An examination of sex differences in the effects of early-life opiate and alcohol exposure

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 371, Issue 1688, 2016, Pages

  Terasaki, Laurne S ^a   Gomez, Julie ^a   Schwarz, Jaclyn M ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Alcohol; Opiates; Placenta; Postnatal; Prenatal; Stress

Indexed keywords

ALCOHOL; CHILD HEALTH; DRUG; LEARNING; RESEARCH METHOD; RODENT; SEX-RELATED DIFFERENCE;

ANIMALIA; RODENTIA;

NARCOTIC AGENT;

ADVERSE EFFECTS; ALCOHOLISM; DRINKING BEHAVIOR; FEMALE; HUMAN; MALE; NEWBORN; PATHOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ALCOHOL DRINKING; ALCOHOL-INDUCED DISORDERS; FEMALE; HUMANS; INFANT, NEWBORN; MALE; NARCOTICS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84956624275     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2015.0123     Document Type: Review

References (103)

1. Burt DR, Creese I, Snyder SH. 1977 Antischizophrenic drugs: chronic treatment elevates dopamine receptor binding in brain. Science 196, 326-328. (doi:10.1126/science.847477)
2. Rosengarten H, Friedhoff AJ. 1979 Enduring changes in dopamine receptor cells of pups from drug administration to pregnant and nursing rats. Science 203, 1133-1135. (doi:10.1126/science.570724)
3. Spear LP, Scalzo FM. 1986 Behavioral, psychopharmacological, and neurochemical effects of chronic neuroleptic treatment during development. In Handbook of behavioral teratology (eds EP Riley, CV Vorhees), p 173. New York, NY: Plenum Press.
4. Joya X et al. 2012 Determination of maternal-fetal biomarkers of prenatal exposure to ethanol: a review. J. Pharm. Biomed. Anal. 69, 209-222. (doi:10.1016/j.jpba.2012.01.006)
5. Burd L, Roberts D, Olson M, Odendaal H. 2007 Ethanol and the placenta: a review. J. Matern. Fetal Neonatal. Med. 20, 361-375. (doi:10.1080/14767050701298365)
6. Ganapathy VV, Prasad PD, Ganapathy ME, Leibach FH. 1999 Drugs of abuse and placental transport. Adv. Drug Deliv. Rev. 38, 99-110. (doi:10.1016/S0169-409X(99)00009-5)
7. Malek A, Obrist C, Wenzinger S, von Mandach U. 2009 The impact of cocaine and heroin on the placental transfer of methadone. Reprod. Biol. Endocrinol. 7, 61. (doi:10.1186/1477-7827-7-61)
8. Paakki P et al. 2000 Maternal drug abuse and human term placental xenobiotic and steroid metabolizing enzymes in vitro. Environ. Health Perspect. 108, 141-145. (doi:10.1289/ehp.00108141)
9. Weaver ICG. 2009 Shaping adult phenotypes through early life environments. Birth Defects Res. C Embryo Today 87, 314-326. (doi:10.1002/bdrc.20164)
10. Wang X, Ho W. 2011 Drugs of abuse and HIV infection/replication: implications for mother–fetus transmission. Life Sci. 88, 972-979. (doi:10.1016/j.lfs.2010.10.029)
11. Seelig LLJr, Steven WM, Stewart GL. 1996 Effects of maternal ethanol consumption on the subsequent development of immunity to Trichinella spiralis in rat neonates. Alcohol Clin. Exp. Res. 20, 514-522. (doi:10.1111/j.1530-0277.1996.tb01085.x)
12. Ahluwalia B, Wesley B, Adeyiga O, Smith DM, Da-Silva A, Rajguru S. 2000 Alcohol modulates cytokine secretion and synthesis in human fetus: an in vivo and in vitro study. Alcohol 21, 207-213. (doi:10.1016/S0741-8329(00)00076-8)
13. Li Y et al. 2003 Morphine enhances HIV infection of neonatal macrophages. Pediatr. Res. 54, 282-288. (doi:10.1203/01.PDR.0000074973.83826.4C)
14. Sedlmeier EM, Brunner S, Much D, Pagel P, Ulbrich SE, Meyer HH, Amann-Gassner U, Hauner H, Bader BL. 2014 Human placental transcriptome shows sexually dimorphic gene expression and responsiveness to maternal dietary n-3 long-chain polyunsaturated fatty acid intervention during pregnancy. BMC Genomics 15, 941. (doi:10.1186/1471-2164-15-941)
15. O’Connell BA, Moritz KM, Walker DW, Dickinson H. 2013 Sexually dimorphic placental development throughout gestation in the spiny mouse (Acomys cahirinus). Placenta 34, 119-126. (doi:10.1016/j.placenta.2012.11.009)
16. O’Connell BA, Moritz KM, Roberts CT, Walker DW, Dickinson H. 2011 The placental response to excess maternal glucocorticoid exposure differs between the male and female conceptus in spiny mice. Biol. Reprod. 85, 1040-1047. (doi:10.1095/biolreprod.111.093369)
17. Osei-Kumah A, Smith R, Jurisica I, Caniggia I, Clifton VL. 2011 Sex-specific differences in placental global gene expression in pregnancies complicated by asthma. Placenta 32, 570-578. (doi:10.1016/j.placenta.2011.05.005)
18. Dobbing J, Sands J. 1979 Comparative aspects of the brain growth spurt. Early Hum. Dev. 3, 79-83. (doi:10.1016/0378-3782(79)90022-7)
19. Amateau SK, Alt JJ, Stamps CL, McCarthy MM. 2004 Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 145, 2906-2917. (doi:10.1210/en.2003-1363)
20. McCarthy MM, Arnold AP. 2011 Reframing sexual differentiation of the brain. Nat. Neurosci. 14, 677-683. (doi:10.1038/nn.2834)
21. McCarthy MM, Wright CL, Schwarz JM. 2009 New tricks by an old dogma: mechanisms of the organizational/activational hypothesis of steroid- mediated sexual differentiation of brain and behavior. Horm. Behav. 55, 655-665. (doi:10.1016/j.yhbeh.2009.02.012)
22. Penaloza C et al. 2009 Sex of the cell dictates its response: differential gene expression and sensitivity to cell death inducing stress in male and female cells. FASEB J. 23, 1869-1879. (doi:10.1096/fj.08-119388)
23. Arnold AP, Chen X, Itoh Y. 2012 What a difference an X or Y makes: sex chromosomes, gene dose, and epigenetics in sexual differentiation. Handb. Exp. Pharmacol. 214, 67-88. (doi:10.1007/978-3-642-30726-3_4)
24. Arnold AP, Lusis AJ. 2012 Understanding the sexome: measuring and reporting sex differences in gene systems. Endocrinology 153, 2551-2555. (doi:10.1210/en.2011-2134)
25. Becker JB, Hu M. 2008 Sex differences in drug abuse. Front. Neuroendocrinol. 29, 36-47. (doi:10.1016/j.yfrne.2007.07.003)
26. Becker JB, Molenda H, Hummer DL. 2001 Gender differences in the behavioral responses to cocaine and amphetamine. Implications for mechanisms mediating gender differences in drug abuse. Ann. NY Acad. Sci. 937, 172-187. (doi:10.1111/j.1749-6632.2001.tb03564.x)
27. Graziani M, Nencini P, Nistico R. 2014 Genders and the concurrent use of cocaine and alcohol: pharmacological aspects. Pharmacol. Res. 87, 60-70. (doi:10.1016/j.phrs.2014.06.009)
28. Sharrett-Field L, Butler TR, Reynolds AR, Berry JN, Prendergast MA. 2013 Sex differences in neuroadaptation to alcohol and withdrawal neurotoxicity. Pflugers Arch. 465, 643-654. (doi:10.1007/s00424-013-1266-4)
29. Hernandez-Avila CA, Rounsaville BJ, Kranzler HR. 2004 Opioid-cannabis-and alcohol-dependent women show more rapid progression to substance abuse treatment. Drug Alcohol Depend. 74, 265-272. (doi:10.1016/j.drugalcdep.2004.02.001)
30. Cicero TJ, Nock B, Meyer ER. 1996 Gender-related differences in the antinociceptive properties of morphine. J. Pharmacol. Exp. Ther. 279, 767-773.
31. Bodnar RJ, Kest B. 2010 Sex differences in opioid analgesia, hyperalgesia, tolerance and withdrawal: central mechanisms of action and roles of gonadal 7 hormones. Horm. Behav. 58, 72-81. (doi:10.1016/j.yhbeh.2009.09.012)
32. United Nations Office on Drugs and Crime. 2012 World Drug Report. Vienna, Austria: UNDOC.
33. Cai R, Crane E, Poneleit K, Paulozzi L. 2010 Emergency department visits involving nonmedical use of selected prescription drugs in the United States, 2004-2008. J. Pain Palliat. Care Pharmacother. 24, 293-297. (doi:10.3109/15360288.2010.503730)
34. Hedegaard H, Chen LH, Warner M. 2015 Drug-poisoning deaths involving heroin: United States, 2000-2013. NCHS Data Brief 190, 8.
35. Fodor A, Timar J, Zelena D. 2014 Behavioral effects of perinatal opioid exposure. Life Sci. 104, 1-8. (doi:10.1016/j.lfs.2014.04.006)
36. Kunko PM, Smith JA, Wallace MJ, Maher JR, Saady JJ, Robinson SE. 1996 Perinatal methadone exposure produces physical dependence and altered behavioral development in the rat. J. Pharmacol. Exp. Ther. 277, 1344-1351.
37. Enters EK, Guo HZ, Pandey U, Ko DJ, Robinson SE. 1991 The effect of prenatal methadone exposure on development and nociception during the early postnatal period of the rat. Neurotoxicol. Teratol. 13, 161-166. (doi:10.1016/0892-0362(91)90006-I)
38. Enters EK, Guo HZ, Pandey U, Ko DJ, Robinson SE. 1990 The effect of prenatal methadone exposure of development and nociception during the early postnatal period of the rat. NIDA Res. Monogr. 105, 376-377.
39. Klausz B, Pinter O, Sobor M, Gyarmati Z, Furst Z, Timar J, Zelena D. 2011 Changes in adaptability following perinatal morphine exposure in juvenile and adult rats. Eur. J. Pharmacol. 654, 166-172. (doi:10.1016/j.ejphar.2010.11.025)
40. Wilson GS, McCreary R, Kean J, Baxter JC. 1979 The development of preschool children of heroin-addicted mothers: a controlled study. Pediatrics 63, 135-141. (doi:10.1016/S0022-3476(79)80107-9)
41. Mattson SN, Schoenfeld AM, Riley EP. 2001 Teratogenic effects of alcohol on brain and behavior. Alcohol Res. Health 25, 185-191.
42. Lu R, Liu X, Long H, Ma L. 2012 Effects of prenatal cocaine and heroin exposure on neuronal dendrite morphogenesis and spatial recognition memory in mice. Neurosci. Lett. 522, 128-133. (doi:10.1016/j.neulet.2012.06.023)
43. Slamberova R, Schindler CJ, Pometlova M, Urkuti C, Purow-Sokol JA, Vathy I. 2001 Prenatal morphine exposure differentially alters learning and memory in male and female rats. Physiol. Behav. 731, 93-103. (doi:10.1016/S0031-9384(01)00469-3)
44. Nasiraei-Moghadam S, Sherafat MA, Safari MS, Moradi F, Ahmadiani A, Dargahi L. 2013 Reversal of prenatal morphine exposure-induced memory deficit in male but not female rats. J. Mol. Neurosci. 50, 58-69. (doi:10.1007/s12031-012-9860-z)
45. Hamilton KL, Harris AC, Gewirtz JC, Sparber SB, Schrott LM. 2005 HPA axis dysregulation following prenatal opiate exposure and postnatal withdrawal. Neurotoxicol. Teratol. 27, 95-103. (doi:10.1016/j.ntt.2004.09.004)
46. Ornoy A, Segal J, Bar-Hamburger R, Greenbaum C. 2001 Developmental outcome of school-age children born to mothers with heroin dependency: importance of environmental factors. Dev. Med. Child Neurol. 43, 668-675. (doi:10.1017/S0012162201001219)
47. de Cubas MM, Field T. 1993 Children of methadone- dependent women: developmental outcomes. Am. J. Orthopsychiatry 63, 266-276. (doi:10.1037/ h0079429)
48. Pulsifer MB, Butz AM, O’Reilly Foran M, Belcher HM. 2008 Prenatal drug exposure: effects on cognitive functioning at 5 years of age. Clin. Pediatr. 47, 58-65. (doi:10.1177/0009922807305872)
49. Baldacchino A, Arbuckle K, Petrie DJ, McCowan C. 2014 Neurobehavioral consequences of chronic intrauterine opioid exposure in infants and preschool children: a systematic review and meta-analysis. BMC Psychiatry 14, 104-244. (doi:10.1186/1471-244X-14-104)
50. Nishinaka T, Kinoshita M, Nakamoto K, Tokuyama S. 2015 Sex differences in depression-like behavior after nerve injury are associated with differential changes in brain-derived neurotrophic factor levels in mice subjected to early life stress. Neurosci. Lett. 592, 32-36. (doi:10.1016/j.neulet.2015.02.053)
51. Elfwing M, Natt D, Goerlich-Jansson VC, Persson M, Hjelm J, Jensen P. 2015 Early stress causes sex- specific, life-long changes in behaviour, levels of gonadal hormones, and gene expression in chickens. PLoS ONE 10, e0125808. (doi:10.1371/journal.pone.0125808)
52. Stormer C. 2011 Sex differences in the consequences of early-life exposure to epidemiological stress-a life-history approach. Am. J. Hum. Biol. 23, 201-208. (doi:10.1002/ajhb.21103)
53. Llorente R, Gallardo ML, Berzal AL, Prada C, Garcia-Segura LM, Viveros MP. 2009 Early maternal deprivation in rats induces gender-dependent effects on developing hippocampal and cerebellar cells. Int. J. Dev. Neurosci. 27, 233-241. (doi:10.1016/j.ijdevneu.2009.01.002)
54. Biglarnia M, Karami M, Hafshejani ZK. 2013 Differences in morphine-induced antinociception in male and female offspring born of morphine exposed mothers. Indian J. Pharmacol. 45, 227-231. (doi:10.4103/0253-7613.111904)
55. Kocherlakota P. 2014 Neonatal abstinence syndrome. Pediatrics 134, e547-e561. (doi:10.1542/peds.2013-3524)
56. Doberczak TM, Kandall SR, Wilets I. 1991 Neonatal opiate abstinence syndrome in term and preterm infants. J. Pediatr. 118, 933-937. (doi:10.1016/S0022-3476(05)82214-0)
57. Strauss ME, Andresko M, Stryker JC, Wardell JN, Dunkel LD. 1974 Methadone maintenance during pregnancy: pregnancy, birth, and neonate characteristics. Am. J. Obstet. Gynecol. 120, 895-900.
58. Coyle MG, Ferguson A, Lagasse L, Oh W, Lester B. 2002 Diluted tincture of opium (DTO) and phenobarbital versus DTO alone for neonatal opiate withdrawal in term infants. J. Pediatr. 140, 561-564. (doi:10.1067/mpd.2002.123099)
59. Unger A, Jagsch R, Bawert A, Winklbaur B, Rohrmeister K, Martin PR, Coyle M, Fischer G. 2011 Are male neonates more vulnerable to neonatal abstinence syndrome than female neonates? Gend. Med. 8, 355-364. (doi:10.1016/j.genm.2011.10.001)
60. Holbrook A, Kaltenbach K. 2010 Gender and NAS: does sex matter? Drug Alcohol Depend. 1121, 156-159. (doi:10.1016/j.drugalcdep.2010.05.015)
61. Behnke M, Smith VC, Committee on Substance Abuse, Committee on Fetus and Newborn 2013 Prenatal substance abuse: short-and long-term effects on the exposed fetus. Pediatrics 131, e1009-e1024. (doi:10.1542/peds.2012-3931)
62. Duhrsen L et al. 2013 Effects of repetitive exposure to pain and morphine treatment on the neonatal rat brain. Neonatology 103, 35-43. (doi:10.1159/000341769)
63. Walker SM. 2014 Overview of neurodevelopment and pain research, possible treatment targets. Best Pract. Res. Clin. Rheumatol. 28, 213-228. (doi:10.1016/j.berh.2014.03.007)
64. Bhutta AT, Rovnaghi C, Simpson PM, Gossett JM, Scalzo FM, Anand KJ. 2001 Interactions of inflammatory pain and morphine in infant rats: long-term behavioral effects. Physiol. Behav. 731, 51-58. (doi:10.1016/S0031-9384(01)00432-2)
65. LaPrairie JL, Murphy AZ. 2007 Female rats are more vulnerable to the long-term consequences of neonatal inflammatory injury. Pain 132(Suppl. 1), S124-S133. (doi:10.1016/j.pain.2007.08.010)
66. Victoria NC, Karom MC, Murphy AZ. 2015 Analgesia for early-life pain prevents deficits in adult anxiety and stress in rats. Dev. Neurosci. 37, 13. (doi:10.1159/000366273)
67. Victoria NC, Karom MC, Eichenbaum H, Murphy AZ. 2014 Neonatal injury rapidly alters markers of pain and stress in rat pups. Dev. Neurobiol. 74, 42-51. (doi:10.1002/dneu.22129)
68. Victoria NC, Inoue K, Young LJ, Murphy AZ. 2013 A single neonatal injury induces life-long deficits in response to stress. Dev. Neurosci. 35, 326-337. (doi:10.1159/000351121)
69. Sampson PD, Streissguth AP, Bookstein FL, Little RE, Clarren SK, Dehaene P, Hanson JW, Graham JM. 1997 Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56, 317-326. (doi:10.1002/(SICI)1096-9926(199711)56:5,317::AID-TERA5.3.0.CO;2-U)
70. US Centers for Disease Control and Prevention. 2015 FASDs Data & Statistics, updated 11-17-2015. See http://www.cdc.gov/ncbddd/fasd/data.html.
71. Weinberg J, Sliwowska JH, Lan N, Hellemans KG. 2008 Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J. Neuroendocrinol. 20, 470-488. (doi:10.1111/j.1365-2826.2008.01669.x)
72. Guerri C, Bazinet A, Riley EP. 2009 Foetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol. 44, 108-114. (doi:10.1093/alcalc/agn105)
73. Hannigan JH, Armant DR. 2000 Alcohol in 8 pregnancy and neonatal outcome. Semin. Neonatol. 5, 243-254. (doi:10.1053/siny.2000.0027)
74. Mattson SN, Riley EP. 1998 A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol. Clin. Exp. Res. 22, 279-294. (doi:10.1111/j.1530-0277.1998.tb03651.x)
75. Thomas SE, Kelly SJ, Mattson SN, Riley EP. 1998 Comparison of social abilities of children with fetal alcohol syndrome to those of children with similar IQ scores and normal controls. Alcohol. Clin. Exp. Res. 22, 528-533. (doi:10.1111/j.1530-0277.1998.tb03684.x)
76. Roebuck TM, Simmons RW, Richardson C, Mattson SN, Riley EP. 1998 Neuromuscular responses to disturbance of balance in children with prenatal exposure to alcohol. Alcohol. Clin. Exp. Res. 22, 1992-1997. (doi:10.1111/j.1530-0277.1998.tb05908.x)
77. Hellemans KG, Sliwowska JH, Verma P, Weinberg J. 2010 Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci. Biobehav. Rev. 34, 791-807. (doi:10.1016/j.neubiorev.2009.06.004)
78. Clarren SK, Smith DW. 1978 The fetal alcohol syndrome. N. Engl. J. Med. 298, 1063-1067. (doi:10.1056/NEJM197805112981906)
79. Landgraf MN, Nothacker M, Kopp IB, Heinen F. 2013 The diagnosis of fetal alcohol syndrome. Dtsch Arztebl Int. 110, 703-710.
80. Thanh NX, Jonsson E, Salmon A, Sebastianski M. 2014 Incidence and prevalence of fetal alcohol spectrum disorder by sex and age group in Alberta, Canada. J. Popul. Ther. Clin. Pharmacol. 21, e395-e404.
81. West JR, Goodlett CR, Bonthius DJ, Pierce DR. 1989 Manipulating peak blood alcohol concentrations in neonatal rats: review of an animal model for alcohol-related developmental effects. Neurotoxicology 10, 347-365.
82. Bonthius DJ, West JR. 1990 Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcohol. Clin. Exp. Res. 14, 107-118. (doi:10.1111/j.1530-0277.1990.tb00455.x)
83. West JR, Goodlett CR, Bonthius DJ, Hamre KM, Marcussen BL. 1990 Cell population depletion associated with fetal alcohol brain damage: mechanisms of BAC-dependent cell loss. Alcohol. Clin. Exp. Res. 14, 813-818. (doi:10.1111/j.1530-0277.1990.tb01820.x)
84. Dikranian K, Qin YQ, Labruyere J, Nemmers B, Olney JW. 2005 Ethanol-induced neuroapoptosis in the developing rodent cerebellum and related brain stem structures. Brain Res. Dev. Brain Res. 22, 13. (doi:10.1016/j.devbrainres.2004.11.005)
85. Klintsova AY, Helfer JL, Calizo LH, Dong WK, Goodlett CR, Greenough WT. 2007 Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcohol. Clin. Exp. Res. 31, 2073-2082. (doi:10.1111/j.1530-0277.2007.00528.x)
86. Olney JW, Wozniak DF, Jevtovic-Todorovic V, Farber NB, Bittigau P, Ikonomidou C. 2002 Drug-induced apoptotic neurodegeneration in the developing brain. Brain Pathol. 12, 488-498. (doi:10.1111/j.1750-3639.2002.tb00467.x)
87. Mooney SM, Napper RM, West JR. 1996 Long-term effect of postnatal alcohol exposure on the number of cells in the neocortex of the rat: a stereological study. Alcohol. Clin. Exp. Res. 20, 615-623. (doi:10.1111/j.1530-0277.1996.tb01663.x)
88. Coleman LGJr, Oguz I, Lee J, Styner M, Crews FT. 2012 Postnatal day 7 ethanol treatment causes persistent reductions in adult mouse brain volume and cortical neurons with sex specific effects on neurogenesis. Alcohol 46, 603-612. (doi:10.1016/j.alcohol.2012.01. 003)
89. Jones KL, Smith DW. 1973 Recognition of the fetal alcohol syndrome in early infancy. Lancet 302, 999-1001. (doi:10.1016/S0140-6736(73)91092-1)
90. Coulter CL, Leech RW, Schaefer GB, Scheithauer BW, Brumback RA. 1993 Midline cerebral dysgenesis, dysfunction of the hypothalamic-pituitary axis, and fetal alcohol effects. Arch. Neurol. 50, 771-775. (doi:10.1001/archneur.1993.00540070083022)
91. Sapolsky RM, Romero LM, Munck AU. 2000 How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55-89. (doi:10.1210/er.21.1.55)
92. Osborn JA, Kim CK, Yu W, Herbert L, Weinberg J. 1996 Fetal ethanol exposure alters pituitary-adrenal sensitivity to dexamethasone suppression. Psychoneuroendocrinology 21, 127-143. (doi:10.1016/0306-4530(95)00037-2)
93. Lee S, Schmidt D, Tilders F, Rivier C. 2000 Increased activity of the hypothalamic-pituitary–adrenal axis of rats exposed to alcohol in utero: role of altered pituitary and hypothalamic function. Mol. Cell Neurosci. 16, 515-528. (doi:10.1006/mcne.2000.0890)
94. Lee S, Schmidt D, Tilders F, Cole M, Smith A, Rivier C. 2000 Prolonged exposure to intermittent alcohol vapors blunts hypothalamic responsiveness to immune and non-immune signals. Alcohol. Clin. Exp. Res. 24, 110-122. (doi:10.1111/j.1530-0277.2000.tb04560.x)
95. Glavas MM, Ellis L, Yu WK, Weinberg J. 2007 Effects of prenatal ethanol exposure on basal limbic-hypothalamic-pituitary-adrenal regulation: role of corticosterone. Alcohol. Clin. Exp. Res. 31, 1598-1610. (doi:10.1111/j.1530-0277.2007.00460.x)
96. Govorko D, Bekdash RA, Zhang C, Sarkar DK. 2012 Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol. Psychiatry 72, 378-388. (doi:10.1016/j.biopsych.2012.04.006)
97. Haley DW, Handmaker NS, Lowe J. 2006 Infant stress reactivity and prenatal alcohol exposure. Alcohol. Clin. Exp. Res. 30, 2055-2064. (doi:10.91111/j.1530-0277.2006.00251.x)
98. Ahlers KE, Karacay B, Fuller L, Bonthius DJ, Dailey ME. 2015 Transient activation of microglia following acute alcohol exposure in developing mouse neocortex is primarily driven by BAX-dependent neurodegeneration. Glia 63, 1694-1713. (doi:10.1002/glia.22835)
99. Wierzba-Bobrowicz T et al. 2003 Dendritic and microglial cells in pups of alcohol-treated female rats. Folia Neuropathol. 41, 131-137.
100. Kelly SJ, Leggett DC, Cronise K. 2009 Sexually dimorphic effects of alcohol exposure during development on the processing of social cues. Alcohol Alcohol. 44, 555-560. (doi:10.1093/alcalc/agp061)
101. Mooney SM, Varlinskaya EI. 2011 Acute prenatal exposure to ethanol and social behavior: effects of age, sex, and timing of exposure. Behav. Brain Res. 216, 358-364. (doi:10.1016/j.bbr.2010.08.014)
102. Sickmann HM, Patten AR, Morch K, Sawchuk S, Zhang C, Parton R, Szlavik L, Christie BR. 2014 Prenatal ethanol exposure has sex-specific effects on hippocampal long-term potentiation. Hippocampus 24, 54-64. (doi:10.1002/hipo.22203)
103. O’Leary-Moore SK, McMechan AP, Mathison SN, Berman RF, Hannigan JH. 2006 Reversal learning after prenatal or early postnatal alcohol exposure in juvenile and adult rats. Alcohol 38, 99-110. (doi:10.1016/j.alcohol.2006.05.005)