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Two-Year Follow-Up Study on Neurodevelopmental Outcomes After Term Intrapartum Asphyxia Using Age and Stages Questionnaire
Zarrin Keihani-Doust, Maryam Saeedi, Tahere Esmaeilni, Massoud Habibi and Seyed Saeed Hashemi Nazari J Child Neurol published online 30 October 2012 DOI: 10.1177/0883073812461564 The online version of this article can be found at: http://jcn.sagepub.com/content/early/2012/10/18/0883073812461564

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PhD3 Abstract Birth asphyxia is one of the multiple causes of neonatal encephalopathy. and existence of mother disease during pregnancy were also associated with lower Age and Stage Questionnaire total score in different stages of life. MPH. duration of signs. To our knowledge. MD1. alertness.3% of 18-month-old infants.com/journalsPermissions. Keshavarz Boulevard. drugs. Delivery type. Iran 2 Iranian center for Breast Cancer. 20% of infants with hypoxic-ischemic encephalopathy die during infancy and 25% suffer from permanent neurodevelopmental impairment.3% of 24-month-old infants had neurodevelopmental delay in gross motor function in the absence of cerebral palsy.nav DOI: 10. MD2. Higher values of Apgar score and bicarbonate levels were associated with higher Age and Stage Questionnaire total score. body posture. School of public Health. or a neurodevelopmental disability. The 5-year incidence of asphyxia was estimated to be 5. the remaining cases are assumed to be asphyxia related. and Seyed Saeed Hashemi Nazari. MD1. few studies have been done on the neurodevelopmental function of term infant with asphyxia in developing countries and in our country this study is the first 1 Department of Pediatrics. In 7. Imam Hospital. asphyxia.Original Article Journal of Child Neurology 00(0) 1-7 ª The Author(s) 2012 Reprints and permission: sagepub. Department of Pediatrics. Imam Hospital. inadequate relaxation of uterus caused by excessive administration of oxytocin. 2012. MPH1. and infections are excluded. Massoud Habibi. inadequate oxygenation of maternal blood.sagepub. Different disorders in mother can cause fetal hypoxia. Encephalopathy is the result of brain malfunction that can be classified as acute versus chronic or stable versus progressive. Tehran University of Medical Sciences. Thirty infants met study criteria for asphyxia.com . Iran Email: m_saidi52@yahoo. 14. MD.1 Birth asphyxia is one of the multiple causes of neonatal encephalopathy. tone. Tehran University of Medical Sciences. 3% have nonhypoxic ischemia and less than 1% have prenatal injuries. Tehran. Apgar. Age and Stage Questionnaire. According to the Age and Stage Questionnaire. MD. including low maternal blood pressure. Moro reflex. Tehran. 2012. Accepted for publication August 27. Iran Corresponding Author: Maryam Saeedi. MPH. and compression of cord.4 Hypoxic-ischemic encephalopathy usually occurs in 1 to 2 per 1000 newborn infants. Stage 2 has varied prognosis and stage 3 or persistence of stage 2 for more than 7 days or failure of EEG to revert to normal is associated with neurodevelopmental impairment or death.1177/0883073812461564 http://jcn. neurodevelopmental delay in problem-solving ability was observed. The prognosis of stage 1 is good.3% of 12. encephalopathy Received June 18.5% of 6-month-old infants. Tehran. in the literature on neonatal encephalopathy. gravidity of mother. Academic Center for Education. and electroencephalogram (EEG) abnormalities into 3 stages. Maryam Saeedi. MD. Tehran University of Medical Sciences. Gharib Street.5 Almost. term infant.2 Although in some studies these 2 terms are considered the same.and 18-month-old infants. Expected outcomes for a term newborn with intrapartum asphyxia are normality. placental insufficiency.5 in 1000. and 5. once infants with major malformations.3 Hypoxic-ischemic encephalopathy is classified according to assessment of feeding. premature separation of placenta. maternal age. metabolic causes. tendon reflexes. Tehran. Culture and Research. death. cornea situation. myoclonus. The objective of this study was to evaluate neurodevelopmental outcomes of newborn term infants with definitive asphyxia. Tahere Esmaeilni. 10.com Two-Year Follow-Up Study on Neurodevelopmental Outcomes After Term Intrapartum Asphyxia Using Age and Stages Questionnaire Zarrin Keihani-Doust. Keywords neurodevelopmental delay. Iran 3 Department of Epidemiology and Biostatistics. About 80% of full-term infants with encephalopathy have acute injuries.

communicative. organ failure. This screening tool assesses cognitive. a total of 5455 term infants were born in the study location. fetal heart rate abnormalities. Asphyxia Definition There is not any global agreement on definition of asphyxia. diabetes mellitus. the need for immediate neonatal resuscitation. 5. The neonatal variables included birth weight.10 Other parameters that are used to diagnose intrapartum hypoxia include the presence of meconium stained liquor. and multiorgan system failure. Maternal disorder during pregnancy was found in 8 cases (diabetes mellitus. The cases that had 1 major criterion and at least 2 minor criteria were diagnosed as intrapartum hypoxia. chest compression. Infants who suffered from metabolic diseases or congenital abnormalities were excluded from this study. Cord blood pH of less than 7. chronic renal diseases. abnormal EEG. hemoglobinopathies. and moderate to severe encephalopathy. and platelets disorder). College Station. infectious diseases with systemic manifestations. According to the American Academy of Pediatrics and the American College of Obstetrics and Gynecology in 1996. The cut-off scores of the questionnaire are presented in the appendix. and 0. asthma. positive pressure ventilation. Our review literature showed that 3 sets of criteria are used mostly for diagnosis of asphyxia. asthma. although none of them have acceptable sensitivity or specificity for diagnosis. The maternal variables included age at pregnancy. Univariate comparisons of maternal and neonatal variables with the Age and Stage Questionnaire scores were made using linear regression. in children from 25 to 36 months at 3-month intervals and in children from 37 to 60 months at 6-month intervals. fine motor. neonatal encephalopathy. 12-. and a base deficit more than 12 mmol/L in the blood sample from the first hour were the major criteria. Apgar score during the fifth minute. and moderate to severe encephalopathy. delivery type (cesarean section versus normal vaginal delivery). Of these children.6 intrapartum hypoxia was defined by profound acidosis (cord pH <7. Low Apgar scores (<5) at 5 minutes or beyond. version 10 (Stata Corporation. bicarbonate level. infant blood pH of less than 7. 73. considering all the above-mentioned definitions.11 In this study. hypothyroidism. and existence of any chronic diseases during pregnancy (eg. problem-solving ability. immunologic disorders. eclampsia. and not yet were converted to points 10. The Student t test was used to compare means of subcategories of patients. intubation and occurrence of seizure. Each questionnaire contains 30 questions.0). fine motor function. and 24-month-old infants. meconium stained liquor. This screening tool contains 5 questionnaires that assess 5 neurodevelopmental areas. and other chronic and systemic disorders).4 In this study. and personal-social area. The 5-year incidence of asphyxia was estimated to be 5. personal-social) with the empirically derived cutoff points for that area. Tehran. These questionnaires are designed to be completed by anyone who spends time with the child on a regular basis. From these infants. Results Between 2007 and 2011. In some studies.3% were male and 26. Journal of Child Neurology 00(0) intervals. The cut-off scores of the questionnaire are presented in the appendix. the need for immediate neonatal resuscitation. thalassemia. chronic hypertension. pH level of blood sample. The responses yes. eclampsia and pre-eclampsia. Categorical data were analyzed using chi-square and Fisher exact test where applicable. 30 met study criteria for asphyxia and were included in our study. Assessment in children older than 4 months and younger than 24 months is performed at 2-month . about the child’s everyday activities. hypothyroidism.8 There is no consensus on pH levels of less than 7 for the definition of fetal hypoxia.9 but the risk of neonatal morbidity and mortality in neonates with an umbilical arterial cord pH of less than 7 is higher. Because the numbers of patients in subcategories were not large. A p value less than . intrapartum hypoxia is defined by metabolic acidosis (infant blood pH <7 in the first blood sample and a base deficit >12 mmol/L. gestational age. in 2003 the essential criteria for assigning the term of intrapartum hypoxia is as follows: metabolic acidosis (pH <7 and a base deficit >12 mmol/L). low Apgar score (<3) at 5 minutes or beyond. Statistical Analysis The questionnaires were scored by converting each answer to a numerical equivalent and comparing the totals for each area (eg. 3 major and 5 minor criteria for defining hypoxia have been used. abnormal EEG. ischemic injuries have been observed with pH levels of more than 7. base deficit.2. 18-.05 was considered to be significant. The objective of our study was to evaluate neurodevelopmental outcomes of a cohort of newborn term infants with defined asphyxia. The mean gestational age was Outcome Measurement The Age and Stage Questionnaire was applied for measuring neurodevelopmental outcomes following asphyxia.7 According to the International Cerebral Palsy Task Force in 1999. greater than 36 weeks’ gestation) were enrolled in a prospective cohort study with a 24-month follow-up. and abnormal imaging studies.2 in this field. gross motor function. grouped by developmental area. we used this tool for 6-. gravidity. The statistical analysis was performed with Stata software. According to the American College of Obstetrics and Gynecology. Infants who met our criteria for definition of intrapartum hypoxia and were born at term (ie. The number of infants with each of the inclusion criteria is presented in Table 1. sometimes.2. platelet disorders. Predictive Variables We assessed the effect of a number of maternal and neonatal variables on the Age and Stage Questionnaire score. we also compared means with the Kruskal-Wallis test for numerical variables.7% were female.5 in the 1000 term neonates. The majority of these children (57%) were the first child of the family. the presence of meconium stained liquor. respectively. These outcomes were measured by Age and Stages Questionnaire. and motor development and helps identify the need for further social and emotional behavior assessment in children at a number of age intervals. Methods Study Population All deliveries were scanned in a university-based pediatric hospital between 2007 and 2011 in the capital city of Iran. 60% were born through cesarean section and 40% through normal vaginal delivery. chronic hypertension. TX). and acute changes in imaging studies were the minor criteria. including communication.

Apgar score and bicarbonate levels in blood were associated positively with the total Age and Stage Questionnaire Score and the base deficit was associated negatively with the total Age and Stage Questionnaire score. gross motor function was lower than the cut-off score. The results of fitted models are presented in Table 3. Numbers of Infants With Each of the Inclusion Criteria Range Inclusion criteria n (%) Min Max Average 7. The infants of mothers who had a disease during pregnancy. periventricular leukomalacia.3) –21 –4. the Age and Stage Questionnaire score decreased by 4. The results of fitted models are presented in Table 3. base deficit. and 13. an Age and Stage Questionnaire Score that was 14 points less than other infants. separate univariate models were fitted to define the maternal and neonatal variables that affect the Age and Stage Questionnaire score. had.1 –12. intubation (P ¼ . From maternal and neonatal variables. and mother disease during pregnancy. Cord blood pH <7. choroid plexus cyst and ventriculomegaly were observed in 5 ultrasonographic and 3 computed tomographic scans. 26. gravidity of mother.022) and death outcome. Acute asphyxia changes including intraventricular hemorrhage. Univariate analysis of the neonatal and maternal factors showed a positive effect for Apgar score on the Age and Stage Questionnaire score. The personal-social score was associated positively with the Apgar score and the bicarbonate level and negatively with the base deficit. . The gross and fine motor scores were associated negatively with base deficit and positively with the bicarbonate level. For a 5-year increment in mother’s age.3% and 7.005). gross motor function was lower than the cut-off score. From the maternal and neonatal variables. and personal-social area.7 5-minute Apgar scores <5 2 (6. The problem-solving ability score was associated negatively with the base deficit and positively with the bicarbonate level. In 10. Again. Age and Stage Questionnaire scores of each of the 5 neurodevelopment areas were also regressed on maternal and neonatal variables. In 14. The problem-solving ability score was associated negatively with base deficit and positively with bicarbonate levels.3) – – Abnormal EEG 3 (10) – – Abnormal brain imaging 8 (26. The results of fitted models are presented in Table 2. and personal-social area.6) – – Abbreviation: EEG. 23. problem-solving ability. on average. From these infants.3 Base deficit >12 13 (43. 23. Age and Stage Questionnaire Scores in 6-Month-Old Infants All the infants received higher than the cut-off score in communication. 3 (10%) died (2 on the first day and 1 on the 19th day of life).7 weeks. The gross motor score was associated positively with bicarbonate levels.3) – – Immediate neonatal resuscitation 25 (83. The gross motor score Age and Stage Questionnaire Scores in 18-Month-Old Infants In this age. The communication score was associated positively with positive-pressure ventilation. electroencephalogram.1 – – – – 3 was associated positively with the Apgar score. problem-solving ability. fine motor function.7) 2 9 Presence ofmeconium-stained liquor 4 (13. The results of fitted models are presented in Table 3.3% had seizures within 3 days following the delivery.2 6. The results of fitted models are presented in Table 2. 38. The personal-social score was not associated with any of the defined maternal and neonatal variables.5% of infants.3% had 38 weeks. and the Apgar score of infants who died in comparison to other infants. 16. the association of the total score of the Age and Stage Questionnaire and the score in each of the 5 neurodevelopmental areas and maternal and neonatal variables were evaluated in separate univariate regression models.Keihani-Doust et al Table 1.3%) received positive-pressure ventilation at the time of delivery. Of 30 infants with asphyxia.1% of infants respectively. and abnormal finding in brain ultrasonography (P ¼ .2 18 (60) 6.25 points. The communication score was associated negatively with the existence of a disease inside the mother during pregnancy. The fine motor score was associated negatively with delivery type (cesarean section vs normal vaginal delivery). The maternal age and the mother’s disease during pregnancy demonstrated a negative effect. only the gross motor function and problem-solving abilities were abnormal in 14. The fine motor score was not associated with any of the defined maternal and neonatal variables. The communication score was not associated with any of the defined maternal and neonatal variables. 20% had 40 weeks. Age and Stage Questionnaire Scores in 12-Month-Old Infants All the infants received higher than the cut-off score in communication.009). We could not find any significant differences in the pH level. The problem-solving ability score and the personal-social score were associated negatively with birth weight.3% of infants. and for 20% intratracheal intubation was performed. fine motor function. the mean bicarbonate level of the blood samples was associated positively with the total Age and Stage Questionnaire score and the base deficit was negatively associated. 20% received cardiac resuscitation.3% had more than 40 weeks. To define the predictors of neurodevelopmental outcomes. The results of fitted models are presented in Table 2.7% had 37 weeks. Brain ultrasonography was performed on 24 infants and brain computed tomography was performed on 7 infants.7% had 39 weeks.8 7. Twenty-five infants (83. Imaging studies were performed on the neonate who had clinical signs of hypoxia. There was a statistically significant association between seizure (P ¼ .

memory.2)* 0.0.2 –4.7 –2.3) –3.4) –14.7) –0.2 (–8. In 7.8 1. 1.5% of patients.6.7 (0.3.7 (0.3 (–0.0 (–16.7 –3.0) 0.7)* 16.4 (–9. The problem-solving ability score was associated negatively with the base deficit and the mother’s disease and positively with the Apgar score and seizure occurrence in infants.6) (–1. 7.3 (–9.5. 43.4. 5.3 (–4. language.2 (–4.4 (–5. mental retardation or intellectual disability.4) (–13.9) 0. problem-solving ability.8) –5. 6. 12-. The communication score was associated negatively with the mother disease during pregnancy and positively with positive pressure ventilation. 4.0.1 (–23. 2.8.9.3) 0.3% of 18-month-old infants.5. 3.3.4.0. learning.5 2. (95% CI) 4.9) (0. 0.5 –3.0) –8. 9.12 Approximately 15% to 20% of infants with neonatal encephalopathy will die during the newborn period.5. such as umbilical artery blood gases or Apgar scores.0) –0. –4.6 (0.1)* 1.3% of 12. 13.3 (–9.2) 2.9.7 6.3. 4.8. 10. 0.7) 1.1 (–6. cognitive. a neurodevelopmental disability is a relatively common consequence of term intrapartum asphyxia. 11.2)* 15. 2.3.4.3) 1. 3. 14.0.5. 1.6 (–7.2) (–9. 18-.2 (–2.5 (–14.0 (–0.0 (–0.5) –3.3.3% of infants and all other neurodevelopmental areas were normal. 5.4. and 24-Month-Old Infants 6th month Coeff.1.5.0 –0. 4.8 (–1.13 In our study. The personalsocial score was associated negatively with the child’s birth weight.2. 12th month Coeff.2) –4. These findings are in accordance with other studies in this field.5 (–9. Higher level of bicarbonate was also a predictor of higher total Age and Stage Questionnaire score and better gross and fine motor function. a higher value of Apgar score was a predictor of higher Age and Stage Questionnaire total score and also better gross motor and personal-social function and problem-solving ability.9. (95% CI) –0.1) 0.2 (–6. and secondary microcephaly) in absence of cerebral palsy in term intrapartum asphyxia.6 (0.3)* 0. 0. developmental language impairment.7 –0.4) 1.7. 9.3 (–37. The lack of an objective marker of term intrapartum asphyxia has clouded efforts to clinically diagnose intrapartum asphyxia and to understand its potential range of adverse outcomes.3.5.1.4. 3 of 30 infants with asphyxia (10%) died. 9. 1.9 (–1.0 (–9.4.001.3) –1.1.1)* (–10. 4.0 29.1. attention deficit hyperactivity disorder.8) –0.8 (0.4.7 (–8.0) 24th month Coeff. personalsocial function and problem solving ability.7) 0.9.6 (–16.4.5 In our study. Univariate analysis showed a positive association between Age and Stage Questionnaire Score and bicarbonate levels and a negative weak association between base deficit and the Age and Stage Questionnaire Score. The results of fitted models are presented in Table 3.1.4) (–10.4) (–10. and 25% of the survivors will sustain permanent clinical deficits.8) –11.4) 0.4. 2.9 (–33.12 Prior studies have shown that clinical and biochemical variables.8) 2.3% of 24-month-old infants had neurodevelopmental delay in gross motor function in the absence of cerebral palsy. neurodevelopmental delay in problem solving ability was observed.2 –0. 6. 9.6 (–16.8. 4.1) Age and Stage Questionnaire Scores in 24-Month-Old Infants At this stage. 1. 4.1 (–10. Base deficit was associated negatively with Age and Stage Questionnaire total score and also gross motor.2 –5.2 (–6.3 (–12.1) (–16.2 (–1. (95% CI) 3.0) 2. and personal-social function.9. The fine motor score was not associated with any of the defined maternal and neonatal variables. 5.4.2) –2.3.5) (–14. 18.4) (–0. 3.1 (–16. 22.1 (–9. which occurs in approximately 41.4 (–2. 1.7 –0. **P < . 4.5.2 (–4.3)* –2.5% of 6-month-old infants. 1.7.3. 3.8 (–0.7) 0. The results of fitted models are presented in Table 2.2. learning disabilities. 71.8 (–12.1. epilepsy.0 (–5. 1.1. 15. 5. 4.6) 0.0.6. 1. 1. (95% CI) Sex Maternal age Gestational age Birth weight Delivery type Gravidity Mother disease during pregnancy Meconium-stained liquor Apgar score in fifth minute pH Base deficit Bicarbonate level Positive pressure ventilation Chest compression Intubation Seizure *P < .3) 5. 6. The gross motor score was associated positively with the Apgar score and negatively with maternal age and maternal disease. autistic spectrum disorders.2)* 1.0 (–14. 14. ***P < .7.2. 13.3.9. 1.4 Journal of Child Neurology 00(0) Table 2.0.0) 3. and behavioral deficits and limitations that may reach the threshold for the diagnosis of a specific neurodevelopmental disability (including global developmental delay.8) 0.6 (–5.8) 0.5 In the current study. 11.and 18-month-old infants and 5.5) –6. are of limited value in predicting neurodevelopmental outcomes.2) 0.0. just the gross motor function was under the cut-off limit in 5.05.0 1.9) 18th month Coeff.3) (-1. 5.6.5 (–2.5 Only 10% of infants with evidence of hypoxic ischemic encephalopathy develop cerebral palsy.2. Regression of Age and Stage Questionnaire Total Scores on Maternal and Neonatal Factors in 6-. .6) 0. 9.9) (–11.8.4) –2.9.2.9)* (0. Some studies have shown that in the absence of cerebral palsy. 8. 0. 5. 15. 2.4.9 (0. including motor. –0. Discussion Intrapartum asphyxia is only one of the many possible causes of neonatal encephalopathy.8 2.4) (–12.7 (–0.5)** 1. 65.0 (–10.7 (–5.12 Some other studies have documented much lower prevalence for a variety of adverse neurologic outcomes. 22.7.5) –4.1) –1. 6. 4. 10.4.0) –4.5.6) (–17.01.1) –0.

–1.3)* Motherage –1.5)* Neurodevelopmental areas Coeff. –1.9)* Fine motor Problem solving Apgar score 7. **P < . 1.2 (0.1.3)** Gravidity –6. –1. –0. 7. (95% CI) 6th month Variable Communication Mother disease –22.5. 16. 5.0 (0.1 (0.3 (–8.0 (2. –2.1.7 (–3.9. 29. –0.1 (0. ***P < . 13. –1.3)* Bicarbonate level 1.1 (–0. –44.7 (–14.3 (0.2)** Mother disease Gross motor Apgar score 1.7 (–14.5.Table 3.4)** Birth weight Base Deficit –1.4 (–27. (95% CI) Variable 18th month 24th month Coeff.2 (0.6 (2.8)* Bicarbonate level 1.3.2)** 1.0 (–7.0.05.3 (1.4)* Birth weight –1.0 (0.4)* Bicarbonate level 3. (95% CI) –49. –1.4 (–54.8)** Bicarbonate level 1.9)** Base Deficit Mother disease Apgar score Seizure –5.4)* Base Deficit –1.8 (–0.7)* Base Deficit –2.5. 1. 2.5.8.1)* *P < .2. –7.6.6.6 (–0.002)* Apgar score 6.4. and 24-Month-Old Infants 12th month Variable Positive pressure ventilation 3 9. 9.2(2. 1.6 (1. (95% CI) Variable Coeff.1 (–32.01.9 (–38.3.3)* Bicarbonate level Mother disease –21.– 2. Regression of Age and Stage Questionnaire Score in Each of 5 Neurodevelopmental Areas on Maternal and Neonatal Factors at 6-.7)* Birth weight –5.2 (–9. 12-.6)** –14.2. –1.7. 18-. – 5. 5 .2 (1.3 (–42.5.4 (–0. –0. 2.1.9.3.4 (–0.0. –2. –1.2.1)* Personal-social Apgar score 3. 10.1.5)* Base Deficit –0.8)** Base Deficit Bicarbonate level –1.1.001.4)* Coeff.0.4 (–11. –0.9 (–0.3.5)* –4.1)* 4.9)* Delivery –7.5)** 16.4)* Mother disease –7.9)* –17. 5.9.2.5. –2.3)*** Positive pressure ventilation3 5.5.

Semin Perinatol. Acta Paediatr.41:399-405. the delivery type (cesarean section versus normal vaginal delivery). Miller SP. Nelson KB. MD: Brookes Publishing. Author Contributions ZKD helped in patient follow-up.199:587-595. 16. Am J Obstet Gynecol. Clinicians should observe all infants with this diagnosis at birth. J Pediatr. Squires & Bricker.14 In this study. Predictive factors for neonatal morbidity in neonates with an umbilical arterial cord pH less than 7. Graham EM. The value of a scoring system for hypoxic ischaemic encephalopathy in predicting neurodevelopmental outcome. data gathering. 1997. Graham E. In some studies.340:c1471. Journal of Child Neurology 00(0) References 1. 4. 15. several other maternal and neonatal factors affect neurodevelopmental disability. Hao Y. Macones GA. Ekert P. 17. 2. Latal B. Although some patients with term intrapartum asphyxia show manifestations of cerebral palsy. BMJ. Pediatr Neurol. Steinlin M. Northington FJ. Am J Obstet Gynecol. Miller SP. rehabilitation and treatment.319:1054-1059. Clinicians should be aware of a full range of these possible adverse outcomes and screen children for fast detection. Ethical Approval This project was confirmed by the ethical committee of the Tehran University of Medical Sciences. Strength of association between umbilical cord pH and perinatal and long term outcomes: systematic review and meta-analysis. Clinical signs predict 30-month neurodevelopmental outcome after neonatal encephalopathy. low arterial umbilical cord pH had a strong and temporal association with neonatal mortality and morbidity. Shevell MI. and intrapartum asphyxia. 10.18-21 We could not find any statistically significant differences between pH levels and base deficit and Age and Stage Questionnaire scores. Philadelphia. eds. Seizure-associated brain injury in term newborns with perinatal asphyxia.86: 339-344. Perlman M. and/or publication of this article. TE helped in data gathering and writing the Introduction and Methods sections. Nelson Textbook of Pediatrics. and/or publication of this article. The importance of neonatal seizures in predicting abnormal outcome. Int J Gynaecol Obstet. Thompson C. Predicting the outcome of postasphyxial hypoxic-ischemic encephalopathy within 4 hours of birth. Namasivayam A. We observed these infants for 2 years. Am J Obstet Gynecol. SSHN helped in statistical analysis of data and in writing the Results section. Shevell M. St Geme J. 1999. Paterson-Brown S. 8. November 1986). authorship. Kumar S. Al-Macki N. Kurinczuk JJ. Morgan MA. Clark H. Use and abuse of the Apgar score (replaces No. Badawi N. 14. 49. 1997. and mother disease during pregnancy were associated with a lower total Age and Stage Questionnaire score in different stages of life. 1998. Stamilio DM. Neurology. 2004. statistical analysis of data. Brain injury in the term infant. Barnwell A. Stanton BMD. Early Human Development. American College of Obstetricians and Gynecologists.58:542-548. Sehdev HM.190:93-99. The ‘‘Bermuda triangle’’ of neonatal neurology: cerebral palsy. . Keogh JM. Perlman JM. 2009. 7. Hall N.86: 757-761. Ages and Stages Questionnaire. ACOG committee opinion. Maternal and neonatal risk factors can be a good predictor for higher rate of adverse neurodevelopmental outcomes in infants with term intrapartum asphyxia. authorship. et al. Semin Pediatr Neurol. Malin GL.317:1554-1558. 2004. is supported by several previous cohort studies. Behrman RE. MH helped in statistical analysis of data and in writing the Discussion section. Third Edition. 2008. A systematic review of the role of intrapartum hypoxia-ischemia in the causation of neonatal encephalopathy. 6. Leviton A. 2004. BMJ. Fox HE. MS helped in data gathering. there was a statistically significant association between seizure and death outcome and problem-solving ability in 18-month-old infants.00. 3. A template for defining a causal relation between acute intrapartum events and cerebral palsy: international consensus statement. et al. How much of neonatal encephalopathy is due to birth asphyxia? Arch Pediatr Adolesc Med. The spectrum of abnormal neurologic outcomes subsequent to term intrapartum asphyxia. Acknowledgment The authors thank the Imam Hospital staff of the pediatric ward and clinic who helped with patient follow-up. 2010. Committee on Obstetric Practice and American Academy of Pediatrics: Committee on Fetus and Newborn.15-17 In our study. 1996. Funding The authors received no financial support for the research. 12. In Kliegman RM.5. 1991. Schor N. and in writing the Results and Discussion sections of the article. Miller S.54:303-305. 13. et al. Baltimore.145:1325. Hypoxic-ischemic encephalopathy. Puterman AS. 2011: 569-571. maternal age. Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research. MacLennan A. PA: Saunders. Ruis KA. 2002. 2010. Khan KS.177:1030-1034. Obstetric aspects of hypoxic ischemic encephalopathy. many others may demonstrate other adverse outcomes. 5. Hartman AL. gravidity of mother. even in the absence of overt neonatal encephalopathy.11:24-30. 9. and writing the Discussion section of the article. 19th ed. neonatal encephalopathy. but an extended followup duration is required to be sure of detecting all possible adverse outcomes. 1997. Weiss J.6 Neonatal encephalopathy is a clinical syndrome of impaired neurologic function of heterogeneous cause. 2012. Morris RK. et al. Linley LL.28:415-424. Although birth asphyxia may be an important cause of neonatal encephalopathy. BMJ. Carlo WA.131:613-617. Intrapartum risk factors for newborn encephalopathy: the Western Australian case-control study. 11.

Keihani-Doust et al 18. Thorp JA.49:735. 1999. Johnston MV. Fahey J. Intrauterine asphyxia: clinical implications for providers of intrapartum care. . 2004.26:695-709. 2001. King TL. Trescher WH. 2005. Umbilical cord blood gas analysis. Neonatal brain injury.351: 1985-1995. Obstet Gynecol Clin North Am.50: 498-506. 19. Nakajima W. Ferriero DM. J Midwif Womens Health. Neurobiology of hypoxic-ischemic injury in the developing brain. 21. Pediatr Res. N Engl J Med. Ishida A. Rushing RS. 7 20.