Prenatal glucocorticoid treatment and later mental health in children and adolescents

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Khalife, Natasha ^a   Glover, Vivette ^a   Taanila, Anja ^b,c   Ebeling, Hanna ^b,c   Järvelin, Marjo Riitta ^a,b,c,d   Rodriguez, Alina ^a,e  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OULU   (Finland)

^c OULU UNIVERSITY HOSPITAL   (Finland)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^e MID SWEDEN UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETAMETHASONE; DEXAMETHASONE; GLUCOCORTICOID; LONG ACTING DRUG;

ADOLESCENT; ADULT; ADVERSE OUTCOME; ARTICLE; ATTENTION DEFICIT DISORDER; ATTENTION DISTURBANCE; BIRTH WEIGHT; BODY MASS; CHILD; CHILDBIRTH; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GESTATIONAL AGE; HUMAN; MAJOR CLINICAL STUDY; MALE; MENTAL DISEASE; PLACENTA WEIGHT; PREGNANCY; PREGNANCY OUTCOME; PRENATAL DRUG EXPOSURE; PROPENSITY SCORE; RATING SCALE; SCHOOL CHILD; SEX; SINGLE DRUG DOSE; STRENGTHS AND WEAKNESSES OF ADHD SYMPTOMS AND NORMAL BEHAVIOR SCALE; TEACHER; YOUTH SELF REPORT SCALE; CASE CONTROL STUDY; ENVIRONMENTAL EXPOSURE; INFANT; MENTAL HEALTH; NEWBORN; PRENATAL EXPOSURE; PRESCHOOL CHILD; RISK FACTOR;

ADOLESCENT; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; FEMALE; GLUCOCORTICOIDS; HUMANS; INFANT; INFANT, NEWBORN; MATERNAL EXPOSURE; MENTAL HEALTH; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS;

EID: 84896719836     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081394     Document Type: Article

References (67)

1. Seckl JR, Meaney MJ (2004) Glucocorticoid Programming. Ann N Y Acad Sci 1032: 63-84. doi:10.1196/annals.1314.006. PubMed: 15677396. (Pubitemid 40298461)
2. Meyer JS (1983) Early adrenalectomy stimulates subsequent growth and development of the rat brain. Exp Neurol 82: 432-446. doi:10.1016/0014-4886(83) 90415-6. PubMed: 6628629.
3. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10: 434-445. doi:10.1038/nrn2639. PubMed: 19401723.
4. O'Donnell K, O'Connor TG, Glover V (2009) Prenatal Stress and Neurodevelopment of the Child: Focus on the HPA Axis and Role of the Placenta. Dev Neurosci 31: 285-292. doi:10.1159/000216539. PubMed: 19546565.
5. Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46: 246-254. doi:10.1111/j.1469-7610.2004.00359.x. PubMed: 15755301. (Pubitemid 40439430)
6. Talge NM, Neal C, Glover V (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48: 245-261. doi:10.1111/j.1469-7610.2006.01714.x. PubMed: 17355398. (Pubitemid 46372120)
7. Subcommittee on Attention-Deficit/Hyperactivity Disorder, Steering Committee on Quality Improvement and Management (2011) ADHD: Clinical Practice Guideline for the Diagnosis, Evaluation, and Treatment of Attention-Deficit/ Hyperactivity Disorder in Children and Adolescents. Pediatrics 128: 1007-1022.
8. Faraone SV, Sergeant J, Gillberg C, Biederman J (2003) The worldwide prevalence of ADHD: is it an American condition? World Psychiatry 2: 104-113. PubMed: 16946911.
9. Rodriguez A, Järvelin M-R, Obel C, Taanila A, Miettunen J et al. (2007) Do inattention and hyperactivity symptoms equal scholastic impairment? evidence from three European cohorts. BMC Public Health 7: 327. doi:10.1186/1471-2458-7-327. PubMed: 17999767.
10. Harris A, Seckl J (2011) Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 59: 279-289. doi:10.1016/j.yhbeh.2010.06.007. PubMed: 20591431.
11. Kapoor A, Petropoulos S, Matthews SG (2008) Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain. Res Rev 57: 586-595. doi:10.1016/j.brainresrev.2007.06. 013. (Pubitemid 351381772)
12. Owen D, Matthews SG (2007) Repeated maternal glucocorticoid treatment affects activity and hippocampal NMDA receptor expression in juvenile guinea pigs. J Physiol 578: 249-257. PubMed: 17068098. (Pubitemid 44971122)
13. Schneider ML, Moore CF, Kraemer GW, Roberts AD, DeJesus OT (2002) The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 27: 285-298. doi:10.1016/S0306-4530(01)00050-6. PubMed: 11750784. (Pubitemid 34028172)
14. Andrews MH, Matthews SG (2003) Antenatal glucocortoids: is there cause for concern? Fetal Matern Med Rev 14: 329-354. doi:10.1017/S0965539503001141. (Pubitemid 38419867)
15. French NP, Hagan R, Evans SF, Mullan A, Newnham JP (2004) Repeated antenatal corticosteroids: Effects on cerebral palsy and childhood behavior. Am J Obstet Gynecol 190: 588-595. doi:10.1016/j.ajog.2003.12.016. PubMed: 15041985. (Pubitemid 38406764)
16. Crowther CA, Doyle LW, Haslam RR, Hiller JE, Harding JE et al. (2007) Outcomes at 2 Years of Age after Repeat Doses of Antenatal Corticosteroids. N Engl J Med 357: 1179-1189. doi:10.1056/NEJMoa071152. PubMed: 17881750. (Pubitemid 47443177)
17. Thorp JA, O'Connor M, Belden B, Etzenhouser J, Hoffman EL et al. (2003) Effects of Phenobarbital and Multiple-Dose Corticosteroids on Developmental Outcome at Age 7 Years. Obstet Gynecol 101: 363-373. doi:10.1016/S0029-7844(02) 02509-7. PubMed: 12576262. (Pubitemid 36170139)
18. Trautman PD, Meyer-Bahlburg HFL, Postelnek J, New MI (1995) Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: Results of a pilot study. Psychoneuroendocrinology 20: 439-449. doi:10.1016/0306-4530(94)00070-0. PubMed: 8532827.
19. Hirvikoski T, Nordenström A, Lindholm T, Lindblad F, Ritzén EM et al. (2008) Long-term follow-up of prenatally treated children at risk for congenital adrenal hyperplasia: does dexamethasone cause behavioural problems? Eur J Endocrinol 159: 309-316. doi:10.1530/EJE-08-0280. PubMed: 18579553.
20. The American College of Obstetricians & Gynecologists (2011) Committee Opinion No. 475: Antenatal Corticosteroid Therapy for Fetal Maturation. Obstet Gynecol 117: 422-424. doi:10.1097/AOG.0b013e31820eee00. PubMed: 21252775.
21. Dalziel SR, Lim VK, Lambert A, McCarthy D, Parag V et al. (2005) Antenatal exposure to betamethasone: psychological functioning and health related quality of life 31 years after inclusion in randomised controlled trial. BMJ 331: 665. doi:10.1136/bmj.38576.494363.E0. PubMed: 16143712.
22. Ali Khan A, Rodriguez A, Kaakinen M, Pouta A, Hartikainen A-L et al. (2011) Does in utero exposure to synthetic glucocorticoids influence birthweight, head circumference and birth length? A systematic review of current evidence in humans. Paediatr Perinat Epidemiol 25: 20-36. doi:10.1111/j.1365- 3016.2010.01147.x. PubMed: 21133966.
23. Schlotz W, Phillips DIW (2009) Fetal origins of mental health: Evidence and mechanisms. Brain Behav Immun 23: 905-916. doi:10.1016/j.bbi.2009.02.001. PubMed: 19217937.
24. Hobel CJ, Goldstein A, Barrett ES (2008) Psychosocial Stress and Pregnancy Outcome. Clin Obstet Gynecol 51: 333-348. doi:10.1097/GRF. 0b013e31816f2709. PubMed: 18463464. (Pubitemid 351655105)
25. Benediktsson R, Calder AA, Edwards CRW, Seckl JR (1997) Placental 11β-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clin Endocrinol 46: 161-166. doi:10.1046/j.1365-2265.1997.1230939.x. (Pubitemid 27122161)
26. Seckl JR, Holmes MC (2007) Mechanisms of Disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nat Clin Pract Endocrinol Metab 3: 479-488. doi:10.1038/ncpneuro0572. PubMed: 17515892. (Pubitemid 46808745)
27. Sawady J, Mercer BM, Wapner RJ, Zhao Y, Sorokin Y et al. (2007) The National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network Beneficial Effects of Antenatal Repeated Steroids study: impact of repeated doses of antenatal corticosteroids on placental growth and histologic findings. Am J Obstet Gynecol 197: 281.e281-281.e288. PubMed: 17826421.
28. Tegethoff M, Greene N, Olsen J, Meyer AH, Meinlschmidt G (2010) Maternal Psychosocial Stress during Pregnancy and Placenta Weight: Evidence from a National Cohort Study. PLOS ONE 5: e14478. doi:10.1371/journal.pone.0014478. PubMed: 21217829.
29. Khalife N, Glover V, Hartikainen A-L, Taanila A, Ebeling H et al. (2012) Placental Size Is Associated with Mental Health in Children and Adolescents. PLOS ONE 7: e40534. doi:10.1371/journal.pone.0040534. PubMed: 22792364.
30. Godfrey KM, Barker DJ (2001) Fetal programming and adult health. Public Health Nutr 4: 611-624. PubMed: 11683554. (Pubitemid 32524581)
31. Glynn RJ, Schneeweiss S, Stürmer T (2006) Indications for Propensity Scores and Review of their Use in Pharmacoepidemiology. Basic Clin Pharmacol Toxicol 98: 253-259. PubMed: 16611199.
32. Rodriguez A, Miettunen J, Henriksen TB, Olsen J, Obel C et al. (2008) Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. Int J Obes (Lond) 32: 550-557. doi:10.1038/sj.ijo.0803741. PubMed: 17938639. (Pubitemid 351414811)
33. Mulder EJH, Robles de Medina PG, Huizink AC, Van den Bergh BRH, Buitelaar JK et al. (2002) Prenatal maternal stress: effects on pregnancy and the (unborn). Child - Early Hum Dev 70: 3-14. doi:10.1016/S0378-3782(02)00075-0. (Pubitemid 35351300)
34. Blanford AT, Murphy BE (1977) In vitro metabolism of prednisolone, dexamethasone, betamethasone, and cortisol by the human placenta. Am J Obstet Gynecol 127: 264-267. PubMed: 835623.
35. Melby JC (1977) Clinical Pharmacology of Systemic Corticosteroids. Annu Rev Pharmacol Toxicol 17: 511-527. doi:10.1146/annurev.pa.17.040177.002455. PubMed: 194533.
36. Rutter M (1967) A children's behaviour questionnaire for completion by teachers: preliminary findings. J Child Psychol Psychiatry 8: 1-11. doi:10.1111/j.1469-7610.1967.tb02175.x. PubMed: 6033260.
37. Swanson JM, Schuck S, Mann M, Carlson C, Hartman K et al. Categorical and dimensional definitions and evaluations of symptoms of ADHD: the SNAP and SWAN ratings scales. Available: http://www.adhd.net/SNAP-SWAN.pdf. Accessed June 27, 2013
38. Achenbach T, Rescorla L (2001) Manual for the ASEBA School Age Forms & Profiles. Burlington, VT, University of Vermont, Research Center for Children, Youth, & Families.
39. Rodriguez A, Olsen J, Kotimaa AJ, Kaakinen M, Moilanen I et al. (2009) Is prenatal alcohol exposure related to inattention and hyperactivity symptoms in children? Disentangling the effects of social adversity. J Child Psychol Psychiatry 50: 1073-1083. doi:10.1111/j.1469-7610.2009.02071.x. PubMed: 19298478.
40. Obel C, Linnet KM, Henriksen TB, Rodriguez A, Järvelin MR et al. (2009) Smoking during pregnancy and hyperactivity-inattention in the offspring - comparing results from three Nordic cohorts. Int J Epidemiol 38: 698-705. doi:10.1093/ije/dym290. PubMed: 18250076.
41. Zahn-Waxler C, Shirtcliff EA, Marceau K (2008) Disorders of Childhood and Adolescence: Gender and Psychopathology. Annu Rev Clin Psychol 4: 275-303. doi:10.1146/annurev.clinpsy.3.022806.091358. PubMed: 18370618. (Pubitemid 351668619)
42. Potijk MR, de Winter AF, Bos AF, Kerstjens JM, Reijneveld SA (2012) Higher rates of behavioural and emotional problems at preschool age in children born moderately preterm. Arch Dis Child 97: 112-117. doi: 10.1136/adc.2011. 300131. PubMed: 22147746.
43. Riordan DV, Morris C, Hattie J, Stark C (2012) Family size and perinatal circumstances, as mental health risk factors in a Scottish birth cohort. Soc Psychiatry Psychiatr Epidemiol 47: 975-983. doi:10.1007/s00127-011-0405-5. PubMed: 21667190.
44. Faul F, Erdfelder E, Lang A-G, Buchner A (2007) G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39: 175-191.
45. Rosenbaum PR, Rubin DB (1983) The Central Role of the Propensity Score in Observational Studies for Causal Effects. Biometrika 70: 41-55. doi:10.1093/biomet/70.1.41.
46. Austin PC (2011) Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat 10: 150-161. doi:10.1002/pst.433. PubMed: 20925139.
47. Ming K, Rosenbaum PR (2000) Substantial Gains in Bias Reduction from Matching with a Variable Number of Controls. Biometrics 56: 118-124. doi:10.1111/j.0006-341X.2000.00118.x. PubMed: 10783785. (Pubitemid 30165098)
48. Wen SW, Smith G, Yang Q, Walker M (2004) Epidemiology of preterm birth and neonatal outcome. Semin Fetal Neonatal Med 9: 429-435. doi:10.1016/j.siny. 2004.04.002. PubMed: 15691780. (Pubitemid 41123649)
49. Eriksson JG, Kajantie E, Osmond C, Thornburg K, Barker DJ (2010) Boys live dangerously in the womb. Am J Hum Biol 22: 330-335. doi:10.1002/ajhb.20995. PubMed: 19844898.
50. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Lai M-C et al. (2012) Fetal Programming Effects of Testosterone on the Reward System and Behavioral Approach Tendencies in Humans. Biol Psychiatry 72: 839-847. doi:10.1016/j. biopsych.2012.05.027. PubMed: 22763187.
51. International Agency for Research of Cancer (1999) Cancer Epidemiology: Principles and Methods. Available: http://www.iarc.fr/en/ publications/pdfs- online/epi/cancerepi/CancerEpi.pdf. Accessed February 1, 2013
52. Bollen K, Stine R (1990) Direct and indirect effects: Classical and bootstrap estimates of variability. Sociol Methodol 20: 115-140. doi:10.2307/271084.
53. Preacher KJ, Hayes AF (2004) SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behav Res Methods Instrum Comput 36: 717-731. doi:10.3758/BF03206553. PubMed: 15641418. (Pubitemid 40251423)
54. MacKinnon DP, Lockwood CM, Williams J (2004) Confidence Limits for the Indirect Effect: Distribution of the Product and Resampling. Methods - Multivariate Behav Res 39: 99-128. doi:10.1207/s15327906mbr3901-4. (Pubitemid 38882481)
55. Reynolds RM (2013) Glucocorticoid excess and the developmental origins of disease: Two decades of testing the hypothesis. Psychoneuroendocrinology 38: 1-11. PubMed: 22998948.
56. Diaz R, Brown RW, Seckl JR (1998) Distinct Ontogeny of Glucocorticoid and Mineralocorticoid Receptor and 11β-Hydroxysteroid Dehydrogenase Types I and II mRNAs in the Fetal Rat Brain Suggest a Complex Control of Glucocorticoid Actions. J Neurosci 18: 2570-2580. PubMed: 9502816.
57. Tijsseling D, Wijnberger LDE, Derks JB, van Velthoven CTJ, de Vries WB et al. (2012) Effects of Antenatal Glucocorticoid Therapy on Hippocampal Histology of Preterm Infants. PLOS ONE 7: e33369. doi:10.1371/journal.pone.0033369. PubMed: 22457757.
58. Scheepens A, van de Waarenburg M, van den Hove D, Blanco CE (2003) A Single Course of Prenatal Betamethasone in the Rat Alters Postnatal Brain Cell Proliferation but not. Apoptosis - J Physiol 552: 163-175. (Pubitemid 37265475)
59. Antonow-Schlorke I, Schwab M, Li C, Nathanielsz PW (2003) Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetal baboon brain. J Physiol 547: 117-123. doi:10.1113/jphysiol.2002.025700. PubMed: 12562943. (Pubitemid 36285167)
60. Uno H, Lohmiller L, Thieme C, Kemnitz JW, Engle MJ et al. (1990) Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus - Brain Res Dev Brain Res 53: 157-167. doi:10.1016/0165-3806(90) 90002-G. (Pubitemid 20161857)
61. Noorlander CW, Visser GHA, Ramakers GMJ, Nikkels PGJ, de Graan PNE (2008) Prenatal corticosteroid exposure affects hippocampal plasticity and reduces lifespan. Dev Neurobiol 68: 237-246. doi:10.1002/dneu.20583. PubMed: 18000831. (Pubitemid 351199420)
62. Plessen KJ, Bansal R, Zhu H, Whiteman R, Amat J et al. (2006) Hippocampus and amygdala morphology in attention-deficit/ hyperactivity disorder. Arch Gen Psychiatry 63: 795-807. doi:10.1001/archpsyc.63.7.795. PubMed: 16818869.
63. Davis EP, Sandman CA, Buss C, Wing DA, Head K (2013) Fetal Glucocorticoid Exposure Is Associated with Preadolescent. Brain Development - Biol Psychiatry. doi:10.1016/j.biopsych.2013.03.009.
64. Alexander N, Rosenlöcher F, Stalder T, Linke J, Distler W et al. (2012) Impact of Antenatal Synthetic Glucocorticoid Exposure on Endocrine Stress Reactivity in Term-Born. Children - J Clin Endocrinol Metab 97: 3538-3544. doi:10.1210/jc.2012-1970.
65. Aarnoudse-Moens CSH, Weisglas-Kuperus N, van Goudoever JB, Oosterlaan J (2009) Meta-Analysis of Neurobehavioral Outcomes in Very Preterm and/or Very Low Birth Weight Children. Pediatrics 124: 717-728. doi:10.1542/peds.2008-2816. PubMed: 19651588.
66. Lindström K, Lindblad F, Hjern A (2011) Preterm Birth and Attention-Deficit/Hyperactivity Disorder in Schoolchildren. Pediatrics 127: 858-865. doi:10.1542/peds.2010-3769. PubMed: 21502231.
67. Rodriguez A (2010) Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children. J Child Psychol Psychiatry 51: 134-143. doi:10.1111/j.1469-7610.2009.02133.x. PubMed: 19674195.