Abstract
Attention problems are thought to be a hallmark feature of prenatal alcohol exposure (PAE). Despite decades of research however, these findings have never been pooled to assess the association between PAE and the different domains of attention functioning. This systematic review and meta-analysis aimed to examine the relationships between low-moderate, binge and heavy PAE with domains of attention functioning (encode, focus, shift, sustain and behavioural) in children. Thirteen studies compared children with PAE to abstinent controls. A significant adverse effect of any PAE on shifting attention (Cohen’s d = -0.61), and a trend towards an adverse effect of heavy PAE on encoding attention (Cohen’s d = -0.79) were identified. Compared to controls, there were trends showing that low-moderate PAE (odds ratio = 1.21) was associated with greater odds of behavioural attention problems. Remaining analyses were limited by insufficient studies or were non-significant. In summary, a vulnerability of higher-level attention skills to PAE was found. Urgent investigation into the effects of low to moderate PAE is needed given the prevalence of this drinking pattern, trends towards behavioural attention problems, the lack of comprehensive and high-quality research and the known impacts of attention difficulties on academic and social development in children.
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References
Anderson, P. (2002). Assessment and development of executive function (EF) during childhood. Child Neuropsychology, 8(2), 71–82 https://doi.org/10.1076/chin.8.2.71.8724
Andrade, B. F., Brodeur, D. A., Waschbusch, D. A., Stewart, S. H., & Mcgee, R. (2009). Selective and sustained attention as predictors of social problems in children with typical and disordered attention abilities. Journal of Attention Disorders, 12(4), 341–352. https://doi.org/10.1177/1087054708320440
Borenstein, M., Hedges, L., Higgins, J., & Rothstein, H. (2009). Introduction to meta-analysis. John Wiley & Sons.
Borenstein, M., Hedges, L., Higgins, J., & Rothstein, H. (2013). Comprehensive Meta-Analysis (Version 3) [Computer software]. Biostat.
Buchsbaum, B. R., Greer, S., Chang, W., Berman, K. F., Fox, P., Laird, A., & Lancaster, J. (2005). Meta-analysis of neuroimaging studies of the Wisconsin Card-Sorting task and component processes. Human Brain Mapping, 25(1), 35–45. https://doi.org/10.1002/hbm.20128
Burden, M., Jacobson, S., Sokol, R., & Jacobson, J. (2005). Effects of prenatal alcoholexposure on attention and working memory at 7.5 years of age. Alcoholism: Clinical and Experimental Research, 29(3), 443–452. https://doi.org/10.1097/01.alc.0000156125.50577.ec
Cameron, C. M., Davey, T. M., Kendall, E., Wilson, A., & McClure, R. J. (2013). Changes in alcohol consumption in pregnant Australian women between 2007 and 2011. Medical Journal of Australia, 199(5), 355–357. https://doi.org/10.5694/mja12.11723
Cohen, J. (1992). Statistical power analysis. Current Directions in Psychological Science, 1(3), 98–101. https://doi.org/10.1111/1467-8721.ep10768783
Coles, C., Kable, D., Keen, J., Jones, A., Wertelecki, C., Granovska, L., … Chambers, L. (2015). Dose and timing of prenatal alcohol exposure and maternal nutritional supplements: developmental effects on 6-month-old infants. Maternal and Child Health Journal, 19(12), 2605–2614. https://doi.org/10.1007/s10995-015-1779-x
Coles, C. D., Platzman, K. A., Lynch, M. E., & Freides, D. (2002). Auditory and visual sustained attention in adolescents prenatally exposed to alcohol. Alcoholism: Clinical & Experimental Research, 26(2), 263–271. https://doi.org/10.1097/00000374200202000-00015
Coles, C. D., Platzman, K. A., Raskind-Hood, C. L., Brown, R. T., Falek, A., & Smith, I. E. (1997). A comparison of children affected by prenatal alcoholexposure and attention deficit, hyperactivity disorder. Alcoholism: Clinical and Experimental Research, 21(1), 150–161.https://doi.org/10.1111/j.15300277.1997.tb03743.x
Comasco, E., Rangmar, J., Eriksson, U. J., & Oreland, L. (2018). Neurological and neuropsychological effects of low and moderate prenatal alcohol exposure. Acta Physiologica, 222(1). https://doi.org/10.1111/apha.12892
Dolan, G. P., Stone, D. H., & Briggs, A. H. (2010). A systematic review of continuous performance task research in children prenatally exposed to alcohol. Alcohol & Alcoholism, 45(1), 30–38. https://doi.org/10.1093/alcalc/agp062
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), 629–634. https://doi.org/10.1136/bmj.315.7109.629
Flak, A. L., Su, S., Bertrand, J., Denny, C. H., Kesmodel, U. S., & Cogswell, M. E. (2014).The association of mild, moderate, and binge prenatal alcohol exposure and child neuropsychological outcomes: A meta-analysis. Alcoholism: Clinical and Experimental Research, 38(1), 214–226. https://doi.org/10.1111/acer.12214
Furtado, E., & Roriz, S. (2016). Inattention and impulsivity associated with prenatal alcoholexposure in a prospective cohort study with 11-years-old Brazilianchildren. European Child & Adolescent Psychiatry, 25(12), 1327–1335. https://doi.org/10.1007/s00787-016-0857-y
Goldschmidt, L., Richardson, G. A., Stoffer, D. S., Geva, D., & Day, N. L. (1996). Prenatal alcohol exposure and academic achievement at age six: A nonlinear fit. Alcoholism, Clinical and Experimental Research, 20(4), 763–770. https://doi.org/10.1111/j.15300277.1996.tb01684.x
Guerri, C., Bazinet, A., & Riley, E. (2009). Foetal Alcohol Spectrum Disorders and Alterations in Brain and Behaviour. Alcohol and Alcoholism, 44(2), 108–114. https://doi.org/10.1093/alcalc/agn105
Hackman, D. A., & Farah, M. J. (2009). Socioeconomic status and the developing brain. Trends in Cognitive Sciences, 13(2), 65–73. https://doi.org/10.1016/j.tics.2008.11.003
Higgins, J., & Green, S. (Eds.) (2011). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Retrieved from https://training.cochrane.org/handbook
Hollingshead, A. B. (1975). Four factor index of social status. Unpublished manuscript. Yale University, New Haven, CT.
IntHout, J., Ioannidis, J., Rovers, M., & Goeman, J. (2016). Plea or routinely presenting prediction intervals in meta-analysis. British Medical Journal Open, 6(7), e010247–e010247. https://doi.org/10.1136/bmjopen-2015-010247
Jacobson, S., Chiodo, L., Sokol, R., & Jacobson, J. (2002). Validity of maternal report of prenatal alcohol, cocaine and smoking in relation toneurobehavioral outcome. Pediatrics, 109(5), 815–825. https://doi.org/10.1542/peds.109.5.815
Jacobson, J. L., Dodge, N. C., Burden, M. J., Klorman, R., & Jacobson, S. W. (2011).Number processing in adolescents with prenatal alcohol exposure and ADHD: Differences in the neurobehavioral phenotype. Alcoholism: Clinical and Experimental Research, 35(3), 431–442. https://doi.org/10.1111/j.15300277.2010.01360.x
Khoury, J., Milligan, E., & Girard, K. (2015). Executive functioning in children and adolescents prenatally exposed to alcohol: A meta-analytic review. Neuropsychology Review, 25(2), 149–170. https://doi.org/10.1076/09297049(200003)6:1;1-B;FT024
Kirova, A. M., Kelberman, C., Storch, B., DiSalvo, M., Woodworth, K. Y., Faraone, S. V., & Biederman, J. (2019). Are subsyndromal manifestations of attention deficit hyperactivity disorder morbid in children? A systematic qualitative review of the literature with meta-analysis. Psychiatry Research, 274, 75–90. https://doi.org/10.1016/j.psychres.2019.02.003
Kodituwakku, P. (2007). Defining the behavioral phenotype in children with fetal alcoholspectrum disorders: A review. Neuroscience and Biobehavioral Reviews, 31(2), 192–201. https://doi.org/10.1016/j.neubiorev.2006.06.020
Kodituwakku, P., Kalberg, W., & May, P. (2001). The effects of prenatal Alcohol exposure on executive functioning. Alcohol Research & Health, 25(3), 192–198.
Kodituwakku, P., Segall, J., & Beatty, G. (2011). Cognitive and behavioral effects of prenatal alcohol exposure. Future Neurology, 6(2), 237–259. https://doi.org/10.2217/fnl.11.4
Lane, K. A., Stewart, J., Fernandes, T., Russo, N., Enns, J., & Burack, J. A. (2014). Complexities in understanding attentional functioning among children with fetal alcohol spectrum disorder. Frontiers in Human Neuroscience, 8(119), 1–8. https://doi.org/10.3389/fnhum.2014.00119
Larsson, G., Bohlin, A. B., & Tunell, R. (1985). Prospective study of children exposed to variable amounts of alcohol un utero. Archives of Disease in Childhood, 60(4), 316–321.
Lebel, C., Roussotte, F., & Sowell, E. (2011). Imaging the impact of prenatal alcohol exposure on the structure of the developing humanbrain. Neuropsychology Review, 21(2), 102–118. https://doi.org/10.1007/s11065-011-9163-0
Lemoine, P., Harousseau, H., Borleyru, J. P., & Menuet, J. C. (1968). Les enfants de parents alcooliques: Anomalies observees a propos de 127 cas. [Children of alcoholic parents: Anomalies observed in 127 cases]. Ouest Medical, 21, 476–482. https://doi.org/10.1097/00007691-200304000-00002
Lie, C. H., Specht, K., Marshall, J. C., & Fink, G. R. (2006). Using fMRI to decompose theneural processes underlying the Wisconsin Card Sorting Test. NeuroImage, 30(3), 1038–1049. https://doi.org/10.1016/j.neuroimage.2005.10.031
Linnet, K. M., Dalsgaard, S., Obel, C., Wisborg, K., Henriksen, T. B., Rodriguez, A., et al. (2003). Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorderand associated behaviors: Review ofthe current evidence. The American journal of psychiatry, 160(6), 1028–1040. https://doi.org/10.1176/appi.ajp.160.6.1028
Mahone, E., & Schneider, M. (2012). Assessment of attention in preschoolers. Neuropsychology Review, 22(4), 361–383. https://doi.org/10.1007/s11065012-9217y
Mattson, S. N., Calarco, K. E., & Lang, A. R. (2006). Focused and shifting attention in children with heavy prenatal alcohol exposure. Neuropsychology, 20(3), 361–369. https://doi.org/10.1037/0894-4105.20.3.361
Mattson, S. N., Crocker, N., & Nguyen, T. T. (2011). Fetal alcohol spectrum disorders: Neuropsychological and behavioral features. Neuropsychology review, 21(2), 81–101. https://doi.org/10.1007/s11065-011-9167-9
May, P. A., Blankenship, J., Marais, A. S., Gossage, J. P., Kalberg, W. O., Barnard, R., Seedat, S. (2013a). Approaching the prevalence of the full spectrumof fetal alcohol spectrum disorders in a South African population-basedstudy. Alcoholism: Clinical & Experimental Research, 37(5), 818–830. https://doi.org/10.1111/acer.12033
May, P. A., Blankenship, J., Marais, A. S., Gossage, J. P., Kalberg, W. O., Joubert, B., Seedat, S. (2013b). Maternal alcohol consumption producing fetalalcohol spectrum disorders (FASD): Quantity, frequency, and timing of drinking. Drug and Alcohol Dependence, 133(2), 502–512. https://doi.org/10.1016/j.drugalcdep.2013.07.013
McCormack, C., Hutchinson, D., Burns, L., Wilson, J., Elliott, E., Allsop, S., Mattick, R. (2017). Prenatal alcohol consumption between conception and recognition ofpregnancy. Alcoholism: Clinical and Experimental Research, 41(2), 369–378. https://doi.org/10.1111/acer.13305
McGee, C. L., Schonfeld, A. M., Roebuck-Spencer, T. M., Riley, E. P., & Mattson, S. N. (2008). Children with heavy prenatal alcohol exposure demonstratedeficits on multiple measures of concept formation. Alcoholism: Clinical & Experimental Research, 32(8), 1388–1397. https://doi.org/10.1111/j.15300277.2008.00707.x
Meir, N., & Armon-Lotem, S. (2017). Independent and combined effects of socioeconomic status (SES) and bilingualism on children’s vocabulary and verbal short-term memory. Frontiers in Psychology, 8, 1442. https://doi.org/10.3389/fpsyg.2017.01442
Mirsky, A. F., Anthony, B. J., Duncan, C. C., Ahearn, M. B., & Kellam, S. G. (1991). Analysis of the elements of attention: A neuropsychological approach. Neuropsychology Review, 2, 109–145. https://doi.org/10.1007/BF01109051
Mirsky, A. F., & Duncan, C. C. (2001). A nosology of disorders of attention. Annals of the New York Academy of Sciences, 931(1), 17–32. https://doi.org/10.1111/j.17496632.2001.tb05771.x
Miyake, A., & Friedman, N. P. (2012). The nature and organization of individual differences in executive functions: Four general conclusions. Current Directions in Psychological Science, 21(1), 8–14. https://doi.org/10.1177/0963721411429458
Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Annals of International Medicine, 151, 264–269. https://doi.org/10.1371/journal.pmed.1000097.
Muggli, E., O’Leary, C., Donath, S., Orsini, F., Forster, D., Anderson, P., & Halliday, J. (2016). “Did you ever drink more?” A detailed description of pregnant womens drinking patterns. BMC Public Health, 16(1), 683. https://doi.org/10.1186/s12889016-3354-9
National Health and Medical Research Council (Australia). (2001). Australian alcohol guidelines: Health risks and benefits. National Health and Medical Research Council.
Niclasen, J. (2015). Prenatal exposure to alcohol and the developing fetus: Methodological issues. BJOG: An International Journal of Obstetrics & Gynaecology, 122(6), 770- 772. https://doi.org/10.1111/1471-0528.13078
Niclasen, J., Nybo Andersen, A. M., Teasdale, T. W., & Strandberg-Larsen, K. (2014). Prenatal exposure to alcohol, and gender differences on child mental health at age seven years. Journal of Epidemiology & Community Health, 68(3), 224–232. https://doi.org/10.1136/jech-2013-202956
O’Callaghan, F., O’Callaghan, M., Najman, J., Williams, G., & Bor, W. (2007). Prenatal alcohol exposure and attention, learning and intellectual ability at 14 years: A prospective longitudinal study. Early Human Development, 83(2), 115–123. https://doi.org/10.1016/j.earlhumdev.2006.05.011
O’Keeffe, L. M., Kearney, P. M., McCarthy, F. P., Khashan, A. S., Greene, R. A., North, R. A., & Kenny, L. C. (2015). Prevalence and predictors of alcoholuse during pregnancy: findings from international multicentre cohortstudies. British Medical Journal Open, 5(7), e006323. https://doi.org/10.1136/bmjopen-2014006323
O’Leary, C. M., Nassar, N., Zubrick, S. R., Kurinczuk, J. J., Stanley, F., & Bower, C. (2010). Evidence of a complex association between dose, pattern and timingof prenatal alcohol exposure and child behaviour problems. Addiction, 105(1), 74–86. https://doi.org/10.1111/j.13600443.2009.02756.x
O’Leary, C., Taylor, C., Zubrick, S., Kurinczuk, J., & Bower, C. (2013). Prenatal alcoholexposure and educational achievement in children aged 8–9 years. Pediatrics, 132(2), e468-475. https://doi.org/10.1542/peds.2012-3002
O’Leary, C., Zubrick, S., Taylor, C., Dixon, G., & Bower, C. (2009). Prenatal alcoholexposure and language delay in 2-year-old children: The importanceof dose and timing on risk. Pediatrics, 123(2), 547–554. https://doi.org/10.1542/peds.2008-0459
Pagnin, D., Zamboni Grecco, M. L., & Furtado, E. F. (2019). Prenatal alcohol use as a risk for attention-deficit/hyperactivity disorder. European Archives of Psychiatry and Clinical Neuroscience, 269(6), 681–687. https://doi.org/10.1007/s00406-018-0946-7
Pascualvaca, D. M., Anthony, B. J., Arnold, L. E., Rebok, G. W., Ahearn, M. B., Kellam, S. G., & Mirsky, A. F. (1997). Attention performance in an epidemiological sample of urban children: The role of gender and verbalintelligence. Child Neuropsychology, 3(1), 13–27. https://doi.org/10.1080/09297049708401365
Pfinder, M., & Lhachimi, S. (2020). Lifestyle-related risk factors during pregnancy: Even low-to-moderate drinking during pregnancy increases the risk for adolescent behavioral problems. Journal of Substance Use, 25(2), 135–140. https://doi.org/10.1080/14659891.2019.1664668
Popova, S., Lang, S., Probst, C., Gmel, G., & Rehm, J. (2017). Estimation of national, regional, and global prevalence of alcohol use during pregnancy and fetal alcohol syndrome: A systematic review and meta-analysis. The Lancet Global Health, 5(3), e290–e299. https://doi.org/10.1016/S2214-109X(17)30021-9
Porter, M., Maravilla, J., Betts, C., & Alati, K. (2019). Low–moderate prenatal alcoholexposure and offspring attention-deficit hyperactivity disorder(ADHD): Systematic review and meta-analysis. Archives of Gynecology and Obstetrics, 300(2), 269–277. https://doi.org/10.1007/s00404-019-05204-x
Rasmussen, C. (2005). Executive functioning and working memory in fetal alcohol spectrum disorder. Alcoholism: Clinical and Experimental Research, 29(8), 1359–1367. https://doi.org/10.1097/01.alc.0000175040.91007.d0
Rodriguez, A., Olsen, J., Kotimaa, A., Kaakinen, M., Moilanen, I., Henriksen, T., & Jarvelin, M. (2009). Is prenatal alcohol exposure related to inattention andhyperactivity symptoms in children? Disentangling the effects of socialadversity. Journal of Child Psychology and Psychiatry, 50(9), 1073–1083. https://doi.org/10.1111/j.1469-7610.2009.02071.x
RStudio Team. (2020). RStudio: Integrated Development for R. RStudio [computer software]. Boston, MA. Retrieved from http://www.rstudio.com/
Schonfeld, A. M., Mattson, S. N., Lang, A., Delis, D. C., & Riley, E. P. (2001). Verbal and nonverbal fluency in children with heavy prenatal alcohol exposure. Journal of Studies on Alcohol, 62(2), 239–246. https://doi.org/10.15288/jsa.2001.62.239
Sood, B., Delaney-Black, V., Covington, C., Nordstrom-Klee, B., Ager, J., Templin, T., Sokol, R. J. (2001). Prenatal alcohol exposure and childhood behaviorat age 6 to 7 years: I. dose-response effect. Pediatrics, 108(2), E34. https://doi.org/10.1542/peds.108.2.e34
Steinmayr, R., Ziegler, M., & Träuble, B. (2010). Do intelligence and sustained attention interact in predicting academic achievement? Learning and Individual Differences, 20(1), 14–18. https://doi.org/10.1016/j.lindif.2009.10.009
Streissguth, A. P., Bookstein, F. L., Sampson, P. D., & Barr, H. M. (1995). Attention: Prenatal alcohol and continuities of vigilance and attentional problems from 4 through 14 years. Development and Psychopathology, 7(3), 419–446. https://doi.org/10.1111/j.1530-0277.1994.tb00904.x
Streissguth, A. P., Sampson, P. D., Olson, H. C., Bookstein, F. L., Barr, H. M., Scott, M., Mirsky, A. F. (1994). Maternal drinking during pregnancy: attention and short‐term memory in 14‐year old offspring: A longitudinal prospective study. Alcoholism: Clinical and Experimental Research, 18(1), 202–218. https://doi.org/10.1111/j.15300277.1994.tb00904.x
Suades-González, E., Forns, J., García-Esteban, R., López-Vicente, M., Esnaola, M., Álvarez-Pedrerol, M., & Sunyer, J. (2017). A longitudinal study on attention development in primary school children with and without teacher-reportedsymptoms of ADHD. Frontiers in Psychology, 8(655), 1–10. https://doi.org/10.3389/fpsyg.2017.00655
Underbjerg, M., Kesmodel, U., Landrø, N., Bakketeig, L., Grove, J., Wimberley, T., Mortensen, E. (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: An International Journal of Obstetrics & Gynaecology, 119(10), 1211–1221. https://doi.org/10.1111/j.1471-0528.2012.03396.x
Veritas Health Innovation, V. (2017). Covidence systematic review software. Melbourne: Australia: Veritas Health Innovation.
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36(3), 1–48. https://www.jstatsoft.org/v36/i03/
Wells, G., Shea, B., O’Connell, D., Peterson, J., Welch, V., Losos, M., & Tugwell, P. (2013). The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
White, R. F., Campbell, R., Echeverria, D., Knox, S. S., & Janulewicz, P. (2009). Assessment of neuropsychological trajectories in longitudinal populationbased studies of children. Journal of Epidemiology and Community Health, 63(Suppl 1), 15–26. https://doi.org/10.1136/jech.2007.071530
Wozniak, J. R., Muetzel, R. L., Mueller, B. A., McGee, C. L., Freerks, M. A., Ward, E. E., ... Lim, K. O. (2009). Microstructural corpus callosum anomalies inchildren with prenatal alcohol exposure: an extension of previous diffusion tensor imaging findings. Alcoholism: Clinical & Experimental Research,33(10), 1825–1835. https://doi.org/10.1111/j.1530-0277.2009.01021.x
Young, C., & Olney, J. W. (2006). Neuroapoptosis in the infant mouse brain triggered by a transient small increase in blood alcohol concentration. Neurobiology of Disease, 22(3), 548–554. https://doi.org/10.1016/j.nbd.2005.12.015.
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NHMRC Project Grants 1011070 and 1146635; Senior Research Fellowship 628371 to PJA; Leadership Fellowship 1176077 to PJA. This research was supported by an Australian Government Research Training Program Scholarship to PP and SEC and a Monash Graduate Excellence Scholarship.
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The original conceptualisation for this article was developed by Philippa Pyman and all authors contributed to refinement of the ideas and design of this study. Study screening and data extraction were completed by Philippa Pyman and Simonne Collins. The literature search, data analysis and drafting of the manuscript was conducted by Philippa Pyman and all authors critically revised the work. Supervision was provided by Peter Anderson and Renee Testa.
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Pyman, P., Collins, S.E., Muggli, E. et al. Cognitive and Behavioural Attention in Children with Low-Moderate and Heavy Doses of Prenatal Alcohol Exposure: a Systematic Review and Meta-analysis. Neuropsychol Rev 31, 610–627 (2021). https://doi.org/10.1007/s11065-021-09490-8
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DOI: https://doi.org/10.1007/s11065-021-09490-8