The menopause transition and women's health at midlife: a progress report from the Study of Women's Health Across the Nation (SWAN)

Samar R El Khoudary, Gail Greendale, Sybil L Crawford, Nancy E Avis, Maria M Brooks, Rebecca C Thurston, Carrie Karvonen-Gutierrez, L Elaine Waetjen, Karen Matthews, Samar R El Khoudary, Gail Greendale, Sybil L Crawford, Nancy E Avis, Maria M Brooks, Rebecca C Thurston, Carrie Karvonen-Gutierrez, L Elaine Waetjen, Karen Matthews

Abstract

Objective: Our initial understanding of the menopause transition (MT) has been framed by clinical samples of women seeking treatment rather than by population-based studies. The Study of Women's Health Across the Nation (SWAN) initiated in 1996 with an overall goal to define the MT, to characterize its biological and psychosocial antecedents and sequelae in an ethnically and racially diverse sample of midlife women.

Methods: This review summarizes the central findings of SWAN to date that can inform women and their healthcare providers about the impact of the MT and midlife aging on overall health and well-being.

Results: SWAN characterized changes in reproductive axis and menstrual cycle patterns that informed the development of the reproductive aging staging system Staging of Reproductive Aging Workshop+10; MT-related symptoms and mental health (vasomotor symptoms, sleep complaints, psychological symptoms, cognitive performance, and urogenital and sexual health); and physiological systems and functions (cardiovascular and cardiometabolic health, bone health, physical function performance) that are influenced by the MT. SWAN demonstrated substantial interrelations among these changes and significant racial/ethnic differences in the rate and magnitude of change in multiple health indictors in midlife women. The findings point to midlife as a critical stage for adopting healthy behavior and preventive strategies.

Conclusions: Over the past 23 years, SWAN has advanced our understanding of the impact of the MT and midlife aging on health and well-being in women. SWAN will be instrumental to determine whether MT-related changes during midlife are related to unfavorable health and well-being in early old age.

Figures

Box 1
Box 1
Take-home messages: the reproductive axis, menstrual cycle patterns, and stages of the menopause transition
Box 2
Box 2
Take-home messages: symptoms and mental health
Box 3
Box 3
Take-home messages: physiological systems and functions
FIG. 1
FIG. 1
Central Illustration Figure. The Contribution of the Menopause Transition and Midlife Aging to Women's Health and Well-being: What Have We Learned from the Study of Women's Health Across the Nation (SWAN)?; SWAN contributed to our understanding of the impacts of the menopause transition versus midlife aging on women's health and well-being in different domains. The figure lists changes occurring during the menopause transition that were reviewed in this paper, and differentiates whether these changes were more driven by the menopause transition or midlife aging using different color schemes. Light orange bars depict changes that were mostly driven by the menopause transition, whereas blue bars depict changes that were mostly driven by midlife aging. Transient changes are identified when applicable by fading color bars and listing the word “Transient” at the end of relevant bars. SWAN has identified midlife as a critical stage for adopting healthy behavior and preventive strategies.

References

    1. Kaufert PA. Women and their health in the middle years: a Manitoba project. Soc Sci Med 1984; 18:279–281.
    1. McKinlay JB, McKinlay SM, Brambilla DJ. Health status and utilization behavior associated with menopause. Am J Epidemiol 1987; 125:110–121.
    1. Matthews KA, Meilahn E, Kuller LH, Kelsey SF, Caggiula AW, Wing RR. Menopause and risk factors for coronary heart disease. N Engl J Med 1989; 321:641–646.
    1. Guthrie JR, Dennerstein L, Taffe JR, Lehert P, Burger HG. The menopausal transition: a 9-year prospective population-based study. The Melbourne Women's Midlife Health Project. Climacteric 2004; 7:375–389.
    1. Woods NF, Mitchell ES. The Seattle Midlife Women's Health Study: a longitudinal prospective study of women during the menopausal transition and early postmenopause. Womens Midlife Health 2016; 2:6.
    1. Sowers M, Crawford S, Sternfeld B, et al. SWAN: a multi-center, multi-ethnic, community-based cohort study of women and the menopausal transition. In: Lobo RA, Kelsey J, Marcus R, editors. Menopause: Biology and Pathobiology. San Diego, CA: Academic press, 2000:175–188.
    1. Zaidi A. Life cycle transitions and vulnerabilities in old age: a review (Occasional Paper). UNDP Human Development Report Office 2014.
    1. 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.
    1. Randolph JF, Jr, Zheng H, Sowers MR, et al. Change in follicle-stimulating hormone and estradiol across the menopausal transition: effect of age at the final menstrual period. J Clin Endocrinol Metab 2011; 96:746–754.
    1. Tepper PG, Randolph JF, Jr, McConnell DS, et al. Trajectory clustering of estradiol and follicle-stimulating hormone during the menopausal transition among women in the Study of Women's Health across the Nation (SWAN). J Clin Endocrinol Metab 2012; 97:2872–2880.
    1. Paramsothy P, Harlow SD, Elliott MR, et al. Influence of race/ethnicity, body mass index, and proximity of menopause on menstrual cycle patterns in the menopausal transition: the Study of Women's Health Across the Nation. Menopause 2015; 22:159–165.
    1. Kassam A, Overstreet JW, Snow-Harter C, DeSouza MJ, Gold EB, Lasley BL. Identification of anovulation and transient luteal function using a urinary pregnanediol-3-glucuronide ratio algorithm. Environ Health Perspect 1996; 104:408–413.
    1. Santoro N, Crawford SL, El Khoudary SR, et al. Menstrual cycle hormone changes in women traversing menopause: study of Women's Health Across the Nation. J Clin Endocrinol Metab 2017; 102:2218–2229.
    1. Soules MR, Sherman S, Parrott E, et al. Executive summary: Stages of Reproductive Aging Workshop (STRAW). Fertil Steril 2001; 76:874–878.
    1. Harlow SD, Mitchell ES, Crawford S, et al. The ReSTAGE Collaboration: defining optimal bleeding criteria for onset of early menopausal transition. Fertil Steril 2008; 89:129–140.
    1. Harlow SD, Crawford S, Dennerstein L, Burger HG, Mitchell ES, Sowers MF. ReSTAGE Collaboration. Recommendations from a multi-study evaluation of proposed criteria for staging reproductive aging. Climacteric 2007; 10:112–119.
    1. Harlow SD, Paramsothy P. Menstruation and the menopausal transition. Obstet Gynecol Clin N Am 2011; 38:595–607.
    1. Paramsothy P, Harlow SD, Nan B, et al. Duration of the menopausal transition is longer in women with young age at onset: the multiethnic Study of Women's Health Across the Nation. Menopause 2017; 24:142–149.
    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; 153:865–874.
    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.
    1. Gold E, Colvin A, Avis N, et al. Longitudinal analysis of the association between vasomotor symptoms and race/ethnicity across the menopausal transition: study of women's health across the nation. Am J Public Health 2006; 96:1226–1235.
    1. Avis NE, Crawford SL, Greendale G, et al. Study of Women's Health Across the Nation. Duration of menopausal vasomotor symptoms over the menopause transition. JAMA Intern Med 2015; 175:531–539.
    1. Tepper PG, Brooks MM, Randolph JF, Jr, et al. Characterizing the trajectories of vasomotor symptoms across the menopausal transition. Menopause 2016; 23:1067–1074.
    1. Thurston RC, Bromberger JT, Joffe H, et al. Beyond frequency: who is most bothered by vasomotor symptoms? Menopause 2008; 15:841–847.
    1. Thurston RC, Bromberger J, Chang Y, et al. Childhood abuse or neglect is associated with increased vasomotor symptom reporting among midlife women. Menopause 2008; 15:16–22.
    1. Thurston RC, Sowers MR, Chang Y, et al. Adiposity and reporting of vasomotor symptoms among midlife women: the study of women's health across the nation. Am J Epidemiol 2008; 167:78–85.
    1. Gold EB, Crawford SL, Shelton JF, et al. Longitudinal analysis of changes in weight and waist circumference in relation to incident vasomotor symptoms: the Study of Women’ Health Across the Nation (SWAN). Menopause 2017; 24:9–26.
    1. Thurston RC, Chang Y, Mancuso P, Matthews KA, Adipokines adiposity, and vasomotor symptoms during the menopause transition: findings from the Study of Women's Health Across the Nation. Fertil Steril 2013; 100:793–800.
    1. Randolph JF, Jr, Sowers M, Bondarenko I, et al. The relationship of longitudinal change in reproductive hormones and vasomotor symptoms during the menopausal transition. J Clin Endocrinol Metab 2005; 90:6106–6112.
    1. Crandall CJ, Crawford SL, Gold EB. Vasomotor symptom prevalence is associated with polymorphisms in sex steroid-metabolizing enzymes and receptors. Am J Med 2006; 119:S52–S60.
    1. Kravitz HM, Ganz PA, Bromberger J, Powell LH, Sutton-Tyrrell K, Meyer PM. Sleep difficulty in women at midlife: a community survey of sleep and the menopausal transition. Menopause 2003; 10:19–28.
    1. Kravitz HM, Zhao X, Bromberger JT, et al. Sleep disturbance during the menopausal transition in a multi-ethnic community sample of women. Sleep 2008; 31:979–990.
    1. Kravitz HM, Janssen I, Bromberger JT, et al. Sleep trajectories before and after the final menstrual period in the Study of Women's Health Across the Nation (SWAN). Curr Sleep Med Rep 2017; 3:235–250.
    1. Sowers MF, Zheng H, Kravitz HM, et al. Sex steroid hormone profiles are related to sleep measures from polysomnography and the Pittsburgh Sleep Quality Index. Sleep 2008; 31:1339–1349.
    1. Campbell IG, Bromberger JT, Buysse DJ, et al. Evaluation of the association of menopausal status with delta and beta EEG activity during sleep. Sleep 2011; 34:1561–1568.
    1. Hale L, Troxel WM, Kravitz HM, Hall MH, Matthews KA. Acculturation and sleep among a multiethnic sample of women: the Study of Women's Health Across the Nation (SWAN). Sleep 2014; 37:309–317.
    1. Hall MH, Matthews KA, Kravitz HM, et al. Race and financial strain are independent correlates of sleep in midlife women: the SWAN Sleep Study. Sleep 2009; 32:73–82.
    1. Matthews KA, Hall M, Lee L, et al. Racial/ethnic disparities in women's sleep duration, continuity, and quality and their statistical mediators: Study of Women's Health Across the Nation. Sleep 2019; 42:pii: zsz042.
    1. Hall MH, Okun ML, Sowers M, Matthews KA, Kravitz HM. Sleep is associated with the metabolic syndrome in a multi-ethnic cohort of midlife women: the SWAN Sleep Study. Sleep 2012; 35:783–790.
    1. Matthews KA, Zheng H, Kravitz HM, et al. Are inflammatory and coagulation biomarkers related to sleep characteristics in mid-life women?: Study of Women's Health Across the Nation sleep study. Sleep 2010; 33:1649–1655.
    1. Matthews KA, Chang Y, Kravitz HM, et al. Sleep and risk for high blood pressure and hypertension in midlife women: the SWAN (Study of Women's Health Across the Nation) sleep study. Sleep Med 2014; 15:203–208.
    1. Taylor BJ, Matthews KA, Hasler BP, et al. Bedtime variability and metabolic health in midlife women: the SWAN sleep study. Sleep 2016; 39:457–465.
    1. Bromberger JT, Matthews KA, Schott LL, et al. Depressive symptoms during the menopausal transition: the Study of Women's Health Across the Nation (SWAN). J Affect Disord 2007; 103:267–272.
    1. Bromberger JT, Schott LL, Kravitz HM, et al. Longitudinal change in reproductive hormones and depressive symptoms across the menopausal transition: results from the Study of Women's Health Across the Nation (SWAN). Arch Gen Psychiatry 2010; 67:598–607.
    1. Bromberger JT, Schott LL, Avis NE, et al. Psychosocial and health-related risk factors for depressive symptom trajectories among midlife women over 15 years: Study of Women's Health Across the Nation (SWAN). Psychol Med 2019; 49:250–259.
    1. Bromberger JT, Kravitz HM, Chang Y, Cyranowski JM, Brown C, Matthews KA. Major depression during and after the menopausal transition: Study of Women's Health Across the Nation. Psychol Med 2011; 41:1879–1888.
    1. Bromberger JT, Kravitz HM, Matthews K, Youk A, Brown C, Feng W. Predictors of first lifetime episodes of major depression in midlife women. Psychol Med 2009; 39:55–64.
    1. Bromberger JT, Kravitz HM, Chang Y, et al. Does risk for anxiety increase during the menopausal transition? Study of Women's Health Across the Nation. Menopause 2013; 20:488–495.
    1. Sullivan Mitchell E, Fugate Woods N. Midlife women's attributions about perceived memory changes: observations from the Seattle Midlife Women's Health Study. J Womens Health Gend Based Med 2001; 10:351–362.
    1. Fuh JL, Wang SJ, Lee SJ, Lu SR, Juang KD. A longitudinal study of cognition change during early menopausal transition in a rural community. Maturitas 2006; 53:447–453.
    1. Greendale GA, Huang MH, Wight RG, et al. Effects of the menopause transition and hormone use on cognitive performance in mid-life women. Neurology 2009; 72:1850–1857.
    1. Greendale GA, Wight RG, Huang MH, et al. Menopause-associated symptoms and cognitive performance: results from the Study of Women's Health Across the Nation. Am J Epidemiol 2010; 171:1214–1224.
    1. Lamar M, Resnick SM, Zonderman AB. Longitudinal changes in verbal memory in older adults: distinguishing the effects of age from repeat testing. Neurology 2003; 60:82–86.
    1. Zakzanis KK, Leach L, Kaplan E. On the nature and pattern of neurocognitive function in major depressive disorder. Neuropsychiatry Neuropsychol Behav Neurol 1998; 11:111–119.
    1. Diekelmann S, Wilhelm I, Born J. The whats and whens of sleep-dependent memory consolidation. Sleep Med Rev 2009; 13:309–321.
    1. Beaudreau SA, O’Hara R. Late-life anxiety and cognitive impairment: a review. Am J Geriatr Psychiatry 2008; 16:790–803.
    1. Blazer DG, Yaffe K, Liverman CT, et al. Cognitive Aging: Progress in Understanding and Opportunities for Action. Washington, DC: The National Academies Press, 2015.
    1. Karlamangla AS, Lachman ME, Han W, Huang M, Greendale GA. Evidence for cognitive aging in midlife women: Study of Women's Health Across the Nation. PLoS One 2017; 12:e0169008.
    1. Waetjen LE, Crawford SL, Chang P, et al. Study of Women's Health Across the Nation (SWAN). Factors associated with developing vaginal dryness symptoms in women transitioning through menopause: a longitudinal study. Menopause 2018; 25:1094–1104.
    1. Avis NE, Colvin A, Karlamangla AS, et al. Change in sexual function over the menopause transition: results from the Study of Women's Health Across the Nation (SWAN). Menopause 2017; 24:379–390.
    1. Waetjen LE, Xing G, Johnson WO, Melnikow J, Gold EB. Study of Women's Health Across the Nation (SWAN). Factors associated with seeking treatment for urinary incontinence across the menopausal transition. Obstet Gynecol 2015; 125:1071–1079.
    1. Waetjen LE, Feng WY, Ye J, et al. Study of Women's Health Across the Nation (SWAN). Factors associated with worsening and improving urinary incontinence across the menopausal transition. Obstet Gynecol 2008; 111:667–677.
    1. Waetjen LE, Ye J, Feng WY, et al. Study of Women's Health Across the Nation (SWAN). Association between menopausal transition and the development of urinary incontinence. Obstet Gynecol 2009; 114:989–998.
    1. Waetjen LE, Johnson WO, Xing G, Feng WY, Greendale GA, Gold EB. Study of Women's Health Across the Nation. Serum estradiol levels are not associated with urinary incontinence in midlife women transitioning through menopause. Menopause 2011; 18:1283–1290.
    1. Waetjen LE, Xing G, Johnson WO, Melnikow J, Gold EB. Study of Women's Health Across the Nation (SWAN). Factors associated with reasons incontinent women report for not seeking urinary incontinence treatment over 9 years across the menopausal transition. Menopause 2018; 25:29–37.
    1. Cain V, Johannes C, Avis NE, et al. Sexual functioning and practices in a multi-ethnic sample of midlife women: Baseline results from SWAN. J Sex Res 2003; 40:266–276.
    1. Avis NE, Brockwell S, Randolph JF, Jr, et al. Longitudinal changes in sexual functioning as women transition through menopause: results from the Study of Women's Health Across the Nation. Menopause 2009; 16:442–452.
    1. Randolph JF, Zheng H, Avis NE, Greendale GA, Harlow SD. Masturbation frequency and sexual function domains are associated with serum reproductive hormone levels across the menopausal transition. J Clin Endocrinol Metab 2015; 100:258–266.
    1. Avis NE, Zhao X, Johannes C, Ory M, Brockwell S, Greendale G. Correlates of sexual functioning among mid-aged women: results from the Study of Women's Health Across the Nation (SWAN). Menopause 2005; 12:385–398.
    1. Benjamin EJ, Muntner P, Alonso A, et al. American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee. Heart Disease and Stroke Statistics-2019 update: a report from the American Heart Association. Circulation 2019; 139:e56–e66.
    1. Grundy SM, Stone NJ, Bailey AL, et al. 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA Guideline on the Management of Blood Cholesterol: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 2018 2019; 73:3168–3209.
    1. Matthews KA, Crawford SL, Chae CU, et al. Are changes in cardiovascular disease risk factors in midlife women due to chronological aging or to the menopausal transition? J Am Coll Cardiol 2009; 54:2366–2373.
    1. Matthews KA, El Khoudary SR, Brooks MM, et al. Lipid changes around the final menstrual period predict carotid subclinical disease in postmenopausal women. Stroke 2017; 48:70–76.
    1. Derby CA, Crawford SL, Pasternak RC, Sowers M, Sternfeld B, Matthews KA. Lipid changes during the menopause transition in relation to age and weight: the Study of Women's Health Across the Nation. Am J Epidemiol 2009; 169:1352–1361.
    1. El Khoudary SR, Wang L, Brooks MM, Thurston RC, Derby CA, Matthews KA. Increase HDL-C level over the menopausal transition is associated with greater atherosclerotic progression. J Clin Lipidol 2016; 10:962–969.
    1. El Khoudary SR, Hutchins PM, Matthews KA, et al. Cholesterol efflux capacity and subclasses of HDL particles in healthy women transitioning through menopause. J Clin Endocrinol Metab 2016; 101:3419–3428.
    1. Matthews KA, Abrams B, Crawford S, et al. Body mass index in mid-life women: relative influence of menopause, hormone use, and ethnicity. Int J Obes Relat Metab Disord 2001; 25:863–873.
    1. Sternfeld B, Wang H, Quesenberry CP, Jr, et al. Physical activity and changes in weight and waist circumference in midlife women: findings from the Study of Women's Health Across the Nation. Am J Epidemiol 2004; 160:912–922.
    1. Janssen I, Powell LH, Crawford S, Lasley B, Sutton-Tyrrell K. Menopause and the metabolic syndrome: the Study of Women's Health Across the Nation. Arch Intern Med 2008; 168:1568–1575.
    1. Greendale GA, Sternfeld B, Huang MH, et al. Changes in body composition and weight during the menopause transition. JCI Insight 2019; 4:e124865.
    1. El Khoudary SR, Shields KJ, Janssen I, et al. Cardiovascular fat, menopause, and sex hormones in women: the SWAN Cardiovascular Fat Ancillary Study. J Clin Endocrinol Metab 2015; 100:3304–3312.
    1. El Khoudary SR, Shields KJ, Janssen I, et al. Postmenopausal women with greater paracardial fat have more coronary artery calcification than premenopausal women: the Study of Women's Health Across the Nation (SWAN) Cardiovascular Fat Ancillary Study. J Am Heart Assoc 2017; 6:pii: e004545.
    1. Iacobellis G, Gao YJ, Sharma AM. Do cardiac and perivascular adipose tissue play a role in atherosclerosis? Curr Diab Rep 2008; 8:20–24.
    1. Mahabadi AA, Berg MH, Lehmann N, et al. Association of epicardial fat with cardiovascular risk factors and incident myocardial infarction in the general population: the Heinz Nixdorf Recall Study. J Am Coll Cardiol 2013; 61:1388–1395.
    1. Thurston RC, El Khoudary SR, Sutton-Tyrrell K, et al. Vasomotor symptoms and lipid profiles in women transitioning through menopause. Obstet Gynecol 2012; 119:753–761.
    1. Thurston RC, El Khoudary SR, Sutton-Tyrrell K, et al. Vasomotor symptoms and insulin resistance in the Study of Women's Health Across the Nation. J Clin Endocrinol Metab 2012; 97:3487–3494.
    1. Jackson EA, El Khoudary SR, Crawford SL, et al. Hot flash frequency and blood pressure: data from the Study of Women's Health Across the Nation. J Womens Health (Larchmt) 2016; 25:1204–1209.
    1. El Khoudary SR, Wildman RP, Matthews K, Thurston RC, Bromberger JT, Sutton-Tyrrell K. Progression rates of carotid intima-media thickness and adventitial diameter during the menopausal transition. Menopause 2013; 20:8–14.
    1. Khan ZA, Janssen I, Mazzarelli JK, et al. Serial studies in subclinical atherosclerosis during menopausal transition (from the Study of Women's Health Across the Nation). Am J Cardiol 2018; 122:1161–1168.
    1. El Khoudary SR, Wildman RP, Matthews K, Thurston RC, Bromberger JT, Sutton-Tyrrell K. Endogenous sex hormones impact the progression of subclinical atherosclerosis in women during the menopausal transition. Atherosclerosis 2012; 225:180–186.
    1. El Khoudary SR, Santoro N, Chen HY, et al. Trajectories of estradiol and follicle-stimulating hormone over the menopause transition and early markers of atherosclerosis after menopause. Eur J Prev Cardiol 2016; 23:694–703.
    1. Thurston RC, Sutton-Tyrrell K, Everson-Rose SA, Hess R, Matthews KA. Hot flashes and subclinical cardiovascular disease: findings from the Study of Women's Health Across the Nation Heart Study. Circulation 2008; 118:1234–1240.
    1. Thurston RC, Sutton-Tyrrell K, Everson-Rose SA, Hess R, Powell LH, Matthews KA. Hot flashes and carotid intima media thickness among midlife women. Menopause 2011; 18:352–358.
    1. Thurston RC, El Khoudary SR, Tepper PG, et al. Trajectories of vasomotor symptoms and carotid intima media thickness in the Study of Women's Health Across the Nation. Stroke 2016; 47:12–17.
    1. Recker RR, Lappe JM, Davies KM, Kimmel DB. Change in bone mass immediately before menopause. J Bone Miner Res 1992; 7:857–862.
    1. Greendale GA, Sowers MF, Han WJ, et al. Bone mineral density loss in relation to the final menstrual period in a multi-ethnic cohort: results from the Study of Women's Health Across the Nation (SWAN). J Bone Miner Res 2012; 27:111–118.
    1. Sowers MR, Zheng H, Greendale GA, et al. Changes in bone resorption across the menopause transition: effects of reproductive hormones, body size, and ethnicity. J Clin Endocrinol Metab 2013; 98:2854–2863.
    1. Randolph JF, Jr, Sowers M, Bondarenko IV, Harlow SD, Luborsky JL, Little RJ. Change in estradiol and follicle-stimulating hormone across the early menopausal transition: effects of ethnicity and age. J Clin Endocrinol Metab 2004; 89:1555–1561.
    1. Heaney RP, Barger-Lux MJ, Davies KM, Ryan RA, Johnson ML, Gong G. Bone dimensional change with age: interactions of genetic, hormonal, and body size variables. Osteoporos Int 1997; 7:426–431.
    1. Ishii S, Cauley JA, Greendale GA, et al. Trajectories of femoral neck strength in relation to the final menstrual period in a multi-ethnic cohort. Osteop Int 2013; 24:2471–2481.
    1. Karlamangla AS, Barrett-Connor E, Young J, Greendale GA. Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study. Osteoporos Int 2004; 15:62–70.
    1. Cauley JA, Wu L, Wampler NS, et al. Clinical risk factors for fractures in multi-ethnic women: the Women's Health Initiative. J Bone Miner Res 2007; 22:1816–1826.
    1. Finkelstein JS, Brockwell SE, Mehta V, et al. Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J Clin Endocrinol Metab 2008; 93:861–868.
    1. World Health Organization Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO study group. World Health Organ Tech Rep Ser 1994; 843:1–129.
    1. Ishii S, Cauley JA, Greendale GA, Danielson ME, Safaei Nili N, Karlamangla A. Ethnic differences in composite indices of femoral neck strength. Osteoporos Int 2012; 23:1381–1390.
    1. Ishii S, Greendale G, Cauley J, et al. Fracture risk assessment without race/ethnicity information. J Clin Endocrin Metab 2012; 97:3593–3602.
    1. Sowers M, Pope S, Welch G, Sternfeld, Albrecht G. The association of menopause and physical functioning in women at midlife. J Am Geriatr Soc 2001; 49:1485–1492.
    1. Sowers M, Jannausch ML, Gross M, et al. Performance-based physical functioning in African-American and Caucasian women at midlife: considering body composition, quadriceps strength, and knee osteoarthritis. Am J Epidemiol 2006; 163:950–958.
    1. Ylitalo KR, Karvonen-Gutierrez CA, Fitzgerald N, et al. Relationship of race-ethnicity, body mass index, and economic strain with longitudinal self-report of physical functioning: the Study of Women's Health Across the Nation. Ann Epidemiol 2013; 23:401–408.
    1. El Khoudary SR, McClure CK, VoPham T, et al. Longitudinal assessment of the menopausal transition, endogenous estradiol, and perception of physical functioning: the Study of Women's Health Across the Nation. J Gerontol A Biol Sci Med Sci 2014; 69:1011–1017.
    1. Tseng LA, El Khoudary SR, Young EA, et al. The association of menopause status with physical function: the Study of Women's Health Across the Nation. Menopause 2012; 19:1186–1192.
    1. Avis NE, Colvin A, Bromberger JT, et al. Change in health-related quality of life over the menopausal transition in a multiethnic cohort of middle-aged women: Study of Women's Health Across the Nation. Menopause 2009; 16:860–869.
    1. Tomey K, Sowers M, Zheng H, Jackson EA. Physical functioning related to C-reactive protein and fibrinogen levels in mid-life women. Exp Gerontol 2009; 44:799–804.
    1. Karvonen-Gutierrez CA, Zheng H, Mancuso P, Harlow SD. Higher leptin and adiponectin concentrations predict poorer performance-based physical functioning in midlife women: the Michigan Study of Women's Health Across the Nation. J Gerontol A Biol Sci Med Sci 2016; 71:508–514.
    1. McClure CK, El Khoudary SR, Karvonen-Gutierrez C, et al. Prospective associations between inflammatory and hemostatic markers and physical functioning limitations in mid-life women: longitudinal results of the Study of Women's Health Across the Nation (SWAN). Exp Gerontol 2014; 49:19–25.
    1. Ylitalo KR, Karvonen-Gutierrez C, McClure C, et al. Is self-reported physical functioning associated with incident cardiometabolic abnormalities or the metabolic syndrome? Diabetes Metab Res Rev 2016; 32:413–420.
    1. Karvonen-Gutierrez CA, Peng Q, Peterson M, Duchowny K, Nan B, Harlow S. Low grip strength predicts incident diabetes among mid-life women: the Michigan Study of Women's Health Across the Nation. Age Ageing 2018; 47:685–691.
    1. El Khoudary SR, Chen HY, Barinas-Mitchell E, et al. Simple physical performance measures and vascular health in late midlife women: the Study of Women's Health Across the Nation. Int J Cardiol 2015; 182:115–120.
    1. Stampfer MJ, Hu FB, Manson JE, Rimm EB, Willett WC. Primary prevention of coronary heart disease in women through diet and lifestyle. N Engl J Med 2000; 343:16–22.
    1. Wang D, Jackson EA, Karvonen-Gutierrez CA, et al. Healthy lifestyle during the midlife is prospectively associated with less subclinical carotid atherosclerosis: the Study of Women's Health Across the Nation. J Am Heart Assoc 2018; 7:e010405.
    1. Mori T, Ishii S, Greendale GA, et al. Physical activity as determinant of femoral neck strength relative to load in adult women: findings from the hip strength across the menopause transition study. Osteoporos Int 2014; 25:265–272.
    1. Cauley JA, Greendale GA, Ruppert K, et al. Serum 25 hydroxyvitamin D, bone mineral density and fracture risk across the menopause. J Clin Endocrinol Metab 2015; 100:2046–2054.
    1. Tomey S, Sowers MR, Crandall C, Johnston J, Jannausch M, Yosef M. Dietary intake related to prevalent functional limitations in midlife women. Am J Epidemiol 2008; 167935–167943.
    1. Sternfeld B, Colvin A, Stewart A, et al. The impact of a healthy lifestyle on future physical functioning in midlife women. Med Sci Sports Exerc 2017; 49:274–282.
    1. Pettee Gabriel K, Sternfeld B, Colvin A, et al. Physical activity trajectories during midlife and subsequent risk of physical functioning decline in late mid-life: the Study of Women's Health Across the Nation (SWAN). Prev Med 2017; 105:287–294.
    1. Tomey S, Sowers MR, Harlow S, Jannausch M, Zheng H, Bromberger J. Physical functioning among mid-life women: associations with trajectory of depressive symptoms. Soc Sci Med 2010; 71:1259–1267.
    1. Chandrasekaran N, Harlow S, Moroi S, Musch D, Peng Q, Karvonen-Gutierrez C. Visual impairment at baseline is associated with future poor physical functioning among middle-aged women: the Study of Women's Health Across the Nation, Michigan Site. Maturitas 2017; 96:33–38.
    1. Sowers M, Karvonen-Gutierrez CA, Jacobson JA, Jiang Y, Yosef M. Associations of anatomical measures from MRI with radiographically defined knee osteoarthritis score, pain, and physical functioning. J Bone Joint Surg Am 2011; 93:241–251.
    1. Ylitalo KR, Herman WH, Harlow SD. Performance-based physical functioning and peripheral neuropathy in a population-based cohort of women at midlife. Am J Epidemiol 2013; 177:810–817.

Source: PubMed

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