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The effect of adverse intrauterine conditions, early childhood growth and famine exposure on age at menopause: a systematic review

Published online by Cambridge University Press:  04 December 2017

S. Sadrzadeh ,
M. Verschuuren ,
L. J. Schoonmade ,
C. B. Lambalk  and
R. C. Painter
S. Sadrzadeh*
Affiliation:
Department of Obstetrics & Gynecology, Division of Reproductive Medicine, VU University Medical Centre (VUMC), Amsterdam, The Netherlands
M. Verschuuren
Affiliation:
Department of Obstetrics and Gynecology, Academic Medical Centre, Amsterdam, The Netherlands
L. J. Schoonmade
Affiliation:
Medical Library, Vrije Universiteit, Amsterdam, The Netherlands
C. B. Lambalk
Affiliation:
Department of Obstetrics & Gynecology, Division of Reproductive Medicine, VU University Medical Centre (VUMC), Amsterdam, The Netherlands
R. C. Painter
Affiliation:
Department of Obstetrics and Gynecology, Academic Medical Centre, Amsterdam, The Netherlands
*
*Address for correspondence: S. Sadrzadeh, Department of Obstetrics & Gynecology, Division of Reproductive Medicine, VU University Medical Centre, PO Box 7057, 1007 MB Amsterdam, The Netherlands. (Email: s.sadrzadeh@vumc.nl)
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Abstract

When the follicle reserve, which is developed solely during the fetal period, is depleted, women enter menopause. Intrauterine and childhood adverse conditions might affect the ovarian capacity by influencing follicle production in the first trimester, limiting the initial follicle pool or mediate an accelerated follicular loss thereafter. To investigate if adverse early life influences result in younger age at menopause, the following online databases were systematically searched: PubMed, EMBASE, CINHAL (EBSCO) and Cochrane library (Wiley) up to 1 January 2017. Eligibility, data extraction and quality assessment was independently performed by two researchers. A total of 5278 studies were identified, 11 studies were deemed eligible and included. Nine were cohort studies, 1 case–control study and 1 twin study. Due to the diversity of reported data and risk estimates we were unable to pool data or perform meta-analysis on pooled data. Prenatal and childhood exposure to famine was significantly associated to an earlier age at menopause in three studies. Mean differences in age at menopause varied from 4 months up to 1.7 years between famine exposed and unexposed women. Three studies described a significant association between a low weight at ages 1 or 2 and a younger age at menopause. A younger age at menopause was associated with a higher weight at birth in only one study and with a high ponderal index, a measure for fatness at birth in another study. None of the nine studies reporting on low birth weight and age at natural menopause find a significant association.

Keywords

birth weightchildhood growthfaminemenopausesystematic review
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 2 , April 2018 , pp. 127 - 136
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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References

1. McKinlay, SM, Brambilla, DJ, Posner, JG. The normal menopause transition. Maturitas. 1992; 14, 103–115.CrossRefGoogle ScholarPubMed
2. Daan, NM, Fauser, BC. Menopause prediction and potential implications. Maturitas. 2015; 82, 257–265.CrossRefGoogle ScholarPubMed
3. Faddy, MJ, Gosden, RG. A model conforming the decline in follicle numbers to the age of menopause in women. Hum Reprod. 1996; 11, 1484–1486.Google Scholar
4. Wallace, WH, Kelsey, TW. Human ovarian reserve from conception to the menopause. PLoS One. 2010; 5, e8772.CrossRefGoogle Scholar
5. Baker, TG. A quantitative and cytological study of germ cells in human ovaries. Proc R Soc Lond B Biol Sci. 1963; 158, 417–433.Google ScholarPubMed
6. Whincup, PH, Kaye, SJ, Owen, CG, et al. Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008; 300, 2886–2897.Google Scholar
7. Risnes, KR, Vatten, LJ, Baker, JL, et al. Birthweight and mortality in adulthood: a systematic review and meta-analysis. Int J Epidemiol. 2011; 40, 647–661.Google Scholar
8. Li, S, Zhang, M, Tian, H, et al. Preterm birth and risk of type 1 and type 2 diabetes: systematic review and meta-analysis. Obes Rev. 2014; 15, 804–811.Google Scholar
9. Newnham, JP, Ross, MG. Early Life Origins of Human Health and Disease. 2009. Karger: Los Angeles, CA.Google Scholar
10. Tarry-Adkins, JL, Ozanne, SE. The impact of early nutrition on the ageing trajectory. Proc Nutr Soc. 2014; 73, 289–301.Google Scholar
11. Barnes, SK, Ozanne, SE. Pathways linking the early environment to long-term health and lifespan. Prog Biophys Mol Biol. 2011; 106, 323–336.Google Scholar
12. Martin-Gronert, MS, Tarry-Adkins, JL, Cripps, RL, Chen, JH, Ozanne, SE. Maternal protein restriction leads to early life alterations in the expression of key molecules involved in the aging process in rat offspring. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R494–500.Google Scholar
13. Karowicz-Bilinska, A, Kedziora-Kornatowska, K, Bartosz, G. Indices of oxidative stress in pregnancy with fetal growth restriction. Free Radic Res. 2007; 41, 870–873.Google Scholar
14. Ozanne, SE, Hales, CN. Lifespan: catch-up growth and obesity in male mice. Nature. 2004; 427, 411–412.CrossRefGoogle ScholarPubMed
15. Li, Q, Geng, X, Zheng, W, et al. Current understanding of ovarian aging. Sci China Life Sci. 2012; 55, 659–669.Google Scholar
16. Wells, GA, Shea, B, O’Connell, D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. Retrieved June 2016 from http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm.Google Scholar
17. Sadrzadeh, S, Painter, RC, van Kasteren, YM, Braat, DD, Lambalk, CB. Premature ovarian insufficiency and perinatal parameters: a retrospective case-control study. Maturitas. 2017; 96, 72–76.Google Scholar
18. Yarde, F, Broekmans, FJ, van der Pal-de Bruin, KM, et al. Prenatal famine, birthweight, reproductive performance and age at menopause: the Dutch hunger winter families study. Hum Reprod. 2013; 28, 3328–3336.CrossRefGoogle ScholarPubMed
19. Tom, SE, Cooper, R, Kuh, D, et al. Fetal environment and early age at natural menopause in a British birth cohort study. Hum Reprod. 2010; 25, 791–798.Google Scholar
20. Kalichman, L, Malkin, I, Kobyliansky, E. Changes in reproductive indices in Chuvashian women whose maturation was during World War II. Maturitas. 2007; 56, 205–211.CrossRefGoogle ScholarPubMed
21. Mishra, G, Hardy, R, Kuh, D. Are the effects of risk factors for timing of menopause modified by age? Results from a British birth cohort study. Menopause. 2007; 14, 717–724.Google Scholar
22. Elias, SG, van Noord, PA, Peeters, PH, den Tonkelaar, I, Grobbee, DE. Caloric restriction reduces age at menopause: the effect of the 1944–1945 Dutch famine. Menopause. 2003; 10, 399–405.Google Scholar
23. Lawlor, DA, Ebrahim, S, Smith, GD. The association of socio-economic position across the life course and age at menopause: the British Women’s Heart and Health Study. BJOG. 2003; 110, 1078–1087.Google Scholar
24. Hardy, R, Kuh, D. Does early growth influence timing of the menopause? Evidence from a British birth cohort. Hum Reprod. 2002; 17, 2474–2479.Google Scholar
25. Treloar, SA, Sadrzadeh, S, Do, KA, Martin, NG, Lambalk, CB. Birth weight and age at menopause in Australian female twin pairs: exploration of the fetal origin hypothesis. Hum Reprod. 2000; 15, 55–59.Google Scholar
26. Cresswell, JL, Egger, P, Fall, CH, et al. Is the age of menopause determined in-utero? Early Hum Dev. 1997; 49, 143–148.CrossRefGoogle ScholarPubMed
27. Diamanti-Kandarakis, E, Papalou, O, Kandaraki, EA, Kassi, G. Mechanisms in endocrinology: nutrition as a mediator of oxidative stress in metabolic and reproductive disorders in women. Eur J Endocrinol. 2017; 176, R79–R99.Google Scholar
28. Wong, JM, Collins, K. Telomere maintenance and disease. Lancet. 2003; 362, 983–988.Google Scholar
29. Aiken, CE, Tarry-Adkins, JL, Ozanne, SE. Suboptimal nutrition in utero causes DNA damage and accelerated aging of the female reproductive tract. FASEB J. 2013; 27, 3959–3965.CrossRefGoogle ScholarPubMed
30. Tarry-Adkins, JL, Chen, JH, Smith, NS, et al. Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J. 2009; 23, 1521–1528.CrossRefGoogle ScholarPubMed
31. Tarry-Adkins, JL, Martin-Gronert, MS, Chen, JH, Cripps, RL, Ozanne, SE. Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J. 2008; 22, 2037–2044.Google Scholar
32. Butts, S, Riethman, H, Ratcliffe, S, et al. Correlation of telomere length and telomerase activity with occult ovarian insufficiency. J Clin Endocrinol Metab. 2009; 94, 4835–4843.Google Scholar
33. Kinugawa, C, Murakami, T, Okamura, K, Yajima, A. Telomerase activity in normal ovaries and premature ovarian failure. Tohoku J Exp Med. 2000; 190, 231–238.Google Scholar
34. Thurner, S, Klimek, P, Szell, M, et al. Quantification of excess risk for diabetes for those born in times of hunger, in an entire population of a nation, across a century. Proc Natl Acad Sci USA. 2013; 110, 4703–4707.CrossRefGoogle Scholar
35. Huang, C, Li, Z, Wang, M, Martorell, R. Early life exposure to the 1959-1961 Chinese famine has long-term health consequences. J Nutr. 2010; 140, 1874–1878.Google Scholar
36. Koupil, I, Plavinskaja, S, Parfenova, N, et al. Cancer mortality in women and men who survived the siege of Leningrad (1941-1944). Int J Cancer. 2009; 124, 1416–1421.CrossRefGoogle ScholarPubMed
37. Fentiman, IS, Allen, DS, Ellison, GT. The impact of the occupation of Guernsey 1940-1945 on breast cancer risk factors and incidence. Int J Clin Pract. 2007; 61, 937–943.Google Scholar
38. Kannisto, V, Christensen, K, Vaupel, JW. No increased mortality in later life for cohorts born during famine. Am J Epidemiol. 1997; 145, 987–994.Google Scholar
39. Nelson, LM, Covington, SN, Rebar, RW. An update: spontaneous premature ovarian failure is not an early menopause. Fertil Steril. 2005; 83, 1327–1332.Google Scholar
40. Pal, L, Santoro, N. Premature ovarian failure (POF): discordance between somatic and reproductive aging. Ageing Res Rev. 2002; 1, 413–423.Google Scholar
41. Harlow, SD, Gass, M, Hall, JE, et al. Executive summary of the Stages of Reproductive Aging Workshop+10: addressing the unfinished agenda of staging reproductive aging. J Clin Endocrinol Metab. 2012; 97, 1159–1168.CrossRefGoogle ScholarPubMed
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