Skip to main content
SpringerLink
Log in

Association between early-term birth and delayed neurodevelopment at the age of 2 years: results from a cohort study in China

  • Original Article
  • Published:
European Journal of Pediatrics Aims and scope Submit manuscript

Abstract

A growing body of evidence indicates that early-term births (37–38 weeks of gestational age) have an increased risk of short-term and long-term complications. Here, we sought to explore the association between early-term births and the risk of delayed neurodevelopment at age 2 years. Pregnant women and their live singleton birth were recruited from a single tertiary hospital between October 2013 and February 2017. Mental and Psychomotor Development Indexes (MDI and PDI) were assessed using the Bayley Scales of Infant Development (BSID). Delayed neurodevelopment was defined as scores of PDI or MDI less than −1SD relative to the mean score of the study population. In total, 1678 full-term infants and 727 early-term infants were assessed when they were 2 years old. After adjustment for potential confounders, early-term birth was related to 43% increased odds of neurodevelopmental delay in the PDI domain as compared with full-term birth (OR: 1.43; 95% CI: 1.12, 1.82). The observed associations were more prominent among those infants born by cesarean (OR: 1.44; 95% CI: 1.03, 2.00) and among males (OR: 1.66; 95% CI: 1.20, 2.28). No statistical difference in the MDI domain was found between early-term and full-term births.

Conclusions: Our findings suggest that early-term birth was associated with increased odds of delayed neurodevelopment in the PDI domain as measured by BSID assessments at age 2 years. Health professionals should be aware of the influence of early-term birth on the risk of delayed neurodevelopment.

What is Known:

• Evidence indicates that early-term births have an increased risk of short-term and long-term complications.

• The association between early-term births and delayed neurodevelopment at their early childhood has not been widely studied.

What is New:

• Early-term birth was associated with increased odds of delayed neurodevelopment in PDI domain as measured by BSID assessments at age 2 years.

• The observed associations were more prominent among infants born by cesarean section and among male infants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

MDI:

Mental Development Index

PDI:

Psychomotor Development Index

BSID:

Bayley Scales of Infant Development

CI:

Confidence interval

SD:

Standard deviation

BMI:

Body mass index

GDM:

Gestational diabetes mellitus

PIH:

Pregnancy-induced hypertension

SGA:

Small gestational age

References

  1. Spong CY, Defining “term” pregnancy: recommendations from the defining “term” pregnancy workgroup. Jama 2013. 309(23): 2445-2446, Defining “Term” Pregnancy.

  2. Paz Levy D, Sheiner E, Wainstock T, Sergienko R, Landau D, Walfisch A (2017) Evidence that children born at early term (37-38 6/7 weeks) are at increased risk for diabetes and obesity-related disorders. Am J Obstet Gynecol 217(5):588.e1–588.e11

    Article  Google Scholar 

  3. Odibo IN, Bird TM, McKelvey SS, Sandlin A, Lowery C, Magann EF (2016) Childhood respiratory morbidity after late preterm and early term delivery: a study of medicaid patients in South Carolina. Paediatr Perinat Epidemiol 30(1):67–75

    Article  Google Scholar 

  4. Dong Y, Chen SJ, Yu JL (2012) A systematic review and meta-analysis of long-term development of early term infants. Neonatology 102(3):212–221

    Article  Google Scholar 

  5. Seikku L, Gissler M, Andersson S, Rahkonen P, Stefanovic V, Tikkanen M, Paavonen J, Rahkonen L (2016) Asphyxia, neurologic morbidity, and perinatal mortality in early-term and postterm birth. Pediatrics 137(6)

  6. Huppi PS, Warfield S, Kikinis R, Barnes PD, Zientara GP, Jolesz FA, Tsuji MK, Volpe JJ (1998) Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann Neurol 43(2):224–235

    Article  CAS  Google Scholar 

  7. Smithers LG, Searle AK, Chittleborough CR, Scheil W, Brinkman SA, Lynch JW (2015) A whole-of-population study of term and post-term gestational age at birth and children’s development. Bjog 122(10):1303–1311

    Article  CAS  Google Scholar 

  8. Quigley MA, Poulsen G, Boyle E, Wolke D, Field D, Alfirevic Z, Kurinczuk JJ (2012) Early term and late preterm birth are associated with poorer school performance at age 5 years: a cohort study. Arch Dis Child Fetal Neonatal Ed 97(3):F167–F173

    Article  Google Scholar 

  9. Chan E, Quigley MA (2014) School performance at age 7 years in late preterm and early term birth: a cohort study. Arch Dis Child Fetal Neonatal Ed 99(6):F451–F457

    Article  Google Scholar 

  10. Richards JL, Drews-Botsch C, Sales JM, Flanders WD, Kramer MR (2016) Describing the shape of the relationship between gestational age at birth and cognitive development in a nationally representative U.S. birth cohort. Paediatr Perinat Epidemiol 30(6):571–582

    Article  Google Scholar 

  11. Shah P, Kaciroti N, Richards B, Oh W, Lumeng JC (2016) Developmental outcomes of late preterm infants from infancy to kindergarten. Pediatrics 138(2)

  12. Bedford R, Pickles A, Lord C (2016) Early gross motor skills predict the subsequent development of language in children with autism spectrum disorder. Autism Res 9(9):993–1001

    Article  Google Scholar 

  13. Richards JL, Kramer MS, Deb-Rinker P, Rouleau J, Mortensen L, Gissler M, Morken NH, Skjaerven R, Cnattingius S, Johansson S, Delnord M, Dolan SM, Morisaki N, Tough S, Zeitlin J, Kramer MR (2016) Temporal trends in late preterm and early term birth rates in 6 high-income countries in North America and Europe and association with clinician-initiated obstetric interventions. Jama 316(4):410–419

    Article  Google Scholar 

  14. Cheng L, Zhang B, Huo W, Cao Z, Liu W, Liao J, Xia W, Xu S, Li Y (2017) Fetal exposure to lead during pregnancy and the risk of preterm and early-term deliveries. Int J Hyg Environ Health 220(6):984–989

    Article  CAS  Google Scholar 

  15. Han Y, Mao LJ, Ge X, Huang K, Yan SQ, Ren LL, Hong SQ, Gao H, Sheng J, Xu YY, Pan WJ, Zhu P, Hao JH, Zhu DF, Tao FB (2018) Impact of maternal thyroid autoantibodies positivity on the risk of early term birth: Ma’anshan Birth Cohort Study. Endocrine 60(2):329–338

    Article  CAS  Google Scholar 

  16. Al Khalaf SY, O’Neill SM, O’Keeffe LM, Henriksen TB, Kenny LC, Cryan JF, Khashan AS (2015) The impact of obstetric mode of delivery on childhood behavior. Soc Psychiatry Psychiatr Epidemiol 50(10):1557–1567

    Article  Google Scholar 

  17. Deoni SC, Adams SH, Li X, Badger TM, Pivik RT, Glasier CM, Ramakrishnaiah RH, Rowell AC, Ou X (2019) Cesarean delivery impacts infant brain development. AJNR Am J Neuroradiol 40(1):169–177

    Article  CAS  Google Scholar 

  18. Gur RE, Gur RC (2016) Sex differences in brain and behavior in adolescence: findings from the Philadelphia Neurodevelopmental Cohort. Neurosci Biobehav Rev 70:159–170

    Article  Google Scholar 

  19. Bale TL (2016) The placenta and neurodevelopment: sex differences in prenatal vulnerability. Dialogues Clin Neurosci 18(4):459–464

    Article  Google Scholar 

  20. Briggs-Gowan MJ, Carter AS (2008) Social-emotional screening status in early childhood predicts elementary school outcomes. Pediatrics 121(5):957–962

    Article  Google Scholar 

  21. Yi S, Luo X, Yang Z, Wan G, Zhang G, Zheng L (1993) The revising of the Bayley Scales of Infant Development (BSID) in China. Chin J Clin Psychol 1(2):71–75

    Google Scholar 

  22. Cheong JL, Doyle LW, Burnett AC, Lee KJ, Walsh JM, Potter CR, Treyvaud K, Thompson DK, Olsen JE, Anderson PJ, Spittle AJ (2017) Association between moderate and late preterm birth and neurodevelopment and social-emotional development at age 2 years. JAMA Pediatr 171(4):e164805

    Article  Google Scholar 

  23. Lee M, Ha M, Hong YC, Park H, Kim Y, Kim EJ, Kim Y, Ha E (2019) Exposure to prenatal secondhand smoke and early neurodevelopment: Mothers and Children’s Environmental Health (MOCEH) study. Environ Health 18(1):22

    Article  Google Scholar 

  24. Chin-Lun Hung G, Hahn J, Alamiri B, Buka SL, Goldstein JM, Laird N, Nelson CA, Smoller JW, Gilman SE (2015) Socioeconomic disadvantage and neural development from infancy through early childhood. Int J Epidemiol 44(6):1889–1899

    Article  Google Scholar 

  25. Hutton JL, Pharoah PO, Cooke RW, Stevenson RC (1997) Differential effects of preterm birth and small gestational age on cognitive and motor development. Arch Dis Child Fetal Neonatal Ed 76(2):F75–F81

    Article  CAS  Google Scholar 

  26. Adane AA, Mishra GD, Tooth LR (2016) Diabetes in pregnancy and childhood cognitive development: a systematic review. Pediatrics:137(5)

  27. Dai L, Deng C, Li Y, Zhu J, Mu Y, Deng Y, Mao M, Wang Y, Li Q, Ma S, Ma X, Zhang Y (2014) Birth weight reference percentiles for Chinese. PLoS One 9(8):e104779

    Article  CAS  Google Scholar 

  28. Kolobe TH, Bulanda M, Susman L (2004) Predicting motor outcome at preschool age for infants tested at 7, 30, 60, and 90 days after term age using the Test of Infant Motor Performance. Phys Ther 84(12):1144–1156

    Article  Google Scholar 

  29. Espel EV, Glynn LM, Sandman CA, Davis EP (2014) Longer gestation among children born full term influences cognitive and motor development. PLoS One 9(11):e113758

    Article  CAS  Google Scholar 

  30. Rose O, Blanco E, Martinez SM, Sim EK, Castillo M, Lozoff B, Vaucher YE, Gahagan S (2013) Developmental scores at 1 year with increasing gestational age, 37-41 weeks. Pediatrics 131(5):e1475–e1481

    Article  Google Scholar 

  31. Schonhaut L, Armijo I, Perez M (2015) Gestational age and developmental risk in moderately and late preterm and early term infants. Pediatrics 135(4):e835–e841

    Article  Google Scholar 

  32. Kinney HC (2006) The near-term (late preterm) human brain and risk for periventricular leukomalacia: a review. Semin Perinatol 30(2):81–88

    Article  Google Scholar 

  33. Moody L, Chen H, Pan YX (2017) Early-life nutritional programming of cognition-the fundamental role of epigenetic mechanisms in mediating the relation between early-life environment and learning and memory process. Adv Nutr 8(2):337–350

    Article  CAS  Google Scholar 

  34. Yanni D, Korzeniewski SJ, Allred EN, Fichorova RN, O’Shea TM, Kuban K, Dammann O, Leviton A (2017) Both antenatal and postnatal inflammation contribute information about the risk of brain damage in extremely preterm newborns. Pediatr Res 82(4):691–696

    Article  Google Scholar 

  35. Young JM, Powell TL, Morgan BR, Card D, Lee W, Smith ML, Sled JG, Taylor MJ (2015) Deep grey matter growth predicts neurodevelopmental outcomes in very preterm children. Neuroimage 111:360–368

    Article  Google Scholar 

  36. Zacharia A, Zimine S, Lovblad KO, Warfield S, Thoeny H, Ozdoba C, Bossi E, Kreis R, Boesch C, Schroth G, Huppi PS (2006) Early assessment of brain maturation by MR imaging segmentation in neonates and premature infants. AJNR Am J Neuroradiol 27(5):972–977

    PubMed  PubMed Central  CAS  Google Scholar 

  37. Dubois J, Dehaene-Lambertz G, Kulikova S, Poupon C, Huppi PS, Hertz-Pannier L (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71

    Article  CAS  Google Scholar 

  38. Obican SG, Small A, Smith D, Levin H, Drassinower D, Gyamfi-Bannerman C (2015) Mode of delivery at periviability and early childhood neurodevelopment. Am J Obstet Gynecol 213(4):578 e1-4

    Article  Google Scholar 

  39. Reuner G, Fields AC, Wittke A, Löpprich M, Pietz J (2013) Comparison of the developmental tests Bayley-III and Bayley-II in 7-month-old infants born preterm. Eur J Pediatr 172(3):393–400

    Article  Google Scholar 

  40. Donald J, Goldstein EEF, Jamie L, Wieber T (1995) Michael O’Shea, Comparison of the Bayley Scales of Infant Development-Second Edition and the Bayley Scales of Infant Development with Premature Infants. J Psychoeduc Assess 13(4):391–396

    Article  Google Scholar 

  41. Sandra G, Gagnon RJ (2000) Comparison of the revised and original versions of the Bayley Scales of Infant Development. 21(3): 293-305

  42. Luttikhuizen dos Santos ES, de Kieviet JF, Königs M, van Elburg RM, Oosterlaan J (2013) Predictive value of the Bayley scales of infant development on development of very preterm/very low birth weight children: a meta-analysis. Early Hum Dev 89(7):487–496

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the mothers and their children for the participation in this study. We give special thanks to Drs. Lulu Song and Bingqing Liu for their hard-working in the process of data collection.

Availability of data and material

N/A

Code availability

N/A

Funding

This work was supported by the National Natural Science Foundation of China (91643207) and the National Natural Science Foundation of China (81273083).

Author information

Authors and Affiliations

  1. Department of Maternal and Child Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China

    Mingyang Wu, Lulin Wang, Yunyun Liu, Jianing Bi, Qing Liu, Kai Chen & Youjie Wang

  2. Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection, and State Key Laboratory of Environmental Health (Incubation), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, #13 Hangkong Road, Wuhan, 430030, Hubei, China

    Mingyang Wu, Lulin Wang, Yunyun Liu, Jianing Bi, Qing Liu, Kai Chen, Yuanyuan Li, Wei Xia, Shunqing Xu & Youjie Wang

  3. Wuhan Children’s Hospital (Wuhan Maternal and Child Healthcare Hospital), Tongji Medical College, Huazhong University of Science and Technology, 100 Hong Kong Road, Wuhan, 430015, Hubei, China

    Aifen Zhou, Zhongqiang Cao & Rong Yang

Authors
  1. Mingyang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lulin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunyun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jianing Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kai Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuanyuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Wei Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shunqing Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Aifen Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zhongqiang Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Youjie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Rong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.Y.W. conceived the idea for the study and drafted the manuscript. M.Y.W., Y.Y.L., J.N.B., Q.L., and K.C. assembled the data under Y.Y.L., W.X., S.Q.X., A.F.Z., and Z.Q.C.’s supervision. R.Y. and Y.J.W. provided a critical review of the manuscript. All authors read and approved the final version of the manuscript. The corresponding author attests that all listed authors meet authorship criteria and that no others meeting the criteria have been omitted.

Corresponding authors

Correspondence to Youjie Wang or Rong Yang.

Ethics declarations

Ethics approval

The research protocol was approved by the ethics committee of Tongji Medical College, Huazhong University of Science and Technology, and Wuhan Children’s Hospital (Wuhan Maternal and Child Healthcare Hospital).

Consent to participate

Written informed consent was obtained from all subjects at enrollment.

Consent for publication

All authors approved this manuscript for publication.

Competing interests

The authors declare no competing interests.

Additional information

Communicated by Gregorio Paolo Milani

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 93 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, M., Wang, L., Liu, Y. et al. Association between early-term birth and delayed neurodevelopment at the age of 2 years: results from a cohort study in China. Eur J Pediatr 180, 3509–3517 (2021). https://doi.org/10.1007/s00431-021-04152-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00431-021-04152-6

Keywords

Search

Navigation