Magnetic Resonance-Based Imaging in Animal Models of Fetal Alcohol Spectrum Disorder

O’Leary-Moore, Shonagh K.; Parnell, Scott E.; Lipinski, Robert J.; Sulik, Kathleen K.

doi:10.1007/s11065-011-9164-z

Cited by 77Prenatal Substance Exposure EffectsFetal and Pediatric Neurological DisordersAdvanced MRI Techniques and Applications

Magnetic Resonance-Based Imaging in Animal Models of Fetal Alcohol Spectrum Disorder

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O’Leary-Moore, Shonagh K., Parnell, Scott E., Lipinski, Robert J., Sulik, Kathleen K.·2011·Neuropsychology Review

DOI 10.1007/s11065-011-9164-zPMC PMC3445286

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Abstract

Magnetic resonance imaging (MRI) techniques, such as magnetic resonance microscopy (MRM), diffusion tensor imaging (DTI), and magnetic resonance spectroscopy (MRS), have recently been applied to the study of both normal and abnormal structure and neurochemistry in small animals. Herein, findings from studies in which these methods have been used for the examination of animal models of Fetal Alcohol Spectrum Disorder (FASD) are discussed. Emphasis is placed on results of imaging studies in fetal and postnatal mice that have highlighted the developmental stage dependency of prenatal ethanol exposure-induced CNS defects. Consideration is also given to the promise of methodological advances to allow in vivo studies of aberrant brain and behavior relationships in model animals and to the translational nature of this work.

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Animal models have shown that all stages of embryonic development are vulnerable to the teratogenic effects of ethanol.
“While human research has not delineated, and perhaps cannot delineate fully, the pattern, amount and/or critical period of alcohol exposure necessary for structural and/or functional teratogenesis, animal models have shown that all stages of embryonic development are vulnerable to the teratogenic effects of ethanol, and that the type and severity of ethanol‐induced birth defects are dependent larg”
From The relationship between different dimensions of alcohol use and the burden of disease—an update (2017) · cites this paper as [62]
The type and severity of ethanol-induced birth defects are dependent largely upon the pattern, dose and developmental stage of the embryo at the time of ethanol exposure.
“While human research has not delineated, and perhaps cannot delineate fully, the pattern, amount and/or critical period of alcohol exposure necessary for structural and/or functional teratogenesis, animal models have shown that all stages of embryonic development are vulnerable to the teratogenic effects of ethanol, and that the type and severity of ethanol‐induced birth defects are dependent larg”
From The relationship between different dimensions of alcohol use and the burden of disease—an update (2017) · cites this paper as [62]

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Unique Facial Features Distinguish Fetal Alcohol Syndrome Patients and Controls in Diverse Ethnic Populations
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Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats
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Neurodevelopment of C57B/L6 mouse brain assessed by in vivo diffusion tensor imaging
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Use of Pup in a Cup Model to Study Brain Development
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Therapeutic motor training ameliorates cerebellar effects of postnatal binge alcohol
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Can prenatal ultrasound detect the effects of in‐utero alcohol exposure? A pilot study
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Holoprosencephaly in a fetal macaque (Macaca nemestrina) following weekly exposure to ethanol
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Alcohol-induced facial dysmorphology in C57BL/6 mouse models of fetal alcohol spectrum disorder
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Binge Drinking During Pregnancy and Risk of Seizures in Childhood: A Study Based on the Danish National Birth Cohort
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Imaging Methods for Morphological and Functional Phenotyping of the Rodent Heart
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Brain deficits associated with fetal alcohol exposure may be protected, in part, by peptides derived from activity-dependent neurotrophic factor and activity-dependent neuroprotective protein
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Staining methods for magnetic resonance microscopy of the rat fetus
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Temporal Vulnerability of Fetal Cerebellar Purkinje Cells to Chronic Binge Alcohol Exposure: Ovine Model
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The Impact of Maternal Age on the Effects of Prenatal Alcohol Exposure on Attention
Chiodo, L. M., da Costa, D. E., Hannigan, J. H., Covington, C. Y., Sokol, R. J., Janisse, J. J., Greenwald, M. K., Ager, J. W., & Delaney‐Black, V. (2010) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01269.x · Cited by 38 · see citing works
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Sequential developmental changes in holoprosencephalic mouse embryos exposed to ethanol during the gastrulation period
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Embryogenesis of holoprosencephaly
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Early-infantile galactosialidosis: Clinical, biochemical, and molecular observations in a new patient
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Chronic prenatal ethanol exposure increases apoptosis in the hippocampus of the term fetal guinea pig
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Characterization of Mouse Brain and Its Development using Diffusion Tensor Imaging and Computational Techniques
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Polymicrogyria in fetal alcohol syndrome
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Concurrent Dietary Administration of D‐SAL and Ethanol Diminishes Ethanol’s Teratogenesis
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Neonatal Alcohol‐Induced Region‐Dependent Changes in Rat Brain Neurochemistry Measured by High‐Resolution Magnetic Resonance Spectroscopy
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A rat model (using a semipurified diet) of the fetal alcohol syndrome.
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Elevated Fatty Acid Ethyl Esters in Meconium of Sheep Fetuses Exposed In Utero to Ethanol—A New Animal Model
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Effect of gestational ethanol exposure on parvalbumin and calretinin expressing hippocampal neurons in a chick model of fetal alcohol syndrome
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The relationship between different dimensions of alcohol use and the burden of disease—an update
Rehm, J., Gmel, G. E., Gmel, G., Hasan, O. S. M., Imtiaz, S., Popova, S., Probst, C., Roerecke, M., Room, R., Samokhvalov, A. V., et al. (2017) · Addiction · doi:10.1111/add.13757 · Cited by 1,204 · see citing works
Global Prevalence of Fetal Alcohol Spectrum Disorder Among Children and Youth
Lange, S., Probst, C., Gmel, G. E., Rehm, J. T., Burd, L., & Popova, S. (2017) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2017.1919 · Cited by 675 · see citing works
Neuroimaging effects of prenatal alcohol exposure on the developing human brain: a magnetic resonance imaging review
Donald, K. A., Eastman, E., Howells, F. M., Adnams, C., Riley, E. P., Woods, R. P., Narr, K. L., & Stein, D. J. (2015) · Acta Neuropsychiatrica · doi:10.1017/neu.2015.12 · Cited by 185 · see citing works
A Longitudinal Study of the Long-Term Consequences of Drinking during Pregnancy: Heavy<i>In Utero</i>Alcohol Exposure Disrupts the Normal Processes of Brain Development
Lebel, C., Mattson, S. N., Riley, E. P., Jones, K. L., Adnams, C. M., May, P. A., Bookheimer, S. Y., O'Connor, M. J., Narr, K. L., Kan, E., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1161-12.2012 · Cited by 164 · see citing works
Neural crest development in fetal alcohol syndrome
Smith, S. M., Garic, A., Flentke, G. R., & Berres, M. E. (2014) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21078 · Cited by 126 · see citing works
What Does Diffusion Tensor Imaging Reveal About the Brain and Cognition in Fetal Alcohol Spectrum Disorders?
Wozniak, J. R., & Muetzel, R. L. (2011) · Neuropsychology Review · doi:10.1007/s11065-011-9162-1 · Cited by 112 · see citing works
A quantitative magnetic resonance histology atlas of postnatal rat brain development with regional estimates of growth and variability
Calabrese, E., Badea, A., WATSON, C. R. R., & Johnson, G. A. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.01.017 · Cited by 110 · see citing works
“A wide range of toxic, vascular, traumatic, and even psychological insults are known to alter this crucial period of brain development (Friess et al., 2007; Herrmann et al., 2008; Jaaro-Peled et al., 2009; Maciag et al., 2006; O'Leary-Moore et al., 2011; Panzer, 2008).”
Background
Alcohol and the Brain
Nutt, D., Hayes, A., Fonville, L., Zafar, R. R., Palmer, E. O. C., Paterson, L. M., & Lingford-Hughes, A. R. (2021) · Nutrients · doi:10.3390/nu13113938 · Cited by 109 · see citing works
“Brain phenotypes of FASD have consistently been recapitulated in animal models and highlight the modulating role of timing and alcohol exposure [60].”
Background
Advances in Diagnosis and Treatment of Fetal Alcohol Spectrum Disorders: From Animal Models to Human Studies
Murawski, N. J. (2015) · Alcohol research · doi:10.35946/arcr.v37.1.07 · Cited by 100 · see citing works
AIE Bioconjugates for Biomedical Applications
Liu, H., Xiong, L., Kwok, R. T. K., He, X., Lam, J. W. Y., & Tang, B. Z. (2020) · Advanced Optical Materials · doi:10.1002/adom.202000162 · Cited by 97 · see citing works
Neurodevelopmental profile of Fetal Alcohol Spectrum Disorder: A systematic review
Lange, S., ROVET, J. F., Rehm, J. T., & Popova, S. (2017) · BMC Psychology · doi:10.1186/s40359-017-0191-2 · Cited by 83 · see citing works
Fetal Alcohol Spectrum Disorders and Neuroimmune Changes
Drew, P. D., & Kane, C. J. M. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-801284-0.00003-8 · Cited by 78 · see citing works
“Other exposure periods produce different unique patterns of structural and functional brain defects as demonstrated in numerous studies (e.g., O’Leary-Moore et al., 2011).”
Background
Fetal Alcohol Spectrum Disorder (FASD) Associated Neural Defects: Complex Mechanisms and Potential Therapeutic Targets
Muralidharan, P., Sarmah, S., Zhou, F., & Marrs, J. A. (2013) · Brain Sciences · doi:10.3390/brainsci3020964 · Cited by 74 · see citing works
Fetal alcohol spectrum disorders and fetal alcohol syndrome: the state of the art and new diagnostic tools
Memo, L., Gnoato, E., Caminiti, S., Pichini, S., & Tarani, L. (2013) · Early Human Development · doi:10.1016/s0378-3782(13)70013-6 · Cited by 68 · see citing works
“Other advanced MRI techniques, such as magnetic resonance microscopy, diffusion tensor imaging and magnetic resonance spectroscopy, have recently been applied to the study of both normal and abnormal structure and neurochemistry in patient or animal models of FASD [19].”
Background
From Research to Practice: An Integrative Framework for the Development of Interventions for Children with Fetal Alcohol Spectrum Disorders
Kodituwakku, P. W., & Kodituwakku, E. L. (2011) · Neuropsychology Review · doi:10.1007/s11065-011-9170-1 · Cited by 65 · see citing works
Postnatal day 7 ethanol treatment causes persistent reductions in adult mouse brain volume and cortical neurons with sex specific effects on neurogenesis
Coleman, L. G., Oğuz, İ., Lee, J., Styner, M. A., & Crews, F. T. (2012) · Alcohol · doi:10.1016/j.alcohol.2012.01.003 · Cited by 59 · see citing works
“O’Leary-Moore et al have also begun to investigate the effects of early gestational ethanol on the adolescent brain (O’Leary-Moore et al., 2011).”
The Impact of Prenatal Ethanol Exposure on Neuroanatomical and Behavioral Development in Mice
Abbott, C. W., Kozanian, O. O., Kanaan, J., Wendel, K. M., & Huffman, K. J. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12936 · Cited by 57 · see citing works
A study of the effects of prenatal alcohol exposure on white matter microstructural integrity at birth
Donald, K. A., Roos, A., Fouché, J., Koen, N., Howells, F. M., Woods, R. P., Zar, H. J., Narr, K. L., & Stein, D. J. (2015) · Acta Neuropsychiatrica · doi:10.1017/neu.2015.35 · Cited by 57 · see citing works
“Animal work and human imaging studies have demonstrated that in utero exposure to alcohol alters brain morphology and neurocircuitry across multiple brain regions (6,7).”
Background
White matter microstructure in fetal alcohol spectrum disorders: A systematic review of diffusion tensor imaging studies
Sherbaf, F. G., Aarabi, M. H., Yazdi, M. H., & Haghshomar, M. (2018) · Human Brain Mapping · doi:10.1002/hbm.24409 · Cited by 55 · see citing works
“Sharing the same progenitor cells, the development of midline facial and cranial structures are proposed to be compromised by cell damage from alcohol exposure (O'Leary-Moore et al., 2011; Sulik, 2005).”
Background
Fetal alcohol exposure leads to abnormal olfactory bulb development and impaired odor discrimination in adult mice
Akers, K. G., Kushner, S. A., Leslie, A. T. F. S., Clarke, L., van der Kooy, D., Lerch, J. P., & Frankland, P. W. (2011) · Molecular Brain · doi:10.1186/1756-6606-4-29 · Cited by 54 · see citing works
“Fetal alcohol exposure results in structural brain abnormalities in adult mice Children whose mothers consumed alcohol during pregnancy possess structural abnormalities in several brain regions [3-5], many of which are also observed in mouse embryos exposed to alcohol during gestation [ 15 ].”
Background
Fetal alcohol spectrum disorder
(2014) · Handbook of Clinical Neurology · doi:10.1016/b978-0-444-62619-6.00026-4 · Cited by 45 · see citing works
“Technologic advances and rapidly increasing knowledge in the fields of genetics, cell, developmental, and neurobiology are essential to accurately piecing together experimental evidence in refining our understanding of the genesis of alcohol-induced birth defects, to the planning and execution of future studies, and t…”
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Neurological and neuropsychological effects of low and moderate prenatal alcohol exposure
Comasco, E., Rangmar, J., Eriksson, U. J., & Oreland, L. (2017) · Acta Physiologica · doi:10.1111/apha.12892 · Cited by 45 · see citing works
“Admittedly, the ethanol levels achieved were high, BAC 75–90 mmol L 1 (346–415 mg dL (1)), but as the insult was limited to a few hours, this work illustrates the pronounced sensitivity to time-restricted ethanol insults.(59,60) Another significant morphogen, all-trans-retinoic acid (denoted atRA)(61) was evaluated in…”
Background
Postnatal choline supplementation selectively attenuates hippocampal microRNA alterations associated with developmental alcohol exposure
Balaraman, S., Idrus, N. M., Miranda, R. C., & Thomas, J. D. (2017) · Alcohol · doi:10.1016/j.alcohol.2016.12.006 · Cited by 43 · see citing works
“Alcohol may alter cell proliferation, migration, differentiation, synaptogenesis, and myelination, depending on the developmental timing and other exposure parameters (Camarillo and Miranda, 2008; Gil-Mohapel et al., 2010; Kane et al., 2012; O'Leary-Moore et al., 2011; Santillano et al., 2005; Tingling et al., 2013; W…”
Background
Long-Lasting Neural Circuit Dysfunction Following Developmental Ethanol Exposure
Sadrian, B., Wilson, D. A., & Saito, M. (2013) · Brain Sciences · doi:10.3390/brainsci3020704 · Cited by 39 · see citing works
The all‐or‐none phenomenon revisited
Adam, M. P. (2012) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.23029 · Cited by 37 · see citing works
Mitogen-activated protein kinase modulates ethanol inhibition of cell adhesion mediated by the L1 neural cell adhesion molecule
Dou, X., Wilkemeyer, M. F., Menkari, C. E., Parnell, S. E., Sulik, K. K., & Charness, M. E. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221386110 · Cited by 36 · see citing works
“May PA, et al. (2009) Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies.”
BackgroundInfluentialSelf-citation
Aggregation‐Induced Emission Materials that Aid in Pharmaceutical Research
Wang, B., Liu, S., Liu, X., Hu, R., Qin, A., & Tang, B. Z. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202101067 · Cited by 34 · see citing works
Neuroimmune mechanisms in fetal alcohol spectrum disorder
Kane, C. J. M., Phelan, K. D., & Drew, P. D. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22035 · Cited by 34 · see citing works
“DTI consistently reveals minor to major defects in the corpus callosum of embryos exposed to alcohol during early gestation even in the absence of distinguishable facial dysmorphology (O’Leary-Moore et al., 2011).”
Background
Moderate Prenatal Alcohol Exposure Alters Functional Connectivity in the Adult Rat Brain
Rodriguez, C. I., Davies, S., Calhoun, V. D., Savage, D. D., & Hamilton, D. A. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13175 · Cited by 31 · see citing works
“Some laboratories have investigated the effects of PAE on the structural connectivity of rodent brains (O'Leary-Moore et al., 2011).”
Background
Interhemispheric Functional Brain Connectivity in Neonates with Prenatal Alcohol Exposure: Preliminary Findings
Donald, K. A., Ipser, J., Howells, F. M., Roos, A., Fouché, J., Riley, E. P., Koen, N., Woods, R. P., Biswal, B. B., Zar, H. J., et al. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12930 · Cited by 33 · see citing works
“, 2009) and human imaging studies in school-age children with FASD have demonstrated that in utero exposure to alcohol alters brain morphology and reduces white matter microstructural integrity (Archibald et al., 2001; Fryer et al., 2009; Lebel et al., 2008, 2012; Leigland et al., 2013; O’Leary-Moore et al., 2011; Sow…”
Background
The Hemodynamic Basis for Positional- and Inter-Fetal Dependent Effects in Dual Arterial Supply of Mouse Pregnancies
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Focus On: Magnetic Resonnance–Based Studies of Fetal Alcohol Spectrum Disorders in Animal Modals
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Self-citation

Authors: O’Leary-Moore, S. K., Parnell, S. E., Lipinski, R. J., & Sulik, K. K.
Affiliations: University of North Carolina at Chapel Hill (US)
ORCID: Parnell, Scott E.
Lipinski, Robert J.
Venue: Neuropsychology Review
Publisher: Springer Science and Business Media LLC
Published: 2011-03-29
Volume: 21
Issue: 2
Pages: 167-185
ISSN: 1040-7308 (ISSN-L)
1573-6660
DOI: 10.1007/s11065-011-9164-z
PMC: PMC3445286
OpenAlex: W1986206338
Cited by: 77
References: 129
Citations by year: 2026: 2 · 2024: 2 · 2023: 7 · 2022: 1 · 2021: 7 · 2020: 2 · 2019: 2 · 2018: 5 · 2017: 8 · 2016: 7 · 2015: 4 · 2014: 7 · 2013: 9 · 2012: 9
FWCI: 1.43
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Neuropsychology Review (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
UNC Libraries
Funders: National Institutes of Health (AA011605, AA007573)
U.S. Public Health Service (NICDH 03110, P4105959)
University of North Carolina at Chapel Hill
National Institute on Alcohol Abuse and Alcoholism (AA011605, AA 007573, U01AA017124, P60AA011605, T32AA007573)
National Cancer Institute (U24 CA0292656, R24CA092656)
National Center for Research Resources (P41RR005959)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD003110)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Keywords: fetal alcohol spectrum disorders, prenatal alcohol exposure, animal models, magnetic resonance microscopy, diffusion tensor imaging, magnetic resonance spectroscopy, mouse model, brain development, neurodevelopmental defects, brain-behavior relationship, translational research
MeSH terms: Ethanol, Animals, Brain, Brain Mapping, Developmental Disabilities, Diagnostic Imaging, Disease Models, Animal, Facial Asymmetry, Female, Male, Pregnancy, Prenatal Exposure Delayed Effects, Imaging, Three-Dimensional, Mice, Fetal Alcohol Spectrum Disorders

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Magnetic Resonance-Based Imaging in Animal Models of Fetal Alcohol Spectrum Disorder

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