Socioeconomic position, lifestyle factors and age at natural menopause: a systematic review and meta-analyses of studies across six continents

Danielle A J M Schoenaker, Caroline A Jackson, Jemma V Rowlands, Gita D Mishra, Danielle A J M Schoenaker, Caroline A Jackson, Jemma V Rowlands, Gita D Mishra

Abstract

Background: Age at natural menopause (ANM) is considered a marker of biological ageing and is increasingly recognized as a sentinel for chronic disease risk in later life. Socioeconomic position (SEP) and lifestyle factors are thought to be associated with ANM.

Methods: We performed a systematic review and meta-analyses to determine the overall mean ANM, and the effect of SEP and lifestyle factors on ANM by calculating the weighted mean difference (WMD) and pooling adjusted hazard ratios. We explored heterogeneity using meta-regression and also included unpublished findings from the Australian Longitudinal Study on Women's Health.

Results: We identified 46 studies across 24 countries. Mean ANM was 48.8 years [95% confidence interval (CI): 48.3, 49.2], with between-study heterogeneity partly explained by geographical region. ANM was lowest among African, Latin American, Asian and Middle Eastern countries and highest in Europe and Australia, followed by the USA. Education was associated with later ANM (WMD middle vs low education 0.30, 95% CI: 0.10, 0.51; high vs low education 0.64, 95% CI 0.26, 1.02). A similar dose-response relationship was also observed for occupation. Smoking was associated with a 1-year reduction of ANM (WMD: -0.91, 95% CI: -1.34, -0.48). Being overweight and moderate/high physical activity were modestly associated with later ANM, but findings were less conclusive.

Conclusions: ANM varies across populations, partly due to differences across geographical regions. SEP and some lifestyle factors are associated with ANM, but further research is needed to examine the impact of the associations between risk factors and ANM on future health outcomes.

Keywords: Menopause; body mass index; meta-analysis; physical activity; smoking; socioeconomic factors; systematic review.

© The Author 2014; all rights reserved. Published by Oxford University Press on behalf of the International Epidemiological Association.

Figures

Figure 1.
Figure 1.
Flow diagram of selection process and inclusion of studies for meta-analysis. 1Studies by Dravta et al. (2009) and Ku et al. (2004) each included two study populations.
Figure 2.
Figure 2.
Meta-analysis of mean age at natural menopause, stratified by geographical region (using random effects). CI, confidence interval. aChinese women in Taiwan; bsecond- or third-generation emigrants from Korea to China; cChinese Malay and Indian women in Singapore; dmean and standard error were calculated from the median and range using recommended formula; eStudy included centres from North, Central and South America (Argentina; Bolivia; Brazil; Chile; Colombia; Costa Rica; Cuba; Dominican Republic; Ecuador; Honduras; Mexico; Panama; Paraguay; Peru; Uruguay. Dotted line represents the overall summary mean age.
Figure 3.
Figure 3.
Meta-analysisa of the unadjusted effect of (a) middle education level, (b) high education level, (c) middle occupation level and (d) high occupation level on age of natural menopause. aRandom effects estimates. Third and fourth columns in the figures give the number of women classified as having a middle, high or low education level, and middle, high or low occupation level, as appropriate.
Figure 4.
Figure 4.
Meta-analysisa of the unadjusted effect of income on age of menopause. aRandom effects estimate.
Figure 5.
Figure 5.
Meta-analysisa of (a) the unadjusted effect of smoking on age of menopause and (b) the unadjusted effect of smoking on age of natural menopause, stratified by whether countries were ‘economically more developed regions’ or ‘other regions’.b WMD, weighted mean difference; CI, confidence interval. aRandom effects estimates; bthe meta-analysis stratified by region excludes one outlying study (Cooper et al.), since the direction of the effect estimate for smoking was clearly contrary to all other studies, and the exclusion of which removed all heterogeneity among ‘economically more developed regions’. The third and fourth columns in each figure give the number of women who were classified as smokers and non-smokers in each study.
Figure 6.
Figure 6.
Meta-analysis of the unadjusted effect of (a) overweighta (b) obesityb and (c) moderate/high physical activitya on age of natural menopause. WMD, weighted mean difference; CI, confidence interval. aRandom effects estimate; bfixed effects estimate. Third and fourth columns in the figures give the number of women classified as being normal weight, overweight or obese, and moderately to highly physically active or physically inactive (low or no physical activity), as appropriate.

References

    1. Kelsey JL, Gammon MD, John EM. Reproductive factors and breast cancer. Epidemiol Rev 1993;15:36.
    1. Franceschi S, La Vecchia C, Booth M, et al. Pooled analysis of 3 European case-control studies of ovarian cancer: II. Age at menarche and at menopause. Int J Cancer 1991;49:57–60
    1. Atsma F, Bartelink M-LEL, Grobbee DE, van der Schouw YT. Postmenopausal status and early menopause as independent risk factors for cardiovascular disease: a meta-analysis. Menopause 2006;13:265–79
    1. Joakimsen O, Bønaa KH, Stensland-Bugge E, Jacobsen BK. Population-based study of age at menopause and ultrasound assessed carotid atherosclerosis: The Tromsø Study. J Clin Epidemiol 2000;53:525–30
    1. Lisabeth LD, Beiser AS, Brown DL, Murabito JM, Kelly-Hayes M, Wolf PA. Age at natural menopause and risk of ischemic stroke: The Framingham Heart Study. Stroke 2009;40:1044–49
    1. Gallagher JC. Effect of early menopause on bone mineral density and fractures. Menopause 2007;14:567–71
    1. Ossewaarde ME, Bots ML, Verbeek ALM, et al. Age at menopause, cause-specific mortality and total life expectancy. Epidemiology 2005;16:556–62
    1. Mondul AM, Rodriguez C, Jacobs EJ, Calle EE. Age at natural menopause and cause-specific mortality. Am J Epidemiol 2005;162:1089–97
    1. Thomas F, Renaud F, Benefice E, De Meeus T, Guegan JF. International variability of ages at menarche and menopause: patterns and main determinants. Hum Biol 2001;73:271–90
    1. Morabia A, Costanza MC, ; World Health Organization Collaborative Study N. International variability in ages at menarche, first livebirth, and menopause. Am J Epidemiol 1998;148:1195–205
    1. Murabito JM, Yang Q, Fox C, Wilson PW, Cupples LA. Heritability of age at natural menopause in the Framingham Heart Study. J Clin Endocrinol Metab 2005;90:3427–30
    1. Sun L, Tan L, Yang F, et al. Meta-analysis suggests that smoking is associated with an increased risk of early natural menopause. Menopause 2012;19:126–32
    1. Parente RC, Faerstein E, Celeste RK, Werneck GL. The relationship between smoking and age at the menopause: A systematic review. Maturitas 2008;61:287–98
    1. Midgette AS, Baron JA. Cigarette smoking and risk of natural menopause. Epidemiology 1990;1:474–80
    1. Harlow BL, Signorello LB. Factors associated with early menopause. Maturitas 2000;35:3–9
    1. Canavez FS, Werneck GL, Parente RCM, Celeste RK, Faerstein E. The association between educational level and age at the menopause: a systematic review. Arch Gynecol Obstet 2011;283:83–90
    1. Brown WJ, Bryson L, Byles JE, et al. Women's Health Australia: recruitment for a national longitudinal cohort study. Women Health 1999;28:23–40
    1. Lee C, Dobson AJ, Brown WJ, et al. Cohort profile: the Australian longitudinal study on women's health. Int J Epidemiol 2005;34:987–91
    1. Berecki-Gisolf J, Begum N, Dobson AJ. Symptoms reported by women in midlife: menopausal transition or aging? Menopause 2009;16: 1021–29
    1. Guthrie J, Dennerstein L, Dudley E. Weight gain and the menopause: a 5-year prospective study. Climacteric 1999;2:205–11
    1. World Health Organization (WHO). Obesity: Preventing and Managing the Global Epidemic. Geneva: WHO, 2000
    1. Nagel G, Altenburg H-P, Nieters A, Boffetta P, Linseisen J. Reproductive and dietary determinants of the age at menopause in EPIC-Heidelberg. Maturitas 2005;52:337–47
    1. Yasui T, Hayashi K, Mizunuma H, et al. Factors associated with premature ovarian failure, early menopause and earlier onset of menopause in Japanese women. Maturitas 2012;72:249–55
    1. Li L, Wu J, Pu D, et al. Factors associated with the age of natural menopause and menopausal symptoms in Chinese women. Maturitas 2012;73:354–60
    1. Henderson KD, Bernstein L, Henderson B, Kolonel L, Pike MC. Predictors of the timing of natural menopause in the multiethnic cohort study. Am J Epidemiol 2008;167:1287–94
    1. Dratva J, Real FG, Schindler C, et al. Is age at menopause increasing across Europe? Results on age at menopause and determinants from two population-based studies. Menopause 2009;16:385–94
    1. Palmer JR, Rosenberg L, Wise LA, Horton NJ, Adams-Campbell LL. Onset of natural menopause in African American women. Am J Public Health 2003;93:299–306
    1. Gold EB, Bromberger J, Crawford S, et al. Factors associated with age at natural menopause in a multiethnic sample of midlife women. Am J Epidemiol 2001;153:865–74
    1. Sterne JAC. Meta-analysis in Stata: An Updated Collection from the Stata Journal. College Station, TX: Stata Press, 2009
    1. Harbord RM, Higgins JP. Meta-regression in Stata. Stata J 2008;8:493–519
    1. World Health Organization (WHO). Research on the Menopause in the 1990s. Geneva: World Health Organization, 1996
    1. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 2009;151:W65–94
    1. Akahoshi M, Soda M, Nakashima E, et al. The effects of body mass index on age at menopause. Int J Obes Relat Metab Disord 2002;26:961–68
    1. Ansari H, Rakhshani F, Vahedi MM, Mostafapour FK. Evaluation of socio-economic factors related to the natural menopause age in Zahedan, Southeastern Iran. Maturitas 2009;63:S67
    1. Ashrafi M, Ashtiani SK, Malekzadeh F, Amirchaghmaghi E, Kashfi F, Eshrati B. Factors associated with age at natural menopause in Iranian women living in Tehran. Int J Gynaecol Obstet 2008;102:175–76
    1. Ayatollahi SMT, Ghaem H, Ayatollahi SAR. Sociodemographic factors and age at natural menopause in Shiraz, Islamic Republic of Iran. East Mediterr Health J 2005;11:146–54
    1. Bener A, Rizk DE, Ezimokhai M, Hassan M, Micallef R, Sawaya M. Consanguinity and the age of menopause in the United Arab Emirates. Int J Gynaecol Obstet 1998;60:155–60
    1. Beser E, Aydemir V, Bozkaya H. Body mass index and age at natural menopause. Gynecol Obstet Invest 1994;37:40–42
    1. Blumel JE, Chedraui P, Calle A, et al. Age at menopause in Latin America. Menopause 2006;13:706–12
    1. Chang C, Chow SN, Hu Y. Age of menopause of Chinese women in Taiwan. Int J Gynaecol Obstet 1995;49:191–92
    1. Chmara-Pawlinska R, Szwed A. Cigarette smoking and the age of natural menopause in women in Poland. Przegl Lek 2004;61:1003–05
    1. Cooper GS, Sandler DP, Bohlig M. Active and passive smoking and the occurrence of natural menopause. Epidemiology 1999;10:771–73
    1. Delavar MA, Hajiahmadi M. Age at menopause and measuring symptoms at midlife in a community in Babol, Iran. Menopause 2011;18:1213–18
    1. Do KA, Treloar SA, Pandeya N, et al. Predictive factors of age at menopause in a large Australian twin study. Hum Biol 1998;70:1073–91
    1. Dorjgochoo T, Kallianpur A, Gao YT, et al. Dietary and lifestyle predictors of age at natural menopause and reproductive span in the Shanghai Women's Health Study. Menopause 2008;15:924–33
    1. Dvornyk V, Long J-R, Liu P-Y, et al. Predictive factors for age at menopause in Caucasian females. Maturitas 2006;54:19–26
    1. Fallahzadeh H. Age at natural menopause in Yazd, Islamic republic of Iran. Menopause 2007;14:900–04
    1. Fleming LE, Levis S, LeBlanc WG, et al. Earlier age at menopause, work, and tobacco smoke exposure. Menopause 2008;15:1103–08
    1. Garrido-Latorre F, Lazcano-Ponce EC, López-Carrillo L, Hernández-Avila M. Age of natural menopause among women in Mexico city. Int J Gynaecol Obstet 1996;53:159–66
    1. Hagstad A. Gynecology and sexuality in middle-aged women. Women Health 1988;13:57–80
    1. Harris AES, Bernstein RM, Kuhle BX. Predicting age at onset of menopause: Testing the “adaptive onset” hypothesis. Maturitas 2009;64:193–95
    1. Hong JS, Yi S-W, Kang HC, et al. Age at menopause and cause-specific mortality in South Korean women: Kangwha Cohort Study. Maturitas 2007;56:411–19
    1. Kaczmarek M. The timing of natural menopause in Poland and associated factors. Maturitas 2007;57:139–53
    1. Kriplani A, Banerjee K. An overview of age of onset of menopause in northern India. Maturitas 2005;52:199–204
    1. Ku SY, Kang JW, Kim H, et al. Regional differences in age at menopause between Korean-Korean and Korean-Chinese. Menopause 2004;11:569–74
    1. Kwawukume E, Ghosh T, Wilson J. Menopausal age of Ghanaian women. Int J Gynaecol Obstet 1993;40:151–55
    1. Lawlor DA, Ebrahim S, Davey Smith G. The association of socio-economic position across the life course and age at menopause: the British Women's Heart and Health Study. Int J Gynaecol Obstet 2003;110:1078–87
    1. Loh F-H, Khin L-W, Saw S-M, Lee JJM, Gu K. The age of menopause and the menopause transition in a multiracial population: a nation-wide Singapore study. Maturitas 2005;52:169–80
    1. Magursky V, Mesko M, Sokolik L. Age at the menopause and onset of the climacteric in women of Martin District, Czechoslovkia. Int J Fertil 1975;20:17–23
    1. McKnight KK, Wellons MF, Sites CK, et al. Racial and regional differences in age at menopause in the United States: findings from the REasons for Geographic And Racial Differences in Stroke (REGARDS) study. Am J Obstet Gynecol 2011;205:353.
    1. Okonofua F, Lawal A, Bamgbose J. Features of menopause and menopausal age in Nigerian women. Int J Gynaecol Obstet 1990;31:341–45
    1. OlaOlorun F, Lawoyin T. Age at menopause and factors associated with attainment of menopause in an urban community in Ibadan, Nigeria. Climacteric 2009;12:352–63
    1. Özdemir O, Çöl M. The age at menopause and associated factors at the health center area in Ankara, Turkey. Maturitas 2004;49:211–19
    1. Sievert LL, Hautaniemi SI. Age at menopause in Puebla, Mexico. Hum Biol 2003;75:205–26
    1. van Noord PAH, Dubas JS, Dorland M, Boersma H, Velde ET. Age at natural menopause in a population-based screening cohort: the role of menarche, fecundity, and lifestyle factors. Fertil Steril 1997;68:95–102
    1. Ortiz AP, Harlow SD, Sowers M, Nan B, Romaguera J. Age at natural menopause and factors associated with menopause state among Puerto Rican women aged 40-59 years, living in Puerto Rico. Menopause 2006;13:116–24
    1. Morris DH, Jones ME, Schoemaker MJ, McFadden E, Ashworth A, Swerdlow AJ. Body mass index, exercise, and other lifestyle factors in relation to age at natural menopause: analyses from the breakthrough generations study. Am J Epidemiol 2012;175:998–1005
    1. Luoto R, Kaprio J, Uutela A. Age at natural menopause and sociodemographic status in Finland. Am J Epidemiol 1994;139:64–76
    1. Cramer DW, Harlow BL, Xu H, Fraer C, Barbieri R. Cross-sectional and case-controlled analyses of the association between smoking and early menopause. Maturitas 1995;22:79–87
    1. Nagata C, Takatsuka N, Inaba S, Kawakami N, Shimizu H. Association of diet and other lifestyle with onset of menopause in Japanese women. Maturitas 1998;29:105–13
    1. Ayatollahi SMT, Ghaem H, Ayatollahi SAR. Determinants of age at natural menopause in Shiraz. Iran J Med Sci 2002;27:131–33
    1. Hardy R, Kuh D. Social and environmental conditions across the life course and age at menopause in a British birth cohort study. BJOG 2005;112:346–54
    1. Mishra GD, Cooper R, Tom SE, Kuh D. Early life circumstances and their impact on menarche and menopause. Women Health 2009;5:175–90
    1. Meek MD, Finch GL. Diluted mainstream cigarette smoke condensates activate estrogen receptor and aryl hydrocarbon receptor-mediated gene transcription. Environ Res 1999;80: 9–17
    1. Michnovicz JJ, Hershcopf RJ, Naganuma H, Bradlow HL, Fishman J. Increased 2-hydroxylation of estradiol as a possible mechanism for the anti-estrogenic effect of cigarette smoking. N Engl J Med 1986;315:1305–09
    1. Bancroft J, Cawood EHH. Androgens and the menopause; a study of 40–60-year-old women. Clin Endocrinol 1996; 45:577–87
    1. Essenberg J, Fagan L, Malerstein A. Chronic poisoning of the ovaries and tests of albino rats and mice by nicotine and cigarette smoke. West J Surg Obstet Gynecol 1951;59:27–32
    1. Mattison D, Thorgeirsson S. Smoking and industrial pollution, and their effects on menopause and ovarian cancer. Lancet 1978;311:187–88
    1. Leidy LE. Timing of menopause in relation to body size and weight change. Hum Biol 1996;68:967–82
    1. Aydin ZD. Determinants of age at natural menopause in the Isparta Menopause and Health Study: premenopausal body mass index gain rate and episodic weight loss. Menopause 2010;17:494–505
    1. Bromberger JT, Matthews KA, Kuller LH, Wing RR, Meilahn EN, Plantinga P. Prospective study of the determinants of age at menopause. Am J Epidemiol 1997;145:124–33
    1. McTiernan A, Tworoger SS, Ulrich CM, et al. Effect of exercise on serum estrogens in postmenopausal women: a 12-month randomized clinical trial. Cancer Res 2004;64:2923–28
    1. Higgins JP. Heterogeneity in meta-analysis should be expected and appropriately quantified (Commentary). Int J Epidemiol 2008;37:1158–60
    1. Ioannidis JP, Patsopoulos NA, Rothstein HR. Reasons or excuses for avoiding meta-analysis in forest plots. BMJ 2008;336:1413.
    1. Den Tonkelaar I. Validity and reproducibility of self-reported age at menopause in women participating in the DOM-project. Maturitas 1997;27:117–23
    1. Gold EB, Crawford SL, Avis NE, et al. Factors related to age at natural menopause: longitudinal analyses from SWAN. Am J Epidemiol 2013;178:70–83

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