Table 1.

Included studies for term born children.

References	Study type	Definition of fetal growth	Participants	Neurology/Neuromotor function	Cognitive/behavior Outcome measure	Cognitive/behavior findings	Conclusion
Beukers (29)	Prospective follow up study comparing term FGR and term AGA children	BWt ratio <10th centile; BWR calculated as BW/expected weight for GA, using the Gardosi customized fetal growth chart 50th centile values (30)	96 term children with FGR; 32 term and birthweight ≥ 2,500 g BY 200–2003 Age at assessment: 12 y	Not assessed	Child assessment: IQ–Wechsler Intelligence Scale for Children (WISC). Executive Functioning– Impulse control (stop task); Verbal working memory (WISC Digit span); Visual working memory (Spatial Temporal Span of the Amsterdam Neuropsychological Tasks–ANT); set shifting (Shifting visual set–ANT); planning (Tower of London). Parent ratings:- Behavior Rating Inventory of Executive Functions Dutch version (BRIEF)	No difference in IQ, executive functioning, attention or parent rating of EF between FGR and controls. Parent report FGR children more social and attention problems	Neurocognitive outcomes including IQ, executive function, memory and attention comparable in FGR children AGA controls Parent ratings suggested elevated levels of social and attention problems
Emond (31)	Population based cohort, north east Brazil	Low BW: BW 1,500–2,499 g (n = 202) Appropriate BW: BW 3,000–3,499 g (n = 212); matched for sex and month of birth	Born ≥37 wGA BY 1993–1994 Age at assessment: 8 y 40% of original cohort assessed (n = 83 low birth weight; n = 81 appropriate birth weight) Analyses adjusted for socio-economic background variables Additional analyses performed to examine head size at birth, age 6 m and 8 y with IQ at age 8 y	Neurological status (muscle tone, focal neurological signs) M-ABC for neuromotor function Findings: No significant difference in frequency of focal neurological signs	WISC-III for Full Scale IQ, Performance IQ, Verbal IQ Memory (auditory and verbal) assessed with WISC-III subtests TeaCH for attention abilities SDQ for behavior	After controlling for socio-economic background no significant difference between BW groups for IQ scores, memory function Significant differences between BW groups for dynamic balance skills and eye-hand coordination, selective attention; peer relationships Head size at birth, age 6 m and 8 y significantly associated with IQ age 8 y	Low birth weight not associated with general cognitive abilities, except selective attention. Neuromotor function poorer in low birth weight children. Post-natal head growth more important than birth weight.
Fattal-Valevski (32)	Prospective follow-up study	BW <10th centile for GA according to Israeli birth weight curves (33); Growth data (weight, height, head circumference) from 1 to 2 y, 2–6 y, and 6–9 y	136 IUGR children BY 1992–2002 Age at assessment: Annual follow-up from birth; current assessment 9–10 y	Neurodevelopmental examination score including soft neurological signs. Score expressed as percentage of optimal items out of the total.	Short term memory, coordination skills; IQ assessed by the Wechsler Intelligence Scale for Children—revised (WISC-R)	BW, BL and GA positively correlated with 9–10 y neurodevelopmental score BW, BL, but not GA, positively correlated with 9–10 y IQ scores Better outcome for those with asymmetric IUGR than symmetric	Correlation of IQ with BW, BL but not GA suggests that there is better outcome for IUGR children delivered early Correlation of GA with neurodevelopmental score, suggests prematurity affects other areas of development
Gale (34)	Prospective cohort study	HC growth–expressed as Standard Deviation Score (SDS), measured at 18 weeks gestation and birth, and 9 y, using the British 1990 growth reference data (35)	221 children assessed at 18 weeks gestation, births, 9 months and 9 years BY 1992–1994 Age at assessment: 9 y	Not assessed	Wechsler Abbreviated Scales of Intelligence (WASI)—Full Scale IQ (FSIQ), Verbal IQ (VIQ) and Performance IQ (PIQ)	No significant associations between head circumference at 18 weeks gestation or birth and 9 years old IQ scores. Post-natal head group was associated with IQ. After adjusting for sex, FSIQ, VIQ and PIQ increased with each SD increase in head circumference up to 9 months, and to 9 years. The highest FSIQ were observed in children who had large increases in HC between birth and 9 months, and a further increase between 9 months and 9 years. This was not linked to maternal or home characteristics other than maternal education	Post-natal brain growth is more important than prenatal brain growth for IQ Post-natal head growth greater in children of mothers educated to degree level, or of higher SES
Gale (36)	Prospective cohort study – the Avon Longitudinal Study of Parents and Children cohort (ALSPAC). The cohort studied is the Children in Focus cohort – a random 10% selected from ALSPAC.	HC growth - measured at birth, 4, 8, 12, 25, 31, 37, 43, 49, 61, and 96 months. HC in analyses –birth, 1, 4, and 8 years—expressed as z scores obtained from the study group. Growth between time points calculated	633 children BY 1991–1992 Age at assessment: 8 y	Not assessed	IQ assessed by Wechsler Intelligence Scale for Children (WISC) at 8 years	Children with larger HC had higher IQ scores For each 1 SD increase in HC– after adjusting for gender, GA, parental factors—FSIQ, VIQ and PIQ increased age 8 years IQ at 8 years was associated with HG during infancy	Above average head growth during infancy associated with above average IQ scores at 8 years Post-natal brain growth during infancy more important to later IQ than growth at other times Brain growth after infancy may not compensate for slower growth in the first year of life
Geva (37)	Population based prospective follow up study of single center (Tel Aviv, Israel)	BW <10th centile for GA according to Israeli birth weight curves (33), those with genetic disorders and unrelated co-morbidities excluded	110 IUGR children born at term, 63 control AGA children BY 1992–1995 Age at assessment: 9 y	Not assessed	Visual aural digit span test for digit span—aural-oral, visual-oral, aural-written, visual-written; RAVLT (superspan list learning test); Rey Osterreith Complex Figure test (ROYCF)	Learning functions over trials were similar for IUGR and controls on RAVLT. IUGR children performed more poorly than controls on ROYCF. IUGR children worse performance on immediate digit span than controls. Performance on digit span output mode did not differ between IUGR and control. IUGR children have memory problems particularly when the input is aural.	Memory difficulties in children born IUGR in the short term, not observed in later stages of learning (i.e., processing, consolidation and retrieval not affected) Difficulties when recalling both verbal and complex visuo-spatial material
Geva (38)	Population based prospective follow up study of single center (Tel Aviv, Israel)	BW <10th centile for GA according to Israeli birth weight curves (33), those with genetic disorders and unrelated co-morbidities excluded	138 IUGR children born at term, 64 control AGA children BY 1992–1995 Age at assessment: 9 y	Not assessed	VADS Digit span–aural-oral, visual-oral, aural-written, visual-written; IQ assessed by Wechsler Intelligence Scale for Children–revised (WISC-R)	IQ significantly lower in IUGR group. IUGR children performed worse than controls on verbal STM tasks.	Short term memory difficulties in IUGR children are particularly observed when material presented aurally and oral response required General cognitive performance also poorer in IUGR children relative to controls
Lawlor (39)	Single center, population based prospective birth cohort -Aberdeen Children of the 1950s cohort.	IUG rate measured as BW standardized for gender and GA. SGA calculated as BW < 10th centile, using a customized birthweight-for-gestation standard for the whole cohort	9,792 singleton children and 1,645 sibling pairs BY 1950–1956 Age at assessment: 7, 9 and 11 y	Not assessed	General ability measured by the Moray House picture test (MHPT)	Positive linear association between BW and MHPT, even when adjusted for SES, Maternal height and age, gender and GA. Within sibling comparison of SGA vs. AGA showed no difference in MHPT scores. If AGE compared to SGA outside of sibling pairs, AGA performed more poorly	While BW correlates with general cognitive ability within-sibling analyses suggest that associations between AGA status and cognitive ability in singletons is explained by within family factors, including SES, parental education and intelligence, genetic factors and fixed maternal factors
Leitner (40)	Prospective birth cohort	BW < 10th centile for gestational age, according to the Israeli percentile curves published by Lieberman et al. (33). Late onset IUGR (mid 2nd to 3rd trimester; verified by fetal ultrasound)	123 children with IUGR and 63 AGA controls, 30% of the sample were preterm BY 1992–2002 Age at assessment: 9–10 y Children with CP or severe neurological deficits were excluded	Neurological examination from birth, follow-up and at 9–10 years. 72 item examination. At age 9 years assessment of co-ordination skills, tone, timed performance, graphomotor skills. Findings: IUGR group poorer performance in coordination, timed performance, graphomotor skills; lower muscle tone	IQ assessed by Wechsler Intelligence Scale for Children (WISC), School achievement by Kauffman Assessment Battery for Children (K-ABC)	IUGR children performed more poorly than AGA controls on IQ and school achievement, where learning difficulties, particularly language-based difficulties were observed. Attention span, speech and language abilities were poorer in the IUGR group. Subgroup analyses compared IUGR children whose height, weight and head circumference were above (“optimal”) or below (“suboptimal”) the 10th growth percentile at age 9–10 years–the “suboptimal” catch up group performed worse in neurodevelopmental and cognitive tests than “optimal” group	Children with IUGR perform more poorly than their AGA peers on tests of IQ, school achievement, and neurological examination. Early growth ameliorates these group differences
Leonard (9)	Population-based record linkage study of children in Western Australia born 1983–1992 with intellectual disability of unknown cause	Percentage of optimal birthweight (POBW) categorized as %–POBW <85% was equivalent to <10th centile of optimal BW based on data from the 1998–2002 Western Australia birth cohort (35)	2,865 children with intellectual disability, including both term and preterm children BY 1983–1992	Not assessed	Registrations with the Disability Services Commission or educational services defined as “mild to moderate” (85.9%), “severe or profound” (7.4%), Autism spectrum disorder (6.7%)	In infants born at term, less than optimal fetal growth (POBW < 85%) was associated with “mild to moderate” intellectual disability, POBW < 75% was associated with “severe” intellectual disability. These were after adjusting for factors including SES and paternal occupation	Less than optimal uterine growth associated with intellectual disability in term born children. This persists after adjusting for sociodemographic factors. Severe growth restriction in term children associated with severe intellectual disability
Lundgren (8)	Population based cohort study of singleton male infants born from 1973 to 1976 and alive aged 18 years	“Light for gestational age” defined as > −2 SDs from mean BW for GA, AGA defined as between −2 and +2 SDS, “heavy for GA” defined as > +2 SDs from mean BW according to Swedish birth standards (41)	168,068 males conscripted for national service BW 1973–1976 Age at assessment: 18–25 y This study includes term and preterm adults	Not assessed	General intellectual performance assessed on four dimensions, logical/inductive, verbal, spatial and theoretical/technical	Being born SGA associated with increased risk of subnormal performance on all outcome measures compared to those born AGA SGA and small HC conferred additional risk of subnormal logical performance, SGA and short adult stature associated with a 40–50% increased risk in all outcome measures	Being born SGA associated with increased risk of impairment on logical/inductive, verbal, spatial and theoretical/technical dimensions of intellectual performance
Sommerfelt (42)	Multicenter study on causes and consequences of in utero growth retardation, the NICHD Study of Successive Small-for-Gestational Age Births (NSSSAB) 3 geographical Scandinavian regions; mothers recruited before 20 wGA	SGA = BW were <15th centile for gestation according to reference standards from the Norwegian Birth Registry (43); above 15th centile AGA	321 SGA and 312 AGA (78% of eligible children) Recruitment <20 w GA between January 1986 and March 1988 Age at assessment: 5 y	PDMS for balance, eye-hand coordination, locomotor abilities., Grooved Pegboard test for manual dexterity Findings: Motor problems more frequent in SGA group but no significance group difference	WPPSI for IQ scores (Verbal IQ, Performance IQ) Norwegian version of the Illinois Test of Psycholinguistic Abilities for receptive language and short-term memory	No significant difference in IQ scores, memory tests SGA with poorer motor performance lower scores on tests of visuospatial, manual dexterity, and verbal function	SGA group differs little from AGA peers on neuropsychologic profile and neuromotor outcome SGA group weakness in visuo-spatial skills and manual dexterity
Tanis (44)	Population based regional cohort—subgroup (Longitudinal Preterm Outcome Project study), Netherlands	BW < −1 SD and BW > −1 SD according to GA; Dutch Kloosterman curve (45). Cut-off for SGA (> 1 SD, below the 16th percentile) according to Etude Epidemiologique sur les Petits Ages Gestationnels study	42 SGA children (10 full term) and 336 AGA children (120 full term), Analyses combine MPT and term –GA range is 31–41. Both SGA and AGA groups consisted of mostly preterm children BY 2002–2003 Age at assessment: 7 y	Motor outcomes assessed by Movement Assessment Battery for Children (M-ABC) Findings: No significant difference in motor skills between AGA and SGA group	Full Scale IQ scores (FSIQ) from the Wechsler Intelligence Scale for Children (WISC). Selective attention and Attention control assessed by the Test of Everyday Attention in Children (TEA-Ch). Verbal memory assessed using Rey's Auditory Verbal Learning Test (RAVLT). Visuomotor integration assessed by Neuropsychological Assessment. Executive functioning in daily life assessed by the Behavior Rating Inventory of Executive Function (BRIEF)	No differences between AGA and SGA children on FSIQ, attention, verbal memory, visuomotor integration, executive functioning. SGA children 4 times more likely to be in the abnormal range on the Attention Control measure than AGA children	SGA and AGA children similar on IQ, verbal memory, executive functioning and movement tests, but SGA children more likely to be in the abnormal range on attention control
Theodore (46)	Case-control follow up study	SGA defined as BW < 10th centile for GA for New Zealand standards (47)	241 SGA children and 348 aGA controls BY 1995–1996 Age at assessment: 7 y	Not assessed	Full Scale IQ scores (FSIQ) from the Wechsler Intelligence Scale for Children (WISC)	No significant difference in FSIQ between SGA and AGA children. In the whole sample, parental education and birth order were associated with FSIQ	No long term negative effect of being born SGA on FSIQ scores

AGA, appropriate for gestational age; BW, birth weight; BL, Birth Length; BY-birth year; FGR, fetal growth restriction; GA, gestational age; HC, Head Circumference; IUGR, intrauterine growth restriction; POBW, Percentage of optimal birthweight; SES, socio-economic status; SGA, small for gestational age; w, week; y, year. ANT, Amsterdam Neuropsychological Tasks; CP, Cerebral Palsy; BRIEF, Behavior Rating Inventory of Executive Function; K-ABC, Kaufmann Assessment Battery for Children; M-ABC, Movement ABC for Children; MHPT-Moray House Picture Test; NEPSY, A Developmental NEuroPSYchological Assessment; RAVLT, Rey's Auditory Verbal Learning Test; ROYCF-Rey Osterreith Complex Figure test; PDMS, Peabody Developmental Motor Scales; SDQ, Strengths and Difficulties Questionnaire; STM, short term memory; TeaCH, Test of Everyday Attention in Children; VADS, Visual aural digit span test; WASI, Wechsler Abbreviated Scales of Intelligence; WISC, Wechsler Intelligence Scales for Children; WISC-R, Wechsler Intelligence Scale for Children – revised; WPPSI, Wechsler Preschool and Primary Scale of Intelligence; WRAT, Wide Range Achievement Test. IQ, Intelligence Quotient Score; FSIQ, Full Scale IQ Score; PIQ, Performance IQ Score; VIQ, Verbal IQ score. The terms SGA, IUGR, FGR were used as in the study that is described.