Paediatrica Indonesiana p-ISSN 0030-9311. e-ISSN 2338-476X. Vol. No. DOI: https://doi. org/10. 14238/pi63. Original Article Cognitive performance of 4 to 6-year-old children: a longitudinal study Nur Handayani Utami1. Rini Sekartini2. Risatianti Kolopaking3. Besral4. Helda Khusun5 Abstract Background Many children in low and middle-income countries (LMIC) have reduced cognitive abilities, but few studies have explored the influencing factors. Objective To determine the determinants of childrenAos low cognitive development at 4 to 6- year-old. Methods This is a retrospective cohort study in year 2021. The data was obtained from Bogor Longitudinal Study of Child Growth and Development (BLSCGD) that started from year 2012. For this analysis, we considered 165 of children aged 4-6 years. The dependent variable in this analysis was cognitive development as measured by the Indonesian Wechsler Preschool and Primary Scale of Intelligence (WPPSI) with the indicators of full-scale IQ (FSIQ), verbal IQ (VIQ), and performance IQ (PIQ). The independent variables were determinants of childrenAos cognitive development at 4-6 years, consisted of socio-demographic factors, determinants from early life . -23 month. , as well as determinants from current conditions. Multivariate analysis done with the logistic regression test. Results Bivariate analysis revealed that paternal education level was significantly associated with FSIQ and inadequate calorie intake in infancy and poor child stimulation were significantly associated with VIQ. In the final model of multivariate analysis, low paternal education level retained a significant association with FSIQ. Psychosocial stimulation was significantly associated with VIQ and inadequate calorie intake during infancy was significantly associated with PIQ. Conclusion Low paternal education level and inadequate psychosocial stimulation are risk factors for reduced child cognitive development in 4-6-year-olds. Inadequate calorie intake in infancy even though not statistically significant it has high OR values for low VIQ and PIQ, thus the results showed the importance of calory intake in infancy. [Paediatr Indones. 63:65-72. DOI: https://doi. org/10. 14238/pi63. 65-72 ]. Keywords: determinant factors. longitudinal study very child has the right to optimal growth and development. 1 However, there are still many children in LMIC unable to reach their optimal potential. 2 Indonesia is one of 34 countries with a 60% or higher prevalence of children at risk of poor development. Children whose cognition does not develop optimally, tend to have poorer school performance as well as negative impacts later in life. As adults, they may attain only low-income levels, have high fertility rates, and continue the process of providing less than optimal care of their own children. 2 Several factors have been identified to influence child cognitive development, such as biological factors . , birth weight, nutrition, and morbidit. , socioeconomic factors . amily income, level of education, and social clas. , environmental factors . , home environment, providing appropriate toys for children, and access From the Department of Nutrition1 and Department of Child Health,2 Universitas Indonesia. Faculty of Psychology. Universitas Islam Negeri Syarif Hidayatullah,3 Department of Biostatistics. Faculty of Public Health. Universitas Indonesia,4 SEAMEO RECFON (Southeast Asian Ministers of Education Organization Regional Centre for Food and Nutritio. Central Jakarta,5 Indonesia. Corresponding author: Nur Handayani Utami. Jl. Salemba Raya no. Central Jakarta. Indonesia. Telp. Email: nur_ handayani80@yahoo. Submitted October 5, 2022. Accepted November 21, 2022. Paediatr Indones. Vol. 63 No. March 2023 A 65 Nur Handayani Utami et al. : Cognitive performance of 4-6-year-old children: a longitudinal study to health facilitie. , and psychosocial factors . parental mental health, child-parent interactions, cognitive stimulation, and opportunity to stud. Several studies also mentioned that factors during early life could determine future child cognitive The importance of the first 1,000 days . ertilization to 24 months of ag. , especially the Aucritical and sensitive periodAy of brain development, have already been discussed and reviewed by many experts in neuroscience. 3 Brain development takes place immediately after conception and continues throughout childhood into adolescence and early Environmental influences can alter both the structure and function of the developing brain. Brain development is modified by the quality of the environment. Animal studies have shown that nutrition, iron deficiency, environmental toxins, stress, as well as poor stimulation and social interaction can affect brain structure and function. Despite the importance of current situation regarding childrenAos cognitive abilities especially among children in LMIC, the potential risk factors of reduced child cognition still need to be explored. Thus, we aimed to determine potential associations between risk factors with children 4 to 6-year-old cognitive development. Methods This is a retrospective cohort study in the year 2021. The data was obtained from Bogor Longitudinal Study of Child Growth and Development (BLSCGD). Indonesia, conducted by National Institute of Health Research and Development (NIHRD. MoH) started from year 2012, and children were followed from Bogor is a city that located near the capital city of Indonesia. Jakarta, and have characteristics of urban community. From total of 1054 children as the subjects of BLSCG in 2021, 540 were born between 2015-2017. From this number of subjects, after checking of the completeness of secondary data from the BLSCGD study, the data of children was available starting from the time of the pregnancy and follow up in monthly. As many as 71 exposed and 94 non exposed group are randomly selected from the list of subjects that met the inclusion and exclusion criteria . otal 165 subject. The inclusion criteria of 66 A Paediatr Indones. Vol. 63 No. March 2023 the exposed group included: had severe linear growth failure and aged 4-6 years at the cognitive assessment, while exclusion criteria were having congenital defects nor congenital abnormalities. The inclusion criteria of the non-exposed group included: having normal linear growth and aged 4-6 years at the cognitive assessment, while exclusion criteria were having congenital defects nor congenital abnormalities. Socio-demographic information was collected from the beginning of subject recruitment through interviews during home visits. The subjects were recruited since the mother was identified as having SubjectsAo birth weights were noted. Food intake was monitored monthly using 24-hr food recall. At subjectsAo follow-up visits at the age of 4-6 years, we collected data on cognitive development, maternal mental health, current child psychosocial stimulation, and exposure to formal/non-formal education. All variables other than cognitive development were collected through home visit interviews, while cognitive development was evaluated at the BLSCGD The primary outcome of this analysis was cognitive development at 4-6 years as measured by the Indonesian Wechsler Preschool and Primary Scale of Intelligence (WPPSI). 7 The manual for the Indonesian version of the WPPSI was issued by the University of Indonesia Faculty of Psychology. The WPPSI test consisted of two scales, namely, verbal and performance. The final results were in the form of full-scale IQ, verbal IQ, and performance IQ. Verbal IQ (VIQ) was a measure of acquired knowledge, verbal reasoning, comprehension, and attention to verbal stimuli. It consisted of 5 subtests, which were information, vocabulary, arithmetic, similarity, and Performance IQ (PIQ) was a measure of fluid reasoning, spatial processing, attentiveness to detail, and visual-motor integration. The scale consisted of five subtests . nimal house, picture completion, mazes, geometric design, and block Full-scale IQ was a combination of verbal and performance IQs. IQ scores were categorized as normal (IQ Ou . or low (< . cognitive ability. The potential predictors of reduced cognition were categorized into socio-demographic factors, exposures from early life . -23 month. , as well as exposures from current conditions. There were six variables under socio-demographic information: child Nur Handayani Utami et al. : Cognitive performance of 4-6-year-old children: a longitudinal study gender, age of child at cognitive assessment, paternal and maternal education level and occupation. Education level was defined as the highest level completed and categorized into AuLowAy . ompleted up to junior high schoo. and AuMiddle and HighAy . ompleted above junior high school/high school or Paternal occupation was categorized into civil servant, private employee, entrepreneur, and laborer/ other job. Maternal occupation was categorized into stay at home mother or working outside the home. Exposures from early life consisted of birth weight and dietary intake . alorie, macronutrients . rotein and fa. , and micronutrients (Fe and zin. Birth weight was measured within 24 hours of birth and categorized as low (< 2,500 . and normal (Ou 2,500 . Dietary intake was measured in the periods of infancy . -11 month. and early childhood . -23 month. and averaged. Adequate energy intake was defined as 70% of the Recommended Daily Allowance (RDA) and macronutrients as 80% of the RDA. Adequate iron and zinc were defined as the Estimated Average Requirement (EAR) values mentioned in the 2018 Widyakarya Nasional Pangan dan Gizi (WNPG). Exposures from current conditions included psychosocial stimulation, maternal mental health, and exposures to formal/informal education. Child psychosocial stimulation was obtained through interviews and observations using the HOME Observation for Measurement of the Environment Inventory (HOME Inventor. 11 for children aged 3-6 years. Scores were categorized into good . core > 80%), average . core 61%-80%), and poor . core O 60%). 12 Maternal mental health was assessed using the Self Rating Questionnaire (SRQ-. , which consisted of 20 questions. Each of the 20 items was scored 0 13 A score of 1 indicated that the symptom was present during the previous month. If subjects answered "yes" to at least six questions, then they were considered to be experiencing stress or mentalemotional disorders. 13 Exposures to formal/informal education were categorized into received education Ou 12 months, received education 1-11 months, and never received education. Interviews were conducted by trained enumerators with backgrounds in health education, using pre-tested questionnaires. Cognitive tests were done by a certified psychologist and limited to only five children per day, as the examination time took 60 to 90 minutes per child. Interrater reliability test for cognitive assessment was performed before data the intraclass correlation coefficients (ICC) showed that the scoring between raters was reliable (ICC > 0. Descriptive, bivariate (Chi- squar. , and multivariate logistic regression analyses were used to assess the factors potentially influencing childrenAos cognitive abilities. The statistical analysis was performed using SPSS version 21. Parents provided written informed consent. This study was approved by the Ethics Commission of the Universitas Indonesia. Faculty of Medicine. Results The characteristics of subjects are described in Table There were more female than male subjects. Around 15% of parents had low education level. More than half of fathers had occupations as laborers/other jobs, while most mothers were stay at home mothers. Almost 10% of the infant subjects had low birth During infancy, almost 20% had inadequate fat intake, 80% had inadequate iron intake, and almost half had inadequate zinc intake. In early childhood, protein, fat, iron, and zinc intake was not a problem in most subjects. During childhood, more than onethird of subjects had inadequate calorie intake, and more than 20% had inadequate fat and iron intake. More than one-third of subjects had received poor psychosocial stimulation. For psychosocial factors, almost one-third of the children had never received formal/informal education. In addition, 6. of mothers had impaired maternal mental health. Table 2 shows the analysis of subject characteristics and cognitive development (FIQ. VIQ, and PIQ). Low paternal education level had a significant association with FIQ (OR 2. 95%CI 0 to 7. P=0. Inadequate calorie intake in infancy and poor child stimulation were significantly associated with VIQ (OR 7. 95%CI 1. 0 to 60. P=0. 025 and OR 22. 95%CI 2 . 4 t o 2 0 0 . P=0. 001, respectivel. We included all factors that had P values < 0. 25 in the multivariate analysis. In the final model of multivariate analysis, low paternal education level retained a significant association with lower FSIQ (OR Paediatr Indones. Vol. 63 No. March 2023 A 67 Nur Handayani Utami et al. : Cognitive performance of 4-6-year-old children: a longitudinal study Table 1. Characteristics of subjects Characteristics (N=. Socio-demographic factors Gender, n(%) Male Female 77 . Age at cognitive assessment, n (%) 45-59 months 60-79 months 63 . Parental education level, n (%) Low paternal Low maternal 25 . Paternal occupation, n (%) Civil servant Private employee Entrepreneur Laborer/other job 4 . Maternal occupation, n (%) Stay at home mother Works outside the home 131 . Exposures from early life Low birth weight (LBW) 16 . Inadequate calorie intake in infancy 13 . Inadequate calorie intake in early childhood 57 . Inadequate protein intake in infancy 17 . Inadequate protein intake in early childhood 19 . Inadequate fat intake in infancy 28 . Inadequate fat intake in early childhood 36 . Inadequate iron intake in infancy 115 . Inadequate iron intake in early childhood 30 . Inadequate zinc intake in infancy 70 . Inadequate zinc intake in early childhood 25 . Exposures from current conditions Poor child stimulation 61 . Received formal/informal education Ou 12 months 10-11 months Never received education 27 . Maternal mental health disorder 10 . 95%CI 1. P=0. compared to children with middle/high paternal education level (Table . Table 4 shows that, in the final model of multivariate analysis, poor child stimulation (OR 95%CI 1. 4 to 127. P=0. were the determinant factor significantly associated with low VIQ. Inadequate calorie intake in infancy even though not statistically significant, a high OR value (OR 6. 95% CI 0. indicated have a significant risk of low VIQ among children. 68 A Paediatr Indones. Vol. 63 No. March 2023 Discussion Education is one of indicators that construct socioeconomic status (SES). Parental low education has been confirmed as one of the factors contributed to child cognitive development. One study found that maternal education and vocabulary levels of mothers were strong predictors of the cognitive development of young children. 14 Furthermore, the Aberdeen Cohort Study also found an association between paternal SES and child cognitive abilities, with paternal social class found to contribute to child intelligence. UNICEF stated that the causes of malnutrition and low development among children are interlinked, whereas socioeconomics was the underlying factor. This is also in line with Lancet that mention socio economic factor as one of the risk factors of child 5 Low parental education can lead to poor care and less than adequate home stimulation. Furthermore, several neuroscience studies have noted relationships between cognitive development and SES. Stress, nutrition, prenatal factors, parent-child interactions, and cognitive stimulation in the home environment are mediating effects of SES on both brain structure and cognitive function in both human and animal models. 17,18 Several cognitive functions are influenced by SES: language, verbal math, attention, executive function, and memory. In language abilities. SES correlated with vocabulary and grammar. Verbal math correlated with SES in the math domain. One present study that examined the neural mechanism using an event-related brain potential (ERP) measure of selective auditory attention according to different SES background, comparing response on simultaneously presented narrative It showed that SES correlated with attentional control, working memory, visual and novelty (N. event-related brain potential (ERP) and ERP suppression response of unattended channel. We found that psychosocial stimulation was significantly associated with VIQ. Consistent with these findings, many studies have found that cognitive stimulation plays a significant role in childrenAos cognitive ability and academic achievement. 21 For example, an intervention study in South Africa aimed to educate mothers about sensitive and responsive The intervention had a significant impact Nur Handayani Utami et al. : Cognitive performance of 4-6-year-old children: a longitudinal study Table 2. Bivariate analysis of potential determinant factors and cognitive development scales of children aged 4 to 6 years (PearsonAos Chi-squar. Variables Full-scale IQ Verbal IQ Performance IQ OR . % CI) P value OR . % CI) P value OR . %CI) P value Female 9 . 5 to 1. 5 to 1. 8 to 2. Age 60-79 months at cognitive 6 . 8 to 2. 8 to 2. 7 to 2. Low paternal education level 7 . 0 to 7. 6 to 3. 8 to 4. Low maternal education level 2 . 9 to 5. 5 to 2. 0 to 4. Paternal occupation Laborer/other job 6 . 2 to 12. 1 to 5. Maternal occupation Stay at home mother 4 . 7 to 3. 5 to 2. 7 to 3. LBW 3 to 2. 7 to 9. 3 to 2. Inadequate calorie intake in infancy 9 . 8 to 11. 0 to 60. 7 to 7. Inadequate calorie intake in early 1 . 5 to 2. 6 to 2. 5 to 1. Inadequate protein intake in infancy 5 . 5 to 4. 6 to 6. 6 to 4. Inadequate protein intake in early 1 . 4 to 2. 4 to 3. 3 to 2. Inadequate fat intake in infancy 6 . 7 to 3. 9 to 6. 7 to 3. Inadequate fat intake in early childhood 5 . 7 to 3. 5 to 2. 5 to 2. Inadequate iron intake in infancy 0 . 4 to 2. 5 to 2. 2 to 1. Inadequate iron intake in early 0 . 5 to 2. 3 to 1. 5 to 2. Inadequate zinc intake in infancy 8 . 4 to 1. 5 to 2. 4 to 1. Inadequate zinc intake in early 7 . 3 to 1. 4 to 2. 2 to 1. Poor child stimulation 7 . 6 to 13. 4 to 200. 2 to 4. Never received formal/informal 3 . 9 to 6. 8 to 5. 4 to 2. Maternal mental health disorder 8 . 4 to 7. 5 to 11. 2 to 3. Socio-demographic factors Exposures from early life Exposures from current conditions on mother-child relationships and predicted child 2 Another intervention study showed that cognitive stimulation significantly improved cognitive function with most effect sizes ranged from 5 SD to 1. 0 SD. 21 Furthermore, follow-up studies consistently report long term effects of early cognitive intervention on child cognition. 22,23 Stimulation improved child cognitive and educational deficits in late adolescence among stunted Overall, stunted non-stimulated participants had significantly poorer scores than the non-stunted group on 11 of 12 cognitive and educational tests. Stunting in early childhood was associated with cognitive and educational deficits in late adolescence, which can be reduced by stimulation at a young 24 Moreover, cognitive stimulation, such as giving materials and experiences, is also well established in global policy practices. Lancet series on Child Development in Developing Countries identified factors with sufficient evidence to recommend implementing prevention strategies. They identified four key risk factors urgently requiring intervention: stunting, inadequate cognitive stimulation, iodine deficiency, and iron deficiency anemia. Paediatr Indones. Vol. 63 No. March 2023 A 69 Nur Handayani Utami et al. : Cognitive performance of 4-6-year-old children: a longitudinal study Table 3. Multivariate analysis of low paternal education and FSIQ Factors Estimated Regression coefficient () SE of () P value OR . % CI) Constant Low paternal education level 7 . 0 to 7. *P value < 0. 05 was considered to be statistically significant Table 4. Multivariate analysis of VIQ and poor child stimulation and inadequate calorie intake in infancy Factors Estimated Regression coefficient () SE of () P value OR . % CI) Constant Poor child stimulation 5 . 4 to 127. Inadequate calorie intake in infancy 3 . 8 to 50. *significant P value < 0. Table 5. Multivariate analysis of PIQ and inadequate intake of calories, iron, and zinc Factors Estimated Regression coefficient () SE of () P value OR . % CI) Inadequate calorie intake in infancy 6 . 0 to 13. Inadequate iron intake in infancy 5 . 2 to 1. Inadequate zinc intake in early childhood 5 . 2 to 1. Constant We found that inadequate calorie intake in infancy is a risk factor for childrenAos low VIQ and PIQ among 4-to-6-year-olds as indicated by high OR values, although not statistically significant. These results demonstrate not only the large effect of inadequate calorie intake on cognitive development, but also its long-lasting impact up to 4-6 years of age. A review stated that the plasticity of the brain, neurons or synapses is the human ability to perform complex mental activities. This depends on the brainAos ability to adapt to the environment and change its functional and structural organization. In addition, to maintain such complex and dynamic brain capabilities and maintain this complex architectural function, an extraordinary supply of energy is required. While the energy requirements of the adult brain are large, energy requirements during early life are even higher and are important for supporting rapid brain development with a growth spurt that begins around the 5th month of pregnancy and continues after birth, increasing brain weight from its adult weight at It becomes 80% by 2 years of age and reaches 70 A Paediatr Indones. Vol. 63 No. March 2023 its maximum size around 7 years of age. Therefore, postnatal growth, especially in early childhood, is not the result of the addition of new neurons, but the development and maturation of neurons, but instead it is the development and the maturation of neurons that already present at birth including axon growth, dendritic arborization elaboration, synaptic formation/ elimination, and axon myelination. The energetic costs associated with brain function in estimation that neurons consume 75-80% of the energy produced, whereas the rest is used for glia-based processes. Two main reasons may explain why neurons have high energetic demands: first, the generation of action potentials along the axons and synaptic transmission from neuron to neuron are based on electrochemical and cellular processes, such as ion fluxes, neurotransmitter release and reuptake, and vesicle cycling, which are energetically A signaling mechanism at the synapse has been suggested to be especially energy consuming. for example, it has been estimated that 80% of the energy in myelinated hippocampal axons is expended Nur Handayani Utami et al. : Cognitive performance of 4-6-year-old children: a longitudinal study by postsynaptic potentials. In addition to its enormous demand of energy, the dramatic brain size expansion that happens during the first years of life requires specific nutrients, such as lipids, proteins, and micronutrients, which are not only the building blocks of brain structures but also support brain and cognitive functions during the rest of the lifespan. Another role of energy on brain function among adults has emerge from evidence that suggests excessive energy intake, together with a sedentary lifestyle places the brain at risk for the development of late life cognitive impairment and AlzheimerAos Conflict of interest None declared. Funding acknowledgment The authors received no specific grants from any funding agency in the public, commercial, or not-for-profit sectors. References