Abstract
Purpose
To evaluate the available evidence on the association between low-to-moderate prenatal alcohol exposure (PAE) and the development of attention-deficit hyperactivity disorder (ADHD) symptoms in the offspring.
Methods
We systematically reviewed and meta-analysed studies reporting an association between low and/or moderate PAE and offspring ADHD symptoms (attention and/or hyperactivity). Systematic searches were performed in EMBASE, Pubmed, Medline, and PsycINFO and reviewed from selected references. Random effects modelling was conducted to pool adjusted odds ratios (OR) in different alcohol consumption levels (≤ 20 g/week, ≤ 50 g/week, and ≤ 70 g/week). Stratified analysis by sex per alcohol level was conducted to investigate the difference on OR and the magnitude between-study heterogeneity.
Results
Ten studies were included in the systematic review and six in the meta-analysis. Eight studies found no association and two studies suggested an apparent protective effect of low PAE in hyperactivity/inattention symptoms in boys. These results were confirmed by the meta-analysis showing no association between ≤ 20 g/week [OR 1.01 (0.68–1.49)], ≤ 50 g/week [OR 0.94 (0.85–1.03)] and ≤ 70 g/week [OR 0.94 (0.86–1.02)] and ADHD symptoms, with no evidence of publication bias. Stratified analysis by sex for a PAE ≤ 50 g/week exposed less risk of ADHD symptoms in boys compared to girls [OR 0.89 (0.83–0.96)].
Conclusions
We found no increased risk of ADHD symptoms in offspring born to mothers who drank alcohol up to 70 g/week.
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References
Sv Faraone, Sergeant J, Gillberg C, Biederman J (2003) The worldwide prevalence of ADHD: is it an American Condition? World Psychiatry 2(2):104–113
Lawrence D, Johnson S, Hafekost J, Boterhoven De Haan K, Sawyer M, Ainley J, Zubrick S (2015) The mental health of children and adolescents. Report On the second australian child and adolescent survey of mental health and wellbeing. Canberra
Km Linnet, Dalsgaard S, Obel C, Wisborg K, Tb Henriksen, Rodriguez A, Kotimaa A, Moilanen I, Thomsen Ph, Olsen J, Mr Jarvelin (2003) Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry 160(6):1028–1040. https://doi.org/10.1176/Appi.Ajp.160.6.1028
Ra Barkley (2002) Major life activity and health outcomes associated with attention-deficit/hyperactivity disorder. J Clin Psychiatry 63(Suppl. 12):10–15
Biederman J, Newcorn J, Sprich S (1991) Comorbidity of attention deficit hyperactivity disorder with conduct, depressive, anxiety, and other disorders. Am J Psychiatry 148(5):564–577. https://doi.org/10.1176/Ajp.148.5.564
Mcgough J, Smalley S, Mccracken J, Yang M, Del’homme M, Lynn D, S Loo (2005) Psychiatric comorbidity in adult attention deficit hyperactivity disorder: findings from multiplex families. Am J Psychiatry 162(9):1621–1627. https://doi.org/10.1176/Appi.Ajp.162.9.1621
Banerjee Td, Middleton F, Sv Faraone (2007) Environmental risk factors for attention-deficit hyperactivity disorder. Acta Paediatr 96(9):1269–1274. https://doi.org/10.1111/J.1651-2227.2007.00430.X
Sciberras E, Mulraney M, Silva D, Coghill D (2017) Prenatal risk factors and the etiology of adhd—review of existing evidence. Curr Psychiatry Rep 19:1. https://doi.org/10.1007/s11920-017-0753-2
Yolton K, Cornelius M, Ornoy A, Mcgough J, Makris S, Schantz S (2014) Exposure to neurotoxicants and the development of attention deficit hyperactivity disorder and its related behaviors in childhood. Neurotoxicol Teratol 44:30–45. https://doi.org/10.1016/J.Ntt.2014.05.003
Popova S, Lange S, Shield K, Mihic A, Ae Chudley, Ra Mukherjee, Bekmuradov D, Rehm J (2016) Comorbidity of fetal alcohol spectrum disorder: a systematic review and meta-analysis. Lancet 387(10022):978–987. https://doi.org/10.1016/S0140-6736(15)01345-8
Tsang TW, Lucas BR, Olson HC, Pinto RZ, Elliott EJ (2016) Prenatal alcohol exposure, FASD, and child behavior: a meta-analysis. Pediatrics 137:3. https://doi.org/10.1542/peds.2015-2542
Flak Al SuS, Bertrand J, Denny Ch, Us Kesmodel, Me Cogswell (2014) The association of mild, moderate, and binge prenatal alcohol exposure and child neuropsychological outcomes: a meta-analysis. Alcoholism 38(1):214–226. https://doi.org/10.1111/acer.12214
Burger Ph, Tw Goecke, Pa Fasching, Moll G, Heinrich H, Mw Beckmann, Kornhuber J (2011) Einfluss Des Mütterlichen Alkoholkonsums Während Der Schwangerschaft Auf Die Entwicklung Von Adhs Beim Kind (How Does Maternal Alcohol consumption during pregnancy affect the development of attention deficit/hyperactivity syndrome in the child). Fortschr Neurol Psychiatr 79(09):500–506. https://doi.org/10.1055/S-0031-1273360
U.S. Department Of Health And Human Services; U.S. Department Of Agriculture (2015) 2015–2020 Dietary Guidelines For Americans. 8th Edn.,
National Health Medical Research Council (2009) Australian Guidelines To Reduce Health Risks From Drinking Alcohol. Canberra
Nhmrc (2001) Australian Alcohol Guidelines: Health Risks And Benefits. Canberra
International Alliance For Responsible Drinking (2016) Drinking Guidelines For Pregnancy And Breastfeeding. http://Www.Iard.Org/Policy-Tables/Drinking-Guidelines-Pregnancy-Breastfeeding/. Accessed Jul-2018
Australian Institute Of Health And Welfare (2014) National drug strategy household survey detailed report 2013, 28th edn. Aihw, Canberra
Todorow M, Te Moore, Koren G (2010) Investigating the effects of low to moderate levels of prenatal alcohol exposure on child behaviour: a critical review. J Popul Ther Clin Pharmacol 17(2):323–330
Moher D, Liberati A, Tetzlaff J, Dg Altman (2009) Preferred reporting items for systematic reviews and meta-analyses: the prisma statement. J Clin Epidemiol 62(10):1006–1012. https://doi.org/10.1016/J.Jclinepi.2009.06.005
Kalinowski A, Humphreys K (2016) Governmental standard drink definitions and low-risk alcohol consumption guidelines in 37 countries. Addiction 111(7):1293–1298. https://doi.org/10.1111/Add.13341
Wells G Sb, O’connell D, Peterson J, Welch V, Losos M, Tugwell P The Newcastle-Ottawa Scale (Nos) For assessing the quality of nonrandomised studies in meta-analyses. http://Www.Ohri.Ca/Programs/Clinical_Epidemiology/Oxford.Asp. Accessed Jan 2017
Bradley R, Corwyn R (2002) Socioeconomic status and child development. Annu Rev Psychol 53(1):371–399. https://doi.org/10.1146/Annurev.Psych.53.100901.135233
Kelly Y, Sacker A, Gray R, Kelly J, Wolke D, Ma Quigley (2009) Light drinking in pregnancy, a risk for behavioural problems and cognitive deficits at 3 years of age? Int J Epidemiol 38(1):129–140. https://doi.org/10.1093/Ije/Dyn230
Yj Kelly, Sacker A, Gray R, Kelly J, Wolke D, Head J, Ma Quigley (2012) Light drinking during pregnancy: still no increased risk for socioemotional difficulties or cognitive deficits at 5 years of age? J Epidemiol Community Health 66(1):41–48. https://doi.org/10.1136/Jech.2009.103002
Niclasen J, Am Nybo Andersen, Tw Teasdale, Strandberg-Larsen K (2014) Prenatal exposure to alcohol, and gender differences on child mental health at age 7 years. J Epidemiol Commun Health 68(3):224–232. https://doi.org/10.1136/Jech-2013-202956
Sayal K, Heron J, Golding J, Emond A (2007) Prenatal alcohol exposure and gender differences in childhood mental health problems: a longitudinal population-based study. Pediatrics 119(2):426–434. https://doi.org/10.1542/Peds.2006-1840
Sayal K, Es Draper, Fraser R, Barrow M, Smith Gd, Gray R (2013) Light drinking in pregnancy and mid-childhood mental health and learning outcomes. Arch Dis Child Fetal Neonatal Ed 98(2):107–111. https://doi.org/10.1111/Acer.12214
Underbjerg M, Us Kesmodel, Ni Landro, Bakketeig L, Grove J, Wimberley T, Tr Kilburn, Svaerke C, Thorsen P, El Mortensen (2012) The effects of low to moderate alcohol consumption and binge drinking in early pregnancy on selective and sustained attention in 5-year-old children. BJOG 119(10):1211–1221. https://doi.org/10.1111/J.1471-0528.2012.03396.X
Us Kesmodel, Bertrand J, Støvring H, Skarpness B, Denny Ch, El Mortensen (2012) The effect of different alcohol drinking patterns in early to mid pregnancy on the child’s intelligence, attention, and executive function. BJOG 119(10):1180–1190. https://doi.org/10.1111/J.1471-0528.2012.03393.X
O’leary CM, Nassar N, Zubrick SR, Kurinczuk JJ, Stanley F, Bower C (2010) Evidence of a complex association between dose, pattern and timing of prenatal alcohol exposure and child behaviour problems. Addiction 105(1):74–86. https://doi.org/10.1111/j.1360-0443.2009.02756.x
O’callaghan FV, O’callaghan M, Najman JM, Williams GM, Bor W (2007) Prenatal alcohol exposure and attention, learning and intellectual ability at 14 years: a prospective longitudinal study. Early Hum Dev 83(2):115–123. https://doi.org/10.1016/j.earlhumdev.2006.05.011
Rodriguez A, Olsen J, Aj Kotimaa, Kaakinen M, Moilanen I, Tb Henriksen, Km Linnet, Miettunen J, Obel C, Taanila A, Ebeling H, Mr Jarvelin (2009) Is prenatal alcohol exposure related to inattention and hyperactivity symptoms in children? Disentangling the effects of social adversity. J Child Psychol Psychiatry 50(9):1073–1083. https://doi.org/10.1111/J.1469-7610.2009.02071.X
Bingol N, Schuster C, Fuchs M, Iosub S, Turner G, Rk Stone, Ds Gromisch (1987) The influence of socioeconomic factors on the occurrence of fetal alcohol syndrome. Adv Alcohol Subst Abuse 6(4):105–118. https://doi.org/10.1300/J251v06n04_08
Smith Gd (2008) Assessing intrauterine influences on offspring health outcomes: can epidemiological studies yield robust findings? Basic Clin Pharmacol Toxicol 102(2):245–256. https://doi.org/10.1111/J.1742-7843.2007.00191.X
Alati R, Macleod J, Hickman M, Sayal K, May M, Smith Gd, Da Lawlor (2008) Intrauterine exposure to alcohol and tobacco use and childhood Iq: findings from a parental-offspring comparison within the avon longitudinal study of parents and children. Pediatr Res 64(6):659. https://doi.org/10.1203/Pdr.0b013e318187cc31
Lipsitch M, Tchetgen Tchetgen E, Cohen T (2010) Negative controls: a tool for detecting confounding and bias in observational studies. Epidemiology 21(3):383–388. https://doi.org/10.1097/Ede.0b013e3181d61eeb
Gustavson K, Ystrom E, Stoltenberg C, Susser E, Suren P, Magnus P, Knudsen GP, Smith GD, Langley K, Rutter M, Aase H, Reichborn-Kjennerud T (2017) Smoking in pregnancy and child adhd. Pediatrics. https://doi.org/10.1542/peds.2016-2509
Zuccolo L, Lewis SJ, Smith DG, Sayal K, Es Draper, Fraser R, Barrow M, Alati R, Ring S, Macleod J, Golding J, Heron J, Gray R (2013) Prenatal alcohol exposure and offspring cognition and school performance. A ‘Mendelian Randomization’ natural experiment. Int J Epidemiol 42(5):1358–1370. https://doi.org/10.1093/ije/dyt172
Acknowledgements
We would like to thank Sean Mitchel for proof reading the final version of the document.
Funding
MSMP is funded by an Australian Postgraduate Award (APA). JCM is funded by The University of Queensland International Scholarship.
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MSMP: project development, manuscript writing/editing, data extraction, and data interpretation. JCM: data extraction, data analysis, data interpretation, and manuscript writing/editing. KSB: data interpretation and manuscript writing/editing. RA: project development, data interpretation, and manuscript writing/editing.
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San Martin Porter, M., Maravilla, J.C., Betts, K.S. et al. Low–moderate prenatal alcohol exposure and offspring attention-deficit hyperactivity disorder (ADHD): systematic review and meta-analysis. Arch Gynecol Obstet 300, 269–277 (2019). https://doi.org/10.1007/s00404-019-05204-x
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DOI: https://doi.org/10.1007/s00404-019-05204-x