Skip to main content
Top
Published in: BMC Pediatrics 1/2019

Open Access 01-12-2019 | Gestational Diabetes | Research article

Maternal age at menarche and offspring body mass index in childhood

Authors: Hui Wang, Yunting Zhang, Ying Tian, Fei Li, Chonghui Yan, Hui Wang, Zhongchen Luo, Fan Jiang, Jun Zhang

Published in: BMC Pediatrics | Issue 1/2019

Login to get access

Abstract

Background

Earlier age of menarche has been associated with an increased risk of chronic diseases during adulthood, but whether early menarche has intergenerational effect is not clear.

Methods

In this population-based cross-sectional study, we recruited children from 26 primary schools using cluster random probability sampling in Shanghai, China, in 2014. We used multiple linear regression models to estimate the adjusted associations of maternal age of menarche (MAM) with offspring body mass index (BMI). We also used the mediation analysis to examine the contribution of maternal BMI and gestational diabetes to offspring BMI.

Results

A total of 17,571 children aged 6–13 years were enrolled, of whom 16,373 had their weight and height measured. Earlier MAM was associated with higher child BMI in boys (− 0.05 z-score per year older MAM, 95% CI − 0.08 to − 0.02) and in girls (− 0.05 z-score per year older MAM, 95% CI − 0.07 to − 0.02). Maternal BMI positively mediated the association of MAM with offspring BMI in both sexes, with mediation effects of 37.7 and 19.4% for boys and girls, respectively.

Conclusion

Early maternal menarche was associated with greater offspring BMI. This study provides evidence for the intergenerational effect in the development of BMI in offspring.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gluckman PD, Hanson MA. Evolution, development and timing of puberty. Trends Endocrinol Metab. 2006;17(1):7–12.CrossRef Gluckman PD, Hanson MA. Evolution, development and timing of puberty. Trends Endocrinol Metab. 2006;17(1):7–12.CrossRef
2.
go back to reference McDowell MA, Brody DJ, Hughes JP. Has age at menarche changed? Results from the National Health and nutrition examination survey (NHANES) 1999–2004. J Adolesc Health. 2007;40(3):227–31.CrossRef McDowell MA, Brody DJ, Hughes JP. Has age at menarche changed? Results from the National Health and nutrition examination survey (NHANES) 1999–2004. J Adolesc Health. 2007;40(3):227–31.CrossRef
3.
4.
go back to reference Golub MS, Collman GW, Foster PM, Kimmel CA, Rajpert-De Meyts E, Reiter EO, Sharpe RM, Skakkebaek NE, Toppari J. Public health implications of altered puberty timing. Pediatrics. 2008;121(Supplement 3):S218–30.CrossRef Golub MS, Collman GW, Foster PM, Kimmel CA, Rajpert-De Meyts E, Reiter EO, Sharpe RM, Skakkebaek NE, Toppari J. Public health implications of altered puberty timing. Pediatrics. 2008;121(Supplement 3):S218–30.CrossRef
5.
go back to reference Jasienska G, Bribiescas RG, Furberg A-S, Helle S, Núñez-de la Mora A: Human reproduction and health: an evolutionary perspective. Lancet 2017, 390(10093):510–520.CrossRef Jasienska G, Bribiescas RG, Furberg A-S, Helle S, Núñez-de la Mora A: Human reproduction and health: an evolutionary perspective. Lancet 2017, 390(10093):510–520.CrossRef
6.
go back to reference Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305(5691):1733–6.CrossRef Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305(5691):1733–6.CrossRef
7.
go back to reference Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res. 2007;61:5R–10R.CrossRef Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res. 2007;61:5R–10R.CrossRef
8.
go back to reference Basso O, Pennell ML, Chen A, Longnecker MP. Mother's age at menarche and offspring size. Int J Obes. 2010;34(12):1766–71.CrossRef Basso O, Pennell ML, Chen A, Longnecker MP. Mother's age at menarche and offspring size. Int J Obes. 2010;34(12):1766–71.CrossRef
9.
go back to reference Ong KK, Northstone K, Wells JC, Rubin C, Ness AR, Golding J, Dunger DB. Earlier mother's age at menarche predicts rapid infancy growth and childhood obesity. PLoS Med. 2007;4(4):e132.CrossRef Ong KK, Northstone K, Wells JC, Rubin C, Ness AR, Golding J, Dunger DB. Earlier mother's age at menarche predicts rapid infancy growth and childhood obesity. PLoS Med. 2007;4(4):e132.CrossRef
10.
go back to reference Lai TC, Yeung SLA, Lin SL, Leung GM, Schooling CM. Brief report: maternal age of menarche and adiposity: evidence from Hong Kong’s “children of 1997” birth cohort. Epidemiology. 2016;27(3):433–7.CrossRef Lai TC, Yeung SLA, Lin SL, Leung GM, Schooling CM. Brief report: maternal age of menarche and adiposity: evidence from Hong Kong’s “children of 1997” birth cohort. Epidemiology. 2016;27(3):433–7.CrossRef
11.
go back to reference Min J, Li Z, Liu X, Wang Y. The association between early menarche and offspring's obesity risk in early childhood was modified by gestational weight gain. Obesity. 2014;22(1):19–23.CrossRef Min J, Li Z, Liu X, Wang Y. The association between early menarche and offspring's obesity risk in early childhood was modified by gestational weight gain. Obesity. 2014;22(1):19–23.CrossRef
12.
go back to reference Dietz WH. Critical periods in childhood for the development of obesity. Am J Clin Nutr. 1994;59(5):955–9.CrossRef Dietz WH. Critical periods in childhood for the development of obesity. Am J Clin Nutr. 1994;59(5):955–9.CrossRef
13.
go back to reference Chen L, Li S, He C, Zhu Y, Louis GMB, Yeung E, Hu FB, Zhang C. Age at menarche and risk of gestational diabetes mellitus: a prospective cohort study among 27,482 women. Diabetes Care. 2016;39(3):469–71.CrossRef Chen L, Li S, He C, Zhu Y, Louis GMB, Yeung E, Hu FB, Zhang C. Age at menarche and risk of gestational diabetes mellitus: a prospective cohort study among 27,482 women. Diabetes Care. 2016;39(3):469–71.CrossRef
14.
go back to reference Li H, Shen L, Song L, Liu B, Zheng X, Xu S, Wang Y. Early age at menarche and gestational diabetes mellitus risk: results from the healthy baby cohort study. Diabetes Metab. 2017;43(3):248–52.CrossRef Li H, Shen L, Song L, Liu B, Zheng X, Xu S, Wang Y. Early age at menarche and gestational diabetes mellitus risk: results from the healthy baby cohort study. Diabetes Metab. 2017;43(3):248–52.CrossRef
15.
go back to reference Schoenaker DA, Mishra GD. Association between age at menarche and gestational diabetes mellitus: the Australian longitudinal study on Women's health. Am J Epidemiol. 2017;185(7):554–61.CrossRef Schoenaker DA, Mishra GD. Association between age at menarche and gestational diabetes mellitus: the Australian longitudinal study on Women's health. Am J Epidemiol. 2017;185(7):554–61.CrossRef
16.
go back to reference Hillier TA, Pedula KL, Schmidt MM, Mullen JA, Charles M-A, Pettitt DJ. Childhood obesity and metabolic imprinting: the ongoing effects of maternal hyperglycemia. Diabetes Care. 2007;30(9):2287–92.CrossRef Hillier TA, Pedula KL, Schmidt MM, Mullen JA, Charles M-A, Pettitt DJ. Childhood obesity and metabolic imprinting: the ongoing effects of maternal hyperglycemia. Diabetes Care. 2007;30(9):2287–92.CrossRef
17.
go back to reference Reynolds R, Osmond C, Phillips D, Godfrey K. Maternal BMI, parity, and pregnancy weight gain: influences on offspring adiposity in young adulthood. J Clin Endocrinol Metab. 2010;95(12):5365–9.CrossRef Reynolds R, Osmond C, Phillips D, Godfrey K. Maternal BMI, parity, and pregnancy weight gain: influences on offspring adiposity in young adulthood. J Clin Endocrinol Metab. 2010;95(12):5365–9.CrossRef
18.
go back to reference Chu S, Zhang Y, Jiang Y, Sun W, Zhu Q, Wang B, Jiang F, Zhang J. Cesarean section without medical indication and risks of childhood allergic disorder, attenuated by breastfeeding. Sci Rep. 2017;7(1):9762.CrossRef Chu S, Zhang Y, Jiang Y, Sun W, Zhu Q, Wang B, Jiang F, Zhang J. Cesarean section without medical indication and risks of childhood allergic disorder, attenuated by breastfeeding. Sci Rep. 2017;7(1):9762.CrossRef
19.
go back to reference Chen C, Zhang Y, Sun W, Chen Y, Jiang Y, Song Y, Lin Q, Zhu L, Zhu Q, Wang X. Investigating the relationship between precocious puberty and obesity: a cross-sectional study in Shanghai, China. BMJ Open. 2017;7(4):e014004.CrossRef Chen C, Zhang Y, Sun W, Chen Y, Jiang Y, Song Y, Lin Q, Zhu L, Zhu Q, Wang X. Investigating the relationship between precocious puberty and obesity: a cross-sectional study in Shanghai, China. BMJ Open. 2017;7(4):e014004.CrossRef
20.
go back to reference Shanghai Census Burean. Shanghai Population in 21st Century. In: Chinese Statistical Press. edn.; 2005: 257–258. Shanghai Census Burean. Shanghai Population in 21st Century. In: Chinese Statistical Press. edn.; 2005: 257–258.
21.
go back to reference Wang Y, Popkin B, Zhai F. The nutritional status and dietary pattern of Chinese adolescents, 1991 and 1993. Eur J Clin Nutr. 1998;52(12):908.CrossRef Wang Y, Popkin B, Zhai F. The nutritional status and dietary pattern of Chinese adolescents, 1991 and 1993. Eur J Clin Nutr. 1998;52(12):908.CrossRef
22.
go back to reference Zhang Y, Zhang D, Li X, Ip P, Ho F, Jiang Y, Sun W, Zhu Q, Zhu W, Zhang J. Daily time-use patterns and obesity and mental health among primary school students in Shanghai: a population-based cross-sectional study. Sci Rep. 2017;7(1):16200.CrossRef Zhang Y, Zhang D, Li X, Ip P, Ho F, Jiang Y, Sun W, Zhu Q, Zhu W, Zhang J. Daily time-use patterns and obesity and mental health among primary school students in Shanghai: a population-based cross-sectional study. Sci Rep. 2017;7(1):16200.CrossRef
23.
go back to reference Md O, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85:660–7.CrossRef Md O, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85:660–7.CrossRef
24.
go back to reference Bennette C, Vickers A. Against quantiles: categorization of continuous variables in epidemiologic research, and its discontents. BMC Med Res Methodol. 2012;12(1):21.CrossRef Bennette C, Vickers A. Against quantiles: categorization of continuous variables in epidemiologic research, and its discontents. BMC Med Res Methodol. 2012;12(1):21.CrossRef
25.
go back to reference VanderWeele TJ, Shpitser I. A new criterion for confounder selection. Biometrics. 2011;67(4):1406–13.CrossRef VanderWeele TJ, Shpitser I. A new criterion for confounder selection. Biometrics. 2011;67(4):1406–13.CrossRef
26.
go back to reference Baron RM, Kenny DA. The moderator–mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986;51(6):1173.CrossRef Baron RM, Kenny DA. The moderator–mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986;51(6):1173.CrossRef
27.
go back to reference Schafer JL. Multiple imputation: a primer. Stat Methods Med Res. 1999;8(1):3–15.CrossRef Schafer JL. Multiple imputation: a primer. Stat Methods Med Res. 1999;8(1):3–15.CrossRef
28.
go back to reference Moons KG, Donders RA, Stijnen T, Harrell FE. Using the outcome for imputation of missing predictor values was preferred. J Clin Epidemiol. 2006;59(10):1092–101.CrossRef Moons KG, Donders RA, Stijnen T, Harrell FE. Using the outcome for imputation of missing predictor values was preferred. J Clin Epidemiol. 2006;59(10):1092–101.CrossRef
29.
go back to reference VanderWeele TJ, Ding P. Sensitivity analysis in observational research: introducing the E-value. Ann Intern Med. 2017;167(4):268–74.CrossRef VanderWeele TJ, Ding P. Sensitivity analysis in observational research: introducing the E-value. Ann Intern Med. 2017;167(4):268–74.CrossRef
30.
go back to reference MacKinnon DP, Dwyer JH. Estimating mediated effects in prevention studies. Eval Rev. 1993;17(2):144–58.CrossRef MacKinnon DP, Dwyer JH. Estimating mediated effects in prevention studies. Eval Rev. 1993;17(2):144–58.CrossRef
31.
go back to reference Toro-Ramos T, Paley C, Pi-Sunyer F, Gallagher D. Body composition during fetal development and infancy through the age of 5 years. Eur J Clin Nutr. 2015;69(12):1279.CrossRef Toro-Ramos T, Paley C, Pi-Sunyer F, Gallagher D. Body composition during fetal development and infancy through the age of 5 years. Eur J Clin Nutr. 2015;69(12):1279.CrossRef
32.
go back to reference Catalano P, Ehrenberg H. The short-and long-term implications of maternal obesity on the mother and her offspring. BJOG Int J Obstet Gynaecol. 2006;113(10):1126–33.CrossRef Catalano P, Ehrenberg H. The short-and long-term implications of maternal obesity on the mother and her offspring. BJOG Int J Obstet Gynaecol. 2006;113(10):1126–33.CrossRef
33.
go back to reference Heerwagen MJ, Miller MR, Barbour LA, Friedman JE. Maternal obesity and fetal metabolic programming: a fertile epigenetic soil. Am J Phys Regul Integr Comp Phys. 2010;299(3):R711–22. Heerwagen MJ, Miller MR, Barbour LA, Friedman JE. Maternal obesity and fetal metabolic programming: a fertile epigenetic soil. Am J Phys Regul Integr Comp Phys. 2010;299(3):R711–22.
34.
go back to reference Cooper R, Blell M, Hardy R, Black S, Pollard T, Wadsworth M, Pearce M, Kuh D. Validity of age at menarche self-reported in adulthood. J Epidemiol Community Health. 2006;60(11):993–7.CrossRef Cooper R, Blell M, Hardy R, Black S, Pollard T, Wadsworth M, Pearce M, Kuh D. Validity of age at menarche self-reported in adulthood. J Epidemiol Community Health. 2006;60(11):993–7.CrossRef
35.
go back to reference Freedman DS, Khan LK, Serdula MK, Dietz WH, Srinivasan SR, Berenson GS. The relation of childhood BMI to adult adiposity: the Bogalusa heart study. Pediatrics. 2005;115(1):22–7.CrossRef Freedman DS, Khan LK, Serdula MK, Dietz WH, Srinivasan SR, Berenson GS. The relation of childhood BMI to adult adiposity: the Bogalusa heart study. Pediatrics. 2005;115(1):22–7.CrossRef
36.
go back to reference Alberga A, Sigal R, Goldfield G, Prud'Homme D, Kenny G. Overweight and obese teenagers: why is adolescence a critical period? Pediatric obesity. 2012;7(4):261–73.CrossRef Alberga A, Sigal R, Goldfield G, Prud'Homme D, Kenny G. Overweight and obese teenagers: why is adolescence a critical period? Pediatric obesity. 2012;7(4):261–73.CrossRef
37.
go back to reference Vetter-O'Hagen CS, Spear LP. Hormonal and physical markers of puberty and their relationship to adolescent-typical novelty-directed behavior. Dev Psychobiol. 2012;54(5):523–35.CrossRef Vetter-O'Hagen CS, Spear LP. Hormonal and physical markers of puberty and their relationship to adolescent-typical novelty-directed behavior. Dev Psychobiol. 2012;54(5):523–35.CrossRef
38.
go back to reference Tu W, Wagner EK, Eckert GJ, Yu Z, Hannon T, Pratt JH, He C. Associations between menarche-related genetic variants and pubertal growth in male and female adolescents. J Adolesc Health. 2015;56(1):66–72.CrossRef Tu W, Wagner EK, Eckert GJ, Yu Z, Hannon T, Pratt JH, He C. Associations between menarche-related genetic variants and pubertal growth in male and female adolescents. J Adolesc Health. 2015;56(1):66–72.CrossRef
39.
go back to reference Ong KK, Elks CE, Li S, Zhao JH, Luan JA, Andersen LB, Bingham SA, Brage S, Smith GD, Ekelund U. Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet. 2009;41(6):729–33.CrossRef Ong KK, Elks CE, Li S, Zhao JH, Luan JA, Andersen LB, Bingham SA, Brage S, Smith GD, Ekelund U. Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet. 2009;41(6):729–33.CrossRef
40.
go back to reference Johnson W, Choh AC, Curran JE, Czerwinski SA, Bellis C, Dyer TD, Blangero J, Towne B, Demerath EW. Genetic risk for earlier menarche also influences peripubertal body mass index. Am J Phys Anthropol. 2013;150(1):10–20.CrossRef Johnson W, Choh AC, Curran JE, Czerwinski SA, Bellis C, Dyer TD, Blangero J, Towne B, Demerath EW. Genetic risk for earlier menarche also influences peripubertal body mass index. Am J Phys Anthropol. 2013;150(1):10–20.CrossRef
41.
go back to reference Coall DA, Chisholm JS. Evolutionary perspectives on pregnancy: maternal age at menarche and infant birth weight. Soc Sci Med. 2003;57(10):1771–81.CrossRef Coall DA, Chisholm JS. Evolutionary perspectives on pregnancy: maternal age at menarche and infant birth weight. Soc Sci Med. 2003;57(10):1771–81.CrossRef
42.
go back to reference Aiken CE, Ozanne SE. Transgenerational developmental programming. Hum Reprod Update. 2013;20(1):63–75.CrossRef Aiken CE, Ozanne SE. Transgenerational developmental programming. Hum Reprod Update. 2013;20(1):63–75.CrossRef
43.
go back to reference Veiga-Lopez A, Steckler TL, Abbott DH, Welch KB, MohanKumar PS, Phillips DJ, Refsal K, Padmanabhan V. Developmental programming: impact of excess prenatal testosterone on intrauterine fetal endocrine milieu and growth in sheep. Biol Reprod. 2011;84(1):87–96.CrossRef Veiga-Lopez A, Steckler TL, Abbott DH, Welch KB, MohanKumar PS, Phillips DJ, Refsal K, Padmanabhan V. Developmental programming: impact of excess prenatal testosterone on intrauterine fetal endocrine milieu and growth in sheep. Biol Reprod. 2011;84(1):87–96.CrossRef
44.
go back to reference Newbold RR, Padilla-Banks E, Snyder RJ, Jefferson WN. Perinatal exposure to environmental estrogens and the development of obesity. Mol Nutr Food Res. 2007;51(7):912–7.CrossRef Newbold RR, Padilla-Banks E, Snyder RJ, Jefferson WN. Perinatal exposure to environmental estrogens and the development of obesity. Mol Nutr Food Res. 2007;51(7):912–7.CrossRef
Metadata
Title
Maternal age at menarche and offspring body mass index in childhood
Authors
Hui Wang
Yunting Zhang
Ying Tian
Fei Li
Chonghui Yan
Hui Wang
Zhongchen Luo
Fan Jiang
Jun Zhang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Pediatrics / Issue 1/2019
Electronic ISSN: 1471-2431
DOI
https://doi.org/10.1186/s12887-019-1659-4

Other articles of this Issue 1/2019

BMC Pediatrics 1/2019 Go to the issue