Prenatal Nicotine Exposure Alters Pulmonary Function in Newborn Rhesus Monkeys
Abstract
Epidemiological studies have shown that offspring of women who smoke during pregnancy have abnormal lung function and associated higher incidences of lower respiratory disorders. The recent identification of nicotinic acetylcholine receptors (nAChR) in fetal lung suggests that the direct interaction between nicotine and nAChR in fetal lung may underlie the postnatal pulmonary abnormalities seen in such infants. This hypothesis was tested in monkeys to determine if maternal nicotine exposure would produce changes in lung mechanics in newborn monkeys similar to those observed in human infants whose mothers smoked during pregnancy. Timed pregnant rhesus monkeys were infused with either nicotine (1.5 mg/kg/d, n = 7) or saline (n = 7) using subcutaneous osmotic pumps from Day 26 to 160 of gestation. On Day 160 of pregnancy (term = 165 d), fetuses were delivered by C-section, and the following day were subjected to pulmonary function testing. After testing, animals were sacrificed, and lungs weighed and fixed. Lung weight and fixed lung volume decreased (16% and 14%, respectively) significantly following in utero nicotine exposure. Peak tidal expiratory flow, FEV(0.2), mean mid-expiratory flow, forced expiratory volume at peak expiratory flow (FEV(PEF)), and FEV(PEF)/FVC% were significantly lower in newborns exposed to nicotine during gestation. Absolute and specific pulmonary resistance increased significantly whereas absolute and specific dynamic compliance remained unchanged in prenatally nicotine-treated pups. These changes in pulmonary function are strikingly similar to the changes observed in offspring of human smokers. This suggests that the interaction of nicotine with nAChR in developing lung is responsible for the altered pulmonary mechanics observed in human infants whose mothers smoked during pregnancy.
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In monkeys and mice, prenatal nicotine alone at levels similar to smokers causes decreases in forced expiratory flow.
“In both monkeys and mice, exposure to prenatal nicotine alone, at levels similar to that of smokers, causes similar decreases in forced expiratory flow.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [207]
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Cites
Lung function. Assessment and application in medicine
(1969) · Tubercle · doi:10.1016/0041-3879(69)90013-0 · Cited by 853 · see citing works
The Effect of Maternal Smoking during Pregnancy on Early Infant Lung Function
Hanrahan, J. P., Tager, I. B., Segal, M. R., Tosteson, T. D., Castile, R. G., Vunakis, H. V., Weiss, S. T., & Speizer, F. E. (1992) · American Review of Respiratory Disease · doi:10.1164/ajrccm/145.5.1129 · Cited by 527 · see citing works
Stick, S. M., Burton, P., Gurrin, L. C., Sly, P. D., & Souëf, P. N. L. (1996) · The Lancet · doi:10.1016/s0140-6736(96)04446-7 · Cited by 452 · see citing works
Luck, W., Nau, H., Hansen, R., & Steldinger, R. (2017) · Developmental Pharmacology and Therapeutics · doi:10.1159/000457063 · Cited by 444 · see citing works
Nicotinic acetylcholine receptors in health and disease
Lindstrom, J. (1997) · Molecular Neurobiology · doi:10.1007/bf02740634 · Cited by 443 · see citing works
Maternal smoking during pregnancy, environmental tobacco smoke exposure and childhood lung function
Gilliland, F. D. (2000) · Thorax · doi:10.1136/thorax.55.4.271 · Cited by 359 · see citing works
THE EFFECTS OF MATERNAL SMOKING ON FETAL AND INFANT MORTALITY
Kleinman, J. C., Pierre, M. B., Madans, J. H., Land, G. H., & SCHRAMM, W. F. (1988) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114803 · Cited by 325 · see citing works
Lung Function, Pre- and Post-natal Smoke Exposure, and Wheezing in the First Year of Life
Tager, I. B., Hanrahan, J. P., Tosteson, T. D., Castile, R. G., Brown, R. W., Weiss, S. T., & Speizer, F. E. (1993) · American Review of Respiratory Disease · doi:10.1164/ajrccm/147.4.811 · Cited by 315 · see citing works
Sekhon, H. S., Jia, Y., Raab, R., Kuryatov, A., Pankow, J. F., Whitsett, J. A., Lindstrom, J., & Spindel, E. R. (1999) · Journal of Clinical Investigation · doi:10.1172/jci5232 · Cited by 311 · see citing works
Self-citationMaternal Smoking During Pregnancy. Effects on Lung Function During the First 18 Months of Life
Tager, I. B., Ngo, L. H., & Hanrahan, J. P. (1995) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.152.3.7663813 · Cited by 304 · see citing works
In utero exposure to cigarette smoking influences lung function at birth
Carlsen, K. L., Jaakkola, J. J. K., Nafstad, P. H. J., & Carlsen, K.-H. (1997) · European Respiratory Journal · doi:10.1183/09031936.97.10081774 · Cited by 260 · see citing works
Maternal smoking during pregnancy and lower respiratory tract illness in early life
Taylor, B., & Wadsworth, J. (1987) · Archives of Disease in Childhood · doi:10.1136/adc.62.8.786 · Cited by 248 · see citing works
Dezateux, C. A., Stocks, J., Dundas, I., & FLETCHER, M. E. (1999) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.159.2.9712029 · Cited by 247 · see citing works
Jacob, P., Yu, L., Wilson, M., & Benowitz, N. L. (1991) · Journal of Mass Spectrometry · doi:10.1002/bms.1200200503 · Cited by 234 · see citing works
Self-citationHuman and Rodent Bronchial Epithelial Cells Express Functional Nicotinic Acetylcholine Receptors
Maus, A. D. J., Pereira, E. F. R., Karachunski, P. I., Horton, R. M., Navaneetham, D., Macklin, K., Cortes, W. S., Albuquerque, E. X., & Conti-Fine, B. M. (1998) · Molecular Pharmacology · doi:10.1124/mol.54.5.779 · Cited by 234 · see citing works
Trends in pregnancy related smoking rates in the United States, 1987–1996
Ebrahim, S. H. (2000) · JAMA · doi:10.1001/jama.283.3.361 · Cited by 233 · see citing works
Maternal Smoking during Pregnancy as a Predictor of Lung Function in Children
Cunningham, J., Dockery, D. W., & Speizer, F. E. (1994) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a116961 · Cited by 230 · see citing works
Respiratory function among preterm infants whose mothers smoked during pregnancy
HOO, A.-F., HENSCHEN, M., DEZATEUX, C., COSTELOE, K., & STOCKS, J. (1998) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.158.3.9711057 · Cited by 220 · see citing works
Fetal Lung Hypoplasia Associated with Maternal Smoking: A Morphometric Analysis
Collins, M. H., Moessinger, A. C., Kleinerman, J. I., Bassi, J. A., Rosso, P., COLLINS, A. M., JAMES, S. L., & Blanc, W. A. (1985) · Pediatric Research · doi:10.1203/00006450-198519040-00018 · Cited by 190 · see citing works
Zia, S., Ndoye, A., Nguyen, V. T., & Grando, S. A. (1997) · PubMed · Cited by 178 · see citing works
Neuronal nicotinic receptors in non-neuronal cells: new mediators of tobacco toxicity?
Conti‐Fine, B. M., Navaneetham, D., Lei, S., & Maus, A. D. J. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00036-4 · Cited by 173 · see citing works
ELLIOT, J., VULLERMIN, P., & ROBINSON, P. (1998) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.158.3.9709055 · Cited by 158 · see citing works
Maternal tobacco exposure and cotinine levels in fetal fluids in the first half of pregnancy
Jauniaux, E. (1999) · Obstetrics & Gynecology · doi:10.1016/s0029-7844(98)00318-4 · Cited by 157 · see citing works
Parental smoking and respiratory illness in infancy
Fergusson, D. M., Horwood, L. J., & Shannon, F. T. (1980) · Archives of Disease in Childhood · doi:10.1136/adc.55.5.358 · Cited by 145 · see citing works
Specific airway conductance in relation to postconceptional age during infancy
Stocks, J., & Godfrey, S. (1977) · Journal of Applied Physiology · doi:10.1152/jappl.1977.43.1.144 · Cited by 128 · see citing works
Nasal resistance during infancy
Stocks, J., & Godfrey, S. (1978) · Respiration Physiology · doi:10.1016/0034-5687(78)90031-2 · Cited by 103 · see citing works
Seidler, F. J., Levin, E. D., Lappi, S. E., & Slotkin, T. A. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90170-2 · Cited by 92 · see citing works
Effects of smoking in pregnancy on neonatal lung function
Milner, A. D., Marsh, M. J., Ingram, D., Fox, G. F., & Susiva, C. (1999) · Archives of Disease in Childhood Fetal & Neonatal · doi:10.1136/fn.80.1.f8 · Cited by 89 · see citing works
The Molecular Biology of Neuronal Nicotinic Acetylcholine Receptors
Boyd, R. T. (1997) · Critical Reviews in Toxicology · doi:10.3109/10408449709089897 · Cited by 84 · see citing works
Association of intrauterine cigarette smoke exposure with indices of fetal lung maturation.
Lieberman, E., Torday, J. S., Barbieri, R., Cohen, A., Vunakis, H. V., & Weiss, S. T. (1992) · PubMed · Cited by 82 · see citing works
Maternal smoking and birthweight: effect modification of period, maternal age and paternal smoking
Haug, K., Irgens, L. M., Skjærven, R., Markestad, T., Baste, V., & Schreuder, P. (2000) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1034/j.1600-0412.2000.079006485.x · Cited by 81 · see citing works
Effect of maternal smoking during pregnancy on passive respiratory mechanics in early infancy
Brown, R. W., Hanrahan, J. P., Castile, R. G., & Tager, I. B. (1995) · Pediatric Pulmonology · doi:10.1002/ppul.1950190105 · Cited by 72 · see citing works
The use of pharmacotherapies for smoking cessation during pregnancy
Benowitz, N., Dempsey, D., Goldenberg, R., Hughes, J., Dolan-Mullen, P., Ogburn, P., Oncken, C., Orleans, C., Slotkin, T., Whiteside, H. P., et al. (2000) · Tobacco Control · doi:10.1136/tc.9.suppl_3.iii91 · Cited by 67 · see citing works
Self-citationPassive Respiratory Mechanics in Healthy Infants. Effects of Growth, Gender, and Smoking
Hanrahan, J. P., Brown, R. W., Carey, V. J., Castile, R. G., Speizer, F. E., & Tager, I. B. (1996) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.154.3.8810604 · Cited by 67 · see citing works
Permanent effects of maternal smoking on offsprings' lung function
Upton, M. N., Watt, G. C. M., Smith, G. D., McConnachie, A., & Hart, C. (1998) · The Lancet · doi:10.1016/s0140-6736(05)79187-x · Cited by 55 · see citing works
CHANGE IN OBSERVED BIRTH WEIGHT ASSOCIATED WITH CHANGE IN MATERNAL CIGARETTE SMOKING
Wainright, R. L. (1983) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a113600 · Cited by 55 · see citing works
Grasso, M. C., Button, B., Allison, D. J., & Sawyer, S. M. (2000) · Pediatric Pulmonology · doi:10.1002/(sici)1099-0496(200005)29:5 · Cited by 55 · see citing works
The effect of amniocentesis and drainage of amniotic fluid on lung development in Macacafascicularis
Hislop, A. A., Fairweather, D. V. I., Blackwell, R. J., & Howard, S. (1984) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1984.tb03693.x · Cited by 52 · see citing works
Cunningham, J. G., Dockery, D. W., Gold, D. R., & Speizer, F. E. (1995) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.152.2.7633708 · Cited by 50 · see citing works
Serum eosinophil cationic protein as a predictor of wheezing after bronchiolitis
Reijonen, T. M., Korppi, M. O., Kuikka, L., Savolainen, K., Kleemola, M., Mononen, I., & Remes, K. (1997) · Pediatric Pulmonology · doi:10.1002/(sici)1099-0496(199706)23:6 · Cited by 48 · see citing works
Nicotine stimulates branching and expression of SP-A and SP-C mRNAs in embryonic mouse lung culture
Wuenschell, C. W., Zhao, J., Tefft, J. D., & Warburton, D. (1998) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1998.274.1.l165 · Cited by 44 · see citing works
Fetal nicotine exposure alters ontogeny of M1-receptors and their link to G-proteins
Zahalka, E. A., Seidler, F. J., Yanai, J., & Slotkin, T. A. (1993) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(93)90069-z · Cited by 43 · see citing works
Lindley, A. A., Gray, R. H., HERMAN, A. A. B., & Becker, S. R. (2000) · American Journal of Public Health · doi:10.2105/ajph.90.3.420 · Cited by 40 · see citing works
Buckner, C. K., Dea, D., Liberati, N., & Krell, R. D. (1991) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24790-5 · Cited by 40 · see citing works
The relationship between tPTEF:tE and specific airway conductance in infancy
Dezateux, C. A., Stocks, J., Dundas, I., Jackson, E. A., & Fletcher, M. E. (1994) · Pediatric Pulmonology · doi:10.1002/ppul.1950180507 · Cited by 38 · see citing works
Expression of the Nicotinic Receptor α7 Gene in Tendon and Periosteum During Early Development
Romano, S. J., Corriveau, R. A., Schwarz, R. I., & Berg, D. K. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.68020640.x · Cited by 34 · see citing works
Pulmonary function alterations after 3 wk of exposure to hypobaria and/or hypoxia in growing rats
Sekhon, H. S., Wright, J. R., & Thurlbeck, W. M. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.78.5.1787 · Cited by 20 · see citing works
Self-citationPerinatal lung function and invasive antenatal procedures
Yuksel, B., Greenough, A., Naik, S., Cheeseman, P., & Nicolaides, K. H. (1997) · Thorax · doi:10.1136/thx.52.2.181 · Cited by 16 · see citing works
Gamiz, F., & López-Villanueva, J. A. (1995) · Journal of Applied Physics · doi:10.1063/1.360209 · Cited by 15 · see citing works
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Towards the elimination of chronic obstructive pulmonary disease: a Lancet Commission
Stolz, D., Mkorombindo, T., Schumann, D., Agustí, A. G. N., Ash, S. Y., Bafadhel, M., Bai, C., Chalmers, J. D., Criner, G. J., Dharmage, S. C., et al. (2022) · The Lancet · doi:10.1016/s0140-6736(22)01273-9 · Cited by 714 · see citing works
Early-Life Origins of Chronic Obstructive Pulmonary Disease
Martínez, F. D. (2016) · New England Journal of Medicine · doi:10.1056/nejmra1603287 · Cited by 475 · see citing works
Early life origins of chronic obstructive pulmonary disease
Svanes, C., Sunyer, J., Plana, E., Dharmage, S., Heinrich, J., Jarvis, D., de Marco, R., Norback, D., Raherison, C., Villani, S., et al. (2010) · Thorax · doi:10.1136/thx.2008.112136 · Cited by 466 · see citing works
Long-Term Consequences of Fetal and Neonatal Nicotine Exposure: A Critical Review
Bruin, J. E., Gerstein, H. C., & Holloway, A. C. (2010) · Toxicological Sciences · doi:10.1093/toxsci/kfq103 · Cited by 370 · see citing works
Nicotine and the Developing Human
England, L. J., Bunnell, R. E., Pechacek, T. F., Tong, V. T., & McAfee, T. A. (2015) · American Journal of Preventive Medicine · doi:10.1016/j.amepre.2015.01.015 · Cited by 320 · see citing works
Air pollutants and early origins of respiratory diseases
Kim, D., Chen, Z., Zhou, L., & Huang, S. (2018) · Chronic Diseases and Translational Medicine · doi:10.1016/j.cdtm.2018.03.003 · Cited by 303 · see citing works
McEvoy, C. T., & Spindel, E. R. (2016) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2016.08.005 · Cited by 262 · see citing works
Self-citationMacaubas, C., de Klerk, N., Holt, B., Wee, C., Kendall, G., Firth, M., Sly, P., & Holt, P. (2003) · The Lancet · doi:10.1016/s0140-6736(03)14542-4 · Cited by 232 · see citing works
McEvoy, C. T., Schilling, D., Clay, N., Jackson, K., Go, M. D., Spitale, P., Bunten, C., Leiva, M., Gonzales, D., Hollister-Smith, J., et al. (2014) · JAMA · doi:10.1001/jama.2014.5217 · Cited by 217 · see citing works
Self-citationProskocil, B. J., Sekhon, H. S., Jia, Y., Savchenko, V. L., Blakely, R., Lindstrom, J. M., & Spindel, E. R. (2004) · Endocrinology · doi:10.1210/en.2003-1728 · Cited by 200 · see citing works
Self-citationEnvironmental factors and developmental outcomes in the lung
Kajekar, R. (2007) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2007.01.011 · Cited by 195 · see citing works
Antenatal Determinants of Bronchopulmonary Dysplasia and Late Respiratory Disease in Preterm Infants
Morrow, L. A., Wagner, B. D., Ingram, D. A., Poindexter, B. B., Schibler, K. R., Cotten, C. M., Dagle, J. M., Sontag, M. K., Mourani, P. M., & Abman, S. H. (2017) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201612-2414oc · Cited by 193 · see citing works
Maternal Nicotine Exposure Upregulates Collagen Gene Expression in Fetal Monkey Lung
Sekhon, H. S., Keller, J. A., Proskocil, B. J., Martin, E. L., & Spindel, E. R. (2002) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.26.1.4170 · Cited by 191 · see citing works
Self-citationEngland, L. J., Aagaard, K., Bloch, M., Conway, K., Cosgrove, K., Grana, R., Gould, T. J., Hatsukami, D., Jensen, F., Kandel, D., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.013 · Cited by 181 · see citing works
Self-citationThe effect of parental smoking on lung function and development during infancy
Stocks, J., & Dezateux, C. A. (2003) · Respirology · doi:10.1046/j.1440-1843.2003.00478.x · Cited by 174 · see citing works
The effects of nicotine on human fetal development
Holbrook, B. D. (2016) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21128 · Cited by 173 · see citing works
Abbott, L. C., & Winzer‐Serhan, U. H. (2012) · Critical Reviews in Toxicology · doi:10.3109/10408444.2012.658506 · Cited by 170 · see citing works
Bonvillain, R. W., Danchuk, S. D., Sullivan, D. E., Betancourt, A. M., Semon, J. A., Eagle, M. E., Mayeux, J. P., Gregory, A. N., Wang, G., Townley, I. K., et al. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0594 · Cited by 163 · see citing works
Spindel, E. R., & McEvoy, C. T. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201510-2013pp · Cited by 154 · see citing works
Self-citationPrenatal Nicotine Exposure Alters Lung Function and Airway Geometry through α7 Nicotinic Receptors
Wongtrakool, C., Wang, N., Hyde, D. M., Roman, J., & Spindel, E. R. (2012) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2011-0028oc · Cited by 147 · see citing works
Self-citationCatassi, A., Servent, D., Paleari, L., Cesario, A., & Russo, P. (2008) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2008.04.002 · Cited by 146 · see citing works
Nicotine, cigarette smoking and cardiac arrhythmia: an overview
D’Alessandro, A., Boeckelmann, I., Hammwhöner, M., & Goette, A. (2011) · European Journal of Preventive Cardiology · doi:10.1177/1741826711411738 · Cited by 142 · see citing works
Present and Future of Bronchopulmonary Dysplasia
Bonadies, L., Zaramella, P., Porzionato, A., Perilongo, G., Muraca, M., & Baraldi, E. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9051539 · Cited by 138 · see citing works
Early-life origins of chronic respiratory diseases: understanding and promoting healthy ageing
Carraro, S., Scheltema, N. M., Bont, L., & Baraldi, E. (2014) · European Respiratory Journal · doi:10.1183/09031936.00084114 · Cited by 137 · see citing works
Perinatal exposure to nicotine causes deficits associated with a loss of nicotinic receptor function
Cohen, G., Roux, J.-C., Grailhe, R., Malcolm, G., Changeux, J.-P., & Lagercrantz, H. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409782102 · Cited by 134 · see citing works
Maritz, G. S., & Harding, R. (2011) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph8030875 · Cited by 129 · see citing works
Magnusson, L. L., Olesen, A. B., Wennborg, H., & Olsen, J. H. (2005) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2005.02374.x · Cited by 129 · see citing works
A three-generation study on the association of tobacco smoking with asthma
Accordini, S., Calciano, L., Johannessen, A., Portas, L., Benediktsdóttir, B., Bertelsen, R. J., Bråbäck, L., Carsin, A.-E., Dharmage, S. C., Dratva, J., et al. (2018) · International Journal of Epidemiology · doi:10.1093/ije/dyy031 · Cited by 125 · see citing works
Persistent Effects of Maternal Smoking during Pregnancy on Lung Function and Asthma in Adolescents
Hollams, E. M., de Klerk, N. H., Holt, P. G., & Sly, P. D. (2013) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201302-0323oc · Cited by 122 · see citing works
The Adult Incidence of Asthma and Respiratory Symptoms by Passive Smoking In Utero or in Childhood
Skorge, T. D., Eagan, T., Eide, G. E., Gulsvik, A., & Bakke, P. S. (2005) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200409-1158oc · Cited by 114 · see citing works
Guerra, S., Stern, D. A., Zhou, M., Sherrill, D. L., Wright, A. L., Morgan, W. J., & Martínez, F. D. (2013) · Thorax · doi:10.1136/thoraxjnl-2013-203538 · Cited by 111 · see citing works
Yeatts, K., Sly, P. D., Shore, S., Weiss, S. T., Martínez, F. D., Geller, A. M., Bromberg, P. A., Enright, P., Koren, H. S., Weissman, D. N., et al. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.8381 · Cited by 102 · see citing works
Slotkin, T. A., Seidler, F. J., Qiao, D., Aldridge, J. E., Tate, C. A., Cousins, M. M., Proskocil, B. J., Sekhon, H. S., Clark, J. A., Lupo, S. L., et al. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300544 · Cited by 101 · see citing works
Self-citationRehan, V. K., Asotra, K., & Torday, J. S. (2009) · Lung · doi:10.1007/s00408-009-9158-2 · Cited by 93 · see citing works
Maouche, K., Polette, M., Jolly, T., Medjber, K., Cloëz-Tayarani, I., Changeux, J., Burlet, H., Terryn, C., Coraux, C., Zahm, J. M., et al. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.090212 · Cited by 88 · see citing works
Smoking cessation in pregnancy: a continuing challenge in the United States
Scherman, A. J., Tolosa, J. E., & McEvoy, C. T. (2018) · Therapeutic Advances in Drug Safety · doi:10.1177/2042098618775366 · Cited by 85 · see citing works
Wongtrakool, C., Roser-Page, S., Rivera, H. N., & Roman, J. (2007) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00038.2007 · Cited by 82 · see citing works
Is There Evidence for Potential Harm of Electronic Cigarette Use in Pregnancy?
Suter, M., Mastrobattista, J. M., Kahr, M. K., & Aagaard, K. M. (2014) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.23333 · Cited by 80 · see citing works
Vitamin C prevents the effects of prenatal nicotine on pulmonary function in newborn monkeys
Proskocil, B. J., Sekhon, H. S., Clark, J. A., Lupo, S. L., Jia, Y., Hull, W. M., Whitsett, J. A., Starcher, B. C., & Spindel, E. R. (2005) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200408-1029oc · Cited by 76 · see citing works
Self-citationThe impact of tobacco chemicals and nicotine on placental development
Suter, M., & Aagaard, K. M. (2020) · Prenatal Diagnosis · doi:10.1002/pd.5660 · Cited by 80 · see citing works
In utero smoke exposure and impaired response to inhaled corticosteroids in children with asthma
Cohen, R. T., Raby, B. A., Van Steen, K., Fuhlbrigge, A. L., Celedón, J. C., Rosner, B. A., Strunk, R. C., Zeiger, R. S., & Weiss, S. T. (2010) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2010.06.016 · Cited by 76 · see citing works
England, L. J., Anderson, B. L., Tong, V. T., Mahoney, J., Coleman‐Cowger, V. H., Melstrom, P. C., & Schulkin, J. A. (2014) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.05.041 · Cited by 74 · see citing works
Mechanism of nicotine-induced pulmonary fibroblast transdifferentiation
Rehan, V. K., Wang, Y., Sugano, S. K., Romero, S., Chen, X., Santos, J., Khazanchi, A., & Torday, J. S. (2005) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00358.2004 · Cited by 70 · see citing works
Obisesan, O. H., Osei, A. D., Uddin, S. M. I., Dzaye, O., Cainzos-Achirica, M., Mirbolouk, M., Orimoloye, O. A., Sharma, G., Al Rifai, M., Stokes, A., et al. (2020) · American Journal of Preventive Medicine · doi:10.1016/j.amepre.2020.02.015 · Cited by 70 · see citing works
Prenatal Nicotine Exposure Increases GABA Signaling and Mucin Expression in Airway Epithelium
Fu, X. W., Wood, K. J., & Spindel, E. R. (2010) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2010-0109oc · Cited by 66 · see citing works
Self-citationNicotine replacement therapy for smoking cessation during pregnancy
Bar‐Zeev, Y., Lim, L. L., Bonevski, B., Gruppetta, M., & Gould, G. S. (2018) · Medical Journal of Australia · doi:10.5694/mja17.00446 · Cited by 66 · see citing works
Nicotine Activates and Up-Regulates Nicotinic Acetylcholine Receptors in Bronchial Epithelial Cells
Fu, X. W., Lindstrom, J. M., & Spindel, E. R. (2008) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2008-0352oc · Cited by 65 · see citing works
Self-citationParental Smoking and Airway Reactivity in Healthy Infants
Tepper, R. S., Williams, T., Martinez, T., Kisling, J., Coates, C., & Daggy, J. (2004) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200406-711oc · Cited by 62 · see citing works
Slotkin, T. A., Seidler, F. J., & Spindel, E. R. (2011) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2011.02.001 · Cited by 60 · see citing works
Self-citationAltered Breathing Pattern after Prenatal Nicotine Exposure in the Young Lamb
Hafström, O., Milerad, J., & Sundell, H. W. (2002) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.2107082 · Cited by 56 · see citing works
Wu, Z.-X., Hunter, D. D., Kish, V. L., Benders, K. M., Batchelor, T., & Dey, R. D. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0800511 · Cited by 56 · see citing works
Trajectories of Lung Function in Infants and Children: Setting a Course for Lifelong Lung Health
Jordan, B. K., & McEvoy, C. T. (2020) · PEDIATRICS · doi:10.1542/peds.2020-0417 · Cited by 54 · see citing works
Why Do Intrauterine Exposure to Air Pollution and Cigarette Smoke Increase the Risk of Asthma?
Wang, B., Chen, H., Chan, Y. L., Wang, G., & Oliver, B. G. G. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00038 · Cited by 53 · see citing works
Epigenetic and long-term effects of nicotine on biology, behavior, and health
Gould, T. J. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106741 · Cited by 58 · see citing works
PPARγ agonist rosiglitazone prevents perinatal nicotine exposure-induced asthma in rat offspring
Liu, J., Sakurai, R., O'Roark, E. M., Kenyon, N. J., Torday, J. S., & Rehan, V. K. (2011) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00337.2010 · Cited by 51 · see citing works
Tobacco Smoking: Patterns, Health Consequencesfor Adults, and the Long-term Health of the Offspring
Maritz, G. S., & Mutemwa, M. (2012) · Global Journal of Health Science · doi:10.5539/gjhs.v4n4p62 · Cited by 51 · see citing works
McEvoy, C. T., Shorey‐Kendrick, L. E., Milner, K. F., Schilling, D., Tiller, C. J., Vuylsteke, B., Scherman, A. J., Jackson, K., Haas, D. M., Harris, J., et al. (2018) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201805-1011oc · Cited by 51 · see citing works
Self-citationMaritz, G. S. (2008) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20116 · Cited by 50 · see citing works
McEvoy, C. T., Shorey‐Kendrick, L. E., Milner, K. F., Harris, J., Vuylsteke, B., Cunningham, M., Tiller, C. J., Stewart, J., Schilling, D., Brownsberger, J., et al. (2022) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2022.4401 · Cited by 48 · see citing works
Self-citationα7-Nicotinic receptor antagonists at the beginning of a clinical era for NSCLC and Mesothelioma?
Paleari, L., Cesario, A., Fini, M., & Russo, P. (2009) · Drug Discovery Today · doi:10.1016/j.drudis.2009.06.016 · Cited by 45 · see citing works
Singh, S., Chand, H., Langley, R., Mishra, N., Barrett, T., Rudolph, K., Tellez, C., Filipczak, P., Belinsky, S., Saeed, A., et al. (2017) · Journal of Immunology · doi:10.4049/jimmunol.1700014 · Cited by 43 · see citing works
Krebs, M., Sakurai, R., Torday, J. S., & Rehan, V. K. (2010) · Experimental Lung Research · doi:10.3109/01902141003714023 · Cited by 43 · see citing works
Simakajornboon, N., Vlašić, V., Li, H., & Sawnani, H. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00935.2003 · Cited by 42 · see citing works
Accordini, S., Calciano, L., Johannessen, A., Benediktsdóttir, B., Bertelsen, R. J., Bråbäck, L., Dharmage, S. C., Forsberg, B., Real, F. G., Holloway, J. W., et al. (2021) · European Respiratory Journal · doi:10.1183/13993003.02791-2020 · Cited by 41 · see citing works
The effects of antenatal smoking on lung function and respiratory symptoms in infants and children
Milner, A. D., Rao, H., & Greenough, A. (2007) · Early Human Development · doi:10.1016/j.earlhumdev.2007.07.014 · Cited by 41 · see citing works
Altered Lung Development after Prenatal Nicotine Exposure in Young Lambs
Sandberg, K. L., Poole, S. D., Hamdan, A., Arbogast, P. G., & Sundell, H. W. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000136276.52104.61 · Cited by 41 · see citing works
Prenatal Nicotine Exposure and Abnormal Lung Function
Pierce, R. A., & Nguyen, N. M. (2002) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.26.1.f225 · Cited by 40 · see citing works
Perinatal exposure to nicotine and implications for subsequent obstructive lung disease
Maritz, G. S. (2013) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2012.03.006 · Cited by 37 · see citing works
Physiological consequences of intrauterine insults
Kallapur, S. G., & Ikegami, M. (2006) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2006.03.005 · Cited by 37 · see citing works
Nicotine Stimulates Nerve Growth Factor in Lung Fibroblasts through an NFκB-Dependent Mechanism
Wongtrakool, C., Grooms, K., Bijli, K. M., Crothers, K. A., Fitzpatrick, A. M., & Hart, C. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109602 · Cited by 35 · see citing works
Price, L. R., & Martinez, J. (2020) · F1000Research · doi:10.12688/f1000research.20062.2 · Cited by 36 · see citing works
Sarmah, S., Chism, G. W., Vaughan, M. A., Muralidharan, P., Marrs, J. A., & Marrs, K. A. (2016) · Zebrafish · doi:10.1089/zeb.2015.1107 · Cited by 35 · see citing works
Impact of electronic cigarette aerosols on pregnancy and early development
Orzabal, M. R., & Ramadoss, J. (2019) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2019.05.001 · Cited by 36 · see citing works
Perinatal nicotine exposure‐induced transgenerational asthma: Effects of reexposure in F1 gestation
Liu, J., Yu, C., Doherty, T. M., Akbari, O., Allard, P., & Rehan, V. K. (2020) · The FASEB Journal · doi:10.1096/fj.201902386r · Cited by 34 · see citing works
Kuniyoshi, K. M., & Rehan, V. K. (2019) · Birth Defects Research · doi:10.1002/bdr2.1595 · Cited by 35 · see citing works
Singh, M., Gundavarapu, S., Smith, K. R., Chand, H. S., Saeed, A. I., Mishra, N. C., Hutt, J. A., Barrett, E. G., Husain, M., Harrod, K. S., et al. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1306611 · Cited by 34 · see citing works
Sex-specific lung functional changes in adult mice exposed only to second-hand smoke in utero
Noël, A., Xiao, R., Perveen, Z., Zaman, H., Donne, V. L., & Penn, A. L. (2017) · Respiratory Research · doi:10.1186/s12931-017-0591-0 · Cited by 32 · see citing works
Impaired Respiratory Health and Life Course Transitions From Health to Chronic Lung Disease
Liu, G. Y., & Kalhan, R. (2021) · CHEST Journal · doi:10.1016/j.chest.2021.04.009 · Cited by 34 · see citing works
McEvoy, C. T., Milner, K. F., Scherman, A. J., Schilling, D., Tiller, C. J., Vuylsteke, B., Shorey‐Kendrick, L. E., Spindel, E. R., Schuff, R. A., Mitchell, J., et al. (2017) · Contemporary Clinical Trials · doi:10.1016/j.cct.2017.05.008 · Cited by 33 · see citing works
Self-citationSex difference in bronchopulmonary dysplasia of offspring in response to maternal PM2.5 exposure
Yue, H., Ji, X., Ku, T., Li, G., & Sang, N. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.122033 · Cited by 30 · see citing works
Nicotine Modulates Growth Factors and MicroRNA to Promote Inflammatory and Fibrotic Processes
Ebrahimpour, A., Shrestha, S., Bonnen, M., Eissa, N. T., Raghu, G., & Ghebre, Y. T. (2018) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.118.252650 · Cited by 33 · see citing works
Predicting Lung Health Trajectories for Survivors of Preterm Birth
Gibbons, J. T. D., Wilson, A. C., & Simpson, S. J. (2020) · Frontiers in Pediatrics · doi:10.3389/fped.2020.00318 · Cited by 32 · see citing works
Petre, M. A., Petrik, J., Ellis, R., Inman, M. D., Holloway, A. C., & Labiris, N. R. (2011) · International Journal of Toxicology · doi:10.1177/1091581810395332 · Cited by 32 · see citing works
Expression of lynx1 in developing lung and its modulation by prenatal nicotine exposure
Sekhon, H. S., Song, P., Jia, Y., Lindstrom, J., & Spindel, E. R. (2005) · Cell and Tissue Research · doi:10.1007/s00441-005-1077-9 · Cited by 31 · see citing works
Self-citationMcEvoy, C. T., Shorey‐Kendrick, L. E., Milner, K. F., Schilling, D., Tiller, C. J., Vuylsteke, B., Scherman, A. J., Jackson, K., Haas, D. M., Harris, J., et al. (2020) · European Respiratory Journal · doi:10.1183/13993003.02208-2019 · Cited by 31 · see citing works
Self-citationMaritz, G. S. (2009) · Therapeutic Advances in Respiratory Disease · doi:10.1177/1753465809343712 · Cited by 30 · see citing works
Sandberg, K. L., Pinkerton, K. E., Poole, S. D., Minton, P. A., & Sundell, H. W. (2010) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2010.12.015 · Cited by 30 · see citing works
Sex-Specific Perinatal Nicotine-Induced Asthma in Rat Offspring
Liu, J., Naeem, E., Tian, J., Lombardi, V., Kwong, K., Akbari, O., Torday, J. S., & Rehan, V. K. (2013) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2011-0344oc · Cited by 29 · see citing works
Comparison of Biomarkers and Parent Report of Tobacco Exposure to Predict Wheeze
Spanier, A. J., Kahn, R. S., Xu, Y. Y., Hornung, R., & Lanphear, B. P. (2011) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2011.04.025 · Cited by 29 · see citing works
Biological effects of nicotine exposure: A narrative review of the scientific literature
Price, L., & Martinez, J. (2019) · F1000Research · doi:10.12688/f1000research.20062.1 · Cited by 53 · see citing works
Maternal tobacco exposure during pregnancy and allergic rhinitis in offspring
Zhou, Y., Chen, J., Dong, Y., Shen, J., Tian, M., Yang, Y., Song, L., & Li, J. (2021) · Medicine · doi:10.1097/md.0000000000026986 · Cited by 25 · see citing works
Lavezzi, A. M., Corna, M. F., Alfonsi, G., & Matturri, L. (2014) · BMC Pulmonary Medicine · doi:10.1186/1471-2466-14-11 · Cited by 25 · see citing works
PPAR-γ agonist rosiglitazone reverses perinatal nicotine exposure-induced asthma in rat offspring
Liu, J., Sakurai, R., & Rehan, V. K. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00234.2014 · Cited by 25 · see citing works
Chen, X., Zhang, C., Wei, T., Chen, J., Pan, T. S., Li, M., Wang, L., Song, J., Chen, C., Zhang, Y., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.162547 · Cited by 24 · see citing works
Cahill, K. M., Johnson, T. K., Perveen, Z., Schexnayder, M., Xiao, R., Heffernan, L. M., Langohr, I. M., Paulsen, D. B., Penn, A. L., & Noël, A. (2022) · Toxicology · doi:10.1016/j.tox.2022.153272 · Cited by 24 · see citing works
Is it safe to use smoking cessation therapeutics during pregnancy?
Long, N. E. D., Barra, N. G., Hardy, D. B., & Holloway, A. C. (2014) · Expert Opinion on Drug Safety · doi:10.1517/14740338.2014.973846 · Cited by 23 · see citing works
Leone, F. T., Carlsen, K., Folan, P. A., Latzka, K., Munzer, A., Neptune, E., Pakhale, S. S., Sachs, D. P. L., Samet, J. M., Upson, D. J., et al. (2015) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201506-1081st · Cited by 22 · see citing works
Rhoades, N. S., Davies, M., Lewis, S. A., Cinco, I. R., Kohama, S. G., Bermudez, L. E., Winthrop, K. L., Fuss, C., Mattison, J. A., Spindel, E. R., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110725 · Cited by 22 · see citing works
Self-citationCahill, K. M., Gartia, M. R., Sahu, S. P., Bergeron, S. R., Heffernan, L. M., Paulsen, D. B., Penn, A. L., & Noël, A. (2021) · Toxicological Research · doi:10.1007/s43188-021-00103-3 · Cited by 22 · see citing works
Effects of maternal nicotine exposure on lung surfactant system in rats
Chen, C., Wang, L.-F., & Yeh, T. (2004) · Pediatric Pulmonology · doi:10.1002/ppul.20122 · Cited by 22 · see citing works
- Authors
- SEKHON, H. S., KELLER, J. A., BENOWITZ, N. L., & SPINDEL, E. R.
- Affiliations
- Oregon Health & Science University (US)
- Venue
- American Journal of Respiratory and Critical Care Medicine
- Publisher
- Oxford University Press (OUP)
- Published
- 2001-09
- Volume
- 164
- Issue
- 6
- Pages
- 989-994
- ISSN
- 1073-449X (ISSN-L)
- 1535-4970
- OpenAlex
- W2053834750
- Cited by
- 182
- References
- 49
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 9 · 2023: 7 · 2022: 7 · 2021: 6 · 2020: 19 · 2019: 4 · 2018: 11 · 2017: 6 · 2016: 10 · 2015: 5 · 2014: 12 · 2013: 5 · 2012: 8
- FWCI
- 6.33
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Respiratory and Critical Care Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (RR-00163.)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD/HL-37131)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Neonatal Respiratory Health Research
- Keywords
- prenatal nicotine exposure, smoking during pregnancy, lung function, rhesus monkeys, nicotinic acetylcholine receptors, fetal lung development, lung mechanics, pulmonary resistance, lung compliance, lung weight, neonates, fetal lung
- MeSH terms
- Amniotic Fluid, Animals, Animals, Newborn, Body Weight, Chromatography, Gas, Cotinine, Data Interpretation, Statistical, Female, Fetus, Humans, Infant, Newborn, Lung, Lung Compliance, Macaca mulatta, Nicotine, Pregnancy, Respiratory Function Tests, Smoking, Mass Spectrometry
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