Prenatal tobacco smoke exposure and risk for cognitive delays in infants born very premature.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
16 Jan 2024
16 Jan 2024
Historique:
received:
23
08
2023
accepted:
02
01
2024
medline:
17
1
2024
pubmed:
17
1
2024
entrez:
16
1
2024
Statut:
epublish
Résumé
Prenatal tobacco smoke exposure (TSE) and prematurity are independent risk factors for abnormal neurodevelopment. The objectives were to compare differences in Bayley-III cognitive, language, and motor scores at 2 years corrected age (CA) in 395 infants born very preterm (≤ 32 weeks gestation) with and without prenatal TSE. We performed multivariable linear regression analyses to examine associations between prenatal TSE and neurodevelopmental outcomes and a mediation analysis to estimate direct effects of prenatal TSE on outcomes and indirect effects through preterm birth. In total, 50 (12.6%) infants had prenatal TSE. Infants with prenatal TSE had lower mean [95% CI] Cognitive score (82.8 [78.6, 87.1]) vs. nonexposed infants (91.7 [90.1, 93.4]). In children with and without prenatal TSE, there were significant differences in mean [95% CI] Language scores (81.7 [76.0, 87.4] vs. 92.4 [90.2, 94.6], respectively) and mean [95% CI] Motor scores (86.5 [82.2, 90.7] vs. 93.4 [91.8, 95.0], respectively); scores remained significant after controlling for confounders. Preterm birth indirectly mediated 9.0% of the total effect of prenatal TSE on Cognitive score (P = NS). However, 91% of the remaining total effect was significant and attributable to TSE's direct harmful effects on cognitive development (β = - 5.17 [95% CI - 9.97, - 0.38]). The significant association is largely due to TSE's direct effect on cognitive development and not primarily due to TSE's indirect effect on preterm birth.
Identifiants
pubmed: 38228701
doi: 10.1038/s41598-024-51263-9
pii: 10.1038/s41598-024-51263-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1397Subventions
Organisme : NIEHS NIH HHS
ID : R01 ES030743
Pays : United States
Organisme : NIEHS NIH HHS
ID : R01 ES027815
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS094200
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS096037
Pays : United States
Investigateurs
Mekibib Altaye
(M)
Anita Arnsperger
(A)
Traci Beiersdorfer
(T)
Kaley Bridgewater
(K)
Tanya Cahill
(T)
Kim Cecil
(K)
Kent Dietrich
(K)
Christen Distler
(C)
Juanita Dudley
(J)
Brianne Georg
(B)
Cathy Grisby
(C)
Lacey Haas
(L)
Lili He
(L)
Scott K Holland
(SK)
V S Priyanka Illapani
(VSP)
Kristin Kirker
(K)
Beth M Kline-Fath
(BM)
Hailong Li
(H)
Matt Lanier
(M)
Stephanie L Merhar
(SL)
Greg Muthig
(G)
Brenda B Poindexter
(BB)
David Russell
(D)
Kari Tepe
(K)
Leanne Tamm
(L)
Julia Thompson
(J)
Hui Wang
(H)
Jinghua Wang
(J)
Brynne Williams
(B)
Kelsey Wineland
(K)
Sandra Wuertz
(S)
Donna Wuest
(D)
Weihong Yuan
(W)
Informations de copyright
© 2024. The Author(s).
Références
Soneji, S. & Beltran-Sanchez, H. Association of maternal cigarette smoking and smoking cessation with preterm birth. JAMA Netw. Open. 2, e192514. https://doi.org/10.1001/jamanetworkopen.2019.2514 (2019).
doi: 10.1001/jamanetworkopen.2019.2514
pubmed: 31002320
pmcid: 6481448
Hawsawi, A. M., Bryant, L. O. & Goodfellow, L. T. Association between exposure to secondhand smoke during pregnancy and low birthweight: A narrative review. Respir. Care. 60, 135–140. https://doi.org/10.4187/respcare.02798 (2015).
doi: 10.4187/respcare.02798
pubmed: 25006271
Xie, S., Monteiro, K. & Gjelsvik, A. The association between adverse birth outcomes and smoking cessation during pregnancy across the United States-43 States and New York City, 2012–2017. Arch. Gynecol. Obstet. 308, 1207–1215. https://doi.org/10.1007/s00404-022-06792-x (2023).
doi: 10.1007/s00404-022-06792-x
pubmed: 36175683
Jamshed, L., Perono, G. A., Jamshed, S. & Holloway, A. C. Early life exposure to nicotine: Postnatal metabolic, neurobehavioral and respiratory outcomes and the development of childhood cancers. Toxicol. Sci. 178, 3–15. https://doi.org/10.1093/toxsci/kfaa127 (2020).
doi: 10.1093/toxsci/kfaa127
pubmed: 32766841
pmcid: 7850035
McGrath-Morrow, S. A. et al. The effects of nicotine on development. Pediatrics. https://doi.org/10.1542/peds.2019-1346 (2020).
doi: 10.1542/peds.2019-1346
pubmed: 32047098
QuickStats: Percentage of births to mothers who reported smoking cigarettes at any time during pregnancy, by urbanization level* of county of residence—United States, 2020. MMWR Morb. Mortal. Wkly. Rep. 70, 1652. https://doi.org/10.15585/mmwr.mm7047a5 (2021).
Diamanti, A. et al. Smoking cessation in pregnancy: An update for maternity care practitioners. Tob. Induc. Dis. 17, 57. https://doi.org/10.18332/tid/109906 (2019).
doi: 10.18332/tid/109906
pubmed: 31582946
pmcid: 6770622
Gould, G. S., Havard, A., Lim, L. L., The Psanz Smoking In Pregnancy Expert Group & Kumar, R. Exposure to tobacco, environmental tobacco smoke and nicotine in pregnancy: A pragmatic overview of reviews of maternal and child outcomes, effectiveness of interventions and barriers and facilitators to quitting. Int. J. Environ. Res. Public Health. 17, 2034. https://doi.org/10.3390/ijerph17062034 (2020).
doi: 10.3390/ijerph17062034
pubmed: 32204415
pmcid: 7142582
Lee, M. et al. Exposure to prenatal secondhand smoke and early neurodevelopment: Mothers and Children’s Environmental Health (MOCEH) study. Environ. Health. 18, 22. https://doi.org/10.1186/s12940-019-0463-9 (2019).
doi: 10.1186/s12940-019-0463-9
pubmed: 30894196
pmcid: 6425627
Lee, B. E. et al. Secondhand smoke exposure during pregnancy and infantile neurodevelopment. Environ. Res. 111, 539–544. https://doi.org/10.1016/j.envres.2011.02.014 (2011).
doi: 10.1016/j.envres.2011.02.014
pubmed: 21397902
Christensen, G. M. et al. In-utero exposure to indoor air pollution or tobacco smoke and cognitive development in a South African birth cohort study. Sci. Total Environ. 834, 155394. https://doi.org/10.1016/j.scitotenv.2022.155394 (2022).
doi: 10.1016/j.scitotenv.2022.155394
pubmed: 35460774
pmcid: 9177804
He, Y., Luo, R., Wang, T., Gao, J. & Liu, C. Prenatal exposure to environmental tobacco smoke and early development of children in rural Guizhou Province, China. Int. J. Environ. Res. Public Health. 15, 2866. https://doi.org/10.3390/ijerph15122866 (2018).
doi: 10.3390/ijerph15122866
pubmed: 30558202
pmcid: 6313710
Cha, J. H. et al. Impact of preterm birth on neurodevelopmental disorders in South Korea: A nationwide population-based study. J. Clin. Med. https://doi.org/10.3390/jcm11092476 (2022).
doi: 10.3390/jcm11092476
pubmed: 36615110
pmcid: 9821092
Jarjour, I. T. Neurodevelopmental outcome after extreme prematurity: A review of the literature. Pediatr. Neurol. 52, 143–152. https://doi.org/10.1016/j.pediatrneurol.2014.10.027 (2015).
doi: 10.1016/j.pediatrneurol.2014.10.027
pubmed: 25497122
Sarda, S. P., Sarri, G. & Siffel, C. Global prevalence of long-term neurodevelopmental impairment following extremely preterm birth: A systematic literature review. J. Int. Med. Res. 49, 3000605211028026. https://doi.org/10.1177/03000605211028026 (2021).
doi: 10.1177/03000605211028026
pubmed: 34284680
Baer, R. J. et al. Risk of preterm and early term birth by maternal drug use. J. Perinatol. 39, 286–294. https://doi.org/10.1038/s41372-018-0299-0 (2019).
doi: 10.1038/s41372-018-0299-0
pubmed: 30573752
Smith, B. L. et al. Rates of substance and polysubstance use through universal maternal testing at the time of delivery. J. Perinatol. 42, 1026–1031. https://doi.org/10.1038/s41372-022-01335-3 (2022).
doi: 10.1038/s41372-022-01335-3
pubmed: 35177791
pmcid: 9356969
Ninan, K., Liyanage, S. K., Murphy, K. E., Asztalos, E. V. & McDonald, S. D. Evaluation of long-term outcomes associated with preterm exposure to antenatal corticosteroids: A systematic review and meta-analysis. JAMA Pediatr. 176, e220483. https://doi.org/10.1001/jamapediatrics.2022.0483 (2022).
doi: 10.1001/jamapediatrics.2022.0483
pubmed: 35404395
pmcid: 9002717
Nygaard, E., Slinning, K., Moe, V. & Walhovd, K. B. Cognitive function of youths born to mothers with opioid and poly-substance abuse problems during pregnancy. Child Neuropsychol. 23, 159–187. https://doi.org/10.1080/09297049.2015.1092509 (2017).
doi: 10.1080/09297049.2015.1092509
pubmed: 26471942
Jain, V. G. et al. Acute histologic chorioamnionitis independently and directly increases the risk for brain abnormalities seen on magnetic resonance imaging in very preterm infants. Am. J. Obstet. Gynecol. 227, 623.e621-623.e613. https://doi.org/10.1016/j.ajog.2022.05.042 (2022).
doi: 10.1016/j.ajog.2022.05.042
Wolf, H. T. et al. Magnesium sulphate for fetal neuroprotection at imminent risk for preterm delivery: A systematic review with meta-analysis and trial sequential analysis. BJOG. 127, 1180–1188. https://doi.org/10.1111/1471-0528.16238 (2020).
doi: 10.1111/1471-0528.16238
pubmed: 32237069
van Wassenaer, A. G. et al. Outcome at 4.5 years of children born after expectant management of early-onset hypertensive disorders of pregnancy. Am. J. Obstet. Gynecol. 204, 510.e511-519. https://doi.org/10.1016/j.ajog.2011.02.032 (2011).
doi: 10.1016/j.ajog.2011.02.032
Parikh, N. A. et al. Perinatal risk and protective factors in the development of diffuse white matter abnormality on term-equivalent age magnetic resonance imaging in infants born very preterm. J. Pediatr. 233, 58-65.e53. https://doi.org/10.1016/j.jpeds.2020.11.058 (2021).
doi: 10.1016/j.jpeds.2020.11.058
pubmed: 33259857
von Elm, E. et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies. Epidemiology. 18, 800–804. https://doi.org/10.1097/EDE.0b013e3181577654 (2007).
doi: 10.1097/EDE.0b013e3181577654
Roberts, G. et al. Rates of early intervention services in very preterm children with developmental disabilities at age 2 years. J. Paediatr. Child Health. 44, 276–280. https://doi.org/10.1111/j.1440-1754.2007.01251.x (2008).
doi: 10.1111/j.1440-1754.2007.01251.x
pubmed: 17999667
Spittle, A. J., Treyvaud, K., Lee, K. J., Anderson, P. J. & Doyle, L. W. The role of social risk in an early preventative care programme for infants born very preterm: A randomized controlled trial. Dev. Med. Child Neurol. 60, 54–62. https://doi.org/10.1111/dmcn.13594 (2018).
doi: 10.1111/dmcn.13594
pubmed: 29058313
Sapiets, S. J., Hastings, R. P. & Totsika, V. Predictors of access to early support in families of children with suspected or diagnosed developmental disabilities in the United Kingdom. J. Autism Dev. Disord. https://doi.org/10.1007/s10803-023-05996-7 (2023).
doi: 10.1007/s10803-023-05996-7
pubmed: 37142908
pmcid: 10159231
Huf, I. U. et al. Neurological examination at 32-weeks postmenstrual age predicts 12-month cognitive outcomes in very preterm-born infants. Pediatr. Res. 93, 1721–1727. https://doi.org/10.1038/s41390-022-02310-6 (2023).
doi: 10.1038/s41390-022-02310-6
pubmed: 36151299
Redline, R. W. et al. Amniotic infection syndrome: Nosology and reproducibility of placental reaction patterns. Pediatr. Dev. Pathol. 6, 435–448. https://doi.org/10.1007/s10024-003-7070-y (2003).
doi: 10.1007/s10024-003-7070-y
pubmed: 14708737
Bayley, N. Bayley Scales of Infant and Toddler Development: Bailey III (Harcourt Assessment Psychological Corporation, 2006).
Amiel-Tison, C. & Gosselin, J. Neurological Development from Birth to Six Years: Guide for Examination and Evaluation (Johns Hopkins University Press, 2001).
Newman, J. E. et al. Improving the Neonatal Research Network annual certification for neurologic examination of the 18–22 month child. J. Pediatr. 161, 1041–1046. https://doi.org/10.1016/j.jpeds.2012.05.048 (2012).
doi: 10.1016/j.jpeds.2012.05.048
pubmed: 22748517
pmcid: 3465479
VanderWeele, T. J. Mediation analysis: A practitioner’s guide. Annu. Rev. Public Health. 37, 17–32. https://doi.org/10.1146/annurev-publhealth-032315-021402 (2016).
doi: 10.1146/annurev-publhealth-032315-021402
pubmed: 26653405
Shi, Z. et al. Chorioamnionitis in the development of cerebral palsy: A meta-analysis and systematic review. Pediatrics. https://doi.org/10.1542/peds.2016-3781 (2017).
doi: 10.1542/peds.2016-3781
pubmed: 28814548
Xing, L. et al. Is chorioamnionitis associated with neurodevelopmental outcomes in preterm infants? A systematic review and meta-analysis following PRISMA. Medicine (Baltimore). 98, e18229. https://doi.org/10.1097/MD.0000000000018229 (2019).
doi: 10.1097/MD.0000000000018229
pubmed: 31852083
pmcid: 6922490
Tsai, M. S. et al. Children’s environmental health based on birth cohort studies of Asia. Sci. Total Environ. 609, 396–409. https://doi.org/10.1016/j.scitotenv.2017.07.081 (2017).
doi: 10.1016/j.scitotenv.2017.07.081
pubmed: 28755589
Polanska, K. et al. Environmental tobacco smoke exposure during pregnancy and child neurodevelopment. Int. J. Environ. Res. Public Health. https://doi.org/10.3390/ijerph14070796 (2017).
doi: 10.3390/ijerph14070796
pubmed: 28934143
pmcid: 5664596
Moore, B. F. et al. Prenatal exposure to tobacco and offspring neurocognitive development in the Healthy Start study. J. Pediatr. 218, 28-34.e22. https://doi.org/10.1016/j.jpeds.2019.10.056 (2020).
doi: 10.1016/j.jpeds.2019.10.056
pubmed: 31759580
Del Rosario, C., Slevin, M., Molloy, E. J., Quigley, J. & Nixon, E. How to use the Bayley Scales of Infant and Toddler Development. Arch. Dis. Child. Educ. Pract. Ed. 106, 108–112. https://doi.org/10.1136/archdischild-2020-319063 (2021).
doi: 10.1136/archdischild-2020-319063
pubmed: 32859738
Dwyer, J. B., Broide, R. S. & Leslie, F. M. Nicotine and brain development. Birth Defects Res. C Embryo Today. 84, 30–44. https://doi.org/10.1002/bdrc.20118 (2008).
doi: 10.1002/bdrc.20118
pubmed: 18383130
Dwyer, J. B., McQuown, S. C. & Leslie, F. M. The dynamic effects of nicotine on the developing brain. Pharmacol. Ther. 122, 125–139. https://doi.org/10.1016/j.pharmthera.2009.02.003 (2009).
doi: 10.1016/j.pharmthera.2009.02.003
pubmed: 19268688
pmcid: 2746456
England, L. J., Bunnell, R. E., Pechacek, T. F., Tong, V. T. & McAfee, T. A. Nicotine and the developing human: A neglected element in the electronic cigarette debate. Am. J. Prev. Med. 49, 286–293. https://doi.org/10.1016/j.amepre.2015.01.015 (2015).
doi: 10.1016/j.amepre.2015.01.015
pubmed: 25794473
pmcid: 4594223
Flemming, K., McCaughan, D., Angus, K. & Graham, H. Qualitative systematic review: Barriers and facilitators to smoking cessation experienced by women in pregnancy and following childbirth. J. Adv. Nurs. 71, 1210–1226. https://doi.org/10.1111/jan.12580 (2015).
doi: 10.1111/jan.12580
pubmed: 25430626
Bauld, L. et al. Barriers to and facilitators of smoking cessation in pregnancy and following childbirth: Literature review and qualitative study. Health Technol. Assess. 21, 1–158. https://doi.org/10.3310/hta21360 (2017).
doi: 10.3310/hta21360
pubmed: 28661375
pmcid: 5502375
Fletcher, C. et al. Isolation, marginalisation and disempowerment—Understanding how interactions with health providers can influence smoking cessation in pregnancy. BMC Pregnancy Childbirth. 22, 396. https://doi.org/10.1186/s12884-022-04720-0 (2022).
doi: 10.1186/s12884-022-04720-0
pubmed: 35538450
pmcid: 9086664
Goszczynska, E., Knol-Michalowska, K. & Petrykowska, A. How do pregnant women justify smoking? A qualitative study with implications for nurses’ and midwives’ anti-tobacco interventions. J. Adv. Nurs. 72, 1567–1578. https://doi.org/10.1111/jan.12949 (2016).
doi: 10.1111/jan.12949
pubmed: 26970542
Kiechl-Kohlendorfer, U. et al. Smoking in pregnancy: A risk factor for adverse neurodevelopmental outcome in preterm infants?. Acta Paediatr. 99, 1016–1019. https://doi.org/10.1111/j.1651-2227.2010.01749.x (2010).
doi: 10.1111/j.1651-2227.2010.01749.x
pubmed: 20178506
Li, X. et al. Etiological subgroups of small-for-gestational-age: Differential neurodevelopmental outcomes. PLOS One. 11, e0160677. https://doi.org/10.1371/journal.pone.0160677 (2016).
doi: 10.1371/journal.pone.0160677
pubmed: 27501456
pmcid: 4976943
Spencer-Smith, M. M., Spittle, A. J., Lee, K. J., Doyle, L. W. & Anderson, P. J. Bayley-III Cognitive and Language Scales in preterm children. Pediatrics. 135, e1258-1265. https://doi.org/10.1542/peds.2014-3039 (2015).
doi: 10.1542/peds.2014-3039
pubmed: 25896835
Anderson, P. J. & Burnett, A. Assessing developmental delay in early childhood—Concerns with the Bayley-III scales. Clin. Neuropsychol. 31, 371–381. https://doi.org/10.1080/13854046.2016.1216518 (2017).
doi: 10.1080/13854046.2016.1216518
pubmed: 27687612
Mansson, J. et al. The ability of Bayley-III scores to predict later intelligence in children born extremely preterm. Acta Paediatr. 110, 3030–3039. https://doi.org/10.1111/apa.16037 (2021).
doi: 10.1111/apa.16037
pubmed: 34289173
Morsan, V., Fantoni, C. & Tallandini, M. A. Age correction in cognitive, linguistic, and motor domains for infants born preterm: An analysis of the Bayley Scales of Infant and Toddler Development, developmental patterns. Dev. Med. Child Neurol. 60, 820–825. https://doi.org/10.1111/dmcn.13735 (2018).
doi: 10.1111/dmcn.13735
pubmed: 29542116