{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T00:59:52Z","timestamp":1792371592443,"version":"4.4.0"},"reference-count":37,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2012,1,27]],"date-time":"2012-01-27T00:00:00Z","timestamp":1327622400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Fetal growth restriction and maternal smoking during pregnancy are independently implicated in lowering intellectual attainment in children. We hypothesized that only reduction of fetal growth that is attributable to extrinsic causes (e.g., maternal smoking) affects intellectual development of a child. Cross-sectional survey of 3,739 students in Nova Scotia (Canada) in 2003 was linked with the perinatal database, parental interviews on socio-demographic factors and the performance on standardized tests when primarily 11\u201312 years of age, thereby forming a retrospective cohort. Data was analyzed using hierarchical logistic regression with correction for clustering of children within schools. The risk of poor test result among children born small-for-gestational-age (SGA) to mothers who smoked was 29.4%, higher than in any other strata of maternal smoking and fetal growth. The adjusted odds ratio among SGA children born to mothers who smoked was the only one elevated compared to children who were not growth restricted and born to mothers who did not smoke (17.0%, OR = 1.46, 95% CI 1.02, 2.09). Other perinatal, maternal and socio-demographic factors did not alter this pattern of effect modification. Heterogeneity of etiology of fetal growth restriction should be consider in studies that address examine its impact on health over life course.<\/jats:p>","DOI":"10.3390\/ijerph9020408","type":"journal-article","created":{"date-parts":[[2012,1,27]],"date-time":"2012-01-27T16:36:52Z","timestamp":1327682212000},"page":"408-420","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["The Role of Maternal Smoking in Effect of Fetal Growth Restriction on Poor Scholastic Achievement in Elementary School"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7153-4478","authenticated-orcid":false,"given":"Igor","family":"Burstyn","sequence":"first","affiliation":[{"name":"Department of Environmental and Occupational Health, School of Public Health, Drexel University, 1505 Race Street, Philadelphia, PA 19102, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Kuhle","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, School of Public Health, University of Alberta, Edmonton, Alberta, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander C.","family":"Allen","sequence":"additional","affiliation":[{"name":"Division of Neonatal-Perinatal Medicine, Perinatal Epidemiology Research Unit, Dalhousie University & IWK Health Centre, Halifax, Nova Scotia, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Veugelers","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, School of Public Health, University of Alberta, Edmonton, Alberta, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2012,1,27]]},"reference":[{"key":"ref_1","unstructured":"Rodeck, C.H., and Whittle, M.J. (2009). Fetal Medicine: Basic Science and Clinical Practice, Elsevier Health Sciences. [2nd]. Chapter 39."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1139\/y06-037","article-title":"The effect of nicotine on in vitro placental perfusion pressure","volume":"84","author":"Bainbridge","year":"2006","journal-title":"Can. J. Physiol Pharmacol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"S125","DOI":"10.1080\/14622200410001669187","article-title":"The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics, and pregnancy outcomes","volume":"6","author":"Cnattingius","year":"2004","journal-title":"Nicotine Tob.Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1016\/S0022-3476(05)83322-0","article-title":"Very low birth weight children: Behavior problems and school difficulty in a national sample","volume":"117","author":"McCormick","year":"1990","journal-title":"J. Pediatr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1499","DOI":"10.1016\/j.socscimed.2004.08.014","article-title":"Association of sociodemographic characteristics of children with intellectual disability in Western Australia","volume":"60","author":"Leonard","year":"2005","journal-title":"Soc. Sci. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1111\/j.1469-8749.2000.tb00019.x","article-title":"Fetal growth and subsequent mental health problems in children aged 4 to 13 years","volume":"42","author":"Zubrick","year":"2000","journal-title":"Dev. Med. Child Neurol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1542\/peds.88.5.943","article-title":"Social environment and vulnerability of low birth weight children: A social-epidemiological perspective","volume":"88","author":"McGauhey","year":"1991","journal-title":"Pediatrics"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/j.siny.2004.03.005","article-title":"Paediatric consequences of fetal growth restriction","volume":"9","author":"Yanney","year":"2004","journal-title":"Semin.Fetal Neonatal Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1542\/peds.2008-2816","article-title":"Meta-analysis of neurobehavioral outcomes in very preterm and\/or very low birth weight children","volume":"124","author":"Oosterlaan","year":"2009","journal-title":"Pediatrics"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e350","DOI":"10.1542\/peds.2007-3851","article-title":"Birth weight and cognitive ability in childhood among siblings and nonsiblings","volume":"122","author":"Yang","year":"2008","journal-title":"Pediatrics"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e894","DOI":"10.1542\/peds.2005-2412","article-title":"Intrauterine growth and intelligence within sibling pairs: Findings from the Aberdeen children of the 1950s cohort","volume":"117","author":"Lawlor","year":"2006","journal-title":"Pediatrics"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1093\/aje\/kwq199","article-title":"Birth weight standardized to gestational age and intelligence in young adulthood: A register-based birth cohort study of male siblings","volume":"172","author":"Eriksen","year":"2010","journal-title":"Am. J. Epidemiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1289\/ehp.99107991","article-title":"Association of prenatal maternal or postnatal child environmental tobacco smoke exposure and neurodevelopmental and behavioral problems in children","volume":"107","author":"Eskenazi","year":"1999","journal-title":"Environ. Health Perspect."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1097\/01.ede.0000231561.49208.be","article-title":"Maternal smoking during pregnancy and school performance at age 15","volume":"17","author":"Lambe","year":"2006","journal-title":"Epidemiology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/j.earlhumdev.2010.06.010","article-title":"Effect of birth weight, maternal education and prenatal smoking on offspring intelligence at school age","volume":"86","author":"Rahu","year":"2010","journal-title":"Early Hum. Dev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.earlhumdev.2009.12.008","article-title":"Is smoking in pregnancy an independent predictor of academic difficulties at 14 years of age? A birth cohort study","volume":"86","author":"Al","year":"2010","journal-title":"Early Hum.Dev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1111\/j.1467-8624.2009.01382.x","article-title":"A quasi-experimental study of maternal smoking during pregnancy and offspring academic achievement","volume":"81","author":"Singh","year":"2010","journal-title":"Child Dev."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1093\/aje\/kwn175","article-title":"Maternal smoking during pregnancy and children\u2019s cognitive and physical development: A causal risk factor?","volume":"168","author":"Gilman","year":"2008","journal-title":"Am. J. Epidemiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1080\/09603123.2010.544032","article-title":"Prenatal exposure to cigarette smoke and childhood externalizing behavioral problems: A propensity score matching approach","volume":"21","author":"Boutwell","year":"2011","journal-title":"Int. J. Environ. Health Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1002\/icd.480","article-title":"Interrelations between maternal smoking during pregnancy, birth weight and sociodemographic factors in the prediction of early cognitive abilities","volume":"15","author":"Huijbregts","year":"2006","journal-title":"Infant Child Dev."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Kramer, M.S., Platt, R.W., Wen, S.W., Joseph, K.S., Allen, A., Abrahamowicz, M., Blondel, B., and Breart, G. (2001). A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics, 108.","DOI":"10.1542\/peds.108.2.e35"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1111\/j.1746-1561.2008.00288.x","article-title":"Diet quality and academic performance","volume":"78","author":"Florence","year":"2008","journal-title":"J. Sch. Health"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"88","DOI":"10.3109\/17477160903060028","article-title":"Perinatal and childhood risk factors for overweight in a provincial sample of Canadian Grade 5 students","volume":"5","author":"Kuhle","year":"2010","journal-title":"Int. J. Pediatr. Obes."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1097\/01.AOG.0000201977.45284.3c","article-title":"Socioeconomic status and receipt of obstetric services in Canada","volume":"107","author":"Joseph","year":"2006","journal-title":"Obstet. Gynecol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1016\/S1701-2163(16)30435-2","article-title":"The influence of hospital closures in Nova Scotia on perinatal outcomes","volume":"26","author":"Allen","year":"2004","journal-title":"J. Obstet. Gynaecol. Can."},{"key":"ref_26","first-page":"8","article-title":"An assessment of the validity of a computer system for probabilistic record linkage of birth and infant death records in Canada. The Fetal and Infant Health Study Group","volume":"21","author":"Fair","year":"2000","journal-title":"Chronic Dis. Can."},{"key":"ref_27","unstructured":"Rothman, K.J., Greenland, S., and Lash, T.L. (2008). Modern Epidemiology, Lippincott Williams & Wilkins. [3rd]. Chapter 5."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1097\/EDE.0b013e318197c0f5","article-title":"Interaction reaction","volume":"20","author":"Kaufman","year":"2009","journal-title":"Epidemiology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/j.ejpn.2008.05.001","article-title":"A review of developmental outcomes of term infants with post-asphyxia neonatal encephalopathy","volume":"13","author":"Pin","year":"2009","journal-title":"Eur. J. Paediatr. Neurol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1007\/s00431-007-0437-8","article-title":"Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: A review","volume":"166","author":"Swaab","year":"2007","journal-title":"Eur. J. Pediatr."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1093\/aje\/kwh121","article-title":"Measurement error and misclassification in statistics and epidemiology: Impacts and Bayesian adjustments","volume":"159","author":"Gustafson","year":"2004","journal-title":"Am. J. Epidemiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1093\/ntr\/ntn010","article-title":"The accuracy of self-reported smoking: A systematic review of the relationship between self-reported and cotinine-assessed smoking status","volume":"11","author":"Gorber","year":"2009","journal-title":"Nicotine Tob.Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"670","DOI":"10.1093\/ntr\/ntp048","article-title":"Evaluation of the accuracy of self-reported smoking in pregnancy when biomarker level in an active smoker is uncertain","volume":"11","author":"Burstyn","year":"2009","journal-title":"Nicotine Tob.Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/BF03404362","article-title":"Substance use of pregnant women and early neonatal morbidity: Where to focus intervention?","volume":"101","author":"Burstyn","year":"2010","journal-title":"Can. J. Public Health"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Al-Sahab, B., Saqib, M., Hauser, G., and Tamim, H. (2010). Prevalence of smoking during pregnancy and associated risk factors among Canadian women: A national survey. BMC Pregnancy Childbirth, 10.","DOI":"10.1186\/1471-2393-10-24"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1007\/BF03403698","article-title":"Changes in maternal characteristics in Nova Scotia, Canada from 1988 to 2001","volume":"96","author":"Fell","year":"2005","journal-title":"Can. J. Public Health"},{"key":"ref_37","first-page":"185","article-title":"Prevalence of smoking among pregnant women in Nova Scotia from 1988 to 1992","volume":"152","author":"Dodds","year":"1995","journal-title":"Can. Med. Assoc. J."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/9\/2\/408\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T21:48:38Z","timestamp":1760219318000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/9\/2\/408"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,1,27]]},"references-count":37,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2012,2]]}},"alternative-id":["ijerph9020408"],"URL":"https:\/\/doi.org\/10.3390\/ijerph9020408","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,1,27]]}}}