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Incomplete Gestation Has an Impact on Cognitive Abilities in Autism Spectrum Disorder

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Title: Incomplete Gestation Has an Impact on Cognitive Abilities in Autism Spectrum Disorder
Language: English
Authors: Brayette, Maëva, Saliba, Elie, Malvy, Joëlle, Blanc, Romuald, Ponson, Laura, Tripi, Gabriele, Roux, Sylvie, Bonnet-Brilhault, Frédérique (ORCID 0000-0003-4763-9066)
Source: Journal of Autism and Developmental Disorders. Oct 2019 49(10):4339-4345.
Availability: Springer. Available from: Springer Nature. 233 Spring Street, New York, NY 10013. Tel: 800-777-4643; Tel: 212-460-1500; Fax: 212-348-4505; e-mail: customerservice@springernature.com; Web site: https://link.springer.com/
Peer Reviewed: Y
Page Count: 7
Publication Date: 2019
Document Type: Journal Articles
Reports - Research
Descriptors: Premature Infants, At Risk Persons, Autism, Pervasive Developmental Disorders, Correlation, Individual Characteristics, Child Behavior, Cognitive Ability, Children, Adolescents, Symptoms (Individual Disorders), Cognitive Development, Verbal Ability, Nonverbal Ability
DOI: 10.1007/s10803-019-04105-x
ISSN: 0162-3257
Abstract: Extreme prematurity is known as a risk factor for autism spectrum disorder (ASD). However, the association between prematurity and ASD, for children born moderately and late preterm (MLPT) and those born early term (ET), is less established. This retrospective study aimed to characterize the phenotypic characteristics (i.e. behavioral profile and cognitive abilities) of 254 children with ASD, between 3 and 15 years of age, born MLPT (19 children), ET (60 children) and full term (175 children). MLPT and ET births do not modify ASD symptomatology, but modify cognitive development. The results highlight that incomplete gestation, i.e., MLPT or ET, has a negative impact on both verbal and nonverbal cognitive abilities, in children with neurodevelopmental vulnerability.
Abstractor: As Provided
Entry Date: 2019
Accession Number: EJ1228780
Database: ERIC
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  Value: <anid>AN0138689622;aut01oct.19;2019Sep20.02:15;v2.2.500</anid> <title id="AN0138689622-1">Incomplete Gestation has an Impact on Cognitive Abilities in Autism Spectrum Disorder </title> <p>Extreme prematurity is known as a risk factor for autism spectrum disorder (ASD). However, the association between prematurity and ASD, for children born moderately and late preterm (MLPT) and those born early term (ET), is less established. This retrospective study aimed to characterize the phenotypic characteristics (i.e. behavioral profile and cognitive abilities) of 254 children with ASD, between 3 and 15 years of age, born MLPT (19 children), ET (60 children) and full term (175 children). MLPT and ET births do not modify ASD symptomatology, but modify cognitive development. The results highlight that incomplete gestation, i.e., MLPT or ET, has a negative impact on both verbal and nonverbal cognitive abilities, in children with neurodevelopmental vulnerability.</p> <p>Keywords: Autism spectrum disorder; Moderately and late preterm; Early term; Cognitive abilities</p> <p>Autism spectrum disorder (ASD) is a set of neurodevelopmental disorders characterized by a dyad of symptoms of social problems including the difficulty to communicate and to interact with others, repetitive behaviors as well as limited interests and activities. Behind this clinical heterogeneity lies an extreme degree of neurophysiological, biological, environmental and genetic heterogeneity. Among the multiple risk factors for ASD, obstetric and neonatal ones have been analyzed in various studies, but the association between ASD and prematurity remains inconsistent (Modabbernia et al. [<reflink idref="bib24" id="ref1">24</reflink>]). Several studies have identified prematurity as a risk factor for ASD, highlighting a greater prevalence of ASD in extremely preterm infants, using either parental screening questionnaires to identify ASD (Johnson et al. [<reflink idref="bib16" id="ref2">16</reflink>]) or ASD-specific diagnostic instruments (Joseph et al. [<reflink idref="bib18" id="ref3">18</reflink>]; Verhaeghe et al. [<reflink idref="bib32" id="ref4">32</reflink>]). Recently, a systematic review and meta-analysis reported a significantly elevated prevalence of ASD in preterm infants [25–31 weeks of gestational age (WGA)] (Agrawal et al. [<reflink idref="bib2" id="ref5">2</reflink>]). Other studies have reported mixed results and highlight methodological challenges (Schieve et al. [<reflink idref="bib28" id="ref6">28</reflink>]). The majority of studies used screening tools for ASD (Gray et al. [<reflink idref="bib13" id="ref7">13</reflink>]; Guy et al. [<reflink idref="bib14" id="ref8">14</reflink>]) and definitions of ASD and prematurity, sample size and confounding factors vary significantly between studies. Bowers et al. ([<reflink idref="bib8" id="ref9">8</reflink>]) reported a significant increase of seizure disorders, sleep apnea and attention-deficit hyperactivity disorder (ADHD) in individuals with ASD born preterm, without a significant increase in other psychiatric comorbidities. Finally, despite the growing number of cohort studies examining prematurity as a risk factor in ASD, few studies have looked at phenotypic characteristics in children with ASD born prematurely.</p> <p>Prematurity, defined as birth before 37 WGA (i.e. weeks of amenorrhea), affects 15 million children a year worldwide. It affects 11% of live births, of which approximately 60,000 are in France (Torchin et al. [<reflink idref="bib31" id="ref10">31</reflink>]). The premature group can be divided into three: 85% who are moderately and late preterm (MLPT, 32–36 WGA), 10% who are very preterm (28–31 WGA) and 5% who are extremely preterm (before 28 WGA). Advances in neonatology have led to an increase in both the numbers of premature births and in their survival. However, they have also caused an increase in the prevalence of developmental, neurological and cognitive disorders, associated with adverse outcomes such as academic difficulties and disruption to socio-professional integration in adulthood (Moster et al. [<reflink idref="bib25" id="ref11">25</reflink>]). Extreme prematurity has also been associated with increased risk of developing psychiatric disorders (i.e., ASD, ADHD) and socio-emotional difficulties (Johnson et al. [<reflink idref="bib16" id="ref12">16</reflink>]).</p> <p>Although outcome data for children born very preterm (before 32 WGA) is now abundant, outcomes for children born MLPT and those born early term (ET, 37–38 WGA) remain uncertain—with systematic follow-up lacking in these populations. It has become clear that gestational age represents a continuum of less to more mature (Gill and Boyle [<reflink idref="bib12" id="ref13">12</reflink>]). It is thus imperative to understand the impact of incomplete gestation (i.e., MLPT and ET) on behavioral and cognitive development in a vulnerable population like ASD.</p> <p>The objective of this study is to compare phenotypic characteristics (i.e., behavioral profile and cognitive abilities) between children with ASD born MLPT, ET and FT (after 38 WGA), fully assessed by a multidisciplinary team in a reference center for ASD.</p> <hd id="AN0138689622-2">Methods</hd> <p></p> <hd id="AN0138689622-3">Participants</hd> <p>In total, 274 children with ASD, between 3 and 15 years of age, were recruited from a University Hospital Center specialized in autism and neurodevelopmental disorders which serves a large geographic area in France. Two individuals were born extremely preterm or very preterm (before 32 WGA). Eighteen were excluded due to medical conditions (known genetic disorder, neurological disorder, epilepsy). The final sample included 254 children born MLPT (32–36 WGA), ET (37–38 WGA) or FT (> 38 WGA). The mean age at assessment was 7 years 7 months, ranging between 3 years 1 month and 15 years 11 months (SD = 3 years 1 month).</p> <hd id="AN0138689622-4">Procedure</hd> <p>Clinical data, including behavioral and cognitive evaluation, were collected from medical records, stored in a bio-clinical database. This was approved by CNIL, the French data protection authority.</p> <hd id="AN0138689622-5">Measures</hd> <p>Children were fully assessed by a specialized, multidisciplinary team (child psychiatrists, clinical psychologists, speech therapists, child neurologists, psychomotor therapists and nurses). ASD was diagnosed using standardized instruments in all subjects. They met the current ICD-10 (WHO [<reflink idref="bib37" id="ref14">37</reflink>]) criteria for pervasive developmental disorders. Standardized instruments (ADI-R and ADOS) (Lord et al. [<reflink idref="bib21" id="ref15">21</reflink>], [<reflink idref="bib22" id="ref16">22</reflink>]) complemented the diagnosis of ASD.</p> <p>Behavioral assessment was carried out using the following three validated tools. The Childhood Autism Rating Scale (CARS) (Schopler et al. [<reflink idref="bib29" id="ref17">29</reflink>]) is a simple diagnostic tool (15 sub-scales rated on a 4-point scale), allowing an objective and quantifiable assessment of abnormal behaviors in ASD; the total raw score evaluates the severity of autistic symptoms. The Revised Behavior Summarized Evaluation Scale (BSE-R, 29 items rated on a 5-point scale) (Barthelemy et al. [<reflink idref="bib4" id="ref18">4</reflink>]) is a composite scale for quantitative assessment of behavioral difficulties of children with ASD followed up in their daily environment; the BSE-R score (sum of 13 items labelled "Interaction Disorder") quantifies the severity of autistic behaviors. The Repetitive and Restricted Behavior scale (RRB, 35 items rated on a 5-point scale) (Bourreau et al. [<reflink idref="bib7" id="ref19">7</reflink>]) evaluates four specific meaningful dimensions in ASD: sensorimotor stereotypies (RRB-F1), reaction to change (RRB-F2), restricted behaviors (RRB-F3) and modulation insufficiency (RRB-F4). Raters were trained on these scales and were experienced with children with ASD; clinical psychologists rated the CARS and nurses who take care of the child rated the BSE-R and RRB scales.</p> <p>Cognitive assessment (verbal and nonverbal quotients, VQ and nVQ) was carried out using age adapted neuropsychological tests: Wechsler intelligence scales (WPPSI-III (Wechsler [<reflink idref="bib34" id="ref20">34</reflink>]), WPPSI-IV (Wechsler [<reflink idref="bib36" id="ref21">36</reflink>]), WISC-IV (Wechsler [<reflink idref="bib35" id="ref22">35</reflink>])); EDEI-R (Perron-Borelli [<reflink idref="bib27" id="ref23">27</reflink>]), a French cognitive test for children 30 months-9 years of age; Brunet-Lézine test BL-R (Brunet and Lézine [<reflink idref="bib9" id="ref24">9</reflink>]), a French baby-test adapted from Gesell' scales; PEP-3 (Schopler et al. [<reflink idref="bib30" id="ref25">30</reflink>]); McCarthy test (McCarthy [<reflink idref="bib23" id="ref26">23</reflink>]) for preschool children; Social Cognitive Evaluation Battery SCEB (Adrien [<reflink idref="bib1" id="ref27">1</reflink>]) for children with a developmental age between 4 and 24 months. An intellectual disability (ID) was also identified according to ICD-10 criteria, and two categories were retained: mild to moderate and severe to profound ID.</p> <hd id="AN0138689622-6">Statistical Analysis</hd> <p>Analyses were performed using statistical software "Statistica 12, Dell Inc.", using Pearson's χ<sups>2</sups> tests and analyses of variance and covariance (ANOVA, ANCOVA) followed by Tukey's HSD post hoc tests. ANCOVAs were computed using age of assessment as a covariate to take into account the wide range of ages.</p> <hd id="AN0138689622-7">Results</hd> <p></p> <hd id="AN0138689622-8">Neonatal and Demographic Characteristics of the ASD Sample</hd> <p>The sample comprised 19 (7.5%) MLPT, 60 (23.6%) ET and 175 FT (68.9%) children with ASD. This distribution was equivalent to the distribution in the general population of newborns in France (Blondel et al. [<reflink idref="bib5" id="ref28">5</reflink>]) (i.e., MLPT: 6.0%; ET: 23.5%; FT: 70.5%), with no statistically significant difference (χ<sups>2</sups> test of goodness of fit; χ<sups>2</sups>(<reflink idref="bib2" id="ref29">2</reflink>) = 0.33; p = 0.85).</p> <p>In total, 212 (83.5%) children were male, giving a rough gender ratio of 5/1, without significant difference between the three groups (χ<sups>2</sups>(<reflink idref="bib2" id="ref30">2</reflink>) = 0.58; p = 0.75). The sample was therefore representative of the ASD population, with the same gender ratio of 5/1 described previously (Fombonne [<reflink idref="bib11" id="ref31">11</reflink>]). Moreover there was no statistically significant difference between the three groups of children for age at assessment (F(<reflink idref="bib2" id="ref32">2</reflink>, 251) = 0.67; p = 0.51).</p> <p>Family background (i.e. know genetic disorder, psychiatric disorder, epilepsy, learning disorder) did not differ between the three groups of children (χ<sups>2</sups>(<reflink idref="bib2" id="ref33">2</reflink>) = 0.46; p = 0.79). No statistically significant difference was observed between the three groups concerning maternal and paternal ages at birth (F(<reflink idref="bib2" id="ref34">2</reflink>, 160) = 1.49; p = 0.23/F(<reflink idref="bib2" id="ref35">2</reflink>, 152) = 2.74; p = 0.07), presence of gestational infection or diabetes. However, there was a statistically significant difference in type of delivery (χ<sups>2</sups>(<reflink idref="bib2" id="ref36">2</reflink>) = 8.83; p = 0.012) between the three groups of children; with premature and early term babies more likely to encounter complications; but no difference was observed in APGAR score (F(<reflink idref="bib2" id="ref37">2</reflink>, 223) = 1.70; p = 0.18).</p> <p>There was a statistically significant difference in head circumference (HC), weight and height at birth (F(<reflink idref="bib2" id="ref38">2</reflink>, 238) = 11.5; p < 0.0001/F(<reflink idref="bib2" id="ref39">2</reflink>, 250) = 55.57; p < 0.0001/F(<reflink idref="bib2" id="ref40">2</reflink>, 244) = 4.16; p < 0.0001) between the three groups. However, the distribution of HC, weight and height at birth between the three groups was equivalent to that of the general population, using the French Audipog Study (2008); i.e., HC, weight and height z-scores (normalized HCs, weights and heights according to gestational age and sex) were not significantly different between the three groups (F(<reflink idref="bib2" id="ref41">2</reflink>, 238) = 1.03; p = 0.36/F(<reflink idref="bib2" id="ref42">2</reflink>, 250) = 1.09; p = 0.34/F(<reflink idref="bib2" id="ref43">2</reflink>, 244) = 1.32; p = 0.27).</p> <p>The neonatal and demographic characteristics of the ASD sample are represented in Table 1.</p> <p>Neonatal and demographic characteristics of the ASD sample</p> <p> <ephtml> <table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="2" /><th align="left" colspan="2"><p>MLPT</p></th><th align="left" colspan="2"><p>ET</p></th><th align="left" colspan="2"><p>FT</p></th><th align="left" colspan="2"><p>Total</p></th></tr><tr><th align="left"><p>N</p></th><th align="left"><p>n (%)</p></th><th align="left"><p>N</p></th><th align="left"><p>n (%)</p></th><th align="left"><p>N</p></th><th align="left"><p>n (%)</p></th><th align="left"><p>N</p></th><th align="left"><p>n (%)</p></th></tr></thead><tbody><tr><td align="left"><p>Gender: male</p></td><td align="left"><p>19</p></td><td align="left"><p>15 (79.0%)</p></td><td align="left"><p>60</p></td><td align="left"><p>49 (81.7%)</p></td><td align="left"><p>175</p></td><td align="left"><p>148 (84.6%)</p></td><td align="left"><p>254</p></td><td align="left"><p>212 (83.5%)</p></td></tr><tr><td align="left"><p>Family background</p></td><td align="left"><p>19</p></td><td align="left"><p>8 (42.1%)</p></td><td align="left"><p>55</p></td><td align="left"><p>27 (49.1%)</p></td><td align="left"><p>161</p></td><td align="left"><p>81 (50.3%)</p></td><td align="left"><p>235</p></td><td align="left"><p>116 (49.4%)</p></td></tr><tr><td align="left"><p>Gestational diabetes</p></td><td align="left"><p>18</p></td><td align="left"><p>1 (5.6%)</p></td><td align="left"><p>54</p></td><td align="left"><p>4 (7.4%)</p></td><td align="left"><p>161</p></td><td align="left"><p>9 (5.6%)</p></td><td align="left"><p>233</p></td><td align="left"><p>14 (6.0%)</p></td></tr><tr><td align="left"><p>Gestational infection</p></td><td align="left"><p>17</p></td><td align="left"><p>0 (0%)</p></td><td align="left"><p>54</p></td><td align="left"><p>1 (1.8%)</p></td><td align="left"><p>159</p></td><td align="left"><p>7 (4.4%)</p></td><td align="left"><p>230</p></td><td align="left"><p>8 (3.5%)</p></td></tr><tr><td align="left"><p>Distocic delivery</p></td><td align="left"><p>16</p></td><td align="left"><p>9 (56.3%)</p></td><td align="left"><p>55</p></td><td align="left"><p>27 (49.1%)</p></td><td align="left"><p>169</p></td><td align="left"><p>52 (30.8%)</p></td><td align="left"><p>240</p></td><td align="left"><p>88 (36.7%)</p></td></tr></tbody></table> </ephtml> </p> <p>Neonatal and demographic characteristics of the ASD sample</p> <p> <ephtml> <table frame="hsides" rules="groups"><thead><tr><th align="left" /><th align="left"><p>N</p></th><th align="left"><p>Mean (SD)</p></th><th align="left"><p>N</p></th><th align="left"><p>Mean (SD)</p></th><th align="left"><p>N</p></th><th align="left"><p>Mean (SD)</p></th><th align="left"><p>N</p></th><th align="left"><p>Mean (SD)</p></th></tr></thead><tbody><tr><td align="left"><p>Birth weight (kg)</p></td><td align="left"><p>19</p></td><td align="left"><p>2.30 (0.49)</p></td><td align="left"><p>60</p></td><td align="left"><p>3.14 (0.52)</p></td><td align="left"><p>174</p></td><td align="left"><p>3.42 (0.42)</p></td><td align="left"><p>253</p></td><td align="left"><p>3.27 (0.54)</p></td></tr><tr><td align="left"><p>Birth weight (z-score)</p></td><td align="left"><p>19</p></td><td align="left"><p>– 0.25 (1.26)</p></td><td align="left"><p>60</p></td><td align="left"><p>0.11 (1.20)</p></td><td align="left"><p>174</p></td><td align="left"><p>– 0.09 (0.99)</p></td><td align="left"><p>253</p></td><td align="left"><p>– 0.06 (1.06)</p></td></tr><tr><td align="left"><p>Birth height (cm)</p></td><td align="left"><p>19</p></td><td align="left"><p>45.2 (2.3)</p></td><td align="left"><p>58</p></td><td align="left"><p>49.2 (2.4)</p></td><td align="left"><p>170</p></td><td align="left"><p>50.5 (1.9)</p></td><td align="left"><p>247</p></td><td align="left"><p>49.8 (2.5)</p></td></tr><tr><td align="left"><p>Birth height (z-score)</p></td><td align="left"><p>19</p></td><td align="left"><p>– 0.26 (1.07)</p></td><td align="left"><p>58</p></td><td align="left"><p>0.19 (1.14)</p></td><td align="left"><p>170</p></td><td align="left"><p>0.07 (1.03)</p></td><td align="left"><p>247</p></td><td align="left"><p>0.07 (1.06)</p></td></tr><tr><td align="left"><p>Birth HC<sup>a</sup> (cm)</p></td><td align="left"><p>18</p></td><td align="left"><p>32.7 (4.6)</p></td><td align="left"><p>58</p></td><td align="left"><p>34.4 (1.60)</p></td><td align="left"><p>165</p></td><td align="left"><p>34.9 (1.4)</p></td><td align="left"><p>241</p></td><td align="left"><p>34.6 (1.9)</p></td></tr><tr><td align="left"><p>Birth HC<sup>a</sup> (z-score)</p></td><td align="left"><p>18</p></td><td align="left"><p>0.31 (2.89)</p></td><td align="left"><p>58</p></td><td align="left"><p>0.20 (1.14)</p></td><td align="left"><p>165</p></td><td align="left"><p>– 0.02 (1.04)</p></td><td align="left"><p>241</p></td><td align="left"><p>0.06 (1.28)</p></td></tr><tr><td align="left"><p>APGAR score</p></td><td align="left"><p>17</p></td><td align="left"><p>9.2 (1.6)</p></td><td align="left"><p>54</p></td><td align="left"><p>9.7 (0.8)</p></td><td align="left"><p>155</p></td><td align="left"><p>9.7 (1.0)</p></td><td align="left"><p>226</p></td><td align="left"><p>9.7 (1.0)</p></td></tr><tr><td align="left"><p>Maternal age at birth (years)</p></td><td align="left"><p>11</p></td><td align="left"><p>27.9 (5.8)</p></td><td align="left"><p>41</p></td><td align="left"><p>30.9 (4.8)</p></td><td align="left"><p>111</p></td><td align="left"><p>29.9 (5.3)</p></td><td align="left"><p>163</p></td><td align="left"><p>30.1 (5.2)</p></td></tr><tr><td align="left"><p>Paternal age at birth (years)</p></td><td align="left"><p>9</p></td><td align="left"><p>32.5 (5.6)</p></td><td align="left"><p>38</p></td><td align="left"><p>36.6 (8.3)</p></td><td align="left"><p>108</p></td><td align="left"><p>33.6 (6.9)</p></td><td align="left"><p>155</p></td><td align="left"><p>34.3 (7.3)</p></td></tr><tr><td align="left"><p>Age at assessment (month)</p></td><td align="left"><p>19</p></td><td align="left"><p>84.0 (32.7)</p></td><td align="left"><p>60</p></td><td align="left"><p>87.9 (38.7)</p></td><td align="left"><p>175</p></td><td align="left"><p>92.5 (37.7)</p></td><td align="left"><p>254</p></td><td align="left"><p>90.8 (37.6)</p></td></tr></tbody></table> </ephtml> </p> <p> <sups>a</sups>Head circumference</p> <hd id="AN0138689622-9">Behavioral Assessment</hd> <p>The average score for the CARS was 31.6 (SD = 6.1) and for the BSE-R was 33.9 (SD = 11.1). The average RRB scores were 19.0 (SD = 6.2) for RRB-F1, 10.3 (SD = 3.7) for RRB-F2, 14.2 (SD = 4.7) for RRB-F3 and 12.6 (SD = 4.2) for RRB-F4. When comparing children born MLPT, ET and FT, there was no statistically significant difference for the CARS (F(<reflink idref="bib2" id="ref44">2</reflink>, 250) = 1.98; p = 0.14), the BSE-R (F(<reflink idref="bib2" id="ref45">2</reflink>, 250) = 1.90; p = 0.15) or the RRB scores (RRB-F1: F(<reflink idref="bib2" id="ref46">2</reflink>, 250) = 0.27; p = 0.77/RRB-F2: F(<reflink idref="bib2" id="ref47">2</reflink>, 250) = 0.24; p = 0.79/RRB-F3: F(<reflink idref="bib2" id="ref48">2</reflink>, 250) = 0.49; p = 0.61/RRB-F4: F(<reflink idref="bib2" id="ref49">2</reflink>, 250) = 2.22; p = 0.11) (Fig. 1). The same results were obtained when age of assessment was not introduced as a covariate.</p> <p>Graph: Fig. 1Mean scores (with standard error of the mean) of the behavioral tools</p> <hd id="AN0138689622-10">Cognitive Assessment</hd> <p>Neuropsychological tests were carried out according to the cognitive abilities of each child: 94 Wechsler scales, 56 EDEI, 70 BL-R, 15 PEP-3, 4 McCarthy tests, 15 SCEB; with similar distributions in the three groups MLPT, ET and FT.</p> <p>No significant difference was found for the presence or absence of an ID between the three groups of children: MLPT, ET and FT (χ<sups>2</sups>(<reflink idref="bib2" id="ref50">2</reflink>) = 5.78; p = 0.06). However, ID was significantly severe to profound in premature and ET children, compared to those born FT (χ<sups>2</sups>(<reflink idref="bib2" id="ref51">2</reflink>) = 9.55; p = 0.008). Among the three groups, a severe to profound ID was noted in 36.8, 26.7 and 13.7% of children respectively (Table 2).</p> <p>Cognitive characteristics of the ASD sample according to Intellectual Deficiency (ID)</p> <p> <ephtml> <table frame="hsides" rules="groups"><thead><tr><th align="left" /><th align="left"><p>MLPT (n = 19)</p></th><th align="left"><p>ET (n = 60)</p></th><th align="left"><p>FT (n = 175)</p></th><th align="left"><p>Total (n = 254)</p></th></tr></thead><tbody><tr><td align="left"><p>ID</p></td><td align="left"><p>15 (78.9%)</p></td><td align="left"><p>45 (75.0%)</p></td><td align="left"><p>106 (60.6%)</p></td><td align="left"><p>166 (65.4%)</p></td></tr><tr><td align="left"><p> Mild to moderate</p></td><td align="left"><p>8 (42.1%)</p></td><td align="left"><p>29 (48.3%)</p></td><td align="left"><p>82 (46.9%)</p></td><td align="left"><p>119 (46.9%)</p></td></tr><tr><td align="left"><p> Severe to profound</p></td><td align="left"><p>7 (36.8%)</p></td><td align="left"><p>16 (26.7%)</p></td><td align="left"><p>24 (13.7%)</p></td><td align="left"><p>47 (18.5%)</p></td></tr><tr><td align="left"><p>No ID</p></td><td align="left"><p>4 (21.1%)</p></td><td align="left"><p>15 (25.0%)</p></td><td align="left"><p>69 (39.4%)</p></td><td align="left"><p>88 (34.6%)</p></td></tr></tbody></table> </ephtml> </p> <p>In the whole sample, the average VQ and nVQ were 51.1 (SD = 31.0) and 66.5 (SD = 29.0) respectively. A statistically significant difference amongst the three groups of children was found for nVQ (F(<reflink idref="bib2" id="ref52">2</reflink>, 250) = 4.96; p = 0.008); post hoc tests showed that MLPT and ET children had significantly lower nVQ compared to those born FT (p = 0.049, p = 0.026), at 54.2 (SD = 28.8) and 59.3 (SD = 27.1) versus 70.4 (SD = 28.8) respectively. For VQ, statistically significant difference was found between the three groups (F(<reflink idref="bib2" id="ref53">2</reflink>, 250) = 3.63; p = 0.028); post hoc tests showed that the ET children had significantly lower VQ compared to FT (p = 0.033), or 43.7 (SD = 26.5) versus 54.8 (SD = 32.3) (Fig. 2).</p> <p>Graph: Fig. 2Mean verbal (VQ) and nonverbal quotients (nVQ) (with standard error of the mean); *p ≤ 0.05</p> <hd id="AN0138689622-11">Discussion</hd> <p>This retrospective study aimed to compare the behavioral profile and cognitive abilities between children with ASD referred to a reference center for ASD, born after 31 WGA, i.e., MLPT (32–36 WGA), ET (37–38 WGA) or FT (> 38 WGA). The observation of similar rates of MLPT and ET in this sample of children with ASD and the general population of newborns does not indicate that it is a causal risk factor. However, an incomplete birth, i.e., MLPT or ET, significantly modifies the cognitive abilities of children with ASD. In contrast, for all behavioral assessments, there was no statistically significant difference between the three groups of children. It should be noted that all results took into account age of assessment.</p> <p>Using tools which allow a subtle and accurate behavioral assessment, our study has shown that the expression of autistic traits is likely to be identical in premature children and in children with normal gestational age, suggesting an autistic profile independent of term. Although non-significant, CARS and BSE-R scores (i.e., severity of autistic symptoms) increased according to prematurity. This effect can be related to intellectual disability, potentially associated with ASD, that may exacerbate the expression of autistic symptoms. No significant difference was observed for the four main domains of RRB scale, specifying the second symptom dimension of ASD. Furthermore, among them, reactivity to change (i.e., RRB-F2 score) has been described as a specific marker of autism, independent of severity of autistic symptoms and intellectual abilities (Bourreau et al. [<reflink idref="bib7" id="ref54">7</reflink>]). Thus, a moderately to late premature birth would not worsen ASD symptomatology. In keeping with our results, Bowers et al. ([<reflink idref="bib8" id="ref55">8</reflink>]) did not find any phenotypic differences between individuals with ASD born prematurely (< 37 WGA) and those born at full term, regarding the diagnostic subtypes of ASD. On the other hand, Movsas and Paneth ([<reflink idref="bib26" id="ref56">26</reflink>]) found significantly higher autistic severity scores in premature children with ASD (< 37 WGA) than in children with ASD born full term. However, the conclusions of this last study must be weighted, due to the use of screening instruments as part of a voluntary parental participation in a web-based registry. Elevated prevalence of ASD is now admitted for very preterm birth (25–31 WGA) (Agrawal et al. [<reflink idref="bib2" id="ref57">2</reflink>]) suggesting that the critical period for atypical brain development underlying autism symptoms occurs before the MLPT period. Thus, recent study on brain growth trajectory during pre and postnatal periods suggests that atypical neurodevelopment would start or be observable after the 22nd week of amenorrhea. These results can help to target key embryological steps in the pathophysiological process leading to the development of ASD (Bonnet-Brilhault et al. [<reflink idref="bib6" id="ref58">6</reflink>]).</p> <p>Regarding cognitive level, we did not find significant between-group differences in the presence or absence of an ID. However, severe to profound ID was more frequent in the MLPT (36.8%) and ET (26.7%) in comparison to the FT group (13.7%). This is concordant with the results of Voigt et al. ([<reflink idref="bib33" id="ref59">33</reflink>]) in a sample of 232 toddlers born very preterm, MLPT or FT. Our study revealed a gradual worsening of the verbal and nonverbal quotients with lowering of gestational age, suggesting a dose–response effect of prematurity on cognitive abilities. Our results are consistent with those of Dueker et al. ([<reflink idref="bib10" id="ref60">10</reflink>]), who observed in a country-wide developmental screening program, a gradual reduction in the overall risk of developmental delay for each week of additional gestation after 35 WGA. Recently, a meta-analysis and systematic review (Allotey et al. [<reflink idref="bib3" id="ref61">3</reflink>]) on cognitive performances of children born preterm pointed out that nonverbal scores were significantly lower in children born MLPT compared with those born at term.</p> <p>Children born MLPT and ET were often considered "born at term" due to their perceived maturity. However, recent studies have highlighted that the unfavorable outcome of infants, associated with extreme preterm, extended beyond 32–36 WGA (Gill and Boyle [<reflink idref="bib12" id="ref62">12</reflink>]). Johnson et al. ([<reflink idref="bib17" id="ref63">17</reflink>]) showed that MLPT infants were twice as likely to have a neurodevelopmental disability at 2 years of age compared to those born ET, notably in the cognitive domain. More specifically, Kerstjens et al. ([<reflink idref="bib19" id="ref64">19</reflink>]) found that, in the first 2 years of development, the fine motor, communication and social domains were more often subject to the effects of gestational age for moderate preterm infants than the other developmental areas. These results challenge common perceptions regarding the fate of babies born during a gestation period considered wrongly as "at term". More recently, Heuvelman et al. ([<reflink idref="bib15" id="ref65">15</reflink>]) suggested that birth at non-optimal gestational duration may be linked causally with greater risk of intellectual disability in the absence of common genetic causes; risk also varied within the term period and was lowest when the child was born at 40–41 completed weeks of gestation. Developmental disorders occurring in the last 6 weeks of gestation, described as a critical period for growth and brain development, should not be underestimated (Kugelman and Colin [<reflink idref="bib20" id="ref66">20</reflink>]).</p> <p>This retrospective study is not a population-based epidemiological study. It was limited to the children with ASD referred to a single center, with a possible over-representation of severe cases of ASD. However, the strength of this analysis lies primarily in the large number of children with ASD diagnosed using standardized criteria and fully examined and assessed with common guidelines, by the same specialized multidisciplinary team.</p> <p>In conclusion, this study highlights that incomplete gestation has an impact on both verbal and nonverbal cognitive abilities in children with neurodevelopmental vulnerability, without changing the ASD symptomatology. It also emphasizes the importance of the last weeks of gestation on brain development.</p> <hd id="AN0138689622-12">Funding</hd> <p>No funding was received.</p> <hd id="AN0138689622-13">Acknowledgments</hd> <p>None.</p> <hd id="AN0138689622-14">Author Contributions</hd> <p>MB conducted the initial analyses, contributed to interpretation of data and draft the initial manuscript; ES interpreted data and help to revised the manuscript critically; JM, RB, LP and GT participated to acquisition of data and contributed to interpretation of data; SR coordinated and supervised data analyses and help to draft the manuscript; FBB conceptualized, designed and coordinated the study, interpreted data, draft and revised the manuscript critically. All authors read and approved the final manuscript as submitted.</p> <hd id="AN0138689622-15">Compliance with Ethical Standards</hd> <p></p> <hd id="AN0138689622-16">Conflict of interest</hd> <p>All authors declare that they have no conflict of interest.</p> <hd id="AN0138689622-17">Ethical Approval</hd> <p>All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Ethical approval was obtained from the Ethics Committee of the Tours University Hospital (No. 2016-009).</p> <hd id="AN0138689622-18">Informed Consent</hd> <p>According to French research regulation (Article L1122-1-1 of the French Public Health Code), written informed consent is not required for clinical database obtained via non interventional research and declared to the CNIL, the French data protection authority.</p> <hd id="AN0138689622-19">Publisher's Note</hd> <p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p> <ref id="AN0138689622-20"> <title> References </title> <blist> <bibl id="bib1" idref="ref27" type="bt">1</bibl> <bibtext> Adrien JL. Batterie d'évaluation cognitive et socio-émotionnelle ECPA. 2007: London; Pearson</bibtext> </blist> <blist> <bibl id="bib2" idref="ref5" type="bt">2</bibl> <bibtext> Agrawal S, Rao SC, Bulsara MK, Patole SK. 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  Data: Incomplete Gestation Has an Impact on Cognitive Abilities in Autism Spectrum Disorder
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  Data: <searchLink fieldCode="DE" term="%22Premature+Infants%22">Premature Infants</searchLink><br /><searchLink fieldCode="DE" term="%22At+Risk+Persons%22">At Risk Persons</searchLink><br /><searchLink fieldCode="DE" term="%22Autism%22">Autism</searchLink><br /><searchLink fieldCode="DE" term="%22Pervasive+Developmental+Disorders%22">Pervasive Developmental Disorders</searchLink><br /><searchLink fieldCode="DE" term="%22Correlation%22">Correlation</searchLink><br /><searchLink fieldCode="DE" term="%22Individual+Characteristics%22">Individual Characteristics</searchLink><br /><searchLink fieldCode="DE" term="%22Child+Behavior%22">Child Behavior</searchLink><br /><searchLink fieldCode="DE" term="%22Cognitive+Ability%22">Cognitive Ability</searchLink><br /><searchLink fieldCode="DE" term="%22Children%22">Children</searchLink><br /><searchLink fieldCode="DE" term="%22Adolescents%22">Adolescents</searchLink><br /><searchLink fieldCode="DE" term="%22Symptoms+%28Individual+Disorders%29%22">Symptoms (Individual Disorders)</searchLink><br /><searchLink fieldCode="DE" term="%22Cognitive+Development%22">Cognitive Development</searchLink><br /><searchLink fieldCode="DE" term="%22Verbal+Ability%22">Verbal Ability</searchLink><br /><searchLink fieldCode="DE" term="%22Nonverbal+Ability%22">Nonverbal Ability</searchLink>
– Name: DOI
  Label: DOI
  Group: ID
  Data: 10.1007/s10803-019-04105-x
– Name: ISSN
  Label: ISSN
  Group: ISSN
  Data: 0162-3257
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Extreme prematurity is known as a risk factor for autism spectrum disorder (ASD). However, the association between prematurity and ASD, for children born moderately and late preterm (MLPT) and those born early term (ET), is less established. This retrospective study aimed to characterize the phenotypic characteristics (i.e. behavioral profile and cognitive abilities) of 254 children with ASD, between 3 and 15 years of age, born MLPT (19 children), ET (60 children) and full term (175 children). MLPT and ET births do not modify ASD symptomatology, but modify cognitive development. The results highlight that incomplete gestation, i.e., MLPT or ET, has a negative impact on both verbal and nonverbal cognitive abilities, in children with neurodevelopmental vulnerability.
– Name: AbstractInfo
  Label: Abstractor
  Group: Ab
  Data: As Provided
– Name: DateEntry
  Label: Entry Date
  Group: Date
  Data: 2019
– Name: AN
  Label: Accession Number
  Group: ID
  Data: EJ1228780
PLink https://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=eric&AN=EJ1228780
RecordInfo BibRecord:
  BibEntity:
    Identifiers:
      – Type: doi
        Value: 10.1007/s10803-019-04105-x
    Languages:
      – Text: English
    PhysicalDescription:
      Pagination:
        PageCount: 7
        StartPage: 4339
    Subjects:
      – SubjectFull: Premature Infants
        Type: general
      – SubjectFull: At Risk Persons
        Type: general
      – SubjectFull: Autism
        Type: general
      – SubjectFull: Pervasive Developmental Disorders
        Type: general
      – SubjectFull: Correlation
        Type: general
      – SubjectFull: Individual Characteristics
        Type: general
      – SubjectFull: Child Behavior
        Type: general
      – SubjectFull: Cognitive Ability
        Type: general
      – SubjectFull: Children
        Type: general
      – SubjectFull: Adolescents
        Type: general
      – SubjectFull: Symptoms (Individual Disorders)
        Type: general
      – SubjectFull: Cognitive Development
        Type: general
      – SubjectFull: Verbal Ability
        Type: general
      – SubjectFull: Nonverbal Ability
        Type: general
    Titles:
      – TitleFull: Incomplete Gestation Has an Impact on Cognitive Abilities in Autism Spectrum Disorder
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Brayette, Maëva
      – PersonEntity:
          Name:
            NameFull: Saliba, Elie
      – PersonEntity:
          Name:
            NameFull: Malvy, Joëlle
      – PersonEntity:
          Name:
            NameFull: Blanc, Romuald
      – PersonEntity:
          Name:
            NameFull: Ponson, Laura
      – PersonEntity:
          Name:
            NameFull: Tripi, Gabriele
      – PersonEntity:
          Name:
            NameFull: Roux, Sylvie
      – PersonEntity:
          Name:
            NameFull: Bonnet-Brilhault, Frédérique
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 01
              M: 10
              Type: published
              Y: 2019
          Identifiers:
            – Type: issn-print
              Value: 0162-3257
          Numbering:
            – Type: volume
              Value: 49
            – Type: issue
              Value: 10
          Titles:
            – TitleFull: Journal of Autism and Developmental Disorders
              Type: main
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