{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T12:39:40Z","timestamp":1791895180097,"version":"4.3.4"},"reference-count":52,"publisher":"Oxford University Press (OUP)","issue":"12","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2000,12,15]]},"DOI":"10.1093\/aje\/152.12.1185","type":"journal-article","created":{"date-parts":[[2002,7,26]],"date-time":"2002-07-26T23:02:40Z","timestamp":1027724560000},"page":"1185-1191","source":"Crossref","is-referenced-by-count":34,"title":["Effect of Maternal Smoking and Coffee Consumption on the Risk of Having a Recognized Down Syndrome Pregnancy"],"prefix":"10.1093","volume":"152","author":[{"given":"Claudine P.","family":"Torfs","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberta E.","family":"Christianson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2000,12,15]]},"reference":[{"key":"key\n\t\t\t\t20170408045800_B1","doi-asserted-by":"crossref","unstructured":"Armstrong BG, McDonald AD, Sloan M. Cigarette, alcohol, and coffee consumption and spontaneous abortion. Am J Public Health1992;82:85\u20137.","DOI":"10.2105\/AJPH.82.1.85"},{"key":"key\n\t\t\t\t20170408045800_B2","unstructured":"Stein Z. Early fetal loss. In: Bloom AD, James LS, Paul NW, eds. The fetus and the newborn. New York, NY: Alan R Liss, Inc, 1981:95\u2013111."},{"key":"key\n\t\t\t\t20170408045800_B3","doi-asserted-by":"crossref","unstructured":"Golding J. Reproduction and caffeine consumption\u2013a literature review. Early Hum Dev1995;43:1\u201314.","DOI":"10.1016\/0378-3782(95)01660-U"},{"key":"key\n\t\t\t\t20170408045800_B4","doi-asserted-by":"crossref","unstructured":"Dlugosz L, Bracken MB. Reproductive effects of caffeine: a review and theoretical analysis. Epidemiol Rev1992;14:83\u2013100.","DOI":"10.1093\/oxfordjournals.epirev.a036093"},{"key":"key\n\t\t\t\t20170408045800_B5","doi-asserted-by":"crossref","unstructured":"Fenster L, Eskenazi B, Windham GC, et al. Caffeine consumption during pregnancy and spontaneous abortion. Epidemiology1991;2:168\u201374.","DOI":"10.1097\/00001648-199105000-00002"},{"key":"key\n\t\t\t\t20170408045800_B6","doi-asserted-by":"crossref","unstructured":"Infante-Rivard C, Fernandez A, Gauthier R, et al. Fetal loss associated with caffeine intake before and during pregnancy. JAMA1993;270:2940\u20133.","DOI":"10.1001\/jama.270.24.2940"},{"key":"key\n\t\t\t\t20170408045800_B7","doi-asserted-by":"crossref","unstructured":"Mills JL, Holmes LB, Aarons JH, et al. Moderate caffeine use and the risk of spontaneous abortion and intrauterine growth retardation. JAMA1993;269:593\u20137.","DOI":"10.1001\/jama.269.5.593"},{"key":"key\n\t\t\t\t20170408045800_B8","doi-asserted-by":"crossref","unstructured":"Wilcox AJ, Weinberg CR, Baird DD. Risk factors for early pregnancy loss. Epidemiology1990;1:382\u20135.","DOI":"10.1097\/00001648-199009000-00008"},{"key":"key\n\t\t\t\t20170408045800_B9","doi-asserted-by":"crossref","unstructured":"Wu T, Buck G, Mendola P. Maternal cigarette smoking, regular use of multivitamin\/mineral supplements, and risk of fetal death. Am J Epidemiol1998;148:215\u201321.","DOI":"10.1093\/oxfordjournals.aje.a009626"},{"key":"key\n\t\t\t\t20170408045800_B10","doi-asserted-by":"crossref","unstructured":"Harlap S, Shiono PH. Alcohol, smoking, and incidence of spontaneous abortions in the first and second trimester. Lancet1980;2:173\u20136.","DOI":"10.1016\/S0140-6736(80)90061-6"},{"key":"key\n\t\t\t\t20170408045800_B11","doi-asserted-by":"crossref","unstructured":"Bou\u00e9 J, Bou\u00e9 A, Lazar P. Retrospective and prospective epidemiological studies of 1500 karyotyped spontaneous human abortions. Teratology1975;12:11\u201326.","DOI":"10.1002\/tera.1420120103"},{"key":"key\n\t\t\t\t20170408045800_B12","unstructured":"Hook EB, Mutton DE, Ide R, et al. The natural history of Down syndrome conceptuses diagnosed prenatally that are not electively terminated. Am J Hum Genet1995;57:875\u201381."},{"key":"key\n\t\t\t\t20170408045800_B13","unstructured":"Eiben B, Bartels I, Bahr-Porsch S, et al. Cytogenetic analysis of 750 spontaneous abortions with the direct-preparation method of chorionic villi and its implications for studying genetic causes of pregnancy wastage. Am J Hum Genet1990;47:656\u201363."},{"key":"key\n\t\t\t\t20170408045800_B14","doi-asserted-by":"crossref","unstructured":"Morris JK, Wald NJ, Watt HC. Fetal loss in Down syndrome pregnancies. Prenat Diagn1999;19:142\u20135.","DOI":"10.1002\/(SICI)1097-0223(199902)19:2<142::AID-PD486>3.0.CO;2-7"},{"key":"key\n\t\t\t\t20170408045800_B15","doi-asserted-by":"crossref","unstructured":"Fortier I, Marcoux S, Beaulac-Baillargeon L. Relation of caffeine intake during pregnancy to intrauterine growth retardation and preterm birth. Am J Epidemiol1993;137:931\u201340.","DOI":"10.1093\/oxfordjournals.aje.a116763"},{"key":"key\n\t\t\t\t20170408045800_B16","doi-asserted-by":"crossref","unstructured":"Hatch EE, Bracken MB. Association of delayed conception with caffeine consumption. Am J Epidemiol1993;138:1082\u201392.","DOI":"10.1093\/oxfordjournals.aje.a116826"},{"key":"key\n\t\t\t\t20170408045800_B17","doi-asserted-by":"crossref","unstructured":"Srisuphan W, Bracken MB. Caffeine consumption during pregnancy and association with late spontaneous abortion. Am J Obstet Gynecol1986;154:14\u201320.","DOI":"10.1016\/0002-9378(86)90385-6"},{"key":"key\n\t\t\t\t20170408045800_B18","unstructured":"Yesair DW, Branfman AR, Callahan MM. Human disposition and some biochemical aspects of methylxanthines. In: Spiller GA, ed. The methylxanthine beverages and foods: chemistry, consumption, and health effects. New York, NY: Alan R Liss, Inc, 1984:215\u201333."},{"key":"key\n\t\t\t\t20170408045800_B19","doi-asserted-by":"crossref","unstructured":"Brown C, Jacob P, Wilson M, et al. Changes in rate and pattern of caffeine metabolism after cigarette abstinence. Clin Pharmacol Ther1988;43:488\u201391.","DOI":"10.1038\/clpt.1988.63"},{"key":"key\n\t\t\t\t20170408045800_B20","doi-asserted-by":"crossref","unstructured":"Parsons WD, Neims AH. Effect of smoking on caffeine clearance. Clin Pharmacol Ther1978;24:40\u20135.","DOI":"10.1002\/cpt197824140"},{"key":"key\n\t\t\t\t20170408045800_B21","doi-asserted-by":"crossref","unstructured":"Bracken MB, Leaderer B, Belanger K. Role of biologic markers in epidemiologic studies of prenatal drug exposure: issues in study design. NIDA Res Monogr1992;117:41\u201360.","DOI":"10.1037\/e496172006-006"},{"key":"key\n\t\t\t\t20170408045800_B22","doi-asserted-by":"crossref","unstructured":"Fenster L, Quale C, Hiatt RA, et al. Rate of caffeine metabolism and risk of spontaneous abortion. Am J Epidemiol1998;147:503\u201310.","DOI":"10.1093\/oxfordjournals.aje.a009477"},{"key":"key\n\t\t\t\t20170408045800_B23","doi-asserted-by":"crossref","unstructured":"Benowitz NL, Hall SM, Modin G. Persistent increase in caffeine concentrations in people who stop smoking. BMJ1989;298:1075\u20136.","DOI":"10.1136\/bmj.298.6680.1075"},{"key":"key\n\t\t\t\t20170408045800_B24","doi-asserted-by":"crossref","unstructured":"Stanton CK, Gray RH. Effects of caffeine consumption on delayed conception. Am J Epidemiol1995;142:1322\u20139.","DOI":"10.1093\/oxfordjournals.aje.a117600"},{"key":"key\n\t\t\t\t20170408045800_B25","doi-asserted-by":"crossref","unstructured":"Jensen TK, Henriksen TB, Hjollund NH, et al. Caffeine intake and fecundability: a follow-up study among 430 Danish couples planning their first pregnancy. Reprod Toxicol1998;12:289\u201395.","DOI":"10.1016\/S0890-6238(98)00002-1"},{"key":"key\n\t\t\t\t20170408045800_B26","doi-asserted-by":"crossref","unstructured":"Wilcox A, Weinberg C, Baird D. Caffeinated beverages and decreased fertility. Lancet1988;2:1453\u20135.","DOI":"10.1016\/S0140-6736(88)90933-6"},{"key":"key\n\t\t\t\t20170408045800_B27","doi-asserted-by":"crossref","unstructured":"Curtis KM, Savitz DA, Arbuckle TE. Effects of cigarette smoking, caffeine consumption, and alcohol intake on fecundability. Am J Epidemiol1997;146:32\u201341.","DOI":"10.1093\/oxfordjournals.aje.a009189"},{"key":"key\n\t\t\t\t20170408045800_B28","unstructured":"SAS Institute, Inc. SAS\/STAT users guide, version 6. 4th ed. Cary, NC: SAS Institute, Inc, 1989."},{"key":"key\n\t\t\t\t20170408045800_B29","doi-asserted-by":"crossref","unstructured":"Snijders RJ, Holzgreve W, Cuckle H, et al. Maternal age-specific risks for trisomies at 9\u201314 weeks' gestation. Prenat Diagn1994;14:543\u201352.","DOI":"10.1002\/pd.1970140706"},{"key":"key\n\t\t\t\t20170408045800_B30","doi-asserted-by":"crossref","unstructured":"Bishop J, Huether CA, Torfs C, et al. Epidemiologic study of Down syndrome in a racially diverse California population, 1989\u20131991. Am J Epidemiol1997;145:134\u201347.","DOI":"10.1093\/oxfordjournals.aje.a009084"},{"key":"key\n\t\t\t\t20170408045800_B31","doi-asserted-by":"crossref","unstructured":"Wilson MG, Chan LS, Herbert WS. Birth prevalence of Down syndrome in a predominantly Latino population: a 15-year study. Teratology1992;45:285\u201392.","DOI":"10.1002\/tera.1420450307"},{"key":"key\n\t\t\t\t20170408045800_B32","unstructured":"Hook EB, Cross PK. Maternal cigarette smoking, Down syndrome in live births, and infant race. Am J Hum Genet1988;42:482\u20139."},{"key":"key\n\t\t\t\t20170408045800_B33","doi-asserted-by":"crossref","unstructured":"Sigler AT, Cohen BH, Lilienfeld AM, et al. Reproductive and marital experience of parents of children with Down's syndrome (mongolism). J Pediatr1967;70:608\u201314.","DOI":"10.1016\/S0022-3476(67)80046-5"},{"key":"key\n\t\t\t\t20170408045800_B34","doi-asserted-by":"crossref","unstructured":"Stoll C, Alembik Y, Dott B, et al. Epidemiology of Down syndrome in 118,265 consecutive births. Am J Med Genet1990;7:79\u201383.","DOI":"10.1002\/ajmg.1320370715"},{"key":"key\n\t\t\t\t20170408045800_B35","doi-asserted-by":"crossref","unstructured":"Harlap S. A time-series analysis of the incidence of Down's syndrome in West Jerusalem. Am J Epidemiol1974;99:210\u201317.","DOI":"10.1093\/oxfordjournals.aje.a121604"},{"key":"key\n\t\t\t\t20170408045800_B36","doi-asserted-by":"crossref","unstructured":"Smith A, Record RG. Fertility and reproductive history of mothers of mongol defectives. Br J Prev Soc Med1955;9:89\u201396.","DOI":"10.1136\/jech.9.2.89"},{"key":"key\n\t\t\t\t20170408045800_B37","doi-asserted-by":"crossref","unstructured":"K\u00e4llen K. Parity and Down syndrome. Am J Med Genet1997;70:196\u2013201.","DOI":"10.1002\/(SICI)1096-8628(19970516)70:2<196::AID-AJMG17>3.0.CO;2-E"},{"key":"key\n\t\t\t\t20170408045800_B38","doi-asserted-by":"crossref","unstructured":"Schimmel MS, Eidelman AI, Zadka P, et al. Increased parity and risk of trisomy 21: review of 37,110 live births. BMJ1997;314:720\u20131.","DOI":"10.1136\/bmj.314.7082.720"},{"key":"key\n\t\t\t\t20170408045800_B39","doi-asserted-by":"crossref","unstructured":"Faden VB, Graubard BI, Dufour M. The relationship of drinking and birth outcome in a US national sample of expectant mothers. Paediatr Perinat Epidemiol1997;11:167\u201380.","DOI":"10.1046\/j.1365-3016.1997.d01-20.x"},{"key":"key\n\t\t\t\t20170408045800_B40","doi-asserted-by":"crossref","unstructured":"Hakim RB, Gray RH, Zacur H. Alcohol and caffeine consumption and decreased fertility. Fertil Steril1998;70:632\u20137.","DOI":"10.1016\/S0015-0282(98)00257-X"},{"key":"key\n\t\t\t\t20170408045800_B41","doi-asserted-by":"crossref","unstructured":"Klebanoff MA, Levine RJ, DerSimonian R, et al. Maternal serum paraxanthine, a caffeine metabolite, and the risk of spontaneous abortion. N Engl J Med1999;341:1639\u201344.","DOI":"10.1056\/NEJM199911253412202"},{"key":"key\n\t\t\t\t20170408045800_B42","doi-asserted-by":"crossref","unstructured":"Kline J, Levin B, Stein Z, et al. Cigarette smoking and trisomy 21 at amniocentesis. Genet Epidemiol1993;10:35\u201342.","DOI":"10.1002\/gepi.1370100105"},{"key":"key\n\t\t\t\t20170408045800_B43","doi-asserted-by":"crossref","unstructured":"K\u00e4llen K. Down's syndrome and maternal smoking in early pregnancy. Genet Epidemiol1997;14:77\u201384.","DOI":"10.1002\/(SICI)1098-2272(1997)14:1<77::AID-GEPI6>3.0.CO;2-2"},{"key":"key\n\t\t\t\t20170408045800_B44","doi-asserted-by":"crossref","unstructured":"Baillargeon-Beaulac L, Desrosiers C. Caffeine-cigarette interaction on fetal growth. Am J Obstet Gynecol1987;157:1236\u201340.","DOI":"10.1016\/S0002-9378(87)80301-0"},{"key":"key\n\t\t\t\t20170408045800_B45","doi-asserted-by":"crossref","unstructured":"Alderete E, Eskenazi B, Sholtz R. Effect of cigarette smoking and coffee drinking on time to conception. Epidemiology1995;6:403\u20138.","DOI":"10.1097\/00001648-199507000-00013"},{"key":"key\n\t\t\t\t20170408045800_B46","doi-asserted-by":"crossref","unstructured":"Pianezza ML, Sellers EM, Tyndale RF. Nicotine metabolism defect reduces smoking. (Letter). Nature1998;393:750.","DOI":"10.1038\/31623"},{"key":"key\n\t\t\t\t20170408045800_B47","doi-asserted-by":"crossref","unstructured":"Perez-Stable E, Herrera B, Jacob P, et al. Nicotine metabolism and intake in black and white smokers. JAMA1998;280:152\u20136.","DOI":"10.1001\/jama.280.2.152"},{"key":"key\n\t\t\t\t20170408045800_B48","doi-asserted-by":"crossref","unstructured":"Caraballo RS, Giovino GA, Pechacek TF, et al. Racial and ethnic difference in serum cotinine levels of cigarette smokers: Third National Health and Nutrition Examination Survey, 1988\u20131991. JAMA1998;280:135\u20139.","DOI":"10.1001\/jama.280.2.135"},{"key":"key\n\t\t\t\t20170408045800_B49","doi-asserted-by":"crossref","unstructured":"English PB, Eskenazi B, Christianson RE. Black-white differences in serum cotinine levels among pregnant women and subsequent effects on infant birthweight. Am J Public Health1994;84:1439\u201343.","DOI":"10.2105\/AJPH.84.9.1439"},{"key":"key\n\t\t\t\t20170408045800_B50","doi-asserted-by":"crossref","unstructured":"Brazier JL, Ritter J, Berland M, et al. Pharmacokinetics of caffeine during and after pregnancy. Dev Pharmacol Ther1983;6:315\u201322.","DOI":"10.1159\/000457332"},{"key":"key\n\t\t\t\t20170408045800_B51","doi-asserted-by":"crossref","unstructured":"Goldstein A, Warren R. Passage of caffeine into human gonadal and fetal tissues. Biochem Pharmacol1962;17:166\u20138.","DOI":"10.1016\/0006-2952(62)90106-5"},{"key":"key\n\t\t\t\t20170408045800_B52","doi-asserted-by":"crossref","unstructured":"Khoury MJ, Flanders WD, James LM, et al. Human teratogens, prenatal mortality, and selection bias. Am J Epidemiol1989;130:361\u201370.","DOI":"10.1093\/oxfordjournals.aje.a115342"}],"container-title":["American Journal of Epidemiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/aje\/article-pdf\/152\/12\/1185\/","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,3,4]],"date-time":"2020-03-04T09:47:36Z","timestamp":1583315256000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/aje\/article-lookup\/doi\/10.1093\/aje\/152.12.1185"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2000,12,15]]},"references-count":52,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2000,12,15]]},"published-print":{"date-parts":[[2000,12,15]]}},"URL":"https:\/\/doi.org\/10.1093\/aje\/152.12.1185","relation":{},"ISSN":["1476-6256","0002-9262"],"issn-type":[{"value":"1476-6256","type":"electronic"},{"value":"0002-9262","type":"print"}],"subject":[],"published":{"date-parts":[[2000,12,15]]}}}