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The impact of prenatal parental tobacco smoking on risk of diabetes mellitus in middle-aged women

Published online by Cambridge University Press:  10 February 2015

M. A. La Merrill*
Affiliation:
Department of Environmental Toxicology, University of California, Davis, CA, USA
P. M. Cirillo
Affiliation:
Child Health and Development Studies, Public Health Institute, Berkeley, CA, USA
N. Y. Krigbaum
Affiliation:
Child Health and Development Studies, Public Health Institute, Berkeley, CA, USA
B. A. Cohn
Affiliation:
Child Health and Development Studies, Public Health Institute, Berkeley, CA, USA
*
*Address for correspondence: M. L. Merrill, Department of Environmental Toxicology, University of California at Davis, 1 Shields Avenue, 4245 Meyer Hall, CA 95616-5270, USA. (Email mlamerrill@ucdavis.edu)

Abstract

Growing evidence indicates that parental smoking is associated with risk of offspring obesity. The purpose of this study was to identify whether parental tobacco smoking during gestation was associated with risk of diabetes mellitus. This is a prospective study of 44- to 54-year-old daughters (n=1801) born in the Child Health and Development Studies pregnancy cohort between 1959 and 1967. Their mothers resided near Oakland California, were members of the Kaiser Foundation Health Plan and reported parental tobacco smoking during an early pregnancy interview. Daughters reported physician diagnoses of diabetes mellitus and provided blood samples for hemoglobin A1C measurement. Prenatal maternal smoking had a stronger association with daughters’ diabetes mellitus risk than prenatal paternal smoking, and the former persisted after adjustment for parental race, diabetes and employment (aRR=2.4 [95% confidence intervals 1.4–4.1] P<0.01 and aRR=1.7 [95% confidence intervals 1.0–3.0] P=0.05, respectively). Estimates of the effect of parental smoking were unchanged when further adjusted by daughters’ birth weight or current body mass index (BMI). Maternal smoking was also significantly associated with self-reported type 2 diabetes diagnosis (2.3 [95% confidence intervals 1.0–5.0] P<0.05). Having parents who smoked during pregnancy was associated with an increased risk of diabetes mellitus among adult daughters, independent of known risk factors, providing further evidence that prenatal environmental chemical exposures independent of birth weight and current BMI may contribute to adult diabetes mellitus. While other studies seek to confirm our results, caution toward tobacco smoking by or proximal to pregnant women is warranted in diabetes mellitus prevention efforts.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. United States. Public Health Service. Office of the Surgeon General. The Health Consequences of Involuntary Exposure to Tobacco Smoke: A Report of the Surgeon General. 2006. US Department of Health and Human Services, Public Health Service, Office of the Surgeon General: Rockville, MD.Google Scholar
2. Henkin, L, Zaccaro, D, Haffner, S, et al. Cigarette smoking, environmental tobacco smoke exposure and insulin sensitivity: the Insulin Resistance Atherosclerosis Study. Ann Epidemiol. 1999; 9, 290296.CrossRefGoogle ScholarPubMed
3. Kowall, B, Rathmann, W, Strassburger, K, et al. Association of passive and active smoking with incident type 2 diabetes mellitus in the elderly population: the KORA S4/F4 cohort study. Eur J Epidemiol. 2010; 25, 393402.CrossRefGoogle ScholarPubMed
4. Weitzman, M, Cook, S, Auinger, P, et al. Tobacco smoke exposure is associated with the metabolic syndrome in adolescents. Circulation. 2005; 112, 862869.CrossRefGoogle ScholarPubMed
5. Thiering, E, Bruske, I, Kratzsch, J, et al. Prenatal and postnatal tobacco smoke exposure and development of insulin resistance in 10 year old children. Int J Hyg Environ Health. 2011; 214, 361368.CrossRefGoogle Scholar
6. Houston, TK, Person, SD, Pletcher, MJ, et al. Active and passive smoking and development of glucose intolerance among young adults in a prospective cohort: CARDIA study. BMJ. 2006; 332, 10641069.CrossRefGoogle Scholar
7. La Merrill, M, Stein, CR, Landrigan, P, Engel, SM, Savitz, DA. Prepregnancy body mass index, smoking during pregnancy, and infant birth weight. Ann Epidemiol. 2011; 21, 413420.CrossRefGoogle ScholarPubMed
8. Leonardi-Bee, J, Smyth, A, Britton, J, Coleman, T. Environmental tobacco smoke and fetal health: systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed. 2008; 93, F351F361.CrossRefGoogle ScholarPubMed
9. El-Mohandes, AA, Kiely, M, Blake, SM, Gantz, MG, El-Khorazaty, MN. An intervention to reduce environmental tobacco smoke exposure improves pregnancy outcomes. Pediatrics. 2010; 125, 721728.CrossRefGoogle ScholarPubMed
10. Behl, M, Rao, D, Aagaard, K, et al. Evaluation of the association between maternal smoking, childhood obesity, and metabolic disorders: a national toxicology program workshop review. Env Health Perspect. 2013; 121, 170180.CrossRefGoogle ScholarPubMed
11. Mattsson, K, Kallen, K, Longnecker, MP, Rignell-Hydbom, A, Rylander, L. Maternal smoking during pregnancy and daughters’ risk of gestational diabetes and obesity. Diabetologia. 2013; 56, 16891695.CrossRefGoogle ScholarPubMed
12. Harris, HR, Willett, WC, Michels, KB. Parental smoking during pregnancy and risk of overweight and obesity in the daughter. Int J Obes (Lond). 2013; 37, 13561363.CrossRefGoogle ScholarPubMed
13. Hales, CN, Barker, DJ, Clark, PM, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991; 303, 10191022.CrossRefGoogle ScholarPubMed
14. Poulsen, P, Vaag, AA, Kyvik, KO, Moller Jensen, D, Beck-Nielsen, H. Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia. 1997; 40, 439446.CrossRefGoogle ScholarPubMed
15. Lindsay, RS, Dabelea, D, Roumain, J, et al. Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes. 2000; 49, 445449.CrossRefGoogle ScholarPubMed
16. Narayan, KM, Boyle, JP, Thompson, TJ, Gregg, EW, Williamson, DF. Effect of BMI on lifetime risk for diabetes in the U.S. Diabetes Care. 2007; 30, 15621566.CrossRefGoogle ScholarPubMed
17. Thomas, C, Hypponen, E, Power, C. Prenatal exposures and glucose metabolism in adulthood: are effects mediated through birth weight and adiposity? Diabetes Care. 2007; 30, 918924.CrossRefGoogle ScholarPubMed
18. Jaddoe, VW, de Jonge, LL, van Dam, RM, et al. Fetal exposure to parental smoking and the risk of type 2 diabetes in adult women. Diabetes Care. 2014; 37, 29662973.CrossRefGoogle ScholarPubMed
19. Webb, DA, Boyd, NR, Messina, D, Windsor, RA. The discrepancy between self-reported smoking status and urine cotinine levels among women enrolled in prenatal care at four publicly funded clinical sites. J Public Health Manag Pract. 2003; 9, 322325.CrossRefGoogle ScholarPubMed
20. Britton, GR, Brinthaupt, J, Stehle, JM, James, GD. Comparison of self-reported smoking and urinary cotinine levels in a rural pregnant population. J Obstet, Gynecol Neonatal Nurs. 2004; 33, 306311.CrossRefGoogle Scholar
21. Shipton, D, Tappin, DM, Vadiveloo, T, et al. Reliability of self reported smoking status by pregnant women for estimating smoking prevalence: a retrospective, cross sectional study. BMJ. 2009; 339, b4347.CrossRefGoogle ScholarPubMed
22. Toschke, AM, Ehlin, A, Koletzko, B, Montgomery, SM. Paternal smoking is associated with a decreased prevalence of type 1 diabetes mellitus among offspring in two national British birth cohort studies (NCDS and BCS70). J Perinat Med. 2007; 35, 4347.CrossRefGoogle ScholarPubMed
23. Rasouli, B, Grill, V, Midthjell, K, et al. Risk of autoimmune diabetes in adults contrasting with increased risk in overweight men with type 2 diabetes: a 22-year follow-up of the Hunt study. Diabetes Care. 2013; 36, 604610.CrossRefGoogle ScholarPubMed
24. Kwok, MK, Schooling, CM, Lam, TH, Leung, GM. Paternal smoking and childhood overweight: evidence from the Hong Kong ‘Children of 1997’. Pediatrics. 2010; 126, e46e56.CrossRefGoogle Scholar
25. von Kries, R, Bolte, G, Baghi, L, Toschke, AM. Parental smoking and childhood obesity – is maternal smoking in pregnancy the critical exposure? Int J Epidemiol. 2008; 37, 210216.CrossRefGoogle ScholarPubMed
26. Leary, SD, Smith, GD, Rogers, IS, et al. Smoking during pregnancy and offspring fat and lean mass in childhood. Obesity (Silver Spring). 2006; 14, 22842293.CrossRefGoogle ScholarPubMed
27. 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 Health. 1994; 84, 14391443.CrossRefGoogle ScholarPubMed
28. van den Berg, BJ, Christianson, RE, Oechsli, FW. The California Child Health and Development Studies of the School of Public Health, University of California at Berkeley. Paediatr Perinat Epidemiol. 1988; 2, 265282.CrossRefGoogle ScholarPubMed
29. Housman, MG. Smoking and health: the 1964 Surgeon General’s report as a turning point in the anti-smoking movement. Harv Health Policy Rev. 2001; 2, 118126.Google Scholar
30. Proctor, RN. The history of the discovery of the cigarette-lung cancer link: evidentiary traditions, corporate denial, global toll. Tob Control. 2012; 21, 8791.CrossRefGoogle ScholarPubMed
31. National Institutes of Health. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults – the evidence report. Obes Res. 1998; 6(Suppl. 2), 51S209S.Google Scholar
32. Boulet, SL, Alexander, GR, Salihu, HM, Pass, M. Macrosomic births in the United States: determinants, outcomes, and proposed grades of risk. Am J Obstet Gynecol. 2003; 188, 13721378.CrossRefGoogle ScholarPubMed
33. Wardlaw, TM, World Health Organization, UNICEF. Low Birthweight: Country, Regional and Global Estimates. 2004. WHO and UNICEF: Geneva and New York, NY.Google Scholar
34. Chiavaroli, V, Giannini, C, D’Adamo, E, et al. Insulin resistance and oxidative stress in children born small and large for gestational age. Pediatrics. 2009; 124, 695702.CrossRefGoogle ScholarPubMed
35. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2012; 35(Suppl. 1), S64S71.CrossRefGoogle Scholar
36. Freinkel, N. Banting lecture 1980. Of pregnancy and progeny. Diabetes. 1980; 29, 10231035.CrossRefGoogle ScholarPubMed
37. Bruin, JE, Kellenberger, LD, Gerstein, HC, Morrison, KM, Holloway, AC. Fetal and neonatal nicotine exposure and postnatal glucose homeostasis: identifying critical windows of exposure. J Endocrinol. 2007; 194, 171178.CrossRefGoogle ScholarPubMed
38. Johansson, A, Hermansson, G, Ludvigsson, J, ABIS Study Group. Tobacco exposure and diabetes-related autoantibodies in children: results from the ABIS Study. Ann N Y Acad Sci. 2008; 1150, 197199.CrossRefGoogle ScholarPubMed
39. Wahlberg, J, Vaarala, O, Ludvigsson, J. Group as Asthma and allergic symptoms and type 1 diabetes-related autoantibodies in 2.5-yr-old children. Pediatr Diabetes. 2011; 12, 604610.CrossRefGoogle Scholar
40. Hummel, M, Schenker, M, Ziegler, AG. Influence of perinatal factors on the appearance of islet autoantibodies in offspring of parents with type 1 diabetes. Pediatr Diabetes. 2001; 2, 4042.Google ScholarPubMed
41. Dahlquist, G, Kallen, B. Maternal-child blood group incompatibility and other perinatal events increase the risk for early-onset type 1 (insulin-dependent) diabetes mellitus. Diabetologia. 1992; 35, 671675.CrossRefGoogle ScholarPubMed
42. Marshall, AL, Chetwynd, A, Morris, JA, et al. Type 1 diabetes mellitus in childhood: a matched case control study in Lancashire and Cumbria, UK. Diabet Med. 2004; 21, 10351040.CrossRefGoogle ScholarPubMed
43. Robertson, L, Harrild, K. Maternal and neonatal risk factors for childhood type 1 diabetes: a matched case-control study. BMC Public Health. 2010; 10, 281.CrossRefGoogle ScholarPubMed
44. Rosenbauer, J, Herzig, P, Kaiser, P, Giani, G. Early nutrition and risk of type 1 diabetes mellitus – a nationwide case-control study in preschool children. Exp Clin Endocrinol Diabetes. 2007; 115, 502508.CrossRefGoogle ScholarPubMed
45. Sipetic, SB, Vlajinac, HD, Kocev, NI, et al. The Belgrade Childhood Diabetes Study: a multivariate analysis of risk determinants for diabetes. Eur J Public Health. 2005; 15, 117122.CrossRefGoogle ScholarPubMed
46. Svensson, J, Carstensen, B, Mortensen, HB, Borch-Johnsen, K, Danish Study Group of Childhood Diabetes. Early childhood risk factors associated with type 1 diabetes – is gender important? Eur J Epidemiol. 2005; 20, 429434.CrossRefGoogle ScholarPubMed
47. Horta, BL, Gigante, DP, Nazmi, A, et al. Maternal smoking during pregnancy and risk factors for cardiovascular disease in adulthood. Atherosclerosis. 2011; 219, 815820.CrossRefGoogle ScholarPubMed
48. Cupul-Uicab, LA, Skjaerven, R, Haug, K, et al. In utero exposure to maternal tobacco smoke and subsequent obesity, hypertension, and gestational diabetes among women in the MoBa cohort. Env Health Perspect. 2012; 120, 355360.CrossRefGoogle ScholarPubMed
49. Montgomery, SM, Ekbom, A. Smoking during pregnancy and diabetes mellitus in a British longitudinal birth cohort. BMJ. 2002; 324, 2627.CrossRefGoogle Scholar
50. Power, C, Atherton, K, Thomas, C. Maternal smoking in pregnancy, adult adiposity and other risk factors for cardiovascular disease. Atherosclerosis. 2010; 211, 643648.CrossRefGoogle ScholarPubMed
51. Health, United States. Special feature on prescription drugs, 2014. Statistics NCfH, Hyattsville, MD.Google Scholar