Brain Sparing Effect on Neurodevelopment in Children with Intrauterine Growth Restriction: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Literature Search
2.2. Inclusion Criteria
2.3. Selection Process
2.4. Data Collection Process
2.5. Quality Assessment
3. Results
3.1. Overall Search Results
3.2. Descriptions of the Tools Used by the Studies
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- Neonatal Behavioral Assessment Scale (NBAS) [30,36]. This test analyzes how newborns control their states and how the transition from one to another progresses. This test evaluates newborns’ habituation to the environment, motor system, social interaction (visual and auditory), organization and regulation state, autonomic system, and attention capacity. The scale evaluates how infants manage these vital tasks that are important for growth and development.
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- Bayley Scales of Infants and Toddlers [27,28,38]. This test evaluates cognition, language, and motor development. One study [38] used the second edition, which evaluates the Mental Developmental Index (MDI). The MDI estimates cognitive skills such as memory, problem-solving, vocalization, language, and social skills.
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- Revision of the Amsterdam Children’s Intelligence (RAKIT) Test [33]. This test assesses the intelligence quotient. The disk test is a subtest that evaluates the integration of visual recognition and fine motor coordination.
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3.3. Summary of the Findings of the Studies
Study | N | Study Group | Control Group | Definition of Brain Sparing | Exclusion Criteria | Age Assessment | Neurodevelpment Assessment | Results |
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Monteith et al. (2019) [27] Ireland Longitudinal multicentre prospective cohort Secondary analysis from PORTO study | 378 | - FGR with normal CPR N = 136 - FGR with abnormal CPR N = 41 GA between 24 + 0 and 36 + 6 | SGA N = 201 | CPR < 1 | - Birthweight < 500 g - major structural and/or chromosomal abnormalities | 3-year-old | Ages and Stages Questionnaire (ASQ) Bayley Scales of Infant and Toddler Development (3rd edition) | - FGR with abnormal CPR value had significantly lower mean scores in ASQ scales and Bayley scales compared with SGA (p < 0.05) - FGR with normal CPR also had lower mean scores compared with SGA, but only significantly in gross and fine motor development (p < 0.05) - When comparing both groups of FGR, only motor score in Bayley Scales reached significance (p = 0.002) |
Stampalija et al. (2017) [28] United Kingdom Longitudinal multicentre prospective cohort Secondary analysis from TRUFFLE study | 342 | Abnormal neurodevelopment outcome in FGR N = 310 GA between 26 + 0 and 31 + 6 | Normal neurodevelopment outcome in FGR. N = 32 | - delivery planned - major structural abnormality - fetal karyotype abnormality - <18 year-old | 2-year-old | Bayley Scales of Infant and Toddler Development (3rd edition) Gross Motor Function Classification System (GMFCS) Neurodevelopmental impairment was defined as:Bayley score < 85 or cognitive delay >3 months Cerebral Palsy (GMFCS > 1) Hearing loss (hearing aids) Severe visual loss | - MCA PI and UCR Z score at study inclusion were associated with 2-year infant survival without neurodevelopmental impairment (p < 0.05) - CPR Z score at study inclusion, MCA I, UCR, and CPR Z score before birth, and the change of these parameters with the time were not associated with 2-year outcome - Gestational age and birth weight at delivery remained the most important factor in determining 2-year infant outcome without neurodevelopmental impairment (p < 0.05) | |
Beukers et al. (2017) [29] The NetherlandsLongitudinal prospective cohort | 128 | FGR (NO Doppler criteria in FGR definition) N = 96 GA between 24 + 0 and 34 + 6 at admission | Children with gestational age ≥ 37 weeks and birth weight ≥ 2500 g at delivery. N = 32 | UCR > 0.72 | - Several fetal distress. - Lethal fetal congenital abnormalities. | 12-year-old | Weschler Intelligence Scale. Amsterdam Neuropsychological Task: Visual memory working, set shifting and focusing attention Tower London Test: Planning. Behavior Rating Inventory of Executive Function (parent report). Strengths and Weaknesses of Attention Deficit Hyperactivity Disorder Symptoms and Normal Behavior Scale (parent report) Child Behavior Checklist (parent report) | - 96% of cases had raised UCR, indicating brain sparing - Mean IQ was similar for FGR and control group (101.1 ± 16.7 vs. 105.9 ± 10.0 p = 0.12) - Parents of FGR reported significantly more social problems (p < 0.001) and FGR tend to have more attention problems (p = 0.07) - All executive functions, attention test performances, and parents’ reports did not differ between groups - For attention problems scores there were no significant difference between groups - UCR was not associated with any of the outcome variables - BWR and low SES were both associated with lower IQ |
Figueras et al. (2011) [30] Spain Longitudinal prospective cohort | 126 | FGR - Normal MCA PI N = 29 - Abnormal MCA PI N = 33 Gestational age at delivery < 34 weeks N = 62 | Singleton AGA N = 64 | MCA PI < 5th percentile | - congenital malformations - congenital infection - chromosomal abnormalities - placental histological chorioamnionitis - infant death before 40 weeks - neurological complication | 40 weeks corrected age | Neonatal Behavioral Assessment Scale (NBAS) | - Neurobehavioral score did not differ between FGR with normal MCA and the control group - Scores were significantly lower in FGR and abnormal MCA, specifically in habituation, motor, social-interactive, and attention areas (p < 0.05) |
Richter et al. (2020) [31] The NetherlandsLongitudinal prospective cohort | 25 | FGR (FAC or EFW < 10th percentile or decreased fetal growth more than 30 percentiles) with FBS N = 11 | FGR (FAC or EFW < 10th percentile or decreased fetal growth more than 30 percentiles) without FBS N = 14 | CPR < 1 | - structural or chromosomal abnormalities - multiple pregnancy - intrauterine infection | 4-year-old | Weschler Preschool and Primary Scale Child Behavior Checklist (parent report).Behavior Rating Inventory of Executive Function Preschool Version (parent report) | - FBS was not associated with IQ - FBS was significantly related with better total behavior and better externalizing behavior (p < 0.05) - FBS tended to have better inhibitory self-control (p < 0.1) - Adjusted for gestational age, which is positively correlated with T-score for total behavior, total executive function, and Emergent Metacognition Index (p < 0.05) |
Scherjon et al. (1998) [32] The Netherlands Longitudinal prospective cohort | 96 | Fetuses with UCR raised N = 34 Gestational age between 26 and 33 weeks at delivery | Fetuses with normal UCR N = 62 | UCR > 0.72 | - structural or chromosomal abnormalities | 3-year-old | Ultrasound findings: intraventricular bleeding or echo densities Hempel neurodevelopmental outcome: motor system, hearing, vision, and eye movements Behavioral Aspects (parent report) | - Lower head circumference was found in infants with raised UCR (p < 0.02) - All infants with abnormal neurological outcomes and all but one middle neurological outcome were found in the normal UCR group (p = 0.23) - Gestational age was lower in abnormal neurological outcomes (p = 0.01) - In the normal UCR group, the association with ultrasound findings and Hempel outcomes was highly significant. No association in raised UCR group (p < 0.0001) - No significant differences in behavioral or language development between groups |
Scherjon et al. (2000) [33] The Netherlands Longitudinal prospective cohort | 73 | Fetuses with UCR raised N = 28 Gestational age between 26 and 33 weeks at delivery | Fetuses with normal UCR N = 45 | UCR > 0.72 | - structural or chromosomal abnormalities | 5-year-old | Visual Evoked Potentials (VEP) RAKIT Test: intelligent quotient Disk Test: integration of visual recognition and fine motor coordination | - Infants with normal UCR were shortening VEP latencies between 6 to 12 months (decreased 20%) (p = 0.0001). UCR raised group had short VEP latencies at 6 months but remained unchanged at 12 months (decreased 5%) (p = 0.10) - Infants with raised UCR showed a 9-point lower IQ at 5 years compared with normal group (p < 0.02) - 54% of infants with raised UCR were IQ < 85 compared with 20% in normal group (p = 0.003) - There was a positive statistical association between a greater difference in VEP latencies at 6–12 months and higher IQ |
Van den Broek et al. (2010) [34] The Netherlands Longitudinal prospective cohort | 89 | Fetuses with UCR raised N = 31 Gestational age between 26 and 33 weeks at delivery | Fetuses with normal UCR N = 58 | UCR > 0.72 | - structural or chromosomal abnormalities | 11-year-old | Child Behavior Checklist (parent report) Teacher’s Report Form (teacher report): based in Child Behavior Checklist | - No significant differences in the incidence of behavioral problems between groups - They found a higher incidence of behavioral problems in the cohort compared with general population - No significant difference in not adequate school performance between groups - Birth weight was more important to predictive behavioral problems (p = 0.003) |
Bellido-Gonzalez et al. (2017) [35] Spain Longitudinal retrospective cohort | 120 | FGR (birth weight < 10th percentile and abnormal MCA PI < 5th percentile): FGR-A: abnormal CPR (<5th percentile) and abnormal UA PI (>95th percentile) N = 32 FGR-B: normal CPR and UA N = 27 Gestational age > 37 weeks | Term AGA | MCA PI < 5th percentile | - parental drugs consumption - multiple gestation - congenital malformation - chromosomopaties - low Apgar score - vision/hearing impairment - cerebral palsy - non-native speaker of Spanish | 6–8-year-old | Wechsler Intelligence Scale for Children IV: III Woodcock–Muñoz Battery: Reading, Written Language, Mathematics Home Observation for Measurement of the Environment (HOME) methods: interview to measure the quality of stimulation and support | WISC-IV: FGR-A presented lower scores than AGA children for all measurements (p < 0.05) Larger differences were observed in working memory FGR-B presented lower scores than AGA only for verbal comprehension and working memory (p < 0.05) Academic achievement: FGR-A presented lower scores than AGA children in reading, written language, and mathematics (p < 0.05) FGR-B presented lower scores than AGA children only in mathematics (p < 0.05) |
Cruz-Martinez et al. (2009) [36] Spain Longitudinal prospective cohort | 120 | SGA N = 60 Gestational age > 37 weeks | Term AGA N = 60 | MCA PI < 5th percentile Or FMBV > 95th percentile | - Congenital malformations or chromosomopaties - UA PI>95th percentile | 40 weeks corrected age | Neonatal Behavioral Assessment Scale (NBAS) | - SGA showed higher mean frontal FMBV values than AGA. The proportion of FMBV > 95th percentile was 35% in SGA and 5% in AGA (p < 0.001) - The proportion of MCA PI < 5th percentile was 15% in SGA and 1.7% in AGA (p < 0.01) - All neurobehavioral areas had lower scores in SGA group (p < 0.05) - SGA with abnormal FMBV showed lower scores in social-interactive, attention, and organization states. SGA with normal FMBV showed similar scores to AGA (p < 0.05) SGA with abnormal MCA showed lower scores in motor area (p < 0.05) |
Eixarch et al. (2008) [37] Spain Longitudinal prospective cohort | 222 | SGA Normal MCA PI N = 100 Abnormal MCA PI N = 25 Gestational age > 37 weeks | Term AGA N = 97 | MCA PI < 5th percentile | - Congenital malformations or chromosomopaties - UA PI > 95th percentile | 24 months corrected age | Age and Stage Questionnaire (ASQ) (parent report) | - 24.7% of control group showed abnormal ASQ scores in more than one area, compared with 31% in the non-redistributed SGA and 52% in redistributed SGA groups - Differences between AGA and SGA non-redistributed group was non-significant - Differences between AGA and SGA redistributed group was significant. They showed lower scores in communication and personal-social areas (p < 0.05) - Compared to both SGA groups, redistributed SGA had a lower score in communication and problem-solving (p < 0.05) |
Leppäpen et al. (2010) [38] Finland Longitudinal multicentre prospective cohort Secondary analysis from PIPARI study | 83 | Preterm delivery < 32 weeks or estimated birth weight < 1500 g In the secondary analysis the antenatal Doppler flow and the relationship with neurodevelopment was studied It was compared: Infants with abnormal UCR N = 16 Infants with normal UCR N = 54 | UCR > 95th percentile | - congenital anomalies or a diagnosed syndrome - non-native speaker of Finnish and ⁄ or Swedish | 2-year-old | Bayley Scales of Infant Development II Hammersmith Infant Neurological Examination (HINE): suboptimal < 74 Cranial nerve function, posture, movements, tone and reflexes, motor functions, behavior | - Abnormal UAPI, UCR, increased Dao PI and DAo/MCA ratio were associated with adverse cognitive performance. When the effect of confounding factor was controlled, only DAo and UCR remained statistically significant (p < 0.05) - When infants with normal and abnormal UCR were compared, no differences in HINE scores were found. The infants with abnormal UCR showed a lower score in MDI compared with normal UCR infants |
3.4. Quality Assessment Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Study | Selection Bias | Study Design | Confounders | Blinding | Data Collection Method | Withdrawals and Dropouts | Global Rating |
---|---|---|---|---|---|---|---|
Monteith et al. (2019) [27] | Moderate | Moderate | Strong | Moderate | Strong | Weak | Moderate |
Stampalija et al. (2017) [28] | Moderate | Moderate | Moderate | Moderate | Strong | Moderate | Strong |
Beukers et al. (2017) [29] | Moderate | Moderate | Strong | Moderate | Strong | Weak | Moderate |
Figueras et al. (2011) [30] | Moderate | Moderate | Moderate | Moderate | Strong | Strong | Strong |
Richter et al. (2020) [31] | Moderate | Moderate | Weak | Moderate | Strong | Weak | Weak |
Scherjon et al. (1998) [32] | Moderate | Moderate | Weak | Moderate | Strong | Strong | Moderate |
Scherjon et al. (2000) [33] | Moderate | Moderate | Weak | Moderate | Strong | Weak | Weak |
Van den Broek et al. (2010) [34] | Moderate | Moderate | Weak | Moderate | Strong | Strong | Moderate |
Bellido-Gonzalez et al. (2016) [35] | Moderate | Moderate | Strong | Moderate | Strong | Strong | Strong |
Cruz-Martinez et al. (2009) [36] | Moderate | Moderate | Strong | Moderate | Strong | Strong | Strong |
Eixarch et al. (2008) [37] | Moderate | Moderate | Strong | Moderate | Strong | Weak | Moderate |
Leppäpen et al. (2010) [38] | Moderate | Moderate | Strong | Moderate | Strong | Strong | Strong |
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Benítez-Marín, M.J.; Marín-Clavijo, J.; Blanco-Elena, J.A.; Jiménez-López, J.; González-Mesa, E. Brain Sparing Effect on Neurodevelopment in Children with Intrauterine Growth Restriction: A Systematic Review. Children 2021, 8, 745. https://doi.org/10.3390/children8090745
Benítez-Marín MJ, Marín-Clavijo J, Blanco-Elena JA, Jiménez-López J, González-Mesa E. Brain Sparing Effect on Neurodevelopment in Children with Intrauterine Growth Restriction: A Systematic Review. Children. 2021; 8(9):745. https://doi.org/10.3390/children8090745
Chicago/Turabian StyleBenítez-Marín, María José, Jesús Marín-Clavijo, Juan Antonio Blanco-Elena, Jesús Jiménez-López, and Ernesto González-Mesa. 2021. "Brain Sparing Effect on Neurodevelopment in Children with Intrauterine Growth Restriction: A Systematic Review" Children 8, no. 9: 745. https://doi.org/10.3390/children8090745