Skip to main content
Log in

Smoking, physical exercise, BMI and late foetal death: a study within the Danish National Birth Cohort

  • PERINATAL EPIDEMIOLOGY
  • Published:
European Journal of Epidemiology Aims and scope Submit manuscript

Abstract

The aim of this paper was to estimate the effect of maternal and paternal smoking on foetal death (miscarriage and stillbirth) and to estimate potential interactions with physical exercise and pre-pregnancy body mass index. We selected 87,930 pregnancies from the population-based Danish National Birth Cohort. Information about lifestyle, occupational, medical and obstetric factors was obtained from a telephone interview and data on pregnancy outcomes came from the Danish population based registries. Cox regression was used to estimate the hazard ratios (adjusted for potential confounders) for predominantly late foetal death (miscarriage and stillbirth). An interaction contrast ratio was used to assess potential effect measure modification of smoking by physical exercise and body mass index. The adjusted hazard ratio of foetal death was 1.22 (95 % CI 1.02–1.46) for couples where both parents smoked compared to non-smoking parents (miscarriage: 1.18, 95 % CI 0.96–1.44; stillbirth: 1.32, 95 % CI 0.93–1.89). On the additive scale, we detected a small positive interaction for stillbirth between smoking and body mass index (overweight women). In conclusion, smoking during pregnancy was associated with a slightly higher hazard ratio for foetal death if both parents smoked. This study suggests that smoking may increase the negative effect of a high BMI on foetal death, but results were not statistically significant for the interaction between smoking and physical exercise.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

BMI:

Body mass index

CI:

Confidence interval

DMBR:

Danish Medical Birth Registry

DNBC:

Danish National Birth Cohort

GP:

General practitioner

HR:

Hazard ratio

HRa:

Adjusted hazard ratio

ICR:

Interaction contrast ratio

M+− and F+−:

Smoking status among mothers and fathers

NHDR:

National Hospital Discharge Register

References

  1. Hocher B, Slowinski T, Bauer C, Halle H. The advanced fetal programming hypothesis. Nephrol Dial Transplant. 2001;16(6):1298–9. doi:10.1093/ndt/16.6.1298.

    Article  CAS  PubMed  Google Scholar 

  2. Hocher B. More than genes: the advanced fetal programming hypothesis. J Reprod Immunol. 2014;104–105:8–11. doi:10.1016/j.jri.2014.03.001.

    Article  PubMed  Google Scholar 

  3. Sun Y, Che Y, Gao E, Olsen J, Zhou W. Induced abortion and risk of subsequent miscarriage. Int J Epidemiol. 2003;32(3):449–54. doi:10.1093/ije/dyg093.

    Article  PubMed  Google Scholar 

  4. Liew Z, Olsen J, Cui X, Ritz B, Arah OA. Bias from conditioning on live birth in pregnancy cohorts: an illustration based on neurodevelopment in children after prenatal exposure to organic pollutants. Int J Epidemiol. 2015;. doi:10.1093/ije/dyu249.

    PubMed Central  Google Scholar 

  5. U.S. Department of Health and Human Services. Women and smoking. Atlanta (GA); 2001. http://www.cdc.gov/tobacco/data_statistics/sgr/2001/complete_report/index.htm.

  6. Nabet C, Ancel P-Y, Burguet A, Kaminski M. Smoking during pregnancy and preterm birth according to obstetric history: French national perinatal surveys. Paediatr Perinat Epidemiol. 2005;19(2):88–96. doi:10.1111/j.1365-3016.2005.00639.x.

    Article  PubMed  Google Scholar 

  7. Suzuki K, Sato M, Zheng W, Shinohara R, Yokomichi H, Yamagata Z. Effect of maternal smoking cessation before and during early pregnancy on fetal and childhood growth. J Epidemiol. 2014;24(1):60–6. doi:10.2188/jea.JE20130083.

    Article  PubMed  Google Scholar 

  8. Wisborg K, Kesmodel U, Henriksen TB, Olsen SF, Secher NJ. Exposure to tobacco smoke in utero and the risk of stillbirth and death in the first year of life. Am J Epidemiol. 2001;154(4):322–7. doi:10.1093/aje/154.4.322.

    Article  CAS  PubMed  Google Scholar 

  9. Högberg L, Cnattingius S. The influence of maternal smoking habits on the risk of subsequent stillbirth: is there a causal relation? BJOG. 2007;114(6):699–704. doi:10.1111/j.1471-0528.2007.01340.x.

    Article  PubMed  PubMed Central  Google Scholar 

  10. George L, Granath F, Johansson ALV, Annerén G, Cnattingius S. Environmental tobacco smoke and risk of spontaneous abortion. Epidemiology. 2006;17(5):500–5. doi:10.1097/01.ede.0000229984.53726.33.

    Article  PubMed  Google Scholar 

  11. Rogers JM. Tobacco and pregnancy. Reprod Toxicol. 2009;28(2):152–60. doi:10.1016/j.reprotox.2009.03.012.

    Article  CAS  PubMed  Google Scholar 

  12. U.S. Department of Health and Human Services. The Health Consequences of Smoking—50 Years of Progress. Atlanta (GA); 2014. http://www.surgeongeneral.gov/library/reports/50-years-of-progress/full-report.pdf.

  13. Christiansen OB. Epidemiological, immunogenetic and immunotherapeutic aspects of unexplained recurrent miscarriage. Dan Med Bull. 1997;44(4):396–424.

    CAS  PubMed  Google Scholar 

  14. Warburton D, Fraser FC. Spontaneous abortion risks in man: data from reproductive histories collected in a medical genetics unit. Am J Hum Genet. 1964;16:1–25.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Naylor AF, Warburton D. Sequential analysis of spontaneous abortion. II. Collaborative study data show that gravidity determines a very substantial rise in risk. Fertil Steril. 1979;31(3):282–6.

    Article  CAS  PubMed  Google Scholar 

  16. Wohlfahrt J, Andersen AM, Melbye M. Interval between pregnancies and risk of spontaneous abortion. Epidemiology. 2000;11(1):92–3. doi:10.1097/00001648-200001000-00021.

    Article  CAS  PubMed  Google Scholar 

  17. Chatenoud L, Parazzini F, di Cintio E, Zanconato G, Benzi G, Bortolus R, et al. Paternal and maternal smoking habits before conception and during the first trimester: relation to spontaneous abortion. Ann Epidemiol. 1998;8(8):520–6. doi:10.1016/S1047-2797(98)00017-9.

    Article  CAS  PubMed  Google Scholar 

  18. Venners SA, Wang X, Chen C, Wang L, Chen D, Guang W, et al. Paternal smoking and pregnancy loss: a prospective study using a biomarker of pregnancy. Am J Epidemiol. 2004;159(10):993–1001. doi:10.1093/aje/kwh128.

    Article  PubMed  Google Scholar 

  19. Centers for Disease Control and Prevention. Preventing smoking and exposure to secondhand smoke before, during, and after pregnancy. Atlanta, GA; 2007. http://www.cdc.gov/nccdphp/publications/factsheets/prevention/pdf/smoking.pdf.

  20. Doyne EJ, Ossip-Klein DJ, Bowman ED, Osborn KM, McDougall-Wilson IB, Neimeyer RA. Running versus weight lifting in the treatment of depression. J Consult Clin Psychol. 1987;55(5):748–54. doi:10.1037/0022-006X.55.5.748.

    Article  CAS  PubMed  Google Scholar 

  21. Ussher MH, Taylor AH, Faulkner GEJ. Exercise interventions for smoking cessation. Cochrane Database Syst Rev. 2014;8:CD002295. doi:10.1002/14651858.CD002295.pub5.

    PubMed  Google Scholar 

  22. Marcus BH, Albrecht AE, King TK, Parisi AF, Pinto BM, Roberts M, et al. The efficacy of exercise as an aid for smoking cessation in women: a randomized controlled trial. Arch Intern Med. 1999;159(11):1229–34. doi:10.1001/archinte.159.11.1229.

    Article  CAS  PubMed  Google Scholar 

  23. Hill JS. Effect of a program of aerobic exercise on the smoking behaviour of a group of adult volunteers. Can J Public Health. 1985;76(3):183–6.

    CAS  PubMed  Google Scholar 

  24. Russell PO, Epstein LH, Johnston JJ, Block DR, Blair E. The effects of physical activity as maintenance for smoking cessation. Addict Behav. 1988;13(2):215–8. doi:10.1016/0306-4603(88)90016-0.

    Article  CAS  PubMed  Google Scholar 

  25. American College of Obstetricians and Gynecologists. ACOG Committee opinion. Number 267, January 2002: exercise during pregnancy and the postpartum period. Obstet Gynecol. 2002;99(1):171–3. http://www.ncbi.nlm.nih.gov/pubmed/11777528.

  26. May LE, Suminski RR, Langaker MD, Yeh H-W, Gustafson KM. Regular maternal exercise dose and fetal heart outcome. Med Sci Sports Exerc. 2012;44(7):1252–8. doi:10.1249/MSS.0b013e318247b324.

    Article  PubMed  Google Scholar 

  27. Clapp JF. The course of labor after endurance exercise during pregnancy. Am J Obstet Gynecol. 1990;163(6 Pt 1):1799–805. doi:10.1016/0002-9378(90)90753-T.

    Article  PubMed  Google Scholar 

  28. Gustafson KM, May LE, Yeh H, Million SK, Allen JJB. Fetal cardiac autonomic control during breathing and non-breathing epochs: the effect of maternal exercise. Early Hum Dev. 2012;88(7):539–46. doi:10.1016/j.earlhumdev.2011.12.017.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Rasmussen S, Albrechtsen S, Irgens LM, Dalaker K, Maartmann-Moe H, Vlatkovic L, et al. Risk factors for unexplained antepartum fetal death in Norway 1967–1998. Early Hum Dev. 2003;71(1):39–52. http://www.ncbi.nlm.nih.gov/pubmed/12614949.

  30. Lashen H, Fear K, Sturdee DW. Obesity is associated with increased risk of first trimester and recurrent miscarriage: matched case-control study. Hum Reprod. 2004;19(7):1644–6. http://www.ncbi.nlm.nih.gov/pubmed/15142995.

  31. Nohr EA, Bech BH, Davies MJ, Frydenberg M, Henriksen TB, Olsen J. Prepregnancy obesity and fetal death: a study within the Danish National Birth Cohort. Obstet Gynecol. 2005;106(2):250–9. doi:10.1097/01.AOG.0000172422.81496.57.

    Article  PubMed  Google Scholar 

  32. Olsen J, Melbye M, Olsen SF, Sørensen TI, Aaby P, Andersen AM, et al. The Danish National Birth Cohort—its background, structure and aim. Scand J Public Health. 2001;29(4):300–7. doi:10.1136/bmj.320.7251.1708.

    Article  CAS  PubMed  Google Scholar 

  33. Pedersen CB, Gøtzsche H, Møller JO, Mortensen PB. The Danish Civil Registration System. A cohort of eight million persons. Dan Med Bull. 2006;53(4):441–9.

    PubMed  Google Scholar 

  34. Andersen TF, Madsen M, Jørgensen J, Mellemkjoer L, Olsen JH. The Danish National Hospital Register. A valuable source of data for modern health sciences. Dan Med Bull. 1999;46(3):263–8.

    CAS  PubMed  Google Scholar 

  35. Knudsen LB, Olsen J. The Danish Medical Birth Registry. Dan Med Bull. 1998;45(3):320–3.

    CAS  PubMed  Google Scholar 

  36. Olesen AW, Westergaard JG, Thomsen SG, Olsen J. Correlation between self-reported gestational age and ultrasound measurements. Acta Obstet Gynecol Scand. 2004;83(11):1039–43. doi:10.1111/j.0001-6349.2004.00193.x.

    Article  PubMed  Google Scholar 

  37. Harrell FEJ. Regression modeling strategies: with applications to linear models, logistic and ordinal regression, and survival analysis. 2nd ed. New York, NY: Springer; 2015. doi:10.1007/978-3-319-19425-7.

    Book  Google Scholar 

  38. Rothman KJ, Greenland S, Lash TL. Modern epidemiology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2008.

    Google Scholar 

  39. Zou GY. On the estimation of additive interaction by use of the four-by-two table and beyond. Am J Epidemiol. 2008;168(2):212–24. doi:10.1093/aje/kwn104.

    Article  PubMed  Google Scholar 

  40. Longo LD. Some health consequences of maternal smoking: issues without answers. Birth Defects Orig Artic Ser. 1982;18(3 Pt A):13–31.

    CAS  PubMed  Google Scholar 

  41. Morrow RJ, Ritchie JW, Bull SB. Maternal cigarette smoking: the effects on umbilical and uterine blood flow velocity. Am J Obstet Gynecol. 1988;159(5):1069–71. doi:10.1016/0002-9378(88)90415-2.

    Article  CAS  PubMed  Google Scholar 

  42. Ylikorkala O, Viinikka L, Lehtovirta P. Effect of nicotine on fetal prostacyclin and thromboxane in humans. Obstet Gynecol. 1985;66(1):102–5.

    CAS  PubMed  Google Scholar 

  43. Lindblad A, Marsál K, Andersson KE. Effect of nicotine on human fetal blood flow. Obstet Gynecol. 1988;72(3 Pt 1):371–82.

    CAS  PubMed  Google Scholar 

  44. Bruner JP, Forouzan I. Smoking and buccally administered nicotine. Acute effect on uterine and umbilical artery Doppler flow velocity waveforms. J Reprod Med. 1991;36(6):435–40.

    CAS  PubMed  Google Scholar 

  45. Rydell M, Magnusson C, Cnattingius S, Granath F, Svensson AC, Galanti MR. Exposure to maternal smoking during pregnancy as a risk factor for tobacco use in adult offspring. Am J Epidemiol. 2014;179(12):1409–17. doi:10.1093/aje/kwu074.

    Article  PubMed  Google Scholar 

  46. Clapp JF. The effects of maternal exercise on early pregnancy outcome. Am J Obstet Gynecol. 1989;161(6 Pt 1):1453–7. doi:10.1016/0002-9378(89)90903-4.

    Article  PubMed  Google Scholar 

  47. Magann EF, Evans SF, Weitz B, Newnham J. Antepartum, intrapartum, and neonatal significance of exercise on healthy low-risk pregnant working women. Obstet Gynecol. 2002;99(3):466–72. doi:10.1016/S0029-7844(01)01754-9.

    PubMed  Google Scholar 

  48. Rose NC, Haddow JE, Palomaki GE, Knight GJ. Self-rated physical activity level during the second trimester and pregnancy outcome. Obstet Gynecol. 1991;78(6):1078–80.

    CAS  PubMed  Google Scholar 

  49. Latka M, Kline J, Hatch M. Exercise and spontaneous abortion of known karyotype. Epidemiology. 1999;10(1):73–5. doi:10.1097/00001648-199901000-00013.

    Article  CAS  PubMed  Google Scholar 

  50. Hjollund NH, Jensen TK, Bonde JP, Henriksen TB, Andersson AM, Kolstad HA, et al. Spontaneous abortion and physical strain around implantation: a follow-up study of first-pregnancy planners. Epidemiology. 2000;11(1):18–23. doi:10.1097/00001648-200001000-00006.

    Article  CAS  PubMed  Google Scholar 

  51. Madsen M, Jørgensen T, Jensen ML, Juhl M, Olsen J, Andersen PK, et al. Leisure time physical exercise during pregnancy and the risk of miscarriage: a study within the Danish National Birth Cohort. BJOG. 2007;114(11):1419–26. doi:10.1111/j.1471-0528.2007.01496.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The Danish National Research Foundation has established the Danish Epidemiology Science Centre that initiated and created the Danish National Birth Cohort. The cohort is furthermore a result of a major grant from this Foundation. Additional support for the Danish National Birth Cohort is obtained from the Pharmacy Foundation, the Egmont Foundation the March of the Dimes Birth Defects Foundation, the Augustinus Foundation, and the Health Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Morales-Suárez-Varela.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morales-Suárez-Varela, M., Nohr, E.A., Bech, B.H. et al. Smoking, physical exercise, BMI and late foetal death: a study within the Danish National Birth Cohort. Eur J Epidemiol 31, 999–1009 (2016). https://doi.org/10.1007/s10654-016-0190-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10654-016-0190-2

Keywords

Navigation