Abstract
BACKGROUND:
Developmental delay in preterm infants in different geographical areas has different risk factors. The present research was a large study aiming to assess developmental delay in preterm infants during the first 12 months after birth and its risk factors in northwest Iran (with multiethnic texture).
MATERIALS AND METHODS:
Eight hundred and seventy preterm infants (25 to 36 weeks; up to 12 months) were included in this descriptive–analytical study from the beginning of 2019 to the end of 2021 in northwest Iran by the convenient sampling method. Patients’ basic and medical information was recorded in the data collection form, and the Ages and Stages Questionnaire (ASQ) was used to assess children’s developmental status.
RESULTS:
The prevalence of developmental delay in this study was 26.4%. Regarding demographic characteristics such as age, height (at birth and one year of age), weight (at birth and one year of age), Apgar score (first and twentieth minutes), duration of ventilator connection, comorbidities and complications after birth, and breastfeeding during the first year of life, there was a statistically significant difference between the two groups of infants with and without developmental delay. Breastfeeding during the first 12 months after birth alone could have the power to predict developmental delay in preterm infants.
CONCLUSION:
Breastfeeding in the first year of life is considered one of the most important predictors of normal development in preterm infants. Therefore, encouraging the parents of these infants to breastfeed their infants at birth can be a positive step in improving the quality of life of these infants in the future.
Keywords: Developmental delay, Iran, preterm, risk factor
Introduction
A preterm infant refers to an infant born less than 37 full weeks of gestation.[1] According to the World Health Organization (WHO), about 15 million preterm infants are born annually worldwide.[2] The prevalence rate of preterm infants is estimated at 5–18% in 184 countries, according to the WHO report.[3,4] Preterm birth disorders have been the leading cause of death for children under 5 and were responsible for the deaths of nearly one million children in 2015.[5]
Studies show that the development of technology in the neonatal intensive care unit (NICU) has reduced the mortality of high-risk and preterm infants, but this issue has affected the prevalence of subsequent disabilities and long-term complications in these infants.[6] Research indicates that the possibility of neurodevelopmental and behavioral disorders is higher in premature-born children and adults.[7,8] For example, Moore et al.’s[9] study on the developmental status of 1,031 three-year-old children with less than 27 weeks of gestational age showed the incidence of moderate-to-severe developmental disorders in 25% of these children. A similar study in Sweden found that 18.8% of preterm infants had cognitive disorders at six years of age.[10,11] Case–control studies also showed that neurodevelopmental delay was significantly higher in preterm infants than in children of normal gestational age.[12,13,14]
After reducing the mortality of preterm infants, attention is focused on improving the quality of life of these infants so that the necessary measures can be taken to improve their future. The incidence of developmental disorders in preterm infants, in addition to the problems it creates for the child and his/her family, also incurs a huge financial cost to the body of the country’s health system.[15,16]
The development of children starts from the fetal period, and with proper care and nutrition during pregnancy, the opportunity for optimal growth and development of the child, which is his natural right, is provided.[17] The most important period of a child’s brain development is the first two years of life, which has a significant role in the child’s mental, physical, psychological, social, and safety performance.[18] Developmental delay is a term that is generally applied to children who have not shown the outstanding developmental characteristics that are expected of them for their age.[19] Due to the many problems faced by having a child with developmental delay, early diagnosis and referral are necessary and very important and can be the most beneficial for children with developmental disabilities and their families.[20] Therefore, it is necessary to monitor the child’s development and screen for the presence of such problems in every visit, especially the first visit of the child to check the child’s health.[21,22]
Therefore, identifying the factors affecting the normal development of these infants and taking the necessary preventive measures will not only improve the quality of life of these infants in the future but also will be a step toward a healthier society. However, different geographical regions differ in the occurrence and prevalence of different risk factors. This study aimed to investigate the factors predisposing to developmental delay in preterm infants (gestational age of 25 to 36 weeks and six days) in the first year of life in northwest Iran, with a multiethnic texture. The results of this study can help pediatricians prevent developmental delay in preterm infants and provide better management of the health status of these infants in the first year of life. According to the mentioned materials and the importance of paying attention to developmental delay in premature infants, this study was conducted with the aim of developmental delay in preterm infants during the first twelve months after birth and its risk factors.
Materials and Method
Study design and setting
The present research is a cross-sectional analytical study with a prospective approach conducted between the beginning of 2019 and the end of 2021 in northwest Iran (including Tabriz, Urmia, Marand, Maragheh, Khoy, Mahabad, Miandoab, Naqadeh, and Ardabil cities). The sampling method in this study is convenient sampling and purposeful. Participants were evaluated according to the inclusion/exclusion criteria.
Study participants and sampling
The sample volume formula was used to estimate the sample size. The following assumptions were observed for this formula. Given the 29% prevalence[3] of developmental disorders in preterm infants, the measurement error was 0.15, the first type error was 0.05, the test power was 80%, and the minimum sample size was equal to 87 people. The sample size reached 870 people to increase the validity of the results (Tabriz = 270 people, Urmia = 190 people, Marand = 55 people, Maragheh = 60 people, Khoy = 50 people, Mahabad = 50 people, Miandoab = 25 people, Naqadeh = 30 people, and Ardabil = 140 people).
Inclusion/exclusion criteria
Inclusion criteria for infants were the gestational age of 25 to 36 weeks and a history of hospitalization in the neonatal ward or NICU. Infants with genetic diseases or severe brain malformations were excluded from the study. If parents wished to participate in the study, the study objectives were explained to them, and written consent was obtained from all of them.
Procedure
Demographic and primary information about infants such as age, gender, height, weight, head circumference, gestational age, duration of ventilator connection, duration of NICU hospitalization, clinical problems observed at birth, Apgar scores at first, fifth, tenth, and twentieth minutes after birth, duration of receiving cuddling support, length of maternal stay in hospital at the time of infant’s hospitalization, type of childbirth, and clinical problems observed in infants’ mothers was collected through infants’ medical records or questions from parents. The Ages and Stages Questionnaire (ASQ) was used to assess the developmental status of infants. In Iran, the sensitivity and specificity of the ASQ test in identifying infants with developmental delay were estimated to be 0.84 and 0.94, respectively. This test examines the child’s developmental status in four areas: gross motor development, fine motor development, cognitive development, and speech development.[23] At the beginning of the research, the test method was explained to the parents, and then, the test was provided to the parents. After one week of monitoring the infant’s abilities, the parents completed the test and were referred to the pediatrician (a member of this study) to review and receive the results. Based on the test results, the developmental status of children was determined by a physician and recorded in information forms specific to each child. In addition to these results, detailed neurological examinations of children were also recorded in the mentioned forms. In this study, any developmental disorder was observed in the ASQ developmental screening test. The Bayley developmental diagnostic test (the Bayley Scales of Infant and Toddler Development) was also performed for infants.[24] This test is a diagnostic test to check for neurodevelopment. Finally, in case of diagnosing developmental delay in the child, an educational occupational therapy session was performed for the child in the presence of the parents, and a doctor of occupational therapy (outside the research group) and the parents were encouraged to continue doing it.
Data analysis
Mean and standard deviation were used to describe quantitative variables, and frequency and frequency percentage were used to describe qualitative variables. The Chi-square test and independent-samples t-test were used to examine the relationships between variables considering the type of variable. A binary logistic regression equation was also used to identify the factors predisposing to developmental delay in preterm infants. In all calculations, the significance level was considered less than 0.05.
Ethical considerations
This study was approved by the Ethics Committee of Tabriz University of Medical Sciences (IR.TBZMED.REC.100). The informed consent was signed by both parents of the infants after explaining the study objectives in plain language. No costs (doctor visits and occupational therapy) were imposed on patients and insurance organizations.
Results
Among the study participants, 420 infants (48%) were female, and the rest (450 infants = 52%) were male. The results of the ASQ, the Bayley test, and neurological examinations were used to determine the developmental status of preterm infants. A developmental delay diagnosis was performed in 160 infants (18%) through the ASQ test results and in 70 infants (8%), despite the normal ASQ, based on clinical examinations. All infants were referred to the comprehensive development center for performing the Bayley test. One hundred and ten infants had performed the Bayley test. According to the Bayley test results, 10 infants in all areas, 10 infants in the fine movement area, and 10 infants in the gross movement area had developmental delays [Table 1]. In total, abnormal development was confirmed in 230 infants and this rate was the basis of analytical studies.
Table 1.
Frequency distribution of the results of developmental screening test indices in preterm infants with abnormal development
| Developmental screening test indices | Normal development n (%) |
-1<standard deviation ≥-2 n (%) |
2< standard deviation n (%) |
|---|---|---|---|
| Cognitive abnormal development | 130 (81.3%) | 10 (6.3%) | 20 (12.5%) |
| Abnormal development of speech reception | 90 (56.3%) | 30 (18.8%) | 30 (18.8%) |
| Abnormal development of speech expression | 120 (75%) | 20 (12.5%) | 20 (12.5%) |
| Abnormal development of gross movements | 50 (31.3%) | 60 (37.5%) | 50 (31.3%) |
| Abnormal development of fine movements | 140 (87.5%) | 10 (6.3%) | 10 (6.3%) |
Studies showed that gender, gestational age, birth weight, head circumference at birth, duration of NICU hospitalization, duration of hospitalization in the neonatal ward, Apgar scores of fifth and tenth minutes, mother’s age, receiving cuddling support, length of maternal stay in hospital at the time of infant’s hospitalization, abnormal brain imaging findings, and infant head circumference at infants’ one year of age were not statistically significantly associated with infants’ developmental status (P > 0.05). However, infants’ age, birth height, duration of ventilator connection, first- and twentieth-minute Apgar scores, one-year-old weight and height, type of feeding in the first year of life, receiving occupational therapy in the first year of life, the presence of retinopathy lesion, and abnormal findings in electrocardiography (ECG) were found to be statistically significantly associated with the developmental status of preterm infants [Table 2].
Table 2.
Frequency distribution of demographic and clinical information of preterm infants at birth and at one year of age by normal and abnormal development
| Variable | Total participants (n=870) |
P | |
|---|---|---|---|
| Normal development (n=640) | Abnormal development (n=230) | ||
| Male gender* | 330 (51.6%) | 120 (52.2%) | 0.96 |
| Age (day)** | 340.59±26.56 | 305.74±12.36 | 0.01 |
| Gestational age (week)** | 31.54±1.29 | 31.02±1.29 | 0.49 |
| Birth weight (g)** | 1958.45±259.63 | 1839.44±239.32 | 0.59 |
| Birth height (cm)** | 43.66±8.96 | 41.03±12.29 | 0.59 |
| Head circumference at birth (cm)** | 29.89±5.29 | 28.21±4.59 | 0.43 |
| One-year-old weight (g)** | 11036.89±556.96 | 8569.41±221.38 | 0.009 |
| One-year-old height (cm)** | 79.55±9.36 | 67.52±5.69 | 0.005 |
| One-year-old head circumference (cm)** | 45.23±9.52 | 44.78±9.24 | 0.37 |
| Duration of ventilator connection (day)** | 79.55±9.36 | 79.55±9.36 | 0.005 |
| Duration of NICU hospitalization (day)** | 1.24±3.45 | 5.7±5.36 | 0.001 |
| Duration of hospitalization in the neonatal ward (week)** | 14.06±8.33 | 26.74±5.39 | 0.004 |
| First-minute Apgar score** | 7.75±0.29 | 6.02±1.25 | 0.011 |
| Fifth-minute Apgar score** | 7.45±0.96 | 7.03±0.96 | 0.25 |
| Tenth-minute Apgar score** | 8.15±0.33 | 8.01±0.25 | 0.059 |
| Twentieth-minute Apgar score** | 8.24±0.36 | 8.15±0.41 | 0.19 |
| Mother’s age (year)** | 28.34±5.59 | 30.15±5.89 | 0.14 |
| Cuddling support* | 630 (98.4%) | 210 (91.3%) | 0.11 |
| Length of maternal stay in hospital* | 630 (98.4%) | 220 (95.7%) | 0.49 |
| Type of feeding in the first year of life* | |||
| No breastfeeding | 30 (4.7%) | 60 (26.1%) | 0.01 |
| Breastfeeding | 170 (26.6%) | 60 (26.1%) | |
| Breastfeeding and complementary food | 440 (68.8%) | 110 (47.8%) | |
| Receiving occupational therapy in the first year of life* | 10 (1.6%) | 60 (26.1%) | 0.001 |
| Presence of retinopathy lesion* | 70 (10.9%) | 80 (34.8%) | 0.009 |
| Abnormal findings in brain imaging* | 0 (0%) | 10 (4.3%) | 0.17 |
| Abnormal findings in electrocardiography* | 10 (1.6%) | 20 (8.7%) | 0.001 |
Chi-square test*, Student’s t-test**
Examining clinical problems observed in preterm infants and their mothers showed that the incidence of seizures, decreased neonatal reflexes, and pneumonia in preterm infants were statistically significantly associated with their developmental status at one year of age. The reported clinical problems in mothers of preterm infants and the type of their childbearing were not statistically significantly associated with the infant’s developmental status at one year of age [Table 3].
Table 3.
Frequency distribution of type of childbearing and clinical problems observed in preterm infants and their mothers by normal and abnormal development
| Variable | Total participants (n=870) |
P | |
|---|---|---|---|
| Normal development (n=640) | Abnormal development (n=230) | ||
| Clinical problems of preterm infants | |||
| Seizure | 10 (1.6%) | 30 (13%) | 0.02 |
| Decreased reflex | 50 (7.8%) | 60 (26.1%) | 0.02 |
| Intracerebral hemorrhage (grades 2–4) | 30 (4.7%) | 20 (8.6%) | 0.36 |
| Germinal matrix hemorrhage (grade 1) | 70 (10.9%) | 30 (13%) | 0.52 |
| Respiratory distress syndrome | 380 (59.4%) | 110 (47.8%) | 0.35 |
| Pneumonia | 30 (4.7%) | 50 (21.7%) | 0.01 |
| Open arterial duct | 50 (7.8%) | 50 (21.7%) | 0.07 |
| Sepsis | 240 (37.5%) | 120 (52.2%) | 0.22 |
| Fungal infection | 30 (4.7%) | 0 (0%) | 0.29 |
| Hypothyroidism | 60 (9.4%) | 10 (4.3%) | 0.44 |
| Feeding intolerance | 140 (21.9%) | 60 (26.1%) | 0.68 |
| Hyperbilirubinemia | 470 (73.7%) | 160 (69.6%) | 0.72 |
| Abnormal brain imaging | 110 (17.2%) | 50 (21.7%) | 0.62 |
| Pneumothorax | 50 (7.8%) | 30 (13%) | 0.45 |
| Use of chest tube | 50 (7.8%) | 30 (13%) | 0.45 |
| Abnormal echo | 260 (40.6%) | 80 (34.8%) | 0.62 |
| Clinical problems of mothers of preterm infants | |||
| Premature rupture of membranes | 140 (21.9%) | 20 (8.7%) | 0.16 |
| Chorioamnionitis | 10 (1.6%) | 20 (8.7%) | 0.10 |
| Intrauterine infection | 0 (0%) | 10 (4.6%) | 0.09 |
| Preeclampsia | 140 (21.9%) | 60 (26.1%) | 0.68 |
| Eclampsia | 10 (1.6%) | 10 (4.6%) | 0.44 |
| Cesarean delivery | 540 (84.4%) | 180 (78.3%) | 0.5 |
The test used: Chi-square
To identify the predictors of abnormal developmental status in preterm infants, all variables that were significantly associated with the developmental status of infants at one year of age were included in the regression equation. Given the duality of the dependent variable (normal and abnormal developmental status), the binary logistic regression equation was used. The findings of these calculations are shown in Table 4. According to the findings of this table, infants’ breastfeeding in the first year of life was the only variable that could predict the developmental status of infants at one year of age.
Table 4.
Binary logistic regression analysis to identify risk factors for abnormal development in preterm infants
| Variable | P* | DF | OR | 95% CI |
|
|---|---|---|---|---|---|
| Lower | Upper | ||||
| Age (day) | 0.24 | 1 | 0.95 | 0.88 | 1.03 |
| Birth height (cm) | 0.15 | 1 | 0.80 | 0.59 | 1.08 |
| One-year-old weight (g) | 0.38 | 1 | 1.00 | 0.99 | 1.00 |
| One-year-old height (cm) | 0.96 | 1 | 0.99 | 0.75 | 1.31 |
| Duration of ventilator connection (day) | 0.52 | 1 | 0.87 | 0.58 | 1.30 |
| First-minute Apgar score | 0.45 | 1 | 0.71 | 0.29 | 1.70 |
| Twentieth-minute Apgar score | 0.35 | 1 | 3.33 | 0.25 | 43.25 |
| Seizure | 0.99 | 1 | 0.00 | 0.00 | - |
| Decreased reflex | 0.99 | 1 | 0.00 | 0.00 | - |
| Pneumonia | 0.38 | 1 | 37.12 | 0.01 | 12.37 |
| Breastfeeding in the first year of life | 0.01 | 1 | 0.18 | 0.04 | 0.75 |
| Presence of retinopathy lesion | 0.53 | 1 | 2.90 | 0.10 | 82.07 |
| Occupational therapy | 0.99 | 1 | 26.50 | 0 | - |
| Abnormal findings in electrocardiography | 0.99 | 1 | 90.69 | 0 | - |
*Logistic regression
Discussion
Since preterm infants are more at risk of developmental delay than term infants, any intervention that can have even a small impact on the normal development of these infants will be valuable. For this reason, the present study focused on identifying the factors predisposing to developmental delay in preterm infants. According to the findings of the present study, 24.6% of the studied infants had abnormal development. The risk of developmental delay in preterm infants has been reported differently in various studies. For example, in Quigley et al.’s study,[13] the rate of abnormal development in preterm infants has been reported much lower than in the present study (13%), and in Bagheri et al.’s study,[25] it has been reported much higher than the present study (42%). In Sierra-García et al.’s study,[26] 5 to 21% of preterm infants had developmental delays in various developmental dimensions. In Pierrat et al.’s study,[27] 5 to 36% of preterm infants with different gestational ages had developmental delays. Since the developmental status of preterm infants in various studies is influenced by different context factors, this variation in the results seems logical.
Analytical studies showed that in the present study, there was no statistically significant relationship between the infants’ gender and their developmental status at one year of age. Similarly, no statistically significant relationship was reported between the gestational age of preterm infants and their developmental status at one year of age. However, after evaluating the data distribution method in the gestational age variable, the results showed that the data distribution of this variable was not normal. That is, the data were significantly accumulated in a certain range. The lack of a relationship between gestational age and developmental status in this study is probably due to the way of data distribution, and this relationship may change as the sample size increases. However, the findings of this part of the study were also consistent with the results of Kazeroono et al.’s study,[28] which showed no statistically significant relationship between gestational age and different developmental areas of preterm infants. According to the results of the present study, the mean age of preterm infants with abnormal developmental status was significantly lower than infants with normal development. The inverse relationship between age and developmental status was also reported in Bagheri et al.’s study,[25] which demonstrated that the rate of developmental delay was reduced from 56% at six months of age to 18% at 24 months of age. Based on the findings of the present study, infants’ weight and head circumference at birth had no statistically significant relationship with their developmental status at one year of age. However, birth height in preterm infants with normal developmental status was significantly higher than in infants with abnormal development. In Bagheri et al.’s study,[25] children with developmental delay had lower birth weight than those with normal development. The difference in the results of this study with the results of the present study may be due to the differences in the assessment time of children’s developmental status because the infants’ developmental status was assessed in the present study at 12 months of age and Bagheri et al.’s study[25] at 24 months of age.
In the present study, the weight of preterm infants with normal development at one year of age was also significantly higher than that of infants with abnormal development. However, the height of preterm infants with normal developmental status at one year of age was significantly higher than that of infants with abnormal development. Studies have shown that the duration of NICU hospitalization and the duration of hospitalization in the neonatal ward were not significantly associated with the developmental status of preterm infants at one year of age. However, in Ballantyne et al.’s study,[29] infant hospitalization or nonhospitalization in the NICU ward was significantly associated with the risk of infants’ developmental delay. The differences in the results of the present study with the findings of Ballantyne et al.’s study[29] may be due to differences in the protocols of the two studies. In the mentioned study, healthy infants were used as a control group, and naturally, there was a significant difference between these infants and preterm infants in the rate of NICU hospitalization, while in the present study, the focus was merely on preterm infants, most of whom (98.9%) had a history of NICU hospitalization.
Examining the Apgar scores of the first, fifth, tenth, and twentieth minutes of preterm infants showed no statistically significant relationship between the Apgar scores of the fifth and tenth minutes of infants and their developmental status at one year of age. However, the Apgar scores of the first and twentieth minutes in preterm infants with normal developmental status were significantly higher than in preterm infants with abnormal development. Contrary to the findings of the present study, in Bagheri et al.’s study,[25] the Apgar score of the fifth minute was significantly lower in children with developmental delay. However, in Kazeroono et al.’s study,[28] in general, no significant relationship was observed between different areas of development and the infant’s Apgar score. The results showed a statistically significant relationship between the infant’s way of feeding in the first year of life and their developmental status at one year of age, so infants who were breastfed or fed with a combination of breast milk and complementary food had a noticeably better developmental status than other infants.
Studies indicated that infants with abnormal developmental status were significantly more exposed to receiving occupational therapy than infants with normal development. Also, the incidence of retinopathy lesion was reported to be significantly higher in infants with abnormal developmental status (34.8%) than in infants with normal developmental status (10.9%). The findings of Rodriguez and Natarajan et al.’s[30,31] studies also showed a significant effect of retinopathy lesion in preterm infants on their neurodevelopmental status.
Based on the results of the present study, there was no statistically significant relationship between the observation of abnormal brain imaging findings and the developmental status of preterm infants at one year of age. However, studies have shown that in infants with abnormal developmental status, the observation of abnormal findings in the ECG is significantly higher than in infants with normal developmental status. Studies to identify the factors predisposing to developmental delay in preterm infants showed that among the variables affecting the developmental status, only the breastfeeding variable in the first year of life had the power to predict the developmental status of preterm infants at one year of age. Thus, the risk of developmental delays in preterm infants who breastfed in the first year of life or fed with a combination of breast milk and complementary food is approximately one-fifth of preterm infants who are not breastfed in the first year of life. Many studies have emphasized the effect of the way of initial feeding in preterm infants on better weight growth, height growth, head circumference growth, and neural development of these infants.[32,33,34] Some studies have also shown the effect of feeding on the body’s resistance to acute diseases in preterm infants.[35,36,37] However, studies by Cormack and Bloomfield FH,[38] and Stephens et al.[39] revealed the positive effect of protein consumption on the growth of preterm infants. Human milk contains precursors of unsaturated fatty acids, especially docosahexaenoic acid (DHA) and arachidonic acid, which play an important role in the growth and development of nerve cells. In Schwarzenberg et al.’s study,[40] and Miller et al.’s study,[41] a statistically significant relationship was also reported between the number of breastfeeding days and better cognitive development outcomes in preterm infants. Meier et al.’s study,[42] and Jobe et al.’s study,[43] also introduced breastfeeding as one of the important predictors of cognitive development outcomes in preterm infants.[42,43] Every study has limitations; sensory and social developmental delay, speech, and communication are more common in boys than in girls. In this study, physical examinations did not focus on the gender of the participants; it is recommended to pay attention to this issue in future studies. Also, considering that the prematurity of the baby is one of the important risk factors for developmental delay, it is recommended to consider the initial visit to the hospital in terms of neurological condition for these children so that early diagnosis can plan other measures.
Conclusion
The present study showed that breastfeeding in the first year of life was considered one of the most important predictors of normal development in preterm infants. Therefore, encouraging the parents of these infants to breastfeed their infants at birth can be a positive step in improving the quality of life of these infants in the future. However, given the significant effect of some infants’ demographic and clinical factors at birth, such as birth height, duration of ventilator connection, Apgar scores (first and twentieth minutes), and the incidence of problems such as seizures, decreased reflex, and pneumonia on the developmental status of these infants at one year of age, neonatal specialists are advised to pay adequate attention to preterm infants, including the mentioned risk factors, and to provide parents with the necessary recommendations regarding the effect of breastfeeding on the developmental process of these infants.
Financial support and sponsorship
This study was supported by the Tuberculosis and Lung Disease Research Center, Tabriz University of Medical Sciences, Tabriz, Iran.
Conflicts of interest
There are no conflicts of interest.
Acknowledgement
This article is supported by the Tabriz University of Medical Sciences; the author of this article is extremely grateful for the support of the Tabriz University of Medical Sciences.
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