Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-30T19:44:28.808Z Has data issue: false hasContentIssue false
  • English
  • Français

Prenatal smoke exposure and mammographic density in mid-life

Published online by Cambridge University Press:  10 November 2011

M. B. Terry ,
C. A. Schaefer ,
J. D. Flom ,
Y. Wei ,
P. Tehranifar ,
Y. Liao ,
S. Buka  and
K. B. Michels
M. B. Terry*
Affiliation:
Department of Epidemiology, Columbia University Medical Center, Mailman School of Public Health, New York, NY, USA Herbert Irving Comprehensive Cancer Center, Columbia Medical Center, New York, NY, USA The Imprints Center for Genetic and Environmental Lifecourse Studies, Columbia University, Mailman School of Public Health, New York, USA
C. A. Schaefer
Affiliation:
Kaiser Permanente Division of Research, 2000 Broadway, Oakland, CA, USA
J. D. Flom
Affiliation:
Department of Epidemiology, Columbia University Medical Center, Mailman School of Public Health, New York, NY, USA
Y. Wei
Affiliation:
Herbert Irving Comprehensive Cancer Center, Columbia Medical Center, New York, NY, USA Department of Biostatistics, Columbia University Medical Center, Mailman School of Public Health, New York, NY, USA
P. Tehranifar
Affiliation:
Department of Epidemiology, Columbia University Medical Center, Mailman School of Public Health, New York, NY, USA Herbert Irving Comprehensive Cancer Center, Columbia Medical Center, New York, NY, USA
Y. Liao
Affiliation:
Department of Epidemiology, Columbia University Medical Center, Mailman School of Public Health, New York, NY, USA
S. Buka
Affiliation:
Department of Epidemiology, Brown University, Providence, RF, USA
K. B. Michels
Affiliation:
Department of Obstetrics, Gynecology and Reproductive Biology, Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA Division of Cancer Epidemiology, Comprehensive Cancer Center Freiburg, Freiburg University, Germany
*
*Address for correspondence: Dr M. B. Terry, Department of Epidemiology, Columbia University, Mailman School of Public Health, 722 West 168th Street, Room 724 A, New York, NY 10032, USA. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Tobacco smoke has both carcinogenic effects and anti-estrogenic properties and its inconsistent association with breast cancer risk in observational studies may be because of these competing effects across the lifecourse. We conducted a prospective study of prenatal smoke exposure, childhood household smoke exposure, and adult active smoke exposure and mammographic density, a strong intermediate marker of breast cancer risk, in an adult follow-up of existing US birth cohorts. Specifically, we followed up women who were born between 1959 and 1967 and whose mothers participated in either the Collaborative Perinatal Project (Boston and Providence sites) or the Childhood Health and Development Study in California. Of the 1134 women interviewed in adulthood (ranging in age from 39 to 49 years at interview), 79% had a screening mammogram. Cigarette smoking was reported by mothers at the time of their pregnancy; 40% of mothers smoked while pregnant. Women whose mothers smoked during pregnancy had a 3.1% (95% confidence interval (CI) = −6.0%, −0.2%) lower mammographic density than women whose mothers did not smoke during pregnancy. When we further accounted for adult body mass index and adult smoking status, the association remained (β = −2.7, 95% CI = −5.0, −0.3). When we examined patterns of smoking, prenatal smoke exposure without adult smoke exposure was associated with a 5.6% decrease in mammographic density (β = −5.6, 95% CI = −9.6, −1.6). Given the strength of mammographic density as an intermediate marker for breast cancer, the inverse associations between mammographic density and smoking patterns across the lifecourse may help explain the complex association between cigarette smoking and breast cancer risk.

Keywords

breast cancermammographic densityprenatal smoke exposure
Type
Original Articles
Information
Journal of Developmental Origins of Health and Disease , Volume 2 , Special Issue 6: The Early Determinants of Adult Health Study , December 2011 , pp. 340 - 352
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Terry, PD, Miller, AB, Rohan, TE. Cigarette smoking and breast cancer risk: a long latency period? Int J Cancer. 2002; 100, 723–728.Google Scholar
2. Johnson, KC, Miller, AB, Collishaw, NE, et al. Active smoking and secondhand smoke increase breast cancer risk: the report of the Canadian Expert Panel on Tobacco Smoke and Breast Cancer Risk (2009). Tob Control. 2011; 20, e2, 1–6.CrossRefGoogle Scholar
3. Terry, PD, Goodman, M. Is the association between cigarette smoking and breast cancer modified by genotype? A review of epidemiologic studies and meta-analysis. Cancer Epidemiol Biomarkers Prev. 2006; 15, 602–611.Google Scholar
4. Shen, J, Gammon, MD, Terry, MB, et al. Polymorphisms in XRCC1 modify the association between polycyclic aromatic hydrocarbon–DNA adducts, cigarette smoking, dietary antioxidants, and breast cancer risk. Cancer Epidemiol Biomarkers Prev. 2005; 14, 336–342.CrossRefGoogle ScholarPubMed
5. Shen, J, Terry, MB, Gammon, MD, et al. MGMT genotype modulates the associations between cigarette smoking, dietary antioxidants and breast cancer risk. Carcinogenesis. 2005; 26, 2131–2137.Google Scholar
6. Terry, MB, Gammon, MD, Zhang, FF, et al. Polymorphism in the DNA repair gene XPD, polycyclic aromatic hydrocarbon–DNA adducts, cigarette smoking, and breast cancer risk. Cancer Epidemiol Biomarkers Prev. 2004; 13, 2053–2058.CrossRefGoogle ScholarPubMed
7. Breast Cancer Family Registry, Kathleen Cuningham Consortium for Research into Familial Breast Cancer (Australasia) and Ontario Cancer Genetics Network (Canada). Smoking and risk of breast cancer in carriers of mutations in BRCA1 or BRCA2 aged less than 50 years. Breast Cancer Res Treat. 2008; 109, 67–75.Google Scholar
8. Bissonauth, V, Shatenstein, B, Fafard, E, et al. Weight history, smoking, physical activity and breast cancer risk among French–Canadian women non-carriers of more frequent BRCA1/2 mutations. J Cancer Epidemiol. 2009; 2009, 1–11.Google Scholar
9. Baron, JA, La Vecchia, C, Levi, F. The antiestrogenic effect of cigarette smoking in women. Am J Obstet Gynecol. 1990; 162, 502–514.CrossRefGoogle ScholarPubMed
10. Band, PR, Le, ND, Fang, R, Deschamps, M. Carcinogenic and endocrine disrupting effects of cigarette smoke and risk of breast cancer. Lancet. 2002; 360, 1044–1049.Google Scholar
11. Xue, F, Willett, WC, Rosner, BA, Hankinson, SE, Michels, KB. Cigarette smoking and the incidence of breast cancer. Arch Intern Med. 2011; 171, 125–133.Google Scholar
12. Xue, F, Michels, KB. Intrauterine factors and risk of breast cancer: a systematic review and meta-analysis of current evidence. Lancet Oncol. 2007; 8, 1088–1100.CrossRefGoogle ScholarPubMed
13. Forman, MR, Cantwell, MM, Ronckers, C, Zhang, Y. Through the looking glass at early-life exposures and breast cancer risk. Cancer Invest. 2005; 23, 609–624.CrossRefGoogle Scholar
14. Herbst, AL, Ulfelder, H, Poskanzer, DC. Adenocarcinoma of the vagina: association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med. 1971; 284, 878–881.CrossRefGoogle ScholarPubMed
15. Giusti, RM, Iwamoto, K, Hatch, EE. Diethylstibestrol revisted: a review of the long-term health effects. Ann Intern Med. 1995; 122, 778–788.CrossRefGoogle Scholar
16. Hatch, EE, Palmer, JR, Titus-Ernstoff, L, Noller, KL, et al. Cancer risk in women exposed to diethylstilbestrol in utero. JAMA. 1998; 280, 630–634.Google Scholar
17. Anbazhagan, R, Nathan, B, Gusterson, BA. Prenatal influences and breast cancer [letter; comment]. Lancet. 1992; 340, 1477–1478.Google Scholar
18. Anbazhagan, R, Gusterson, BA. Prenatal factors may influence predisposition to breast cancer. Eur J Cancer. 1994; 30A, 1–3.CrossRefGoogle ScholarPubMed
19. Standfast, SJ. Birth characteristics of women dying from breast cancer. J Natl Cancer Inst. 1967; 39, 33–42.Google Scholar
20. Rothman, KJ, MacMahon, B, Lin, TM, et al. Maternal age and birth rank of women with breast cancer. J Natl Cancer Inst. 1980; 65, 719–722.CrossRefGoogle ScholarPubMed
21. Thompson, WD, Janerich, DT. Maternal age at birth and risk of breast cancer in daughters. Epidemiology. 1990; 1, 101–106.CrossRefGoogle ScholarPubMed
22. Janerich, DT, Hayden, CL, Thompson, WD, Selenskas, SL, Mettlin, C. Epidemiologic evidence of the perinatal influence in the etiology of adult cancers. Clin Epidemiol. 1989; 42, 151–158.CrossRefGoogle ScholarPubMed
23. Hsieh, CC, Tzonou, A, Trichopoulos, D. Birth order and breast cancer risk. Cancer Causes Control. 1991; 2, 95–98.Google Scholar
24. Weiss, HA, Potischman, NA, Brinton, LA, et al. Prenatal and perinatal risk factors for breast cancer in young women. Epidemiology. 1997; 8, 181–187.Google Scholar
25. Swerdlow, AJ, De Stavola, BL, Swanwick, MA, Maconochie, NES. Risks of breast and testicular cancer in young adult twins in England and Wales: evidence on prenatal and genetic aetilogy. Lancet. 1997; 350, 1723–1728.Google Scholar
26. Ekbom, A, Trichopoulos, D, Adami, HO, Hsieh, CC, Lan, SJ. Evidence of prenatal influences on breast cancer risk. Lancet. 1992; 340, 1015–1018.Google Scholar
27. Ekbom, A. Growing evidence that several human cancers may originate in utero. Semin Cancer Biol. 1997; 8, 237–244.CrossRefGoogle Scholar
28. Braun, MM, Ahlbom, A, Floderus, B, Brinton, LA, Hoover, RN. Effect of twinship on incidence of cancer of the testis, breast, and other sites (Sweden). Cancer Causes Control. 1995; 6, 519–524.CrossRefGoogle ScholarPubMed
29. Verkasalo, PK, Kaprio, J, Pukkala, E, Koskenvuo, M. Breast cancer risk in monozygotic and dizygotic female twins: a 20-year population-based cohort study in Finland from 1976 to 1995. Cancer Epidemiol Biomarkers Prev. 1999; 8, 271–274.Google Scholar
30. Michels, KB, Trichopoulos, D, Robins, JM, et al. Birthweight as a risk factor for breast cancer. Lancet. 1996; 348, 1542–1546.Google Scholar
31. Sanderson, M, Williams, MA, Malone, KE, et al. Perinatal factors and risk of breast cancer. Epidemiology. 1996; 7, 34–37.Google Scholar
32. Mogren, I, Damber, L, Tavelin, B, Hogberg, U. Characteristics of pregnancy and birth and malignancy in the offspring (Sweden). Cancer Causes Control. 1999; 10, 85–94.Google Scholar
33. Tehranifar, P, Liao, Y, Flom, JD, Terry, MB. Validity of self-reported birth weight by adult women: sociodemographic influences and implications for life-course studies. Am J Epidemiol. 2009; 170, 910–917.Google Scholar
34. Liu, T, Gatsonis, CA, Baylin, A, Buka, SL. Prenatal exposure to cigarette smoke and benign breast disease. Epidemiology. 2010; 21, 736–743.Google Scholar
35. Sanderson, M, Williams, MA, Daling, JR, et al. Maternal factors and breast cancer risk among young women. Paediatr Perinat Epidemiol. 1998; 12, 397–407.CrossRefGoogle ScholarPubMed
36. Sandler, DP, Everson, RB, Wilcox, AJ, Browder, JP. Cancer risk in adulthood from early life exposure to parents’ smoking. Am J Public Health. 1985; 75, 487–492.Google Scholar
37. Boyd, NF, Guo, H, Martin, LJ, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med. 2007; 356, 227–236.Google Scholar
38. Boyd, NF, Lockwood, GA, Byng, JW, Tritchler, DL, Yaffe, MJ. Mammographic densities and breast cancer risk. Cancer Epidemiol Biomarkers Prev. 1998; 7, 1133–1144.Google ScholarPubMed
39. Boyd, NF, Byng, JW, Jong, RA, et al. Quantitative classification of mammographic densities and breast cancer risk: results from the Canadian National Breast Screening Study. J Natl Cancer Inst. 1995; 87, 670–675.Google Scholar
40. Ciatto, S, Zappa, M. A prospective study of the value of mammographic patterns as indicators of breast cancer risk in a screening experience. Eur J Radiol. 1993; 17, 122–125.Google Scholar
41. Byrne, C, Schairer, C, Wolfe, J, et al. Mammographic features and breast cancer risk: effects with time, age, and menopause status. J Natl Cancer Inst. 1995; 87, 1622–1629.Google Scholar
42. Kato, I, Beinart, C, Bleich, A, et al. A nested case–control study of mammographic patterns, breast volume, and breast cancer (New York City, NY, United States). Cancer Causes Control. 1995; 6, 431–438.Google Scholar
43. Oza, AM, Boyd, NF. Mammographic parencymal patterns: a marker of breast cancer risk. Epidemiol Rev. 1993; 15, 196–208.CrossRefGoogle Scholar
44. Butler, LM, Gold, EB, Conroy, SM, et al. Active, but not passive cigarette smoking was inversely associated with mammographic density. Cancer Causes Control. 2010; 21, 301–311.Google Scholar
45. Bremnes, Y, Ursin, G, Bjurstam, N, Gram, IT. Different measures of smoking exposure and mammographic density in postmenopausal Norwegian women: a cross-sectional study. Breast Cancer Res. 2007; 9(5), R73. 1–8.Google Scholar
46. Jeffreys, M, Warren, R, Gunnell, D, McCarron, P, Smith, GD. Life course breast cancer risk factors and adult breast density (United Kingdom). Cancer Causes Control. 2004; 15, 947–955.Google Scholar
47. Van den Berg, BJ. The California child health and development studies. In Hanbook of Longitudinal Studies (eds. Mednick SA, Harway M, Finello KM), 1984 pp. 166–179. New York, Praeger.Google Scholar
48. Broman, S. The Collaborative Perinatal Project: an overview. In Handbook of Longitudinal Research, Vol. I (eds. Mednick SA, Harway M, Finello KM), 1984, pp. 185–227. Praeger Publishers: New York.Google Scholar
49. Susser, E, Buka, SL, Schaefer, CA, et al. The Early Determinants of Adult Health (EDAH) Study, 2011. DOHAD.Google ScholarPubMed
50. Benirschke, K. Examination of the placenta. Obstet Gynecol. 1961; 18, 309–333.Google Scholar
51. Byng, JW, Boyd, NF, Fishell, E, Jong, RA, Yaffe, MJ. The quantitative analysis of mammographic densities. Phys Med Biol. 1994; 39, 1629–1638.Google Scholar
52. Byng, JW, Boyd, NF, Little, L, et al. Symmetry of projection in the quantitative analysis of mammographic images. Eur J Cancer Prev. 1996; 5, 319–327.Google Scholar
53. Strohsnitter, WC, Noller, KL, Titus-Ernstoff, L, et al. Breast cancer incidence in women prenatally exposed to maternal cigarette smoke. Epidemiology. 2005; 16, 342–345.Google Scholar
54. Ferris, JS, Flom, JD, Tehranifar, P, Mayne, ST, Terry, MB. Prenatal and childhood environmental tobacco smoke exposure and age at menarche. Paediatr Perinat Epidemiol. 2010; 24, 515–523.Google Scholar
55. MacMahon, B, Trichopoulos, D, Cole, P, Brown, J. Cigarette smoking and urinary estrogens. N Engl J Med. 1982; 307, 1062–1065.Google Scholar
56. Evans, P, Wheeler, T, Anthony, F, Osmond, C. Maternal serum vascular endothelial growth factor during early pregnancy. Clin Sci. 1997; 92, 567–571.Google Scholar
57. Kandel, DB, Udry, JR. Prenatal effects of maternal smoking on daughters’ smoking: nicotine or testosterone exposure? Am J Public Health. 1999; 89, 1377–1383.Google Scholar
58. Martin, LJ, Minkin, S, Boyd, NF. Hormone therapy, mammographic density, and breast cancer risk. Maturitas. 2009; 64, 20–26.Google Scholar
59. Galobardes, B, Shaw, M, Lawlor, DA, Lynch, JW, Davey Smith, G. Indicators of socioeconomic position (part 1). J Epidemiol Community Health. 2006; 60, 7–12.CrossRefGoogle ScholarPubMed
60. Giovino, GA. Epidemiology of tobacco use in the United States. Oncogene. 2002; 21, 7326–7340.CrossRefGoogle ScholarPubMed
61. Giovino, GA, Schooley, MW, Zhu, BP, et al. Surveillance for selected tobacco-use behaviors – United States, 1900–1994. MMWR CDC Surveill Summ. 1994; 43, 1–43.Google Scholar
62. Link, BG, Phelan, J. The social shaping of health and smoking. Drug Alcohol Depend. 2009; 104, S6–S10.CrossRefGoogle ScholarPubMed
63. Link, BG. Epidemiological sociology and the social shaping of population health. J Health Soc Behav. 2008; 49, 367–384.Google Scholar
64. Mortensen, LH, Diderichsen, F, Smith, GD, Andersen, AM. The social gradient in birthweight at term: quantification of the mediating role of maternal smoking and body mass index. Hum Reprod. 2009; 24, 2629–2635.Google Scholar
65. Terry, MB, Flom, J, Tehranifar, P, Susser, E. The role of birth cohorts in studies of adult health: the New York women's birth cohort. Paediatr Perinat Epidemiol. 2009; 23, 431–445.Google Scholar
66. Susser, E, Terry, MB, Matte, T. The birth cohorts grow up: new opportunities for epidemiology. Paediatr Perinat Epidemiol. 2000; 14, 98–100.Google Scholar
67. Susser, E, Terry, MB. A conception-to-death cohort. Lancet. 2003; 361, 797–798.Google Scholar
68. Hemachandra, AH, Howards, PP, Furth, SL, Klebanoff, MA. Birth weight, postnatal growth, and risk for high blood pressure at 7 years of age: results from the Collaborative Perinatal Project. Pediatrics. 2007; 119, e1264–e1270.Google Scholar
69. Klebanoff, MA, Zemel, BS, Buka, S, Zierler, S. Long-term follow-up of participants in the Collaborative Perinatal Project: tracking the next generation. Paediatr Perinat Epidemiol. 1998; 12, 334–346.Google Scholar