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    J Korean Med Sci. 2020 Apr 13;35(14):e97. English.
    Published online Feb 26, 2020.
    https://doi.org/10.3346/jkms.2020.35.e97
    © 2020 The Korean Academy of Medical Sciences.
    Original Article

    Trends of Premature and Early Menopause: a Comparative Study of the US National Health and Nutrition Examination Survey and the Korea National Health and Nutrition Examination Survey

    Seung-Ah Choe,1,2 and Joohon Sung3
      • 1CHA Fertility Center, Seoul Station, Seoul, Korea.
      • 2Department of Epidemiology, Graduate School of Public Health, Brown University, Providence, RI, USA.
      • 3Graduate School of Public Health, Institute of Health and Environment, Seoul National University, Seoul, Korea.
    • Address for Correspondence: Joohon Sung, MD, PhD. Graduate School of Public Health, Institute of Health and Environment, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Korea. Email: jsung@snu.ac.kr
    Received September 02, 2019; Accepted February 13, 2020.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Background

    While evidence shows a tendency toward delays in menopause worldwide, whether prevalence of premature (< 40 years) or early menopause (40–44 years) is also reduced in different ethnic groups is uncertain. The aim of this study was to explore birth cohort effect in the prevalence of premature and early menopause in United States (US) and Korea.

    Methods

    This is a retrospective study using the National Health and Nutrition Examination Survey (NHANES, 1999–2014) and the Korea NHANES (KNHANES, 2007–2012). We analyzed prevalence of premature and early menopause in three ethnic groups of US and Korea. We restricted our analysis to women aged ≥ 45 years at the time of the survey born between 1920 and 1969. The data of both eligible 9,209 US women and 9,828 Korean was included in final analysis. We calculated odds ratios (OR) for each outcome adjusting for biological and socioeconomic factors, respectively.

    Results

    Prevalence of premature menopause was 1.7% in US, 2.8% in Korean women. Early menopause occurred in 3.4% and 7.2% of US and Korean, respectively. In US women, prevalence of premature and early menopause did not change and did not differ across three ethnicities. Korean women showed highest and consistently decreasing prevalence (P < 0.001). When we adjusted for covariates, birth lower risk for premature menopause was evident in US Non-Hispanic black born in 1950s and in Korean born between 1940s and 1960s compared to those born in 1920s. In the analysis of early menopause, excluding premature menopause patients, lower risk of more recent generation (born in 1940s and later) was evident in Korean women.

    Conclusion

    The trend and birth cohort effect in occurrence of premature and early menopause among the US and Korea women are different. Prevalences of premature and early menopause decrease only in Korean.

    Graphical Abstract

    Keywords
    Menopause; Ethnicity; Socioeconomic Status

    INTRODUCTION

    The majority of women experience natural menopause at their age between late 40s and early 50s globally.1, 2 Although population-based data are limited, premature menopause is known to occur in approximately 1%–8.6% and early menopause occurs in 4.9%–9.4% of women.3, 4, 5 Earlier menopause is an irreversible event and has lifelong consequences, including an increased risk of neurological impairment, glaucoma, cardiovascular disease, osteoporosis, mental disorders, and general mortality.6, 7, 8, 9 Hormone therapy alleviates some of the adverse effects.10, 11 Thus, if possible, prediction and prevention through the modification of risk factors would be crucial for improving women's health.

    The etiology of earlier menopause remains elusive. Although several genes identified play roles particularly in the development of premature menopause,12, 13 they cannot explain majority of cases.14 Environmental and behavioral factors, such as obesity, ethnicity (African–American or Hispanic ancestry), early onset of smoking, higher parity, and lower socioeconomic status, are also associated with early menopause.15, 16 Early menarche is associated with earlier menopause in several studies,17, 18 which was not replicated in others.19, 20 Likewise, nulliparity was associated with higher risk of early menopause in European cohort,5, 21 but not in a study of Japanese women.22 Socioeconomic factors that were found to be associated with early menopause in European women,23, 24, 25 but not significant in Northern India population.26 This heterogeneity in the effect of biologic and social factors on age at menopause across ethnicities, cultural context, or data source may contribute to general incidence of premature or early menopause.27

    Globally, age at natural menopause is increasing across populations.28 Considering that reported risk factors for earlier menopause, such as smoking in women, nulliparity, obesity, and early menarche, are increasing, this change might have exerted pressure toward increase in premature or early menopause, rather than decrease, which seemingly conflicts with observed trends of delays in menopause.29 In addition, environmental studies suggested that exposures to endocrine disruptors are constantly increasing, which might deplete ovarian reserve and fasten natural menopause.30 However, whether the general trend in the delay of menopause is parallel to the reduction of earlier menopause is not clear.

    Few studies have depicted the trends of premature or early menopause and possible birth cohort effects controlling for multiple covariates in different ethnic groups. Because prevalence of premature menopause is as low as 1%, large population would be necessary to conduct epidemiologic study. We aimed to explore and compare the trends of premature or early menopause between women in three ethnic groups in the US and Korea using nationally representative population data collected through similar survey methods.

    METHODS

    Study population

    Our study comprised two groups of women groups (women from the US and Korea aged 45 or over). Data of US women was retrieved from eight waves of the National Health and Nutrition Examination Survey (NHANES) conducted from 1999 to 2014. Korean data was obtained from seven waves of the Korea National Health and Nutrition Examination Survey (KNHANES) conducted from 2007 to 2012, which used the same questionnaire on the onset of smoking as the NHANES. Although the general survey method and questionnaires are not completely identical, the survey method and modalities of the KNHANES are similar to those of the NHANES because the survey was developed in reference to the NHANES.

    The NHANES is among the series of health-related programs conducted by the Centers for Disease Control and Prevention of the National Center for Health Statistics. Approximately 5,000 people per year participated in the NHANES. It is a collection of demographic, socioeconomic, dietary, and health survey data for a nationally representative sample of the resident civilian non-institutionalized US population.31 As described elsewhere, a four-stage sample design was used in the NHANES.32

    The KNHANES is a nation-wide survey in Korea, organized by the Korea Centers for Disease Control. Each wave provides nationally representative data for the Korean population. For stratification, survey population was sampled using “rolling survey sampling,” which is described previously.33 In each wave, a new sample of about 10,000 individuals comprised approximately 200,000 geographically defined primary sampling units (PSUs). Each PSU contained approximately an average of 60 households, and 20 final target households were selected by systematic sampling from each PSU.

    During both surveys, participants were interviewed on their socio-demographic characteristics by trained interviewers. Information about age at menarche, level of education, relative quartiles of household income (reference to the household income level of the total population) was obtained from a face-to-face interview. Body mass index (BMI) data was obtained from examination data. We assessed smoking history using self-reporting questionnaires. Because both datasets are publicly available survey datasets which do not contain identifiable private information, this study does not require IRB approval.

    Study variables

    Based on the NHANES data, the participants were classified as one of the following: all Hispanic (Mexican American and other Hispanics), non-Hispanic white, non-Hispanic black, and other races (including multi-racial). As an indicator for individual economic status, household income that falls below the poverty line ratio was used, which measures the relative household income that considers family size.34 The relative level of household income that falls below the poverty line ratio in each ethnic group was included in the model as quartile scales. Educational attainment status was categorized into three groups: middle school graduation or lower, high school graduation, and college graduation or higher. Based on the NHANES data obtained from 1999 to 2014, smoking history (onset of smoking) was available among the relevant lifestyle factors during the premenopausal period. Because only smoking was associated with the occurrence of menopause,35 women who started smoking before the age of 40 were considered as smokers. Reproductive history included early menarche, primiparity, and age at last menstrual period. Early menarche was defined as menarche before the age of 12. Age at menopause was considered as age at natural menopause for all the women excluding those with a history of hysterectomy or bilateral oophorectomy before menopause.

    The KNHANES shared survey questions for age at menarche, number of live births, and age at last menstrual period which are well-known determinants for timing of menopause.36, 37 For an economic status indicator, the ratio of family income to poverty line was used in the NHANES and relative household income for family size in KNHANES were used because no identical indicator for relative household income were available for both datasets. For both survey data, oral contraceptive use and current alcohol drinking were not included in the covariates because its information at the time of the survey does not represent the past exposure.

    Determination of premature and early menopause

    The menopause state was assessed by asking “What is the reason not having a period these days?” The information on age at menopause was obtained only from participants who have answered “naturally menopaused”. We defined natural menopause as menopausal state which is not the consequence of medical treatment, hysterectomy or bilateral oophorectomy. Those who did not experience menopause at the time of survey were considered to have neither premature nor early menopause. We excluded women who had any history of hysterectomy or bilateral oophorectomy and reported menopause induced by medical treatment before 40. Women without menstrual history who were born before 1920 or after 1969 or with unclear cause of menopause were also excluded from the final analysis. Due to the limited number of populations (5.7%) and unknown composition of nationality, US ethnic group classified ‘others’ were excluded from the final analysis. The ‘others’ ethnic group included peoples from the Far East, Southeast Asia, or the Indian subcontinent were among the Asians.32 Following previous studies, we defined premature menopause as having final menstruation before the age of 40 years. Early menopause is defined as being menopaused at the age of 40-45 years.5, 38

    Statistical analysis

    We compared mean and proportions calculated with weighted values considering sampling design to explore homogeneities among three ethnic groups and Korean. Correlation structures among the key covariates, such as menarcheal age, number of deliveries, BMI, level of education, and household income, were assessed using R (ver. 3.5.0; R Foundation for Statistical Computing, Vienna, Austria). We used weighted results for all of the analyses stratified by four ethnic groups: all US Hispanic, US non-Hispanic white, US non-Hispanic black (from NHANES), and Koreans (from KNHANES). We defined birth cohort based on the reported year of birth. We explored linear trend of birth cohort-specific prevalence of premature and early menopause using logistic linear regression analysis. We calculated adjusted odds ratios (ORs) and 95% confidence intervals for each of birth cohort. When calculating ORs for early menopause, reference group excluded premature menopause cases. We adopted sampling weight-based survey analytics using SAS 9.4 software (SAS Institute, Cary, NC, USA).

    RESULTS

    Among 12,669 women aged 45 or over at the time of the survey in the NHANES data, 9,209 (72.7%) US women met the inclusion criteria and were included in the study. In the KNHANES, among 11,463 women aged 45 or over at the time of the survey, 9,828 (85.7%) women were included in the analysis (Fig. 1).

    Fig. 1
    Exclusion of study population of US (NHANES, 1999–2014) and Korean women (KNHANES, 2007–2012).
    NHANES = National Health and Nutrition Examination Survey, KNHANES = Korea National Health and Nutrition Examination Survey.

    In pooled data, prevalence of premature menopause was 1.7% in US, 2.8% in Korean women. Early menopause occurred in 3.4% and 7.2% of US and Korean, respectively. Premature and early menopause in Korean women peaked among those born in 1920s and consistently decreased in younger generations (P < 0.001 for premature and early menopause) (Fig. 2). In the US women, there was no secular change in all three ethnic groups for both premature and early menopause.

    Fig. 2
    Trend of cohort-specific prevalence of premature and early menopause in the three ethnic groups in US and Korean women. (A) Premature menopause (< 40 years), (B) Early menopause (40–44 years).

    Median age at the time of survey ranged from 57.3 to 61.0 years. Median age of at natural menopause was 47.3–49.4 years (Table 1). US non-Hispanic white women had the lowest prevalence of premature (1.7%) and early (3.2%) menopause, and Koreans had the highest (2.8% of premature and 7.2% of early menopause). Prevalence of premature and early menopause was not different among the three ethnic groups of the US. Korean women had higher premature (< 0.001) and early (< 0.001) menopause rate. A higher proportion of US women (27.7%–43.8%) started smoking before 40 compared than Korean (5.6%). The weighted mean age at menarche was higher in Korean women (15.2 years) than that of US women (12.7–12.9 years). The majority of non-Hispanic white (59.5%) and black (47.3%) women had college education. On the other hand, more than half of the US Hispanic and Korean women had middle school or lower education. Mean number of deliveries ranged from 2.6 to 3.8. There was weak and moderate correlation between each pair of covariates, including menarcheal age, number of deliveries, BMI, level of education, and household income (Supplementary Fig. 1). Among non-Hispanic black women, those born in 1950s showed lower risk for premature menopause. Birth cohort effect was evident in Korean women showing decreasing risk for premature menopause for those born in 1940 or later (Table 2). For early menopause, none of the birth cohorts showed higher risk in the three US ethnic groups. Korean women born in 1940s and later showed consistently lower risk for early menopause.

    Table 1
    Demographic characteristics of study population of US (NHANES, 1999–2014) and Korean women (KNHANES, 2007–2012)

    Table 2
    Adjusted OR for premature (< 40 years) and early (40–44 years) menopause in the three ethnic groups in US (NHANES, 1999–2014) and Korean women (KNHANES, 2007–2012)

    DISCUSSION

    The present study explored temporal trend and risk factors for premature and early menopause among women in the US and Korea using population-based data which is based on the same questionnaires. Particularly, when controlling for BMI, number of deliveries, education, household income, smoking and birth cohort, association of year of birth with premature and early menopause was not identical across three ethnic groups and Korean. This finding suggests that birth cohort effect can be different across ethnicities and national context. Premature or early menopause did not decrease in the three US ethnic groups. We observed downward trend only in Korean women. Specifically, premature menopause decreased in US black women born in 1950s and Korean women born in 1940s and later. To the best of our knowledge, this is the first study exploring premature and early menopause using combined dataset from NHANES and KNHANES.

    Our finding shows similar prevalence of premature and early menopause across three ethnic groups and birth cohorts in the US women. However, ethnic difference in prevalence have been reported both for premature and early menopause. In the US population, African American (1.4%) and Hispanic (1.4%) women showed highest and Asian (0.1%–0.5%) women had lowest risk for premature menopause.3 Recent observational study of UK, Scandinavia, Australia and Japan women showed generally higher risk in UK population (1.0%–3.6%) compared to the others.5 For early menopause, the prevalence was between 4.9% and 9.4% in the same study population.5 Although the size of population is small, 22.9% of Nigerian women experience menopause before age of 45 years.39 This similar prevalence of premature and early menopause among different ethnic groups within the US population would be due to potential effect of early childhood on menopausal timing.20 Similar environment in early stage of life would have affected the more similar menopausal timing within the country. In a clinical study of single medical center, women whose birthplace is outside of US had higher incidence of premature menopause.40

    Given the increasing trend of age at natural menopause, we can expect the numbers of women who experience premature or early menopause to decrease over time accordingly. However, downward pattern of premature and early menopause was evident only in Korean women. According to a previous multi-ethnic study, both the incidence of premature and early menopause in Korean women born before 1940s is even higher than in Japanese born during the similar period.3 Korean women born in 1920s and 1930s would have been malnourished and socially deprived during their adolescence or young adulthood because of the Korean War occurred in the early 1950s. Epidemiological studies have indicated that caloric restriction or malnutrition during childhood is linked with earlier age at natural menopause.41, 42, 43 Weight gain in early childhood, however, was associated with later menopause.44 Downward trend of premature and early menopause prevalence in younger generation may reflect improved nutritional status and better environment.

    As a cross-sectional study using a combined national data, we have several limitations. First, covariates such as BMI and household income were assessed at the time of survey and might have led misclassification. However, the effect of this bias would be minimized because BMI classification is likely to remain consistent through middle and older age groups.45 Second, several predictors for earlier menopause were unavailable in our study. Information of family history of premature menopause (US and Korean), history of unilateral oophorectomy (Korean), history of oral contraceptives use (Korean) and environmental exposure to heavy metals at the time of menopause were missing and alcohol dose at the time of menopause was incomplete (US). According to a survey conducted in 2015–2017, most common contraceptive methods used were found to be female sterilization (18.6%), oral contraceptive pill (12.6%), and long-acting reversible contraceptives (LARCs) (10.3%) all of which are potentially associated with timing of menopause.46, 47, 48, 49 Duration and type of contraception is known to be associated with timing of menopause but they are also affected by menopausal status.50 Given that the composition of oral contraceptives was similar between 2008 and 2014,51 we believe the effect of oral contraceptive use on the trend of premature or early menopause would have been minimal. Lastly, cultural or lifestyle differences between the US and Korean women could have interfered comparability. For example, a study reported a stronger association of dietary carbohydrate with metabolic syndrome in Korean than in American which was due to higher consumption of carbohydrate.52 Likewise, dietary or nutritional difference between Western and Asian cultures could have affected on the associations in this study. Considering the cultural and ethnical diversity within the US women, we believe that the impact of dissimilarities would have been minimal in our analyses.

    In conclusion, despite the generally increasing mean age of menopause of the US and Korea, we found downward trend of premature and early menopause only in Korean women. The understanding of the ethnic-specific difference in the trend may attribute to more effective prevention and management of premature and early menopause.

    SUPPLEMENTARY MATERIAL

    Supplementary Fig. 1

    Correlation structure of covariates stratified by ethnic groups of National Health and Nutrition Examination Survey and Korea National Health and Nutrition Examination Survey.

    Click here to view.(2M, ppt)

    Notes

    Funding:This work was supported by Basic Science Research Program through the National Research Foundation of Korea (grant No. NRF-2016R1D1A1B03933410 and 2018R1D1A1B07048821).

    Disclosure:The authors have no potential conflicts of interest to disclose.

    Author Contributions:

    • Conceptualization: Sung J.

    • Formal analysis: Choe SA.

    • Methodology: Choe SA.

    • Writing - original draft: Choe SA.

    • Writing - review & editing: Sung J.

    ACKNOWLEDGMENTS

    The authors would like to thank all participants involved in the NHANES and KNHANES.

    References

      1. McKinlay SM. The normal menopause transition: an overview. Maturitas 1996;23(2):137–145.
      1. Reynolds RF, Obermeyer CM. Age at natural menopause in Spain and the United States: results from the DAMES project. Am J Hum Biol 2005;17(3):331–340.
      1. Luborsky JL, Meyer P, Sowers MF, Gold EB, Santoro N. Premature menopause in a multi-ethnic population study of the menopause transition. Hum Reprod 2003;18(1):199–206.
      1. Haller-Kikkatalo K, Uibo R, Kurg A, Salumets A. The prevalence and phenotypic characteristics of spontaneous premature ovarian failure: a general population registry-based study. Hum Reprod 2015;30(5):1229–1238.
      1. Mishra GD, Pandeya N, Dobson AJ, Chung HF, Anderson D, Kuh D, et al. Early menarche, nulliparity and the risk for premature and early natural menopause. Hum Reprod 2017;32(3):679–686.
      1. Wu X, Cai H, Kallianpur A, Li H, Yang G, Gao J, et al. Impact of premature ovarian failure on mortality and morbidity among Chinese women. PLoS One 2014;9(3):e89597
      1. Podfigurna-Stopa A, Czyzyk A, Grymowicz M, Smolarczyk R, Katulski K, Czajkowski K, et al. Premature ovarian insufficiency: the context of long-term effects. J Endocrinol Invest 2016;39(9):983–990.
      1. Muka T, Oliver-Williams C, Kunutsor S, Laven JS, Fauser BC, Chowdhury R, et al. Association of age at onset of menopause and time since onset of menopause with cardiovascular outcomes, intermediate vascular traits, and all-cause mortality: a systematic review and meta-analysis. JAMA Cardiol 2016;1(7):767–776.
      1. Kim YE, Park H, Jo MW, Oh IH, Go DS, Jung J, et al. Trends and patterns of burden of disease and injuries in Korea using disability-adjusted life years. J Korean Med Sci 2019;34 Suppl 1:e75
      1. Faubion SS, Kuhle CL, Shuster LT, Rocca WA. Long-term health consequences of premature or early menopause and considerations for management. Climacteric 2015;18(4):483–491.
      1. Girard R, Météreau E, Thomas J, Pugeat M, Qu C, Dreher JC. Hormone therapy at early post-menopause increases cognitive control-related prefrontal activity. Sci Rep 2017;7(1):44917.
      1. Tibiletti MG, Testa G, Vegetti W, Alagna F, Taborelli M, Dalprà L, et al. The idiopathic forms of premature menopause and early menopause show the same genetic pattern. Hum Reprod 1999;14(11):2731–2734.
      1. Hoyos LR, Thakur M. Fragile X premutation in women: recognizing the health challenges beyond primary ovarian insufficiency. J Assist Reprod Genet 2017;34(3):315–323.
      1. Beck-Peccoz P, Persani L. Premature ovarian failure. Orphanet J Rare Dis 2006;1(1):9.
      1. Persani L, Rossetti R, Cacciatore C. Genes involved in human premature ovarian failure. J Mol Endocrinol 2010;45(5):257–279.
      1. Hewlett M, Mahalingaiah S. Update on primary ovarian insufficiency. Curr Opin Endocrinol Diabetes Obes 2015;22(6):483–489.
      1. Zsakai A, Mascie-Taylor N, Bodzsar EB. Relationship between some indicators of reproductive history, body fatness and the menopausal transition in Hungarian women. J Physiol Anthropol 2015;34(1):35.
      1. Hardy R, Kuh D. Reproductive characteristics and the age at inception of the perimenopause in a British National Cohort. Am J Epidemiol 1999;149(7):612–620.
      1. Gold EB. The timing of the age at which natural menopause occurs. Obstet Gynecol Clin North Am 2011;38(3):425–440.
      1. Forman MR, Mangini LD, Thelus-Jean R, Hayward MD. Life-course origins of the ages at menarche and menopause. Adolesc Health Med Ther 2013;4:1–21.
      1. Chang SH, Kim CS, Lee KS, Kim H, Yim SV, Lim YJ, et al. Premenopausal factors influencing premature ovarian failure and early menopause. Maturitas 2007;58(1):19–30.
      1. Yasui T, Hayashi K, Mizunuma H, Kubota T, Aso T, Matsumura Y, et al. Factors associated with premature ovarian failure, early menopause and earlier onset of menopause in Japanese women. Maturitas 2012;72(3):249–255.
      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(3):346–354.
      1. Luoto R, Kaprio J, Uutela A. Age at natural menopause and sociodemographic status in Finland. Am J Epidemiol 1994;139(1):64–76.
      1. 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(12):1078–1087.
      1. Kriplani A, Banerjee K. An overview of age of onset of menopause in northern India. Maturitas 2005;52(3-4):199–204.
      1. Kaczmarek M. The timing of natural menopause in Poland and associated factors. Maturitas 2007;57(2):139–153.
      1. Nichols HB, Trentham-Dietz A, Hampton JM, Titus-Ernstoff L, Egan KM, Willett WC, et al. From menarche to menopause: trends among US Women born from 1912 to 1969. Am J Epidemiol 2006;164(10):1003–1011.
      1. Pakarinen M, Raitanen J, Kaaja R, Luoto R. Secular trend in the menopausal age in Finland 1997–2007 and correlation with socioeconomic, reproductive and lifestyle factors. Maturitas 2010;66(4):417–422.
      1. Wang D, Wang M, Cheng N, Zheng T, Hu X, Li H, et al. Sulfur dioxide exposure and other factors affecting age at natural menopause in the Jinchuan cohort. Climacteric 2015;18(5):722–732.
      1. Mirel LB, Mohadjer LK, Dohrmann SM, Clark J, Burt VL, Johnson CL, et al. National health and nutrition examination survey: estimation procedures, 2007–2010. Vital Health Stat 2 2013;(159):1–17.
      1. Curtin LR, Mohadjer LK, Dohrmann SM, Kruszon-Moran D, Mirel LB, Carroll MD, et al. National health and nutrition examination survey: sample design, 2007–2010. Vital Health Stat 2 2013;(160):1–23.
      1. Park HA. The Korea national health and nutrition examination survey as a primary data source. Korean J Fam Med 2013;34(2):79.
      1. Wise LA, Krieger N, Zierler S, Harlow BL. Lifetime socioeconomic position in relation to onset of perimenopause. J Epidemiol Community Health 2002;56(11):851–860.
      1. Tawfik H, Kline J, Jacobson J, Tehranifar P, Protacio A, Flom JD, et al. Life course exposure to smoke and early menopause and menopausal transition. Menopause 2015;22(10):1076–1083.
      1. Park YJ, Kim HS, Kang HC. The age at menopause and related factors in Korean women. J Korean Acad Nurs 2002;32(7):1024–1031.
      1. Shin YJ, Song JY, Kim MJ, Choi JI, Han KD, Lee HN. Relationship between age at last delivery and age at menopause: the Korea national health and nutrition examination survey. Obstet Gynecol Sci 2017;60(4):362–368.
      1. Committee Opinion No. 605: primary ovarian insufficiency in adolescents and young women. Obstet Gynecol 2014;123:193–197.
      1. Agaba P, Meloni S, Sule H, Ocheke A, Agaba E, Idoko J, et al. Factors associated with early menopause among women in Nigeria. J Virus Erad 2017;3(3):145–151.
      1. Deering VA. In: Prevalence of premature ovarian failure and premature menopause in refugee and immigrant women in the U.S. compared to that of women born in the United States [Thesis]. New York, NY: Stony Brook University; 2014.
      1. 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(5):399–405.
      1. Wang N, Huang Y, Wen J, Su Q, Huang Y, Cai L, et al. Early life exposure to famine and reproductive aging among Chinese women. Menopause 2019;26(5):463–468.
      1. Yarde F, Broekmans FJ, van der Pal-de Bruin KM, Schönbeck Y, te Velde ER, Stein AD, et al. Prenatal famine, birthweight, reproductive performance and age at menopause: the Dutch hunger winter families study. Hum Reprod 2013;28(12):3328–3336.
      1. Hardy R, Kuh D. Does early growth influence timing of the menopause? Evidence from a British birth cohort. Hum Reprod 2002;17(9):2474–2479.
      1. Wang M, Yi Y, Roebothan B, Colbourne J, Maddalena V, Wang PP, et al. Body mass index trajectories among middle-aged and elderly Canadians and associated health outcomes. J Environ Public Health 2016;2016:7014857
      1. de Vries E, den Tonkelaar I, van Noord PA, van der Schouw YT, te Velde ER, Peeters PH. Oral contraceptive use in relation to age at menopause in the DOM cohort. Hum Reprod 2001;16(8):1657–1662.
      1. van Noord PA, Dubas JS, Dorland M, Boersma H, te Velde E. Age at natural menopause in a population-based screening cohort: the role of menarche, fecundity, and lifestyle factors. Fertil Steril 1997;68(1):95–102.
      1. Daniels K, Abma JC. Current contraceptive status among women aged 15–49: United States, 2015–2017. [Updated 2018].
        https://nchstats.com/2018/12/19/current-contraceptive-status-among-women-aged-15-49-united-states-2015-2017/.
      1. Pokoradi AJ, Iversen L, Hannaford PC. Factors associated with age of onset and type of menopause in a cohort of UK women. Am J Obstet Gynecol 2011;205(1):34.e1–34.13.
      1. Ferreira JM, Monteiro I, Castro S, Villarroel M, Silveira C, Bahamondes L. The use of long acting reversible contraceptives and the relationship between discontinuation rates due to menopause and to female and male sterilizations. Rev Bras Ginecol Obstet 2016;38(5):210–217.
      1. Kavanaugh ML, Jerman J. Contraceptive method use in the United States: trends and characteristics between 2008, 2012 and 2014. Contraception 2018;97(1):14–21.
      1. Ha K, Kim K, Chun OK, Joung H, Song Y. Differential association of dietary carbohydrate intake with metabolic syndrome in the US and Korean adults: data from the 2007-2012 NHANES and KNHANES. Eur J Clin Nutr 2018;72(6):848–860.
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    MeSH Terms
    Menopause*
    Adult
    Female
    Humans
    Menopause, Premature
    Middle Aged
    Nutrition Assessment
    Premature Birth/epidemiology
    Prevalence
    Republic of Korea/epidemiology
    Retrospective Studies
    Socioeconomic Factors
    Surveys and Questionnaires
    United States/epidemiology
    Metrics
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