Abstract
Embryonic movements (EM) are considered to be the first sign of life and cigarette smoking during pregnancy has been linked to affect EM. Exposure to sidestream smoke, produced from the emissions of a smoldering cigarette, may result in poor pregnancy outcome and increased risk of serious perinatal morbidity and mortality. In this study, the chicken embryo bioassay was used to systematically assess the effects of short-term exposure to sidestream whole smoke solutions (SSWSS) on EM, recorded in real time by a video camera for 60 min and each EM was counted for every 3-min interval. Application of different types of SSWSS to the embryos caused significant changes in all types of EM from 15 to 18 min of recording time. Extensive reduction (P<0.001) and some time complete stoppage of swing-like movements and whole-body movements were observed in almost all treated embryos. Our data clearly link between exposure of SSWSS and substantial decrease in EM. It is unclear whether nicotine and/or other ingredients present in sidestream smoke are responsible for these alterations in EM. This article provides an outline of the relevance of SSWSS on EM for evolutionary developmental biology and this assay can be used to investigate the complex mixtures with regard to their effects on EM.
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References
ACOG Practice bulletin (2000) Antepartum fetal surveillance. Clinical management guidelines for obstetrician-gynecologists. Int J Gynaecol Obstet 68:175–185
Baker RR (1984) The effect of ventilation on cigarette combustion mechanisms. Recent Adv Tobacco Sci 10:88–150
Bartal M (2001) Health effects of tobacco use and exposure. Monaldi Arch Chest Dis 56(6):545–554
Baskett TF, Liston RM (1989) Fetal movement monitoring: clinical application. Clin Perinatol 16:613–625
Bekoff A (1992) Neuroethological approaches to the study of motor development in chicks: achievements and challenges. J Neurobiol 23:1486–1505
Bhat RV, Turner SL, Selvaag SR, Marks MJ, Collins AC (1991) Regulation of brain nicotinic receptors by chronic agonist infusion. J Neurochem 56:1932–1939
Bos AF, Einspieler C, Prechtl HF (2001) Intrauterine growth retardation, general movements, and neurodevelopmental outcome: a review. Dev Med Child Neurol 43:61–68
Churg DF, Prior WA (1985) Free radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect 64:111–126
DiFranza JR, Lew RA (1995) Effect of maternal cigarette smoking on pregnancy complications and sudden infant death syndrome. J Family Pract 40:385–394
Dube M, Green CR (1982) Methods of collections of smoke for analytical purposes. Recent Adv Tobacco Sci 8:42–102
Eckstein LW, Shibley IA, Pennington JS, Carver FM, Pennington SN (1997) Changes in brain glucose levels and glucose transporter protein isoforms in alcohol- or nicotine-treated chick embryos. Dev Brain Res 103:59–65
Economides D, Braithwaite J (1994) Smoking, pregnancy and the fetus. J R Soc Health 114(4):198–201
Ehrström C (1979) Fetal movement monitoring in normal and high-risk pregnancy. Acta Obstet Gynecol Scand 80:1–32
Ejaz S, Kim BS, Lim CW (2005) Toxicological effects of mainstream whole smoke solutions on embryonic movements of the developing embryo. Drug Chem Toxicol 28(1):1–15
EPA (1992) Respiratory health effects of passive smoking: lung cancer and other disorders. 1992, Report Number EPA/ 600/6–90/006F:3.1–3.1
Ernst M, Moolchan ET, Robinson ML (2001) Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 40(6):630– 641
Gusella JL, Fried PA (1984) Effects of maternal social drinking and smoking on offspring at 13 months. Neurobehav Toxicol Teratol 6:13–17
Habek D, Habek JC, Ivanisevic M, Djelmis J (2002) Fetal tobacco syndrome and perinatal outcome. Fetal Diagn Ther 17(6):367–371
Hamburger V (1963) Some aspects of the embryology of behaviour. Q Rev Biol 38:342–365
Hamburger V, Balaban M (1963) Observations and experiments on spontaneous rhythmical behavior in the chick embryo. Dev Biol 7:533–545
Hamburger V, Oppenheim RW (1967) Prehatching motility and hatching behavior in the chick. J Exp Zool 166:171–204
Hamburger V, Balaban M, Oppenheim R, Wenger E (1965) Periodic motility of normal and spinal chick embryos between 8 and 17 days of incubation. J Exp Zool 159:1–14
Harrington K, Thompson O, Jordan L, Page J, Carpenter RG, Campbell S (1998) Obstetric outcome in women who present with a reduction in fetal movements in the third trimester of pregnancy. J Perinat Med 26:77–82
Hijar MA, Costa-e-Silva VL (1991) Epidemiologia do tabagismo no Brasil. JBM 60:50–71
Law RL, Hackshaw AK (1996) Environmental tobacco smoke. Br Med Bull 52:22–34
Leader LR, Baillie P, VanSchalkwyk DJ (1981) Fetal movements and fetal outcome: a prospective study. Obstet Gynecol 57:431–436
Leston GW, Rosenberg KD, Wu L (2002) Association between smoking during pregnancy and breast feeding at about 2 weeks of age. J Hum Lact 18(4):368–372
Lichtensteiger W, Ribary U, Schlumpf M, Odermatt B, Widmer HR (1988) Prenatal adverse effects of nicotine on the developing brain. Prog Brain Res 73:137–157
Lofroth G (1989) Environmental tobacco smoke: overview of chemical composition and genotoxic components. Mutat Res 222:73–80
Luck W, Nau H, Hansen R, Steldinger R (1985) Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev Pharmacol Ther 8:384–395
Marsal K (1983) Ultrasonic assessment of fetal activity. Clin Obstet Gynaecol 10:541–563
Moore TR, Piacquadio K (1989) A prospective evaluation of fetal movement screening to reduce the incidence of antepartum fetal death. Am J Obstet Gynecol 160:1075–1080
Nordberg A, Zhang XA, Fredriksson A, Eriksson P (1991) Neonatal nicotine exposure induces permanent changes in brain nicotinic receptors and behaviour in adult mice. Dev Brain Res 63:201–207
Olsen J (1992) Cigarette smoking in pregnancy and fetal growth. Does the type of tobacco play a role? Int J Epidemiol 21:279–284
Pauly JR, Marks MJ, Gross SD, Collins AC (1991) An autoradiographic analysis of cholinergic receptors in mouse brain after chronic nicotine treatment. J Pharmacol Exp Ther 258:1127–1136
Pearson JF, Weaver JB (1976) Fetal activity and fetal wellbeing: an evaluation. Br Med J 1:1305–1307
Peng X, Gerzanich V, Anand R, Whiting PG, Lindstrom J (1994) Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol Pharmacol 46:523–530
Pennington N, Sandstrom LP, Shibley IA, Long SD, Beeker KR, Smith CP, Lee K, Jones TA, Cummings KM, Means LW (1994) Biochemical changes, early brain growth suppression and impaired detour learning in nicotine-treated chicks. Dev Brain Res 83:181–189
Pirkle JL, Flegal KM, Bernert JT, Brody DJ, Etzel RA, Maurer KR (1996) Exposure of the US population to environmental tobacco smoke: the Third National Health and Nutrition Examination Survey, 1988 to 1991. JAMA 275:1233–1240
Rayburn WF (1990) Fetal body movement monitoring. Obstet Gynecol Clin North Am 17:95–110
Ribatti D, Nico B, Vacca A, Roncali L, Burri PH, Djonov V (2001) Chorioallantoic membrane capillary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo. Anat Rec 264:317–324
de Roode DF, Balk L, Koeman JH, Bosveld ATC (2000) Development of a bioassay to test the possible role of thiamine disturbance as a mechanism behind pollution-induced reproductive failures in birds. Arch Environ Contam Toxicol 39:386–391
Sadovsky E, Yaffe H (1973) Daily fetal movement recording and fetal prognosis. Obstet Gynecol 41:845–850
Scherer G, Conze C, Meyrinck LV (1990) Importance of exposure to gaseous and particulate phase components of tobacco smoke in active and passive smokers. Arch Occup Environ Health 62:459–466
Soothill PW, Ajayi RA, Campbell S, Ross EM, Nicolaides KH (1995) Fetal oxygenation at cordocentesis, maternal smoking, and childhood neuro-development. Eur J Obstet Gynaecol Reprod Biol 59:21–24
Su Y, Han W, Giraldo C, DeLi Y, Block ER (1998) Effect of cigarette smoke extract on nitric oxide synthase in pulmonary artery endothelial cells. Am J Respir Cell Mol Biol 19:819–825
Thaler I, Goodman JD, Dawes GS (1980) Effects of maternal cigarette smoking on fetal breathing and fetal movements. Am J Obstet Gynecol 138:282–287
Valentin L, Marsal K (1987) Pregnancy outcome in women perceiving decreased fetal movement. Eur J Obstet Gynecol Reprod Biol 24:23–32
Valentin L, Marsal K, Wahlgren L (1986) Subjective recording of fetal movements. III. Screening of a pregnant population; the clinical significance of decreased fetal movement counts. Acta Obstet Gynecol Scand 65:753–758
Visintini F, Levi-Montalcini R (1939) Relazione tra differenziazione strutturale e funzionale dei centri e delle vie nervose nell’ embrione di pollo. Schweiz Archiv Neurol Psychol 43:1–45
Weiss ST, Tager IB, Schenker M, Speizer FE (1983) The health effects of involuntary smoking. Am Rev Respir Dis 128:933–942
Witschi H, Joad JP, Pinkerton KE (1997) The toxicology of environmental tobacco smoke. Annu Rev Pharmacol Toxicol 37:29–52
Xu Z, Seidler FJ, Ali SF, Slikker JrW, Slotkin TA (2001) Fetal and adolescent nicotine administration: effects on CNS serotonergic systems. Brain Res 914:166–178
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This study was financially supported by Korean Research Foundation Grant (KRF-2004-04-1-56).
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Ejaz, S., Woong, L.C. Diminished embryonic movements of developing embryo by direct exposure of sidestream whole smoke solutions. Arch Toxicol 80, 107–114 (2006). https://doi.org/10.1007/s00204-005-0012-x
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DOI: https://doi.org/10.1007/s00204-005-0012-x