>0.086</td></tr><tr><td>GSA at 5-year</td><td>1427</td><td>0.559 (0.522, 0.595)</td><td>&lt;0.001</td><td>1643</td><td>0.75 (0.72-0.78)</td><td>1429</td><td>0.01 (-0.03, 0.05)</td><td>0.526</td></tr><tr><td colspan="9"><strong>Among imputed cases</strong></td></tr><tr><td>ASQ 18 months</td><td>2599</td><td>0.276</td><td>&lt;0.001</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>ASQ 24 months</td><td>2599</td><td>0.284</td><td>&lt;0.001</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>ASQ 3-year</td><td>2599</td><td>0.304</td><td>&lt;0.001</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>ASQ 4-year</td><td>2599</td><td>0.408</td><td>&lt;0.001</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>ASQ 5-year</td><td>2599</td><td>0.451</td><td>&lt;0.001</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>GSA at 5-year</td><td>2599</td><td>0.588</td><td>&lt;0.001</td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

CI: confidence interval; AUC: area under the curve

<figure><img src="image_4.png" /><figcaption>**Fig. 2.** Multivariable analysis for academic difficulties at age 7-year.</figcaption></figure>

(Model 1) exposition to enter school a year earlier without adjustment. (Model 2) exposition to enter school a year earlier, adjusted for gestational age, sex, birth weight Z-score, socio-economic environment, severe bronchopulmonary dysplasia at 36weeks and severe cerebral lesions. (Model 3) exposition to enter school a year earlier, adjusted for gestational age, sex, birth weight Z-score, socio-economic environment, severe bronchopulmonary dysplasia at 36 weeks, severe cerebral lesions and Ages and Stages Questionaires score at 60 months. The position of each square represents the point estimate of the exposition effect. Horizontal lines represent 95 % confidence intervals. Results are expressed as number of event / number of patients.

were all lower in children with difficulties at age 7, as were sub-scores, domain by domain (Supplemental Table S2).

ASQ scores from 18 months to 5 years of age all showed statistically significant correlations with the GSA score at age 7 and the levels of correlation among imputed cases were similar (Table 3). Each ASQ subscore is also significantly correlated with GSA 7 years (Supplemental Table S3). Academic difficulties at age 7 were predicted by the ASQ score as early as 18 months' corrected age, but with a low accuracy, ROC AUC being less than 0.70. There was a statistically important improvement in the predictive value of the ASQ at 48 months (4 years) of age, with accuracy increasing to give an AUC of 0.73 (0.70 - 0.75) (Table 2).

Starting school a year earlier than expected during pregnancy was associated with an increase risk for academic difficulties (p < 0.001): the rate of academic difficulties at age 7 is 35.4 % (154/435) in exposed group versus 20.2 % (304/1508) in non-exposed group. This association was remained evident after adjustment for perinatal and neonatal characteristics, and the ASQ score at 5-year of age with a relative risk of 1.83 (95 % confidence interval, 1.52 - 2.22). When we searched an

interaction between ASQ score at 5-year and Global school adaptation score, we observed a significant interaction (p < 0.001). Associations seen using imputed data were similar to those seen among complete cases (Fig. 2). Path analysis is represented on Supplemental Figure S1. Starting school a year earlier and ASQ at 5 year-old were independently associated with GSA at 7 years of age: standardized β = -0.15 (95 %CI:-0.10;-0.20) and 0.40 (95 %CI: 0.35;0.45) respectively, whereas the association between starting school a year earlier and academic difficulties was partially mediated by GSA at 5 years of age.

## 4. Discussion

In this large population-based prospective geographical cohort of French very preterm infants, we confirmed that starting school according to policies based exclusively on birth date and thus a year earlier than would otherwise be expected during pregnancy is associated with a 70 % increase in the risk of academic difficulties at age seven in comparison with the non-exposed group of children born preterm. This association is independent of neurodevelopment at 5 years of age, which is
itself strongly associated with academic difficulties at age seven but not with the exposure to start school a year early.

The months of birth associated with starting school a year earlier than would have been estimated during the pregnancy are, In France, mainly November and December whereas in the United Kingdom they are July and August [11,18]; this is due to differences between the time of the school year in these two countries. Despite this difference, in both cases, the association between starting school a year earlier than expected and subsequent academic difficulties has been observed, suggesting there is a true link. A similar effect has also been observed for children born at term in France, with those born at the end of the year having lower school performance [12]. Indeed, month of birth was the variable leading to the largest differences for school abilities after socioeconomic background, suggesting that high-level cognitive abilities are less mature at school entry amongst those who are at the younger end of the school admission year.

In our study, starting school one year earlier than expected was associated with academic difficulties at age seven, independent of which earlier stage of neurodevelopment was examined with the ASQ. In this cohort, this association appears to be mediated by poorer school adaptation at five years of age. This probable difficult initial adaptation is then reflected in poorer academic performance at ages seven. These findings suggest that preterm birth is not a "developmental shortcut" and that the notion of corrected age should not stop at 2 years as is currently the case.

We believe that delayed school entry – when admission is based on the expected date of delivery and not on the date of birth – should be advocated. If this were the case, academic difficulties are likely to be substantially attenuated. Such an approach seems logically consistent with avoiding the “double disadvantage” [18] suffered by these very preterm born children, which is known to be a risk factor for poor school achievement. Nevertheless, the impact of delayed time to preschool entry should be tempered – and probably not modified at all – as it is well demonstrated that inclusion in nurseries improve psycho-social abilities of the children (i.e. cognitive, emotional and social skills). Educational authorities should therefore allow individually-based decisions by informed parents to delay only school (and not preschool) entry.

The main limitation of this study is the use of the ASQ score to monitor neurodevelopment at different ages during the longitudinal follow-up. The ASQ score is obtained from parental questionnaires which allows us to approximate the development of gross developmental modalities (communication abilities, gross motor skills, fine motor skills, problem solving abilities and personal-social skills) but is insufficient to assess specific cognitive abilities that are associated with academic difficulties. The low sensitivity to predict academic difficulties at 7 years of age using the ASQ is notable in our study. Another limitation is the absence of other potential confounding factors for which data were not available, but we believe we accounted for the most important confounders (specifically, severe neonatal morbidities as well as family socio-economic status), and residual confounding potentially affects all observational studies. Particular strengths of the LIFT cohort are its population-based geographical cohort design and the prospective enrollment of all infants born preterm in the region between 2007 and 2014. Another strength is the quality of the follow-up and the high (74 %) rate of information about school difficulties in this cohort.

## 5. Conclusion

In children born very preterm, entry into school one year earlier than previously anticipated during pregnancy was associated with an increase of 70 % in academic difficulties at age 7, independent of neurodevelopmental impairments identified by low ASQ scores. These results support the idea of changing rules concerning school entry age for countries where school admission is based exclusively on the date of birth, by permitting children born very preterm to be schooled according

to their corrected age.

## E-component

### Supplemental Figure S1: Path analysis.

**Supplemental Table S1:** Perinatal characteristics, Age and Stages Questionnaires (ASQ) score from 18 months to 60 months, and Global Scholar Adaptation score (GSA) at 5 in children with unknown and known school behaviour at age 7.

**Supplemental Table S2:** Age and Stages Questionnaires (ASQ) scores from 18 months to 60 months in children with or without academic difficulties at age 7.

**Supplemental Table S3:** Correlations between Age and Stages Questionnaires (ASQ) sub-scores from 24 months to 60 months and Global School Adaptation score at 7 years

### Declaration of competing interest

None.

### Supplementary materials

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.arcped.2024.10.007.

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