Top

Published in:

01-10-2016

Maternal Pre-pregnancy BMI and Reproductive Health of Daughters in Young Adulthood

Authors: Saga Elise Mariansdatter, Andreas Ernst, Gunnar Toft, Sjurdur Frodi Olsen, Anne Vested, Susanne Lund Kristensen, Mette Lausten Hansen, Cecilia Høst Ramlau-Hansen

Published in: Maternal and Child Health Journal | Issue 10/2016

Abstract

Objective To investigate the possible associations between maternal pre-pregnancy body mass index (BMI) and daughters’ age of menarche and subsequent markers of reproductive health. Methods Nine hundred eighty-five pregnant women (80 %) were enrolled at their routine 30th week examinations in 1988–1989. In 2008, a follow-up questionnaire was completed for 365 daughters (83 %), while 267 daughters (61 %) participated in a subsequent clinical examination. Main outcome measures were age of menarche, reproductive hormone profile, and ovarian follicle count in daughters. Results Daughters of mothers in the highest pre-pregnancy BMI tertile (BMI ≥ 22.0 kg/m²) had an adjusted 4.1 (0.3; 8.0) months earlier menarche compared with the middle tertile group (BMI 20.0–21.9 kg/m²). Among non-users of hormonal contraceptives, daughters of mothers in the highest pre-pregnancy BMI tertile had non-significantly lower dehydroepiandrosterone-sulphate (DHEAS), estradiol, and free estrogen index (FEI), compared to the middle BMI tertile. This was supported by a sub-analysis using the WHO classification (underweight, BMI < 18.50; normal range, BMI 18.50–24.99; overweight/obese, BMI ≥ 25.00 kg/m²) as exposure groups, in which daughters of overweight mothers had lower levels of DHEAS and estradiol, and lower FEI compared to daughters of normal weight mothers. No associations were found for ovarian follicle count in any of the groups. Conclusions for Practice We found that higher maternal BMI is associated with earlier age of menarche in daughters. A possible impact of maternal pre-pregnancy BMI on DHEAS and estradiol serum levels, and FEI in non-users of hormonal contraceptives was indicated, but the results were not statistically significant.

Available only for authorised users

Aksglaede, L., Sorensen, K., Petersen, J. H., Skakkebaek, N. E., & Juul, A. (2009). Recent decline in age at breast development: The copenhagen puberty study. Pediatrics, 123(5), e932–e939. doi:10.1542/peds.2008-2491.CrossRefPubMed

Anderson, E. L., Fraser, A., McNally, W., Sattar, N., Lashen, H., Fleming, R., et al. (2013). Anti-mullerian hormone is not associated with cardiometabolic risk factors in adolescent females. PLoS One, 8(5), e64510. doi:10.1371/journal.pone.0064510.CrossRefPubMedPubMedCentral

Baird, D. D., Weinberg, C. R., Zhou, H., Kamel, F., McConnaughey, D. R., Kesner, J. S., et al. (1999). Preimplantation urinary hormone profiles and the probability of conception in healthy women. Fertility and Sterility, 71(1), 40–49.CrossRefPubMed

Biro, F. M., Khoury, P., & Morrison, J. A. (2006). Influence of obesity on timing of puberty. International Journal of Andrology, 29(1), 272–277. (discussion 286–90).CrossRefPubMed

Da Silva, P., Aitken, R. P., Rhind, S. M., Racey, P. A., & Wallace, J. M. (2002). Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses. Reproduction (Cambridge, England), 123(6), 769–777.CrossRef

Davies, M. J., & Norman, R. J. (2002). Programming and reproductive functioning. Trends in Endocrinology and Metabolism: TEM, 13(9), 386–392.CrossRefPubMed

De Pergola, G., Maldera, S., Tartagni, M., Pannacciulli, N., Loverro, G., & Giorgino, R. (2006). Inhibitory effect of obesity on gonadotropin, estradiol, and inhibin B levels in fertile women. Obesity (Silver Spring, Md.), 14(11), 1954–1960.CrossRef

de Vries, G. J., Fields, C. T., Peters, N. V., Whylings, J., & Paul, M. J. (2014). Sensitive periods for hormonal programming of the brain. Current Topics in Behavioral Neurosciences, 16, 79–108. doi:10.1007/7854_2014_286.CrossRefPubMed

Deardorff, J., Berry-Millett, R., Rehkopf, D., Luecke, E., Lahiff, M., & Abrams, B. (2013). Maternal pre-pregnancy BMI, gestational weight gain, and age at menarche in daughters. Maternal and Child Health Journal, 17(8), 1391–1398. doi:10.1007/s10995-012-1139-z.CrossRefPubMedPubMedCentral

10.

Ernst, A., Kristensen, S. L., Toft, G., Thulstrup, A. M., Hakonsen, L. B., Olsen, S. F., et al. (2012). Maternal smoking during pregnancy and reproductive health of daughters: A follow-up study spanning two decades. Human Reproduction (Oxford, England), 27(12), 3593–3600. doi:10.1093/humrep/des337.CrossRef

11.

Fraser, A., McNally, W., Sattar, N., Anderson, E. L., Lashen, H., Fleming, R., et al. (2013). Prenatal exposures and anti-mullerian hormone in female adolescents: The avon longitudinal study of parents and children. American Journal of Epidemiology, 178(9), 1414–1423. doi:10.1093/aje/kwt137.CrossRefPubMedPubMedCentral

12.

Fritz, M. A., & Speroff, L. (2011). Clinical gynecologic endocrinology and infertility (8th ed.). Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins.

13.

Helm, P., & Grolund, L. (1998). A halt in the secular trend towards earlier menarche in denmark. Acta Obstetricia et Gynecologica Scandinavica, 77(2), 198–200.CrossRefPubMed

14.

Karapanou, O., & Papadimitriou, A. (2010). Determinants of menarche. Reproductive Biology and Endocrinology: RB&E, 8, 115-7827-8-115. doi:10.1186/1477-7827-8-115.CrossRef

15.

Keim, S. A., Branum, A. M., Klebanoff, M. A., & Zemel, B. S. (2009). Maternal body mass index and daughters’ age at menarche. Epidemiology (Cambridge, Mass.), 20(5), 677–681. doi:10.1097/EDE.0b013e3181b093ce.CrossRef

16.

Kristensen, S. L., Ramlau-Hansen, C. H., Andersen, C. Y., Ernst, E., Olsen, S. F., Bonde, J. P., et al. (2012). The association between circulating levels of antimullerian hormone and follicle number, androgens, and menstrual cycle characteristics in young women. Fertility and Sterility, 97(3), 779–785. doi:10.1016/j.fertnstert.2011.12.017.CrossRefPubMed

17.

Kristensen, S. L., Ramlau-Hansen, C. H., Ernst, E., Olsen, S. F., Bonde, J. P., Vested, A., et al. (2010). A very large proportion of young danish women have polycystic ovaries: Is a revision of the rotterdam criteria needed? Human Reproduction (Oxford, England), 25(12), 3117–3122. doi:10.1093/humrep/deq273.CrossRef

18.

Laitinen, J., Power, C., & Jarvelin, M. R. (2001). Family social class, maternal body mass index, childhood body mass index, and age at menarche as predictors of adult obesity. The American Journal of Clinical Nutrition, 74(3), 287–294.PubMed

19.

Maisonet, M., Christensen, K. Y., Rubin, C., Holmes, A., Flanders, W. D., Heron, J., et al. (2010). Role of prenatal characteristics and early growth on pubertal attainment of british girls. Pediatrics, 126(3), e591–e600. doi:10.1542/peds.2009-2636.CrossRefPubMed

20.

Marcondes, R. R., Carvalho, K. C., Duarte, D. C., Garcia, N., Amaral, V. C., Simoes, M. J., et al. (2015). Differences in neonatal exposure to estradiol or testosterone on ovarian function and hormonal levels. General and Comparative Endocrinology, 212, 28–33. doi:10.1016/j.ygcen.2015.01.006.CrossRefPubMed

21.

Meseguer, A., Puche, C., & Cabero, A. (2002). Sex steroid biosynthesis in white adipose tissue. Hormone and Metabolic Research = Hormon- Und Stoffwechselforschung = Hormones Et Metabolisme, 34(11–12), 731–736. doi:10.1055/s-2002-38249.CrossRefPubMed

22.

Must, A., Phillips, S. M., Naumova, E. N., Blum, M., Harris, S., Dawson-Hughes, B., et al. (2002). Recall of early menstrual history and menarcheal body size: After 30 years, how well do women remember? American Journal of Epidemiology, 155(7), 672–679.CrossRefPubMed

23.

Ogden, C. L., Yanovski, S. Z., Carroll, M. D., & Flegal, K. M. (2007). The epidemiology of obesity. Gastroenterology, 132(6), 2087–2102.CrossRefPubMed

24.

Olsen, S. F., Hansen, H. S., Secher, N. J., Jensen, B., & Sandstrom, B. (1995). Gestation length and birth weight in relation to intake of marine n-3 fatty acids. The British Journal of Nutrition, 73(3), 397–404.CrossRefPubMed

25.

Rubin, C., Maisonet, M., Kieszak, S., Monteilh, C., Holmes, A., Flanders, D., et al. (2009). Timing of maturation and predictors of menarche in girls enrolled in a contemporary british cohort. Paediatric and Perinatal Epidemiology, 23(5), 492–504. doi:10.1111/j.1365-3016.2009.01055.x.CrossRefPubMed

26.

Shrestha, A., Olsen, J., Ramlau-Hansen, C. H., Bech, B. H., & Nohr, E. A. (2011). Obesity and age at menarche. Fertility and Sterility, 95(8), 2732–2734. doi:10.1016/j.fertnstert.2011.02.020.CrossRefPubMed

27.

Shrier, I., & Platt, R. W. (2008). Reducing bias through directed acyclic graphs. BMC Medical Research Methodology, 8, 70-2288-8-70. doi:10.1186/1471-2288-8-70.CrossRef

28.

Towne, B., Czerwinski, S. A., Demerath, E. W., Blangero, J., Roche, A. F., & Siervogel, R. M. (2005). Heritability of age at menarche in girls from the Fels Longitudinal Study. American Journal of Physical Anthropology, 128(1), 210–219. doi:10.1002/ajpa.20106.CrossRefPubMed

29.

Tworoger, S. S., Eliassen, A. H., Missmer, S. A., Baer, H., Rich-Edwards, J., Michels, K. B., et al. (2006). Birthweight and body size throughout life in relation to sex hormones and prolactin concentrations in premenopausal women. Cancer Epidemiology, Biomarkers and Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 15(12), 2494–2501.CrossRef

30.

Venners, S. A., Liu, X., Perry, M. J., Korrick, S. A., Li, Z., Yang, F., et al. (2006). Urinary estrogen and progesterone metabolite concentrations in menstrual cycles of fertile women with non-conception, early pregnancy loss or clinical pregnancy. Human Reproduction (Oxford, England), 21(9), 2272–2280.CrossRef

31.

Waylen, A. L., Jones, G. L., & Ledger, W. L. (2010). Effect of cigarette smoking upon reproductive hormones in women of reproductive age: A retrospective analysis. Reproductive Biomedicine Online, 20(6), 861–865. doi:10.1016/j.rbmo.2010.02.021.CrossRefPubMed

32.

WHO. (1995). Physical status: The use and interpretation of anthropometry. Report of a WHO expert committee. World Health Organization Technical Report Series, 854, 1–452.

33.

Yeung, E. H., Zhang, C., Albert, P. S., Mumford, S. L., Ye, A., Perkins, N. J., et al. (2013). Adiposity and sex hormones across the menstrual cycle: The BioCycle study. International Journal of Obesity (2005), 37(2), 237–243. doi:10.1038/ijo.2012.9.CrossRef

34.

Yu, Z., Han, S., Zhu, J., Sun, X., Ji, C., & Guo, X. (2013). Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: A systematic review and meta-analysis. PLoS One, 8(4), e61627. doi:10.1371/journal.pone.0061627.CrossRefPubMedPubMedCentral

35.

Ziomkiewicz, A., Ellison, P. T., Lipson, S. F., Thune, I., & Jasienska, G. (2008). Body fat, energy balance and estradiol levels: A study based on hormonal profiles from complete menstrual cycles. Human Reproduction (Oxford, England), 23(11), 2555–2563. doi:10.1093/humrep/den213.CrossRef

Title: Maternal Pre-pregnancy BMI and Reproductive Health of Daughters in Young Adulthood
Authors: Saga Elise Mariansdatter
Andreas Ernst
Gunnar Toft
Sjurdur Frodi Olsen
Anne Vested
Susanne Lund Kristensen
Mette Lausten Hansen
Cecilia Høst Ramlau-Hansen
Publication date: 01-10-2016
Publisher: Springer US
Published in: Maternal and Child Health Journal / Issue 10/2016
Print ISSN: 1092-7875
Electronic ISSN: 1573-6628
DOI: https://doi.org/10.1007/s10995-016-2062-5

At a glance: The STEP trials

Springer Medicine

Maternal Pre-pregnancy BMI and Reproductive Health of Daughters in Young Adulthood

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 10/2016

Association Between Caregiver Stress and Behavioral Problems in the Children of Incarcerated Fathers in Hong Kong

Relationship Between Common Mental Disorder Symptoms During Pregnancy and Preterm Birth Among Chinese Women in Wuhan

Prenatal Stress and the Cortisol Awakening Response in African-American and Caucasian Women in the Third Trimester of Pregnancy

Children’s Media Use and Self-Regulation Behavior: Longitudinal Associations in a Nationwide Japanese Study

Prevalence of Ethanol Use Among Pregnant Women in Southwestern Uganda

The Effectiveness of a Physical Activity Educational Campaign in a Rural Obstetrics and Gynecology Office