Optical coherence tomography angiography to evaluate murine fetal brain vasculature changes caused by prenatal exposure to nicotine.

Maternal smoking causes several defects ranging from intrauterine growth restriction to sudden infant death syndrome and spontaneous abortion. While several studies have documented the effects of prenatal nicotine exposure in development and behavior, acute vasculature changes in the fetal brain due to prenatal nicotine exposure have not been evaluated yet. This study uses correlation mapping optical coherence angiography to evaluate changes in fetal brain vasculature flow caused by maternal exposure to nicotine during the second trimester-equivalent of gestation in a mouse model. The effects of two different doses of nicotine were evaluated. Results showed a decrease in the vasculature for both doses of nicotine, which was not seen in the case of the sham group.

[1]  R. Perera,et al.  Nicotine replacement therapy for smoking cessation. , 2012, The Cochrane database of systematic reviews.

[2]  J E Henningfield,et al.  Toward a comprehensive long term nicotine policy , 2005, Tobacco Control.

[3]  Carlo Tomasi,et al.  Automated non-rigid registration and mosaicing for robust imaging of distinct retinal capillary beds using speckle variance optical coherence tomography , 2013, Biomedical optics express.

[4]  T. Slotkin,et al.  Prenatal exposure to nicotine via maternal infusions: effects on development of catecholamine systems. , 1988, The Journal of pharmacology and experimental therapeutics.

[5]  P. Romundstad,et al.  Prenatal smoking exposure and psychiatric symptoms in adolescence , 2007, Acta paediatrica.

[6]  H. Gerstein,et al.  Long-Term Consequences of Fetal and Neonatal Nicotine Exposure: A Critical Review , 2010, Toxicological sciences : an official journal of the Society of Toxicology.

[7]  L. C. Murrin,et al.  Nicotine administration to rats: methodological considerations. , 1987, Life sciences.

[8]  L. Porter,et al.  Electronic Cigarette and Traditional Cigarette Use among Middle and High School Students in Florida, 2011–2014 , 2015, PloS one.

[9]  Narendran Sudheendran,et al.  Optical coherence tomography for live phenotypic analysis of embryonic ocular structures in mouse models. , 2012, Journal of biomedical optics.

[10]  Martin J Leahy,et al.  Cellular phone‐based photoplethysmographic imaging , 2011, Journal of biophotonics.

[11]  M. Chisolm,et al.  Knowledge, Attitudes, and Practice of Electronic Cigarette Use Among Pregnant Women , 2015, Journal of addiction medicine.

[12]  T. Slotkin.  Fetal nicotine or cocaine exposure: which one is worse? , 1998, The Journal of pharmacology and experimental therapeutics.

[13]  Cerine Lal,et al.  Feasibility of correlation mapping optical coherence tomography angiographic technique using a 200  kHz vertical-cavity surface-emitting laser source for in vivo microcirculation imaging applications. , 2018, Applied optics.

[14]  R. Lew,et al.  Effect of maternal cigarette smoking on pregnancy complications and sudden infant death syndrome. , 1995, The Journal of family practice.

[15]  Ruikang K. Wang,et al.  Doppler optical micro-angiography for volumetric imaging of vascular perfusion in vivo. , 2009, Optics express.

[16]  D. Knol,et al.  Child behavior problems increased by maternal smoking during pregnancy. , 1999, Archives of environmental health.

[17]  T. Slotkin.  Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. , 2004, Toxicology and applied pharmacology.

[18]  Michael G. Turner,et al.  Maternal Cigarette Smoking During Pregnancy and Life-Course-Persistent Offending , 2002, International journal of offender therapy and comparative criminology.

[19]  K. Farsalinos,et al.  Nicotine absorption from electronic cigarette use: comparison between experienced consumers (vapers) and naïve users (smokers) , 2015, Scientific Reports.

[20]  Adrian Mariampillai,et al.  Speckle variance detection of microvasculature using swept-source optical coherence tomography. , 2008, Optics letters.

[21]  R. Perera,et al.  Nicotine replacement therapy for smoking cessation. , 2012, The Cochrane database of systematic reviews.

[22]  V. Conter,et al.  Weight growth in infants born to mothers who smoked during pregnancy , 1995, BMJ.

[23]  K. Bucholz,et al.  Contributions of parental alcoholism, prenatal substance exposure, and genetic transmission to child ADHD risk: a female twin study , 2005, Psychological Medicine.

[24]  J. Barton,et al.  Flow measurement without phase information in optical coherence tomography images. , 2005, Optics express.

[25]  N. Benowitz,et al.  Risks and Benefits of Nicotine to Aid Smoking Cessation in Pregnancy , 2001, Drug safety.

[26]  Wallace C. H. Choy,et al.  Plasmon-Electrical Effects on Organic Solar Cells by Incorporation of Metal Nanostructures , 2016, IEEE Journal of Selected Topics in Quantum Electronics.

[27]  A. Fowden,et al.  Endocrine Regulation of Feto-Placental Growth , 2009, Hormone Research in Paediatrics.

[28]  S. Hamid,et al.  Do the Number of Cigarettes Smokes per Day Contribute to the Incident of Malignant Cancer? , 2019, Asian Pacific journal of cancer prevention : APJCP.

[29]  Chen Wu,et al.  Evaluating the effects of maternal alcohol consumption on murine fetal brain vasculature using optical coherence tomography , 2018, Journal of biophotonics.

[30]  Irina V. Larina,et al.  In vivo micro-scale tomography of ciliary behavior in the mammalian oviduct , 2015, Scientific Reports.

[31]  T. Slotkin,et al.  Persistent c-fos Induction by Nicotine in Developing Rat Brain Regions: Interaction with Hypoxia , 1999, Pediatric Research.

[32]  R. Kirby,et al.  In Utero Nicotine Exposure and Fetal Growth Inhibition among Twins , 2005, American journal of perinatology.

[33]  Ruikang K. Wang,et al.  Stripe motion artifact suppression in phase-resolved OCT blood flow images of the human eye based on the frequency rejection filter , 2013 .

[34]  J. Hecksher-Sørensen,et al.  Optical Projection Tomography as a Tool for 3D Microscopy and Gene Expression Studies , 2002, Science.

[35]  M. Schlumpf,et al.  Pre- and postnatal development of high-affinity [3H]nicotine binding sites in rat brain regions: an autoradiographic study. , 1992, Brain research. Developmental brain research.

[36]  Manmohan Singh,et al.  Rotational imaging optical coherence tomography for full-body mouse embryonic imaging , 2016, Journal of biomedical optics.

[37]  Matthew S. Goodwin,et al.  Maternal Smoking During Pregnancy and Neonatal Behavior: A Large-Scale Community Study , 2009, Pediatrics.

[38]  J. Fujimoto,et al.  Optical Coherence Tomography , 1991 .

[39]  S. Chokron,et al.  Effects of prenatal stress on fetal and child development: A critical literature review , 2014, Neuroscience & Biobehavioral Reviews.

[40]  L. Goldschmidt,et al.  Prenatal tobacco effects on neuropsychological outcomes among preadolescents. , 2001, Journal of developmental and behavioral pediatrics : JDBP.

[41]  T. Slotkin,et al.  Cryptic brain cell injury caused by fetal nicotine exposure is associated with persistent elevations of c-fos protooncogene expression 1 Supported by a grant from the Smokeles Tobacco Research Council. 1 , 1997, Brain Research.

[42]  N. Benowitz.  Nicotine and Cardiovascular Disease , 1991 .

[43]  L. Abbott,et al.  Smoking during pregnancy: lessons learned from epidemiological studies and experimental studies using animal models , 2012, Critical reviews in toxicology.

[44]  Ruikang K. Wang,et al.  Ultrahigh sensitive optical microangiography for in vivo imaging of microcirculations within human skin tissue beds. , 2010, Optics express.

[45]  Alex Cable,et al.  Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography. , 2008, Journal of biomedical optics.

[46]  N. Benowitz,et al.  Daily intake of nicotine during cigarette smoking , 1984, Clinical pharmacology and therapeutics.

[47]  R. Watts,et al.  Connecting vascular and nervous system development: angiogenesis and the blood-brain barrier. , 2010, Annual review of neuroscience.

[48]  B. Leventhal,et al.  Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review. , 2002, American journal of public health.

[49]  S Cnattingius,et al.  Cigarette smoking as a risk factor for sudden infant death syndrome: a population-based study. , 1990, American journal of public health.

[50]  Hsiao-ye Yi,et al.  An Epidemiologic Analysis of Co-Occurring Alcohol and Tobacco Use and Disorders , 2006, Alcohol research & health : the journal of the National Institute on Alcohol Abuse and Alcoholism.

[51]  Martin F. Kraus,et al.  Split-spectrum amplitude-decorrelation angiography with optical coherence tomography , 2012, Optics express.

[52]  R. Mark Henkelman,et al.  Three-Dimensional Analysis of Vascular Development in the Mouse Embryo , 2008, PloS one.

[53]  K. Larin,et al.  Development of phase-stabilized swept-source OCT for the ultrasensitive quantification of microbubbles , 2008 .

[54]  Rebecca Knight,et al.  Risk Factors for Exclusive E-Cigarette Use and Dual E-Cigarette Use and Tobacco Use in Adolescents , 2015, Pediatrics.

[55]  T. Slotkin,et al.  Cholinergic receptors in heart and brainstem of rats exposed to nicotine during development: implications for hypoxia tolerance and perinatal mortality. , 1999, Brain research. Developmental brain research.

[56]  Dianne C Barker,et al.  Helping pregnant smokers quit: meeting the challenge in the next decade , 2000, The Western journal of medicine.

[57]  R. Naeye.  EFFECTS OF MATERNAL CIGARETTE SMOKING ON THE FETUS AND PLACENTA , 1978, British journal of obstetrics and gynaecology.

[58]  M. Dickinson,et al.  Multimodal imaging of mouse development: Tools for the postgenomic era , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[59]  G. L. Bell,et al.  Perinatal and neonatal issues of substance abuse. , 1995, Pediatric clinics of North America.

[60]  T. Slotkin.  If nicotine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescents? , 2007, Neurotoxicology and teratology.

[61]  P. Franco,et al.  Heart rate variability in preterm infants and maternal smoking during pregnancy , 2009, Clinical Autonomic Research.

[62]  Kirill V Larin,et al.  Dynamic imaging and quantitative analysis of cranial neural tube closure in the mouse embryo using optical coherence tomography. , 2017, Biomedical optics express.

[63]  H. Kranzler,et al.  Pharmacotherapies to enhance smoking cessation during pregnancy. , 2003, Drug and alcohol review.

[64]  T. Coleman,et al.  A randomized trial of nicotine-replacement therapy patches in pregnancy. , 2012, The New England journal of medicine.

[65]  T. Slotkin,et al.  Development of [3H]nicotine binding sites in brain regions of rats exposed to nicotine prenatally via maternal injections or infusions. , 1987, The Journal of pharmacology and experimental therapeutics.

[66]  Ruikang K. Wang,et al.  Three dimensional optical angiography. , 2007, Optics express.

[67]  Luping Z. Huang,et al.  Chronic nicotine induces growth retardation in neonatal rat pups. , 2006, Life sciences.

[68]  H. Dunn,et al.  Cigarette smoking and the fetus and child. , 1977, Pediatrics.

[69]  R. Kessler,et al.  Prevalence and demographic correlates of symptoms of last year dependence on alcohol, nicotine, marijuana and cocaine in the U.S. population. , 1997, Drug and alcohol dependence.

[70]  N. Saliba,et al.  Effects of user puff topography, device voltage, and liquid nicotine concentration on electronic cigarette nicotine yield: measurements and model predictions. , 2015, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[71]  W. Griffith,et al.  Chronic neonatal nicotine exposure increases excitation in the young adult rat hippocampus in a sex-dependent manner , 2012, Brain Research.

[72]  Linda A Corey,et al.  The role of the children of twins design in elucidating causal relations between parent characteristics and child outcomes. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[73]  N. Benowitz.  The role of nicotine in smoking-related cardiovascular disease. , 1997, Preventive medicine.

[74]  S. Temple,et al.  Functional Nicotinic Acetylcholine Receptor Expression on Stem and Progenitor Cells of the Early Embryonic Nervous System , 2002, Annals of the New York Academy of Sciences.

[75]  J. Fava,et al.  The transtheoretical model of smoking: comparison of pregnant and nonpregnant smokers. , 2000, Addictive behaviors.

[76]  M. M. Lefkowitz.  Smoking during pregnancy: Long-term effects on offspring. , 1981 .

[77]  J. Ockene,et al.  Nicotine Replacement Prescription Practices of Obstetric and Pediatric Clinicians , 2000, Obstetrics and gynecology.

[78]  Ruikang K. Wang,et al.  Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina. , 2011, Journal of biomedical optics.

[79]  S. Goderie,et al.  Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. , 2001, Developmental biology.

[80]  S. Cnattingius,et al.  Maternal smoking and causes of very preterm birth , 2005, Acta obstetricia et gynecologica Scandinavica.

[81]  T. Slotkin.  Developmental cholinotoxicants: nicotine and chlorpyrifos. , 1999, Environmental health perspectives.

[82]  H. Goldstein,et al.  Smoking in Pregnancy and Subsequent Child Development , 1973, British medical journal.

[83]  L. Wright,et al.  Low Birth Weight and Preterm Births: Etiologic Fraction Attributable to Prenatal Drug Exposure , 2005, Journal of Perinatology.

[84]  Mohammad Sultan Mahmud,et al.  Review of speckle and phase variance optical coherence tomography to visualize microvascular networks , 2013, Journal of biomedical optics.

[85]  Manuel Guizar-Sicairos,et al.  Efficient subpixel image registration algorithms. , 2008, Optics letters.

[86]  Raksha Raghunathan,et al.  Optical coherence tomography for embryonic imaging: a review , 2016, Journal of biomedical optics.

[87]  J. Seckl,et al.  Glucocorticoids, prenatal stress and the programming of disease , 2011, Hormones and Behavior.

[88]  Shuichi Makita,et al.  Noise-immune complex correlation for optical coherence angiography based on standard and Jones matrix optical coherence tomography. , 2016, Biomedical optics express.

[89]  Raksha Raghunathan,et al.  Assessing the acute effects of prenatal synthetic cannabinoid exposure on murine fetal brain vasculature using optical coherence tomography , 2019, Journal of biophotonics.

[90]  Naeye Rl.  Cognitive and behavioral abnormalities in children whose mothers smoked cigarettes during pregnancy. , 1992 .

[91]  M. Norman,et al.  The Growth and Development of Microvasculature in Human Cerebral Cortex , 1986, Journal of neuropathology and experimental neurology.

[92]  T. Coleman,et al.  Nicotine replacement therapy in pregnancy , 2004, BMJ : British Medical Journal.

[93]  Edward D Levin,et al.  Mode of Action: Disruption of Brain Cell Replication, Second Messenger, and Neurotransmitter Systems During Development Leading to Cognitive Dysfunction—Developmental Neurotoxicity of Nicotine , 2005, Critical reviews in toxicology.

[94]  Chen Wu,et al.  Applicability, usability, and limitations of murine embryonic imaging with optical coherence tomography and optical projection tomography. , 2016, Biomedical optics express.

[95]  J. Izatt,et al.  In vivo bidirectional color Doppler flow imaging of picoliter blood volumes using optical coherence tomography. , 1997, Optics letters.

[96]  Naeye Rl,et al.  Mental development of children whose mothers smoked during pregnancy. , 1984 .

[97]  David Huang,et al.  Projection-resolved optical coherence tomographic angiography. , 2016, Biomedical optics express.

[98]  K. Fahy,et al.  Why do women continue to smoke in pregnancy? , 2007, Women and birth : journal of the Australian College of Midwives.

[99]  P M Whitaker-Azmitia,et al.  Role of serotonin and other neurotransmitter receptors in brain development: basis for developmental pharmacology. , 1991, Pharmacological reviews.

[100]  K. Janda,et al.  A previously undescribed chemical link between smoking and metabolic disease , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[101]  G Gennser,et al.  A Study of Smoking and Pregnancy with Special Reference to Fetal Growth , 1978, Acta obstetricia et gynecologica Scandinavica. Supplement.

[102]  M. V. van Gemert,et al.  Noninvasive imaging of in vivo blood flow velocity using optical Doppler tomography. , 1997, Optics letters.

[103]  H. A. Navarro,et al.  Prenatal exposure to nicotine impairs nervous system development at a dose which does not affect viability or growth , 1989, Brain Research Bulletin.

[104]  M. Takigawa,et al.  Prenatal nicotine exposure affects the development of the central serotonergic system as well as the dopaminergic system in rat offspring: involvement of route of drug administrations. , 1997, Brain research. Developmental brain research.

[105]  S. Yun,et al.  Real-time fiber-based multi-functional spectral-domain optical coherence tomography at 1.3 microm. , 2005, Optics express.

[106]  Kirill V. Larin,et al.  Label-free optical imaging in developmental biology [Invited]. , 2020, Biomedical optics express.

[107]  A. C. Collins,et al.  Guidelines on nicotine dose selection for in vivo research , 2007, Psychopharmacology.

[108]  G. Dekker,et al.  Spontaneous preterm birth and small for gestational age infants in women who stop smoking early in pregnancy: prospective cohort study , 2009, BMJ : British Medical Journal.

[109]  C. Aligne,et al.  The effects of tobacco exposure on children's behavioral and cognitive functioning: implications for clinical and public health policy and future research. , 2002, Neurotoxicology and teratology.

[110]  Yongyang Huang,et al.  Optical Coherence Tomography for Brain Imaging and Developmental Biology , 2016, IEEE Journal of Selected Topics in Quantum Electronics.

[111]  B. Finlay,et al.  Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species , 2013, The Journal of Neuroscience.