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Identifying the contribution of prenatal risk factors to offspring development and psychopathology: What designs to use and a critique of literature on maternal smoking and stress in pregnancy

Published online by Cambridge University Press:  02 August 2018

Frances Rice ,
Kate Langley ,
Christopher Woodford ,
George Davey Smith  and
Anita Thapar
Frances Rice*
Affiliation:
MRC Centre for Neuropsychiatric Genetics and Genomics
Kate Langley
Affiliation:
Cardiff University
Christopher Woodford
Affiliation:
MRC Centre for Neuropsychiatric Genetics and Genomics
George Davey Smith
Affiliation:
Bristol University
Anita Thapar
Affiliation:
MRC Centre for Neuropsychiatric Genetics and Genomics
*
Address correspondence and reprint requests to: Frances Rice, MRC Centre for Neuropsychiatric Genetics and Genomics, Division of Psychological Medicine and Clinical Neurosciences, Hadyn Ellis Building, Maindy Road, Cardiff University, CF24 4HQ, UK; Email: ricef2@cardiff.ac.uk.
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Abstract

Identifying prenatal environmental factors that have genuinely causal effects on psychopathology is an important research priority, but it is crucial to select an appropriate research design. In this review we explain why and what sorts of designs are preferable and focus on genetically informed/sensitive designs. In the field of developmental psychopathology, causal inferences about prenatal risks have not always been based on evidence generated from appropriate designs. We focus on reported links between maternal smoking during pregnancy and offspring attention-deficit/hyperactivity disorder or conduct problems. Undertaking a systematic review of findings from genetically informed designs and “triangulating” evidence from studies with different patterns of bias, we conclude that at present findings suggest it is unlikely that there is a substantial causal effect of maternal smoking in pregnancy on either attention-deficit/hyperactivity disorder or conduct problems. In contrast, for offspring birth weight (which serves as a positive control) findings strongly support a negative causal effect of maternal smoking in pregnancy. For maternal pregnancy stress, too few studies use genetically sensitive designs to draw firm conclusions, but continuity with postnatal stress seems important. We highlight the importance of moving beyond observational designs, for systematic evaluation of the breadth of available evidence and choosing innovative designs. We conclude that a broader set of prenatal risk factors should be examined, including those relevant in low- and middle-income contexts. Future directions include a greater use of molecular genetically informed designs such as Mendelian randomization to test causal hypotheses about prenatal exposure and offspring outcome.

Type
Special Issue Articles
Information
Development and Psychopathology , Volume 30 , Special Issue 3: Developmental Origins of Psychopathology: Mechanisms, Processes, and Pathways Linking the Prenatal Environment to Postnatal Outcomes , August 2018 , pp. 1107 - 1128
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

George Davey Smith works within the Medical Research Council Integrative Epidemiology Unit at the University of Bristol (MC_UU_12013/1).

References

Abraham, M., Alramadhan, S., Iniguez, C., Duijts, L., Jaddoe, V. W., Den Dekker, H. T., … Turner, S. (2017). A systematic review of maternal smoking during pregnancy and fetal measurements with meta-analysis. PLOS ONE, 12, e0170946. doi:10.1371/journal.pone.0170946Google Scholar
Academy of Medical Sciences. (2007). Identifying the environmental causes of disease: How should we decide what to believe and when to take action? London: Author.Google Scholar
Ahmed, I., Sutton, A. J., & Riley, R. D. (2012). Assessment of publication bias, selection bias, and unavailable data in meta-analyses using individual participant data: A database survey. British Medical Journal, 344, d7762. doi:10.1136/bmj.d7762Google Scholar
Anderson, K. E., Hytton, H., & Romney, D. M. (1986). Mothers' interactions with normal and conduct-disordered boys: Who affects whom? Developmental Psychology, 22, 604–609.Google Scholar
Avella-Garcia, C. B., Julvez, J., Fortuny, J., Rebordosa, C., Garcia-Esteban, R., Galan, I. R., … Sunyer, J. (2016). Acetaminophen use in pregnancy and neurodevelopment: Attention function and autism spectrum symptoms. International Journal of Epidemiology, 45, 1987–1996. doi:10.1093/ije/dyw115Google Scholar
Barker, D. J. (2007). The origins of the developmental origins theory. Journal of Internal Medicine, 261, 412–417. doi:10.1111/j.1365-2796.2007.01809.xGoogle Scholar
Bell, R. Q. (1968). A reinterpretation of the direction of effects in studies of socialization. Psychological Review, 75, 81–95.Google Scholar
Brown, A. S., Gyllenberg, D., Malm, H., McKeague, I. W., Hinkka-Yli-Salomaki, S., Artama, M., … Sourander, A. (2016). Association of selective serotonin reuptake inhibitor exposure during pregnancy with speech, scholastic, and motor disorders in offspring. JAMA Psychiatry, 73, 1163–1170. doi:10.1001/jamapsychiatry.2016.2594Google Scholar
Brown, A. S., van Os, J., Driessens, C., Hoek, H. W., & Susser, E. S. (2000). Further evidence of relation between prenatal famine and major affective disorder. American Journal of Psychiatry, 157, 190–195.Google Scholar
Brown, H. K., Ray, J. G., Wilton, A. S., Lunsky, Y., Gomes, T., & Vigod, S. N. (2017). Association between serotonergic antidepressant use during pregnancy and autism spectrum disorder in children. Journal of the American Medical Association, 317, 1544–1552. doi:10.1001/jama.2017.3415Google Scholar
Button, K. S., Ioannidis, J. P., Mokrysz, C., Nosek, B. A., Flint, J., Robinson, E. S., & Munafo, M. R. (2013). Power failure: Why small sample size undermines the reliability of neuroscience. Nature Reviews Neuroscience, 14, 365–376. doi:10.1038/nrn3475Google Scholar
Davey Smith, G. (2008). Assessing intrauterine influences on offspring health outcomes: Can epidemiological studies yield robust findings? Basic Clinical Pharmacology Toxicology, 102, 245–256. doi:10.1111/j.1742-7843.2007.00191.xGoogle Scholar
Davey Smith, G., & Ebrahim, S. (2003). “Mendelian randomization”: Can genetic epidemiology contribute to understanding environmental determinants of disease? International Journal of Epidemiology, 32, 1–22.Google Scholar
Davey Smith, G., & Ebrahim, S. (2004). Mendelian randomization: Prospects, potentials, and limitations. International Journal of Epidemiology, 33, 30–42. doi:10.1093/ije/dyh132Google Scholar
Davey Smith, G., & Hemani, G. (2014). Mendelian randomization: Genetic anchors for causal inference in epidemiological studies. Human Molecular Genetics, 23, R89–R98. doi:10.1093/hmg/ddu328Google Scholar
Demontis, D., Walters, R. K., Martin, J., Mattheisen, M., Als, T. D., Agerbo, E., … ADHD Working Group of the Psychiatric Genomics Consortium. (2017). Discovery of the first genome-wide significant risk loci For ADHD. bioRxiv.Google Scholar
Dolan, C. V., Geels, L., Vink, J. M., van Beijsterveldt, C. E., Neale, M. C., Bartels, M., & Boomsma, D. I. (2016). Testing causal effects of maternal smoking during pregnancy on offspring's externalizing and internalizing behavior. Behavioral Genetics, 46, 378–388. doi:10.1007/s10519-015-9738-2Google Scholar
D'Onofrio, B. M., Class, Q. A., Lahey, B. B., & Larsson, H. (2014). Testing the developmental origins of health and disease hypothesis for psychopathology using family-based quasi-experimental designs. Child Development Perspectives, 8, 151–157. doi:10.1111/cdep.12078Google Scholar
D'Onofrio, B. M., Lahey, B. B., Turkheimer, E., & Lichtenstein, P. (2013). Critical need for family-based, quasi-experimental designs in integrating genetic and social science research. American Journal of Public Health, 103(Suppl. 1), S46–S55. doi:10.2105/AJPH.2013.301252Google Scholar
D'Onofrio, B. M., Singh, A. L., Iliadou, A., Lambe, M., Hultman, C. M., Grann, M., … Lichtenstein, P. (2010). Familial confounding of the association between maternal smoking during pregnancy and offspring criminality: A population-based study in Sweden. Archives of General Psychiatry, 67, 529–538. doi:10.1001/archgenpsychiatry.2010.33Google Scholar
D'Onofrio, B. M., Turkheimer, E. N., Eaves, L. J., Corey, L. A., Berg, K., Solaas, M. H., & Emery, R. E. (2003). The role of the children of twins design in elucidating causal relations between parent characteristics and child outcomes. Journal of Child Psychology and Psychiatry, 44, 1130–1144.Google Scholar
D'Onofrio, B. M., van Hulle, C. A., Goodnight, J. A., Rathouz, P. J., & Lahey, B. B. (2012). Is maternal smoking during pregnancy a causal environmental risk factor for adolescent antisocial behavior? Testing etiological theories and assumptions. Psychological Medicine, 42, 1535–1545. doi:10.1017/S0033291711002443Google Scholar
D'Onofrio, B. M., van Hulle, C. A., Waldman, I. D., Rodgers, J. L., Harden, K. P., Rathouz, P. J., & Lahey, B. B. (2008). Smoking during pregnancy and offspring externalizing problems: An exploration of genetic and environmental confounds. Development and Psychopathology, 20, 139–164. doi:10.1017/S0954579408000072Google Scholar
Easterbrook, P. J., Berlin, J. A., Gopalan, R., & Matthews, D. R. (1991). Publication bias in clinical research. Lancet, 337, 867–872.Google Scholar
Ellingson, J. M., Goodnight, J. A., van Hulle, C. A., Waldman, I. D., & D'Onofrio, B. M. (2014). A sibling-comparison study of smoking during pregnancy and childhood psychological traits. Behavioral Genetics, 44, 25–35. doi:10.1007/s10519-013-9618-6Google Scholar
Fewell, Z., Davey Smith, G., & Sterne, J. A. (2007). The impact of residual and unmeasured confounding in epidemiologic studies: A simulation study. American Journal of Epidemiology, 166, 646–655. doi:10.1093/aje/kwm165Google Scholar
Frisell, T., Öberg, S., Kuja-Halkola, R., & Sjölander, A. (2012). Sibling comparison designs: Bias from non-shared confounders and measurement error. Epidemiology, 23, 713–720.Google Scholar
Gage, S. H., Munafo, M. R., & Davey-Smith, G. (2016). Causal inference in developmental origins of health and disease (DOHaD) research. Annual Review of Psychology, 67, 567–585. doi:10.1146/annurev-psych-122414-033352Google Scholar
Gaysina, D., Fergusson, D. M., Leve, L. D., Horwood, J., Reiss, D., Shaw, D. S., … Harold, G. T. (2013). Maternal smoking during pregnancy and offspring conduct problems: Evidence from 3 independent genetically sensitive research designs. JAMA Psychiatry, 70, 956–963. doi:10.1001/jamapsychiatry.2013.127Google Scholar
Ge, X., Conger, R. D., Cadoret, R. J., Neiderhiser, J. M., Yates, W., Troughton, E., & Stewart, M. A. (1996). The developmental interface between nature and nurture: A mutual influence model of child antisocial behaviour and parent behaviour. Developmental Psychology, 32, 574–589.Google Scholar
George, L., Granath, F., Johansson, A. L., & Cnattingius, S. (2006). Self-reported nicotine exposure and plasma levels of cotinine in early and late pregnancy. Acta Obstetricia et Gynecologica Scandinavica, 85, 1331–1337. doi:10.1080/00016340600935433Google Scholar
Gilman, S. E., Breslau, J., Subramanian, S. V., Hitsman, B., & Koenen, K. C. (2008). Social factors, psychopathology, and maternal smoking during pregnancy. American Journal of Public Health, 98, 448–453. doi:10.2105/AJPH.2006.102772Google Scholar
Gilman, S. E., Gardener, H., & Buka, S. L. (2008). Maternal smoking during pregnancy and children's cognitive and physical development: A causal risk factor? American Journal of Epidemiology, 168, 522–531. doi:10.1093/aje/kwn175Google Scholar
Golombok, S. (2017). Parenting in new family forms. Current Opinion in Psychology, 15, 76–80. doi:10.1016/j.copsyc.2017.02.004Google Scholar
Golombok, S., & MacCallum, F. (2003). Practitioner review: Outcomes for parents and children following non-traditional conception: What do clinicians need to know? Journal of Child Psychology and Psychiatry, 44, 303–315.Google Scholar
Grizenko, N., Fortier, M. E., Zadorozny, C., Thakur, G., Schmitz, N., Duval, R., & Joober, R. (2012). Maternal stress during pregnancy, ADHD symptomatology in children and genotype: Gene–environment interaction. Journal of the Canadian Academy of Child and Adolescent Psychiatry, 21, 9–15.Google Scholar
Grzeskowiak, L. E., Morrison, J. L., Henriksen, T. B., Bech, B. H., Obel, C., Olsen, J., & Pedersen, L. H. (2016). Prenatal antidepressant exposure and child behavioural outcomes at 7 years of age: A study within the Danish National Birth Cohort. International Journal of Obstetrics & Gynaecology, 123, 1919–1928. doi:10.1111/1471-0528.13611Google Scholar
Gustavson, K., Ystrom, E., Stoltenberg, C., Susser, E., Suren, P., Magnus, P., … Reichborn-Kjennerud, T. (2017). Smoking in pregnancy and child ADHD. Pediatrics. Advance online publication. doi:10.1542/peds.2016-2509Google Scholar
Huizink, A. C., & Mulder, E. J. (2006). Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neuroscience and Biobehavioral Reviews, 30, 24–41. doi:10.1016/j.neubiorev.2005.04.005Google Scholar
Instanes, J. T., Halmoy, A., Engeland, A., Haavik, J., Furu, K., & Klungsoyr, K. (2017). Attention-deficit/hyperactivity disorder in offspring of mothers with inflammatory and immune system diseases. Biological Psychiatry, 81, 452–459. doi:10.1016/j.biopsych.2015.11.024Google Scholar
Jaffee, S. R., & Price, T. S. (2008). Genotype-environment correlations: Implications for determining the relationship between environmental exposures and psychiatric illness. Psychiatry, 7, 496–499.Google Scholar
Kaaja, R. J., & Greer, I. A. (2005). Manifestations of chronic disease during pregnancy. Journal of the American Medical Association, 294, 2751–2757.Google Scholar
Kendler, K. S., & Baker, J. H. (2007). Genetic influences on measures of the environment: A systematic review. Psychological Medicine, 37, 615–626.Google Scholar
Kendler, K. S., Neale, M. C., Sullivan, P., Corey, L. A., Gardner, C. O., & Prescott, C. A. (1999). A population-based twin study in women of smoking initiation and nicotine dependence. Psychological Medicine, 29, 299–308.Google Scholar
Keyes, K. M., Davey Smith, G., & Susser, E. (2014). Associations of prenatal maternal smoking with offspring hyperactivity: Causal or confounded? Psychological Medicine, 44, 857–867. doi:10.1017/S0033291713000986Google Scholar
Knopik, V. S., Marceau, K., Bidwell, L. C., Palmer, R. H., Smith, T. F., Todorov, A., … Heath, A. C. (2016). Smoking during pregnancy and ADHD risk: A genetically informed, multiple-rater approach. American Journal of Medical Genetics, 171, 971–981. doi:10.1002/ajmg.b.32421Google Scholar
Kovess, V., Keyes, K. M., Hamilton, A., Pez, O., Bitfoi, A., Koc, C., … Susser, E. (2015). Maternal smoking and offspring inattention and hyperactivity: Results from a cross-national European survey. European Child and Adolescent Psychiatry, 24, 919–929. doi:10.1007/s00787-014-0641-9Google Scholar
Kuja-Halkola, R., D'Onofrio, B. M., Larsson, H., & Lichtenstein, P. (2014). Maternal smoking during pregnancy and adverse outcomes in offspring: Genetic and environmental sources of covariance. Behavioral Genetics, 44, 456–467. doi:10.1007/s10519-014-9668-4Google Scholar
Langley, K., Heron, J., Smith, G. D., & Thapar, A. (2012). Maternal and paternal smoking during pregnancy and risk of ADHD symptoms in offspring: Testing for intrauterine effects. American Journal of Epidemiology, 176, 261–268. doi:10.1093/aje/kwr510Google Scholar
Langley, K., Rice, F., van den Bree, M. B., & Thapar, A. (2005). Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour: A review. Minerva Pediatrics, 57, 359–371.Google Scholar
Lawlor, D., Richmond, R., Warrington, N., McMahon, G., Davey Smith, G., Bowden, J., & Evans, D. M. (2017). Using Mendelian randomization to determine causal effects of maternal pregnancy (intrauterine) exposures on offspring outcomes: Sources of bias and methods for assessing them. Wellcome Open Research, 2, 11. doi:10.12688/wellcomeopenres.10567.1Google Scholar
Lawlor, D. A., Tilling, K., & Davey Smith, G. (2016). Triangulation in aetiological epidemiology. International Journal of Epidemiology, 45, 1866–1886. doi:10.1093/ije/dyw314Google Scholar
Lessov, C. N., Martin, N. G., Statham, D. J., Todorov, A. A., Slutske, W. S., Bucholz, K. K., … Madden, P. A. (2004). Defining nicotine dependence for genetic research: Evidence from Australian twins. Psychological Medicine, 34, 865–879.Google Scholar
Li, M. D., Cheng, R., Ma, J. Z., & Swan, G. E. (2003). A meta-analysis of estimated genetic and environmental effects on smoking behavior in male and female adult twins. Addiction, 98, 23–31.Google Scholar
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P., … Moher, D. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. Journal of Clinical Epidemiology, 62, e1–e34.Google Scholar
Lindblad, F., & Hjern, A. (2010). ADHD after fetal exposure to maternal smoking. Nicotine & Tobacco Research, 12, 408–415. doi:10.1093/ntr/ntq017Google Scholar
Linnet, K. M., Dalsgaard, S., Obel, C., Wisborg, K., Henriksen, T. B., Rodriguez, A., … Jarvelin, M. R. (2003). Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: Review of the current evidence. American Journal of Psychiatry, 160, 1028–1040. doi:10.1176/appi.ajp.160.6.1028Google Scholar
Lumey, L. H., Stein, A. D., & Susser, E. (2011). Prenatal famine and adult health. Annual Review of Public Health, 32, 237–262. doi:10.1146/annurev-publhealth-031210-101230Google Scholar
Mackay, E., Dalman, C., Karlsson, H., & Gardner, R. M. (2017). Association of gestational weight gain and maternal body mass index in early pregnancy with risk for nonaffective psychosis in offspring. JAMA Psychiatry, 74, 339–349. doi:10.1001/jamapsychiatry.2016.4257Google Scholar
Maes, H. H., Sullivan, P. F., Bulik, C. M., Neale, M. C., Prescott, C. A., Eaves, L. J., & Kendler, K. S. (2004). A twin study of genetic and environmental influences on tobacco initiation, regular tobacco use and nicotine dependence. Psychological Medicine, 34, 1251–1261.Google Scholar
Man, K. K. C., Chan, E. W., Ip, P., Coghill, D., Simonoff, E., Chan, P. K. L., … Wong, I. C. K. (2017). Prenatal antidepressant use and risk of attention-deficit/hyperactivity disorder in offspring: Population based cohort study. British Medical Journal, 357, j2350. doi:10.1136/bmj.j2350Google Scholar
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E. (2004). Prenatal smoking and early childhood conduct problems: Testing genetic and environmental explanations of the association. Archives of General Psychiatry, 61, 836–843.Google Scholar
McDonald, S.D., Malinowski, A., Zhou, Q., Yusuf, S., & Devereaux, P. J. (2008). Cardiovascular sequelae of preeclampsia/eclampsia: A systematic review and meta-analyses. American Heart Journal, 156, 918–930.Google Scholar
Obel, C., Olsen, J., Henriksen, T. B., Rodriguez, A., Jarvelin, M. R., Moilanen, I., … Gissler, M. (2011). Is maternal smoking during pregnancy a risk factor for hyperkinetic disorder? Findings from a sibling design. International Journal of Epidemiology, 40, 338–345. doi:10.1093/ije/dyq185Google Scholar
Obel, C., Zhu, J. L., Olsen, J., Breining, S., Li, J., Gronborg, T. K., … Rutter, M. (2016). The risk of attention deficit hyperactivity disorder in children exposed to maternal smoking during pregnancy—A re-examination using a sibling design. Journal of Child Psychology and Psychiatry, 57, 532–537. doi:10.1111/jcpp.12478Google Scholar
O'Donnell, K. J., & Meaney, M. J. (2017). Fetal origins of mental health: The developmental origins of health and disease hypothesis. American Journal of Psychiatry, 174, 319–328. doi:10.1176/appi.ajp.2016.16020138Google Scholar
Oerlemans, A. M., Hartman, C. A., De Bruijn, Y. G., van Steijn, D. J., Franke, B., Buitelaar, J. K., & Rommelse, N. N. (2015). Simplex and multiplex stratification in ASD and ADHD families: A promising approach for identifying overlapping and unique underpinnings of ASD and ADHD? Journal of Autism and Developmental Disorders, 45, 645–657. doi:10.1007/s10803-014-2220-9Google Scholar
Paradis, A. D., Shenassa, E. D., Papandonatos, G. D., Rogers, M. L., & Buka, S. L. (2017). Maternal smoking during pregnancy and offspring antisocial behaviour: Findings from a longitudinal investigation of discordant siblings. Journal of Epidemiology and Community Health, 71, 889–896. doi:10.1136/jech-2016-208511Google Scholar
Plomin, R., DeFries, J. C., & Loehlin, J. C. (1977). Genotype-environment interaction and correlation in the analysis of human behavior. Psycholical Bulletin, 84, 309–322.Google Scholar
Rai, D., Lee, B. K., Dalman, C., Newschaffer, C., Lewis, G., & Magnusson, C. (2017). Antidepressants during pregnancy and autism in offspring: Population based cohort study. British Medical Jouranl, 358, j2811. doi:10.1136/bmj.j2811Google Scholar
Rasmussen, S. A., Jamieson, D. J., Honein, M. A., & Petersen, L. R. (2016). Zika virus and birth defects—Reviewing the evidence for causality. New England Journal of Medicine, 374, 1981–1987. doi:10.1056/NEJMsr1604338Google Scholar
Ray, J. G., Vermeulen, M. J., Schull, M. J., & Redelmeier, D. A. (2005). Cardiovascular health after maternal placental syndromes (CHAMPS): Population-based retrospective cohort study. Lancet, 366, 1797–1803.Google Scholar
Reiss, D., Neiderhiser, J. M., Hetherington, E. M., & Plomin, R. (2000). The relationship code: Deciphering genetic and social patterns in adolescent development. Cambridge, MA: Harvard University Press.Google Scholar
Repetti, R. l., Taylor, S. E., & Seeman, T. E. (2002). Risky families: Family social environments and the mental and physical health of offspring. Psychological Bulletin, 128, 330–366.Google Scholar
Rice, F., Harold, G. T., Boivin, J., Hay, D. F., van den Bree, M., & Thapar, A. (2009). Disentangling prenatal and inherited influences in humans with an experimental design. Proceedings of the National Academy of Sciences USA, 106, 2464–2467. doi:10.1073/pnas.0808798106Google Scholar
Rice, F., Harold, G. T., Boivin, J., van den Bree, M., Hay, D. F., & Thapar, A. (2010). The links between prenatal stress and offspring development and psychopathology: Disentangling environmental and inherited influences. Psycholical Medicine, 40, 335–345. doi:10.1017/S0033291709005911Google Scholar
Rice, F., Jones, I., & Thapar, A. (2007). The impact of gestational stress and prenatal growth on emotional problems in offspring: A review. Acta Obstetricia et Gynecologica Scandinavica, 115, 171–183. doi:10.1111/j.1600-0447.2006.00895.xGoogle Scholar
Rice, F., Lewis, A., Harold, G., van den Bree, M., Boivin, J., Hay, D. F., … Thapar, A. (2007). Agreement between maternal report and antenatal records for a range of pre- and peri-natal factors: The influence of maternal and child characteristics. Early Human Development, 83, 497–504. doi:10.1016/j.earlhumdev.2006.09.015Google Scholar
Ruisch, I. H., Dietrich, A., Glennon, J. C., Buitelaar, J. K., & Hoekstra, P. J. (2017). Maternal substance use during pregnancy and offspring conduct problems: A meta-analysis. Neuroscience and Biobehavioral Reviews. Advance online publication. doi:10.1016/j.neubiorev.2017.08.014Google Scholar
Rutter, M. (2007). Proceeding from observed correlation to causal inference: The use of natural experiments. Perspectives on Psychological Science, 2, 377–395. doi:10.1111/j.1745-6916.2007.00050.xGoogle Scholar
Rutter, M., Moffitt, T. E., & Caspi, A. (2006). Gene-environment interplay and psychopathology: Multiple varieties but real effects. Journal of Child Psychology and Psychiatry, 47, 226–261.Google Scholar
Rutter, M., Pickles, A., Murray, R., & Eaves, L. (2001). Testing hypotheses on specific environmental causal effects on behavior. Psycholical Bulletin, 127, 291–324.Google Scholar
Rutter, M., & Thapar, A. (2016). Using natural experiments to test environmental mediation hypotheses. In Cicchetti, D. (Ed.), Developmental psychopathology: Vol. 1. Theory and method (pp. 129–155). Hoboken, NJ: Wiley.Google Scholar
Sellers, R., Hammerton, G., Harold, G. T., Mahedy, L., Potter, R., Langley, K., … Collishaw, S. (2016). Examining whether offspring psychopathology influences illness course in mothers with recurrent depression using a high-risk longitudinal sample. Journal of Abnormal Psychology, 125, 256–266. doi:10.1037/abn0000080Google Scholar
Shelton, K. H., Boivin, J., Hay, D. F., van den Bree, M. M. B., Rice, F., Harold, G. T., & Thapar, A. (2009). Examining differences in psychological adjustment problems among children conceived by assisted reproductive technologies International Journal of Behavioral Development, 33, 1–8.Google Scholar
Shiner, R., & Caspi, A. (2003). Personality differences in childhood and adolescence: Measurement, development, and consequences. Journal of Child Psychology and Psychiatry, 44, 2–32.Google Scholar
Silberg, J. L., Maes, H., & Eaves, L. J. (2010). Genetic and environmental influences on the transmission of parental depression to children's depression and conduct disturbance: An extended Children of Twins study. Journal of Child Psychology and Psychiatry, 51, 734–744. doi:10.1111/j.1469-7610.2010.02205.xGoogle Scholar
Sjölander, A., Frisell, T., Kuja-Halkola, R., Öberg, S., & Zetterqvist, J. (2016). Carryover effects in sibling comparison designs. Epidemiology, 27, 852–858.Google Scholar
Sjölander, A., & Zatterqvist, J. (2017). Confounders, mediators, or colliders: What types of shared covariates does a sibling comparison design control for? Epidemiology, 28, 540–547.Google Scholar
Skoglund, C., Chen, Q., D'Onofrio, B. M., Lichtenstein, P., & Larsson, H. (2014). Familial confounding of the association between maternal smoking during pregnancy and ADHD in offspring. Journal of Child Psychology and Psychiatry, 55, 61–68. doi:10.1111/jcpp.12124Google Scholar
Slotkin, T. A. (2013). Maternal smoking and conduct disorder in the offspring. JAMA Psychiatry, 70, 901–902. doi:10.1001/jamapsychiatry.2013.1951Google Scholar
St. Clair, D., Xu, M., Wang, P., Yu, Y., Fang, Y., Zhang, F., … He, L. (2005). Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959–1961. Journal of the American Medical Association, 294, 557–562. doi:10.1001/jama.294.5.557Google Scholar
Stergiakouli, E., Thapar, A., & Davey Smith, G. (2016). Association of acetaminophen use during pregnancy with behavioral problems in childhood: Evidence against confounding. JAMA Pediatrics, 170, 964–970. doi:10.1001/jamapediatrics.2016.1775Google Scholar
Susser, E., Neugebauer, R., Hoek, H. W., Brown, A. S., Lin, S., Labovitz, D., & Gorman, J. M. (1996). Schizophrenia after prenatal famine: Further evidence. Archives of General Psychiatry, 53, 25–31.Google Scholar
Talati, A., Keyes, K. M., & Hasin, D. S. (2016). Changing relationships between smoking and psychiatric disorders across twentieth century birth cohorts: Clinical and research implications. Molecular Psychiatry, 21, 464–471. doi:10.1038/mp.2015.224Google Scholar
Talati, A., Wickramaratne, P. J., Keyes, K. M., Hasin, D. S., Levin, F. R., & Weissman, M. M. (2013). Smoking and psychopathology increasingly associated in recent birth cohorts. Drug and Alcohol Dependence, 133, 724–732. doi:10.1016/j.drugalcdep.2013.08.025Google Scholar
Talge, N. M., Neal, C., Glover, V., & Early Stress Translational Research Prevention Science Network: Fetal and Neonatal Experience on Child and Adolescent Mental Health. (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: How and why? Journal of Child Psychology and Psychiatry, 48, 245–261. doi:10.1111/j.1469-7610.2006.01714.xGoogle Scholar
Thapar, A., Harold, G. T., Rice, F., Ge, X., Boivin, J., Hay, D., … Lewis, A. (2007). Do intrauterine or genetic influences explain the foetal origins of chronic disease? A novel experimental method for disentangling effects. BMC Medical Research Methodology, 7, 25.Google Scholar
Thapar, A., Rice, F., Hay, D., Boivin, J., Langley, K., van den Bree, M., … Harold, G. (2009). Prenatal smoking might not cause attention-deficit/hyperactivity disorder: Evidence from a novel design. Bioligical Psychiatry, 66, 722–727. doi:10.1016/j.biopsych.2009.05.032Google Scholar
Thapar, A., & Rutter, M. (2009). Do prenatal risk factors cause psychiatric disorder? Be wary of causal claims. British Journal of Psychiatry, 195, 100–101. doi:10.1192/bjp.bp.109.062828Google Scholar
Thapar, A., & Rutter, M. (2015). Using natural experiments and animal models to study causal hypotheses in relation to child mental health problems. In Thapar, A., Pine, D. S., Leckman, J. F., Scott, S., Snowling, M. J., & Taylor, E. A. (Eds.), Rutter's child and adolescent psychiatry (6th ed., pp. 145–162). London: Wiley-Blackwell.Google Scholar
Tobacco and Genetics Consortium. (2010). Genome-wide meta-analyses identify multiple loci associated with smoking behavior. Nature Genetics, 42, 441.Google Scholar
Tully, L. A., Arseneault, L., Caspi, A., Moffitt, T. E., & Morgan, J. (2004). Does maternal warmth moderate the effects of birth weight on twins' attention-deficit/hyperactivity disorder (ADHD) symptoms and low IQ? Journal of Consulting and Clinical Psychology, 72, 218–226.Google Scholar
Tyrrell, J., Huikari, V., Christie, J. T., Cavadino, A., Bakker, R., Brion, M. J., … Early Growth Genetics Consortium. (2012). Genetic variation in the 15q25 nicotinic acetylcholine receptor gene cluster (CHRNA5-CHRNA3-CHRNB4) interacts with maternal self-reported smoking status during pregnancy to influence birth weight. Human Molecular Genetics, 21, 5344–5358. doi:10.1093/hmg/dds372Google Scholar
Veisani, Y., Jenabi, E., Delpisheh, A., & Khazaei, S. (2017). Effect of prenatal smoking cessation interventions on birth weight: Meta-analysis. Journal of Maternal–Fetal & Neonatal Medicine. Advance online publication. doi:10.1080/14767058.2017.1378335Google Scholar
Weiner, D. J., Wigdor, E. M., Ripke, S., Walters, R. K., Kosmicki, J. A., Grove, J., … Robinson, E. B. (2017). Polygenic transmission disequilibrium confirms that common and rare variation act additively to create risk for autism spectrum disorders. Nature Genetics, 49, 978–985. doi:10.1038/ng.3863Google Scholar