Early maternal alcohol consumption alters hippocampal DNA methylation, gene expression and volume in a mouse model

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Marjonen, Heidi ^a   Sierra, Alejandra ^b   Nyman, Anna ^a   Rogojin, Vladimir ^a   Gröhn, Olli ^b   Linden, Anni Maija ^c   Hautaniemi, Sampsa ^a   Kaminen Ahola, Nina ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; GENOMIC DNA; MICRORNA; HISTONE; OLFACTORY RECEPTOR; PRE-B LYMPHOCYTE GENE 2 PROTEIN, MOUSE; SURROGATE IMMUNOGLOBULIN LIGHT CHAIN;

ADOLESCENT; ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRAIN ASYMMETRY; BRAIN DISEASE; BRAIN FUNCTION; BRAIN SIZE; CONTROLLED STUDY; CPG ISLAND; DEVELOPMENTAL STAGE; DNA METHYLATION; EMBRYO; EMBRYOTOXICITY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPIGENETICS; FEMALE; GENE CONTROL; GENE EXPRESSION; GENETIC ANALYSIS; GESTATION PERIOD; HIPPOCAMPUS; MALE; MOLECULAR MECHANICS; MOUSE; NEURULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR REPROGRAMMING; OLFACTORY BULB; OLFACTORY EPITHELIUM; PROGENY; UPREGULATION; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRINKING BEHAVIOR; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GENOME; HUMAN; METABOLISM; OLFACTORY RECEPTOR; PATHOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ALCOHOL DRINKING; ANIMALS; BONE MARROW; CPG ISLANDS; DISEASE MODELS, ANIMAL; DNA METHYLATION; EPIGENESIS, GENETIC; ETHANOL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HIPPOCAMPUS; HISTONES; HUMANS; IMMUNOGLOBULIN LIGHT CHAINS, SURROGATE; MICE; MICE, INBRED C57BL; MICRORNAS; NEURULATION; OLFACTORY BULB; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, ODORANT;

EID: 84929376807     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124931     Document Type: Article

References (90)

1. Abel EL, Hannigan JH. Maternal risk factors in fetal alcohol syndrome: provocative and permissive influences. Neurotoxicol Teratol 17: 445-462. Review. Erratum in: Neurotoxicol Teratol. 1995; 17: 689. PMID: 7565491
2. Sokol RJ, Delaney-Black V, Nordstrom B. Fetal alcohol spectrum disorder. Jama. 2003; 290: 2996-2999. PMID: 14665662
3. Maier SE, West JR. Drinking patterns and alcohol-related birth defects. Alcohol Res Health. 2001; 25: 168-174. PMID: 11810954
4. Sulik KK. Critical periods for alcohol teratogenesis in mice, with special reference to the gastrulation stage of embryogenesis. Ciba found Symp. 1984; 105: 124-141. PMID: 6563984
5. Guerri C. Mechanisms involved in central nervous system dysfunctions induced by prenatal ethanol exposure. Neurotox. 2002; Res 4: 327-335. PMID: 12829422
6. Sulik KK. Genesis of alcohol-induced craniofacial dysmorphism. Exp Biol Med (Maywood). 2005; 230: 366-375. PMID: 15956766
7. Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet. 2012; 13: 97-109. doi: 10.1038/nrg3142 PMID: 22215131
8. Liu Y, Balaraman Y, Wang G, Nephew KP, Zhou FC. Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation. Epigenetics. 2009; 4: 500-511. PMID: 20009564
9. Kaminen-Ahola N, Ahola A, Maga M, Mallitt KA, Fahey P, Cox TC, et al. Maternal ethanol consumption alters the epigenotype and the phenotype of offspring in a mouse model. PLoS Genet 2010; 6: e1000811. doi: 10.1371/journal.pgen.1000811 PMID: 20084100
10. Zhou FC, Balaraman Y, Teng M, Liu Y, Singh RP, Nephew KP. Alcohol alters DNA methylation patterns and inhibits neural stem cell differentiation. Alcohol Clin Exp Res. 2011; 35: 735-746. doi: 10.1111/j.1530-0277.2010.01391.x PMID: 21223309
11. Laufer BI, Mantha K, Kleiber ML, Diehl EJ, Addison SM, Singh SM. Long-lasting alterations to DNA methylation and ncRNAs could underlie the effects of fetal alcohol exposure in mice. Dis Model Mech. 2013; 6: 977-992. doi: 10.1242/dmm.010975 PMID: 23580197
12. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001; 293: 1089-1093. PMID: 11498579
13. Hemberger M, Dean W, Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging waddington's canal. Nat Rev Mol Cell Biol. 2009; 10: 526-537. doi: 10.1038/nrm2727 PMID: 19603040
14. Morgan HD, Jin XL, Li A, Whitelaw E, O'Neill C. The culture of zygotes to the blastocyst stage changes the postnatal expression of an epigentically labile allele, agouti viable yellow, in mice. Biol Reprod. 2008; 79: 618-623. doi: 10.1095/biolreprod.108.068213 PMID: 18562706
15. Rivera RM, Stein P, Weaver JR, Mager J, Schultz RM, Bartolomei MS. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet. 2008; 17: 1-14. PMID: 17901045
16. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008; 105: 17046-17049. doi: 10.1073/pnas.0806560105 PMID: 18955703
17. Tobi EW, Slagboom PE, van Dongen J, Kremer D, Stein AD, Putter H, et al. Prenatal famine and genetic variation are independently and additively associated with DNA methylation at regulatory loci within IGF2/H19. PLoS One. 2012; 7: e37933. doi: 10.1371/journal.pone.0037933 PMID: 22666415
18. Susiarjo M, Sasson I, Mesaros C, Bartolomei MS (2013) Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet 9: e1003401. doi: 10.1371/journal.pgen.1003401 PMID: 23593014
19. Kaminen-Ahola N, Ahola A, Flatscher-Bader T, Wilkins SJ, Anderson GJ, Whitelaw E, et al. (2010) Postnatal growth restriction and gene expression changes in a mouse model of fetal alcohol syndrome. Birth Defects Res A Clin Mol Teratol 88: 818-826. doi: 10.1002/bdra.20729 PMID: 20878912
20. Sanchez Vega MC, Chong S, Burne TH. Early gestational exposure to moderate concentrations of ethanol alters adult behaviour in C57BL/6J mice. Behav Brain Res. 2013; 252: 326-333. doi: 10.1016/j.bbr.2013.06.003 PMID: 23756143
21. McClearn G, Rodgers D. Differences in alcohol preference among inbred strains of mice. Q J Stud Alcohol. 1959; 20: 691-695.
22. Belknap JK, Crabbe JC, Young ER. Voluntary consumption of ethanol in 15 inbred mouse strains. Psychopharmacology (Berl). 1993; 112: 503-510. PMID: 7871064
23. Barnes DE, Walker DW. Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Brain Res. 1981; 227: 333-340. PMID: 7260643
24. Diaz Perez H, Espinosa Villanueva J, Machado Salas J. Behavioral and hippocampal morphological changes induced by ethanol administered to pregnant rats. Ann N Y Acad Sci. 1991; 625: 300-4. PMID: 2058890
25. Miller MW. Generation of neurons in the rat dentate gyrus and hippocampus: effects of prenatal and postnatal treatment with ethanol. Alcohol Clin Exp Res. 1995; 19: 1500-9. PMID: 8749817
26. Choi IY 1, Allan AM, Cunningham LA. Moderate fetal alcohol exposure impairs the neurogenic response to an enriched environment in adult mice. Alcohol Clin Exp Res. 2005; 29: 2053-62. PMID: 16340464
27. Gil-Mohapel J, Titterness AK, Patten AR, Taylor S, Ratzlaff A, Ratzlaff T, et al. Prenatal ethanol exposure differentially affects hippocampal neurogenesis in the adolescent and aged brain. Neuroscience. 2014; 273: 174-88. doi: 10.1016/j.neuroscience.2014.05.012 PMID: 24846617
28. West JR, Hodges CA, Black AC Jr. Prenatal exposure to ethanol alters the organization of hippocampal mossy fibers in rats. Science. 1981; 211: 957-9. PMID: 7466371
29. Abel EL, Jacobson S, Sherwin BT. In utero alcohol exposure: functional and structural brain damage. Neurobehav Toxicol Teratol. 1983; 5: 363-6. PMID: 6877477
30. Allan AM, Chynoweth J, Tyler LA, Caldwell KK. A mouse model of prenatal ethanol exposure using a voluntary drinking paradigm. 2003; Alcohol Clin Exp Res 27: 2009-16. PMID: 14691390
31. WHO (World Health Organization) World Health Report 2002: Reducing Risks, Promoting Healthy Life, World Health Organization, Geneva. PMID: 14741909
32. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet. 2001; 29: 365-371. PMID: 11726920
33. Dalma-Weiszhausz DD, Warrington J, Tanimoto EY, Miyada CG. The affymetrix GeneChip platform: an overview. In DNA Microarrays, Part A: Array Platforms and Wet-Bench Protocols, Methods in Enzymology (ed. Kimmel A. and Oliver B.),2006; 410 pp. 3-28. San Diego: Elsevier Academic Press. PMID: 16938544
34. Chen P, Lepikhova T, Hu Y, Monni O, Hautaniemi S. Comprehensive exon array data processing method for quantitative analysis of alternative spliced variants. Nucleic Acids Res. 2011; 39: 123.
35. Ovaska K, Laakso M, Haapa-Paananen S, Louhimo R, Chen P, Aittomäki V, et al. Large-scale data integration framework provides a comprehensive view on glioblastoma multiforme. Genome Med. 2010; 2: 65. doi: 10.1186/gm186 PMID: 20822536
36. Carnahan MN, Veazey KJ, Muller D, Tingling JD, Miranda RC, Golding MC. Identification of cell-specific patterns of reference gene stability in quantitative reverse-transcriptase polymerase chain reaction studies of embryonic, placental and neural stem models of prenatal ethanol exposure. Alcohol. 2013; 47: 109-120. doi: 10.1016/j.alcohol.2012.12.003 PMID: 23317542
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001; 25: 402-408. PMID: 11846609
38. Bock C, Reither S, Mikeska T, Paulsen M, Walter J, Lengauer T. BiQ analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics. 2005; 21: 4067-4068. PMID: 16141249
39. Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal. 2001; 5: 143-156. PMID: 11516708
40. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2001; 17: 825-841.
41. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B. 1996; 111: 209-219. PMID: 8661285
42. Akers KG, Kushner SA, Leslie AT, Clarke L, van der Kooy D, Lerch JP, et al. Fetal alcohol exposure leads to abnormal olfactory bulb development and impaired odor discrimination in adult mice. Mol Brain. 2011; 4: 29. doi: 10.1186/1756-6606-4-29 PMID: 21736737
43. Houbaviy HB, Murray MF, Sharp PA. Embryonic stem cell-specific MicroRNAs. Dev Cell. 2003; 5: 351-358. PMID: 12919684
44. Tata PR, Tata NR, Kuhl M, Sirbu IO. Identification of a novel epigenetic regulatory region within the pluripotency associated microRNA cluster, EEmiRC. Nucleic Acids Res. 2011; 39: 3574-3581. doi: 10.1093/nar/gkq1344 PMID: 21247880
45. Siegel G, Obernosterer G, Fiore R, Oehmen M, Bicker S, Christensen M, et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat Cell Biol. 2009; 11: 705-716. doi: 10.1038/ncb1876 PMID: 19465924
46. Ishii T, Hirota J, Mombaerts P. Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr Biol. 2003; 13: 394-400. PMID: 12620187
47. Loconto J, Papes F, Chang E, Stowers L, Jones EP, Takada T, et al. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class ib molecules. Cell. 2003; 112: 607-618. PMID: 12628182
48. Leinders-Zufall T, Ishii T, Chamero P, Hendrix P, Oboti L, Schmid A, et al. A family of nonclassical class I MHC genes contributes to ultrasensitive chemodetection by mouse vomeronasal sensory neurons. J Neurosci. 2014; 34: 5121-5133. doi: 10.1523/JNEUROSCI.0186-14.2014 PMID: 24719092
49. Parnell SE, O'Leary-Moore SK, Godin EA, Dehart DB, Johnson BW, Allan Johnson G, et al. Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: effects of acute insult on gestational day 8. Alcohol Clin Exp Res. 2009; 33: 1001-1011. doi: 10.1111/j.1530-0277.2009.00921.x PMID: 19302087
50. Godin EA, O'Leary-Moore SK, Khan AA, Parnell SE, Ament JJ, Dehart DB, et al. Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: effects of acute insult on gestational day 7. Alcohol Clin Exp Res. 2010; 34: 98-111. doi: 10.1111/j.1530-0277.2009.01071.x PMID: 19860813
51. Parnell SE, Holloway HE, Baker LK, Styner MA, Sulik KK. Dysmorphogenic effects of first trimester-equivalent ethanol exposure in mice: a magnetic resonance microscopy-based study. Alcohol Clin Exp Res. 2014; 38: 2008-2014. doi: 10.1111/acer.12464 PMID: 24931007
52. Kleiber ML, Laufer BI, Wright E, Diehl EJ, Singh SM. Long-term alterations to the brain transcriptome in a maternal voluntary consumption model of fetal alcohol spectrum disorders. Brain Res. 2012; 1458: 18-33. doi: 10.1016/j.brainres.2012.04.016 PMID: 22560501
53. Zhou FC, Zhao Q, Liu Y, Goodlett CR, Liang T, McClintick JN, et al. Alteration of gene expression by alcohol exposure at early neurulation. BMC Genomics. 2011; 12: 124. doi: 10.1186/1471-2164-12-124 PMID: 21338521
54. Magklara A, Yen A, Colquitt BM, Clowney EJ, Allen W, Markenscoff-Papadimitriou E, et al. An epigenetic signature for monoallelic olfactory receptor expression. Cell. 2011; 145: 555-570. doi: 10.1016/j.cell.2011.03.040 PMID: 21529909
55. Kang N, Koo J. Olfactory receptors in non-chemosensory tissues. BMB Rep. 2012; 45: 612-622. PMID: 23186999
56. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science. 2003; 302: 890-893. PMID: 14593184
57. Jones B, Chen J. Inhibition of IFN-gamma transcription by site-specific methylation during T helper cell development. EMBO J. 2006; 25: 2443-2452. PMID: 16724115
58. Mundt C, Licence S, Maxwell G, Melchers F, Martensson IL. Only VpreB1, but not VpreB2, is expressed at levels which allow normal development of B cells. Int Immunol. 2006; 18: 163-172. PMID: 16361315
59. Rauch TA, Wu X, Zhong X, Riggs AD, Pfeifer GP. A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci U S A. 2009; 106: 671-678. doi: 10.1073/pnas.0812399106 PMID: 19139413
60. Aran D, Toperoff G, Rosenberg M, Hellman A. Replication timing-related and gene body-specific methylation of active human genes. Hum Mol Genet. 2011; 20: 670-680. doi: 10.1093/hmg/ddq513 PMID: 21112978
61. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in purkinje neurons and the brain. Science. 2009; 324: 929-930. doi: 10.1126/science.1169786 PMID: 19372393
62. Ruzov A, Tsenkina Y, Serio A, Dudnakova T, Fletcher J, Bai Y, et al. Lineage-specific distribution of high levels of genomic 5-hydroxymethylcytosine in mammalian development. Cell Res. 2011; 21: 1332-1342. doi: 10.1038/cr.2011.113 PMID: 21747414
63. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009; 324: 930-935. doi: 10.1126/science.1170116 PMID: 19372391
64. Guo JU, Su Y, Zhong C, Ming GL, Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell. 2011; 145: 423-434. doi: 10.1016/j.cell.2011.03.022 PMID: 21496894
65. Hanson KL, Medina KL, Nagel BJ, Spadoni AD, Gorlick A, Tapert SF. Hippocampal volumes in adolescents with and without a family history of alcoholism. Am J Drug Alcohol Abuse. 2010; 36: 161-167. doi: 10.3109/00952991003736397 PMID: 20465374
66. Nagel BJ, Schweinsburg AD, Phan V, Tapert SF. Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Res. 2005; 139: 181-190. PMID: 16054344
67. Clayton NS, Krebs JR. Hippocampal growth and attrition in birds affected by experience. Proc Natl Acad Sci U S A. 1994; 91: 7410-7414. PMID: 8052598
68. Biegler R, McGregor A, Krebs JR, Healy SD. A larger hippocampus is associated with longer-lasting spatial memory. Proc Natl Acad Sci U S A. 2001; 98: 6941-6944. PMID: 11391008
69. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A. 2000; 97: 4398-4403. PMID: 10716738
70. Sparks BF, Friedman SD, Shaw DW, Aylward EH, Echelard D, Artru AA, et al. Brain structural abnormalities in young children with autism spectrum disorder. Neurology. 2002; 59: 184-192. PMID: 12136055
71. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Reiss AL, et al. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci. 2004; 24: 6392-6401. PMID: 15254095
72. Edalatmanesh MA, Nikfarjam H, Vafaee F, Moghadas M. Increased hippocampal cell density and enhanced spatial memory in the valproic acid rat model of autism. Brain Res. 2013; 1526: 15-25. doi: 10.1016/j.brainres.2013.06.024 PMID: 23806776
73. Blanchard BA, Riley EP, Hannigan JH. Deficits on a spatial navigation task following prenatal exposure to ethanol. Neurotoxicol Teratol. 1987; 9:253-258. PMID: 3627089
74. Gianoulakis C. Rats exposed prenatally to alcohol exhibit impairment in spatial navigation test. Behav Brain Res. 1990; 36:217-228. PMID: 2310487
75. Richardson DP, Byrnes ML, Brien JF, Reynolds JN, Dringenberg HC. Impaired acquisition in the water maze and hippocampal long-term potentiation after chronic prenatal ethanol exposure in the guineapig. Eur J Neurosci. 2002; 16:1593-1598. PMID: 12405973
76. Christie BR, Swann SE, Fox CJ, Froc D, Lieblich SE, Redila V, et al. Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. Eur J Neurosci. 2005; 21: 1719-1726. PMID: 15845099
77. Osborne GL, Caul WF, Fernandez K. Behavioral effects of prenatal ethanol exposure and differential early experience in rats. Pharmacol Biochem Behav. 1980; 12: 393-401. PMID: 7393938
78. Vorhees CV, Fernandez K. Effects of short-term prenatal alcohol exposure on maze, activity, and olfactory orientation performance in rats. Neurobehav Toxicol Teratol. 1986; 8:23-28. PMID: 3703092
79. Clausing P, Ferguson SA, Holson RR, Allen RR, Paule MG. Prenatal ethanol exposure in rats: long-lasting effects on learning. Neurotoxicol Teratol. 1995; 17: 545-552. PMID: 8552000
80. Cullen CL, Burne TH, Lavidis NA, Moritz KM. Low dose prenatal alcohol exposure does not impair spatial learning and memory in two tests in adult and aged rats. PLoS One. 2014; 9: e101482. doi: 10.1371/journal.pone.0101482 PMID: 24978807
81. Sadrian B, Lopez-Guzman M, Wilson DA, Saito M. Distinct neurobehavioral dysfunction based on the timing of developmental binge-like alcohol exposure. Neuroscience. 2014; 280: 204-219. doi: 10. 1016/j.neuroscience.2014.09.008 PMID: 25241068
82. Mattson SN, Riley EP, Jernigan TL, Garcia A, Kaneko WM, Ehlers CL, et al. A decrease in the size of the basal ganglia following prenatal alcohol exposure: a preliminary report. Neurotoxicol Teratol. 1994; 16: 283-289. PMID: 7935262
83. Zhou FC, Sari Y, Powrozek T, Goodlett CR, Li TK. Moderate alcohol exposure compromises neural tube midline development in prenatal brain. Brain Res Dev Brain Res. 2003; 144: 43-55. PMID: 12888216
84. Sakata-Haga H, Sawada K, Ohnishi T, Fukui Y. Hydrocephalus following prenatal exposure to ethanol. Acta Neuropathol. 2004; 108: 393-398. PMID: 15365720
85. O'Leary-Moore SK, Parnell SE, Godin EA, Dehart DB, Ament JJ, Khan AA, et al. Magnetic resonance microscopy-based analyses of the brains of normal and ethanol-exposed fetal mice. Birth Defects Res A Clin Mol Teratol. 2010; 88:953-964. doi: 10.1002/bdra.20719 PMID: 20842647
86. Johnson VP, Swayze VW II, Sato Y, Andreasen NC. Fetal alcohol syndrome: craniofacial and central nervous system manifestations. Am J Med Genet. 1996; 61: 329-339. PMID: 8834044
87. Swayze VW 2nd, Johnson VP, Hanson JW, Piven J, Sato Y, Gledd JN, et al. Magnetic resonance imaging of brain anomalies in fetal alcohol syndrome. Pediatrics. 1997; 99: 232-240. PMID: 9024452
88. Klingenberg CP, Wetherill L, Rogers J, Moore E, Ward R, Autti-Rämö I, et al. Prenatal Alcohol Exposure Alters the Patterns of Facial Asymmetry. Alcohol. 2010; 44: 649-657. doi: 10.1016/j.alcohol.2009.10.016 PMID: 20060678
89. Riikonen R, Salonen I, Partanen K and Verho S. Brain perfusion SPECT and MRI in foetal alcohol syndrome. Dev Med Child Neurol. 1999; 41: 652-659. PMID: 10587040
90. Sowell ER, Thompson PM, Peterson BS, Mattson SN, Welcome SE, Henkenius AL, et al. Mapping cortical gray matter asymmetry patterns in adolescents with heavy prenatal alcohol exposure. Neuroimage. 2002; 17: 1807-1819. PMID: 12498754