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Abstract

Aim: It has been reported that women in their midlife were more likely to have worse physical functioning (PF) limitations than men of a similar age. Since PF limitations are significant predictors for disability, healthcare utility, healthcare cost, and mortality in the elderly, the higher prevalence of PF limitations reported in middle-aged women is considered a public health issue. Given that the accelerated decline of PF is coincident with the menopausal transition, whether the menopausal transition, rather than normal aging, is related to lower levels of physical functioning in middle aged women remains uncertain. The primary aim of this work was to review systematically the literature that evaluates the associations between menopausal status and measures of PF. Related literature addressing the associations between sex hormones and PF were also reviewed. Methods: Published articles between March 24, 1999 and March 24, 2014 were retrieved from the Pubmed database using selective keywords in the “Title/Abstract”. Only English non-review articles in Humans that evaluated PF measures as outcome variables and menopausal status or sex hormones as independent variables were included in this literature review. Results: Nineteen articles were reviewed. In summary, the natural transition through the menopause was associated with declines in PF independent of the effect of aging. However, few studies used performance-based measurements to evaluate PF declines. Additionally, women undergoing surgical menopause were more likely to experience lower levels of PF compared to premenopausal women. These studies, however, did not evaluate comprehensively the impact of underlying medical conditions leading to surgical menopause on the levels of PF. Finally, the association between sex hormones and PF was still not clear. Conclusion: First, further studies that use performance-based measures of PF, are needed to support the findings that natural menopause is associated with lower level of PF as reported in studies used self-reported measures. Second, underlying medical conditions of surgical menopause should be considered in future studies evaluating surgical menopause and PF. Lastly, the role of the dynamic changes of sex hormones during the menopausal transition in the corresponding changes of PF needs to be explored further.

Table of contents

preface x

1.0 Introduction 1

2.0 Background 3

2.1 Physical functioning assessments 3

2.2 Menopause 4

2.3 Potential Confounding factors for menopause and physical functioning assessments 5

3.0 methods 7

4.0 Results 9

4.1 Summary of the results of the systemic review search process 9

4.2 Menopausal Status and Physical functioning 10

4.2.1 Cross-sectional Studies Examining the Association between Menopausal Status and Performance-based Physical Functioning 10

4.2.2 Cross-Sectional Studies Examining the Association between Menopausal Status and Self-reported Physical Functioning 12

4.2.3 Cross-Sectional Studies Examining the Association between Menopausal Status and Both Self-reported and Performance-based Physical Functioning 14

4.2.4 Longitudinal Studies Examining the Association of Menopausal Status and Performance-based Physical Functioning 15

4.2.5 Longitudinal Studies Examining the Association between Menopausal Status and Self-reported Physical Functioning 16

4.2.6 Longitudinal Studies Examining the Association between Menopausal Status and Both Self-reported and Performance-based Physical Functioning 17

4.3 Sex Hormones and Physical Functioning 18

4.3.1 Endogenous Sex Hormones and Self-reported Physical Functioning 18

4.3.2 Exogenous Sex Hormones and Self-reported Physical Functioning 19

4.3.3 Exogenous Sex Hormones and Performance-based Physical Functioning 21

5.0 Discussion 24

5.1 Natural Menopause and physical functioning limitations 24

5.2 Surgical Menopause and Physical Functioning limitations 28

5.3 Sex Hormones and Physical Functioning limitations 29

5.4 Limitation 31

5.5 Direction for Future Studies 33

6.0 Conclusion 36

APPENDIX: TABLES 37

bibliography 44

List of tables

Table 1. Physical Functioning and Menopausal Status 37

Table 2 Physical Functioning and Sex Hormones 41

List of figures

Figure 1 Flow chart of searching process………………………………………………………8

preface

I would like to thank Dr. Samar R El Khoudary, Dr. Faith Selzer and Dr. Charity Moore for their edits and comments. I would also like to thank the staff on the Writing Center at the University of Pittsburgh for their help with the grammar of this paper.

Introduction

Physical functioning is the ability to perform daily activities, such as walking, getting up, climbing stairs, dressing, bathing, and carrying groceries[pic]1. As published in a World Health Organization report, over one’s life course, physical functional capacity increases and peaks during adulthood and then declines with advancing age2.

It has been reported that 15% of the population between the age of 45 and 64 in the United States was classified as having severe functional limitations3. There is also evidence linking physical functioning limitations with a higher risk of mortality in later life4-6. Poor physical functioning is also associated with more subsequent disability,7, 8 and higher healthcare utilization and cost among those 65 years or older compared to individuals free of physical functioning limitation9. With a longer life expectancy in the United States10 and a rising number of elderly people, it is believed that the rate of disability and the amount of healthcare utilization and costs will increase among the middle-aged and the elderly. These shifts in the demographics of the population coupled with the morbidity and mortality associated with physical functioning limitations are vital public health issues.

The prevalence of physical functional limitations varies by sex. Several studies suggested that women were more likely to have worse physical functioning limitations than men11-14. Among women older than 70 years, 41.5% reported at least one physical function limitation and 17.6% reported more than four limitations in 199412. Although it had been observed that declines in physical functioning begins around age 18-23 years in women, the rate of decline has shown to be greater between the ages of 45 to 50 than at younger age15. Other studies provided evidence that midlife (45-50 years old) women still had higher prevalence of physical functioning limitations compared to midlife men16. Since the accelerated decline of physical functioning occurs around the time of the menopausal transition15, several studies have speculated on possible associations between menopausal factors (menopausal status and menopause-associated sex hormone changes) and physical functioning limitations. These studies hypothesized that the physical functioning limitations were related to the alteration of endogenous sex hormones across the menopausal transition. Presently, potential associations between physical functioning limitations and both menopause and sex hormones and how menopause affects physical functioning remain uncertain.

This literature review will focus on published studies that examined associations between measures of physical functioning and menopausal characteristics, specifically menopausal status and sex hormones. Both cross-sectional and longitudinal studies that enrolled population-based samples of women were evaluated. Finally, possible mechanisms to explain the findings of the manuscripts included in this literature review were discussed.

Background

1 Physical functioning assessments

There are two broad categories of physical functioning assessments used in clinical and community settings: self-reported measures and performance-based measures. Self–reported measures rely on the study subjects’ estimation of their own health status. Several of the most commonly used self-reported measures are the Medical Outcomes Study 36 Item Short Form Health Survey (SF-36) subscale of physical functioning17 and the RAND 36-Item Health Survey 1.0 (RAND-36) subscale of physical functioning18. The SF-36 subscale of physical functioning contains ten questions in the dimension of physical functioning. Item scores are coded, summed, and transformed to a scale from 0 (worst) to 100 (best) 18. The RAND-36 subscale of physical functioning includes the same items as the SF-36 but uses a different scoring algorithm for bodily pain and general health scales19. Performance-based measures require physical parameters. Frequently used performance-based measures include grip strength 19, and the Short Physical Performance Battery (SBBP), which includes three items: a standing balance test, a timed 4-meter walk and a chair rise test 20.

Grip strength assessment measures the average muscle strength of both hands, and the results are recorded in kilograms. The SBBP measures lower extremity functions by assessing 1) the ability to maintain up to 3 hierarchal standing postures for up to 10 seconds (standing balance), 2) the time needed to walk at a comfortable speed across four meters, 3) the time needed to rise from an armless chair five times. Each of the three subscales of SBBP could be scored from 0 (unable to complete the task) to 4 (highest level of performance) and a summary score for the SBBP is created by adding the three scores21. All of these measurements have high reliability and validity1, 19, 22, 23.

It is important to note that self-reported measurement could be influenced by psychological factors, such as expectations and beliefs24 and cognitive impairments25 as well as language, culture, education level26 and pain27. On the other hand, performance-based measurement could be influenced by observer bias28 and the motivation to participate29. Discrepancies between these two types of measurements were usually explained by inaccurate reporting, measurement error or the different constructs that these measurements assess26. In other words, both types of measures complement each other because performance-based measurements can detect deficits in physical functioning before they are identified by self-reported measures30.

2 Menopause

Menopause is the natural reproductive change in women that permanently ends menstruation and fertility in one’s late 40s or early 50s15. The menopausal transition period could last from four to ten years during which the menstrual cycle becomes irregular31. A hallmark of natural menopause is the loss of hormone produced cyclically by ovarian follicles, including estradiol and progesterone32. The natural menopausal status can be classified in to three main classes based on women’s menstrual cycle bleeding patterns as follow: 1) premenopause, which is defined as having menstrual periods in last three months and no change in menstrual regularity in the preceding year, 2) perimenopause, defined as having irregular menstruation during the prior twelve months, and 3) postmenopause, defined as no menses for over twelve months without surgery31. In some studies, the perimenopause is classified more specifically into two separate phases: early perimenopause (menses in the previous three months and changes in regularity in the past year)33 and late perimenopause (no menses in the previous three months but menses within last twelve months)33. Women who undergo bilateral oophorectomy or/and hysterectomy were identified as surgical menopause in some studies3, 34. However, hysterectomy alone will not directly cause the menstruation cessation but will make menstruation not traceable.

3 Potential Confounding factors for menopause and physical functioning assessments

On one hand, the level of physical functioning declines with advancing age2. Higher risk of physical functioning decline was associated with lower levels of physical activity35, depression36, self-reported pain37, and being overweight or obese (body mass index (BMI)>25.0)38. The presence of physical functional limitations were also associated with the stroke, hip fracture, knee osteoarthritis, and heart disease39. Some studies also reported a strong association between physical functioning declines and menopausal symptoms, such as hot flashes and night sweat40.

On the other hand, menopausal transition progresses with age advancing41. Additionally, menopausal transition is associated with menopausal symptoms, including hot flashes, night sweats, depression, joint pain, and sleeping problems.42, 43, 41 Women transitioning naturally were more likely to report hot flashes and night sweats than premenopausal women33. Experiencing a long perimenopause (greater than 27 months) was also associated with higher risk of depression44. Postmenopausal women experienced greater musculoskeletal pain symptoms than premenopausal women45. Other than menopausal symptoms, postmenopausal status was also observed to be related with lower lean body mass but a higher mean BMI compared to premenopausal status46. Menopause was also reported to be associated with the presence of comorbid medical conditions, such as coronary heart disease and osteoarthritis47.

Given that risk factors associated with the menopausal transition, such as aging, BMI, depression, menopausal symptoms, and comorbid medical conditions, are also associated with physical functioning2, 35-40, it is important to consider aging, BMI, depression, menopausal symptoms and comorbid medical conditions as potential confounders or effect modifiers in studies examining the association between physical functioning and the menopausal transition.

methods

A Pubmed literature search was performed pertaining to articles published between March 24, 1999 and March 24, 2014.

To evaluate articles that examined the potential association between menopause status and physical functioning, the following steps were performed. The first search was performed using keywords: “physical function”, “physical functioning”, “physical performance”, “physical health” or “physical limitation” in the “Title/Abstract” section. The second search was also performed using the keywords: “menopause”, “menopausal”, “postmenopause”, “perimenopause” or “premenopause” in the “Title/Abstract” section. The third search was the intersection between the first and the second search results.

All searches were limited using the following parameters: “Humans,” and “English” language. Articles that combined both physical functioning and menopause were examined by reviewing the study title, abstract and full text for the following inclusion criteria: 1) menopausal status or levels of sex hormones were investigated as main independent variables and 2) physical functioning was investigated as primary outcome variables. Review articles and comment articles were excluded. The searching process is shown in Figure 1, and all qualified articles are summarized in Table 1 and 2.

Results

1 Summary of the results of the systemic review search process

The first search using the keywords “physical function” or “physical functioning” or “physical performance” or “physical limitation” or “physical health” yielded 17,867 articles (Figure 1). The second search using the keywords “menopause” or “menopausal” or “postmenopause” or “perimenopause” or “premenopause” yielded 17,084 articles. The intersection between the two, or the third search, yielded 102 articles. The independent and outcome variables of these 102 articles were reviewed to determine eligibility. Of these 102 articles, 10 examined the association between physical function/physical performance and menopausal status (Table 1), and another 9 articles examined the association between physical function/physical performance and sex hormones among women in menopausal transition (Table 2). In total 83 articles were excluded due to the following reasons: 1) Menopausal status or sex hormones were not evaluated as independent variables (n=53), 2) Physical function were not assessed as an outcome (n=16), 3) Retrieved articles were either review or comment articles (n=9), and 4) The Full-text access was not available online (n=5).

2 Menopausal Status and Physical functioning

Among the 10 studies that examined the relationship between menopausal status and physical functioning, 6 of the studies were cross-sectional3, 48-52 and 4 studies were longitudinal53-56. In terms of measures of physical functioning among the 6 cross-sectional studies, 2 used performance-based assessments, 3 used the SF-36 physical functioning subscale, and 1 study incorporated both self-reported and performance-based measurements. In the 4 longitudinal studies, 2 studies measured physical functioning via the SF-36, 1 study used performance-based measures and 1 study used both types of physical functioning measures.

1 Cross-sectional Studies Examining the Association between Menopausal Status and Performance-based Physical Functioning

Cooper et al48 (2008, Table 1, Study #1) studied 1386 women from a British birth cohort (born in March 1946). Grip strength, chair rises and standing balance test were measured when the participants were 53 years old (5.5% premenopause, 15.4% perimenopause, 33.2% postmenopause, 8.2% hysterectomy and/or oophorectomy and no hormone users, 14.1% hysterectomy and/or oophorectomy and hormone users, 23.52% other hormone users). Menopausal status was determined from annual questionnaires responses between the ages of 47 and 54 years. No significant associations between menopausal status and grip strength, chair rises time and standing balance time were found in the full model with adjustment for height and weight, father’s occupational class, head of household occupational class, cognition at age 8, current smoking status, and parity. In a sub-group analysis conducted among naturally postmenopausal women and women who had undergone a hysterectomy with or without an oophorectomy, Cooper et al found that women who had undergone a hysterectomy before age 40 years old had significantly weaker grip strength than women who underwent a hysterectomy between ages 50-53 years old. However, no associations between the age at natural menopause and mean grip strength, chair rise time and standing balance time were found. Since there was small percentage of women in the reference group (5.5% premenopausal women), this study may not have enough statistical power to detect a significant association between menopausal status and grip strength, timed chair rises and standing balance test. Also, the effect of potential confounders between menopausal status and physical functioning such as comorbidities and menopausal symptoms were not assessed.

Cheng et al49 (2009, Table 1, Study #2) examined 979 Taiwanese women between 43 to 57 years old who lived on Kinmen Island (44.4% premenopause, 25.8% perimenopause, 29.7% postmenopause). Physical function parameters included grip strength, key pinch strength, standing balance and flexibility. Balance was measured by single-legged standing and flexibility was measured by stand-and-reach and sit-and-reach tests. The authors reported that postmenopausal women had significantly weaker grip strength and shorter standing balance time than perimenopausal women, whereas perimenopausal women had significantly weaker grip strength and shorter standing balance time than premenopausal women. These results were independent of age, hormone therapy, and history of hysterectomy, hypertension, diabetes mellitus, BMI, hospital anxiety and depression scale, waist circumference and self-reported exercise level. A notable limitation of this study is that only women of the Han race were recruited. Additionally, most people living on Kinmen Island were engaged in farming activities. On one hand, this lifestyle requires more physical activity, which may lead to a slower decline of physical functioning35. On the other hand, the living standard of the study participants was only comparable to those in rural Taiwan community. Therefore, the participants in this study may not be representative of women who are not Han, live in urban areas or are less physical active.

2 Cross-Sectional Studies Examining the Association between Menopausal Status and Self-reported Physical Functioning

Sowers et al3 (2001, Table 1, Study #3) evaluated 14,427 women aged 40-55 years old from the Study of Women’s Health Across the Nation (SWAN), which included 32% premenopausal women, 30% perimenopausal women, 13% naturally postmenopausal women not using hormones, 14% surgically postmenopausal women not using hormones, and 11% women using hormones in last 3 months. Women who responded that they were not “limited in any way in activities because of any impairments or health problems” were categorized as having “no limitation”. For those who responded affirmatively to this question, the self-reported SF-36 physical function subscale was administered and women scoring between 51 and 100 were categorized as having “some limitation” and women scoring between 0-50 were categorized as having “substantial limitation”. Sowers et al found that naturally postmenopausal women who were not hormone users had 56% greater odds of reporting “substantial limitation” in physical functioning when compared to premenopausal women. Additionally, surgically postmenopausal women who were not hormone users had double the odds of reporting “substantial limitations” and 1.5 greater odds of reporting “some limitation” in physical functioning compared to premenopausal women. All results were adjusted for age, race/ethnicity, study center, BMI, and being able to pay for basics. The limitation of this study was that only those women who self-reported being “limited in any way in activities because of any impairments or health problems” completed the SF- 36 subscale. This may lead to the misclassification and result in an overestimation of the relationship between menopausal status and physical functional limitations. Also, this analysis did not assess the potential confounding factors such as comorbidities and menopausal symptoms33, 47.

Anderson et al50 (2007, Table 1, Study #4) examined 1,734 Australian and Japanese women aged 40-60 years enrolled in the Australian and Japanese Midlife Women’s Health Study (AJMWHS). Physical functioning was measured by the SF-36 physical function subscale and analyzed as a continuous variable in this study. Menopausal status was determined by asking women about their menstruation and categorized as premenopausal (12.3%), perimenopausal (14.5%), postmenopausal (53.1%) and surgical menopause (20.1%). Using a two-way between-group analyses of variance, Anderson et al found that for physical functioning, there was no statistically significant association with menopausal status (P=0.09). However, post-hoc comparisons showed that both naturally postmenopausal women and surgically postmenopausal women had significantly lower physical functioning scores compared to premenopausal women. These results were adjusted for age, physical activity, dietary phytoestrogen intake, BMI, smoking status, alcohol use, education, income, marital status, employment status, and menopausal symptoms measured by the Greene Climacteric Scale. However, the ethnicity of studied women, especially the ethnicity of Australian participants, was not assessed and remain unknown, the generalizability of this study to different ethnic groups was hard to evaluate.

Tseng et al51 (2012, Table 1, Study #5) analyzed data collected on 2,236 women enrolled in the SWAN study with a mean age of 49.9 years (7.7% premenopause, 51.1% early perimenopause, 12.1% late perimenopause, 24% natural postmemopause, and 5.1% surgical postmenopause). Tseng et al also used the SF-36 physical function subscale to measure physical functioning. But in contrast to Sowers et al, women who scored between 86-100 were categorized as having “no limitation” and those with a score between 51- 85 were classified as “moderate limitation”. Women scoring 0-50 were classified as “substantial limitation,” which was consistent with Sowers et al. Tseng et al found that surgically postmenopausal women and naturally postmenopausal women had 3-fold higher odds of having “substantial limitations” compared with premenopausal women after adjusting for age, race/ethnicity, education, BMI, diabetes, hypertension, arthritis, depression, hormone use, smoking status, and study site. However, no significant associations between menopausal status and moderate limitations were identified. One limitation of this study was that the percentage of premenopausal women (6.1%) and surgical menopausal women (4.4%) with “moderate limitations” were small, which may have reduced the statistical power to detect an association between moderate limitations and menopausal status. Also, the study did not adjust for potentially confounding menopausal symptoms, such as hot flashes33.

3 Cross-Sectional Studies Examining the Association between Menopausal Status and Both Self-reported and Performance-based Physical Functioning

Using National Health and Nutrition Examination Survey (NHANES) III, Tom et al52 (2012, Table 1, Study #6) interviewed 1,765 women aged 60 and older. Physical functioning was measured via a timed 8-foot walk, timed five consecutive chair rises, as well as self-reported functional limitations. Self-reported functional limitation was defined as reporting difficulty in at least three of five tasks (walking, stair climbing, kneeling, lifting and chair rising), and coded as a binary variable. Menopausal status was based on recalled age at final menstrual period and age at removal of the uterus and ovaries, if applicable. Women who did not undergo a hysterectomy or bilateral oophorectomy before their final menstrual period were grouped as natural menopause while women whose periods stopped because of hysterectomy and/or bilateral oophorectomy comprised the group with surgical menopause. The study reported that women who underwent surgical menopausal experienced an average chair rise time that was 4.3% slower than women who transitioned naturally. But there were no differences in walking speed and self-reported functional limitations. Women reporting a later age of surgical menopause (>=55 years) also had lower odds of self-reported functional limitations (OR = 0.52, 95% CI: 0.29-0.95) compared to those with earlier age ( women not taking.

-No association between repeated chair stands, usual 6-m walk, narrow 6-m walk and standing balance and estrogen replacement therapy. |-Only white women were included.

-This is a study among elderly and not midlife women which affected representative nature of the study participants. | |18 |Kenny et al, 2005 |RCT

36 months |N=167

Healthy, community-dwelling women

Age at baseline:

Low-dose estrogen user group:73.9±0.6

Placebo user group:74.7±0.6

Race: Not stated |Postmenopausal |17-beta estradiol |-SPPB

-Single leg stance time |No covariate |After 3 years follow-up, no significant changes were noted in chair rise time, single-leg stance, walking speed or SPPB. |The study recruited a relatively older population than middle aged women which may limit the generalizability of this study. | |19 |Huang et al, 2014 |RCT

24 weeks |N=71

Women who underwent hysterectomy

Mean age: 53

Ethnicity: not stated |Postmenopausal |testosterone |-Grip strength

-12-step stair climb

-40-m walk |No covariate |-Stair-climb power significantly increased in the 25-mg testosterone injection group compared to placebo group.

-Other performance based measures of physical function did not change significantly in any group. |The sample size was small which reduced the power to detect significant improvements. | |

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PHYSICAL FUNCTIONING AND MENOPAUSE IN MIDDLE AGED WOMEN

by

Yiting Wang

BMed, Nanjing Medical School, China, 2012

Submitted to the Graduate Faculty of

Department of Epidemiology

Graduate School of Public Health in partial fulfillment

of the requirements for the degree of

Master of Public Health

University of Pittsburgh

2014

UNIVERSITY OF PITTSBURGH

GRADUATE SCHOOL OF PUBLIC HEALTH

This essay is submitted

by

Yiting Wang

on

April 24, 2014

and approved by

Essay Advisor:

Samar R El Khoudary, PhD, MPH ______________________________________

Assistant Professor

Department of Epidemiology

Graduate School of Public Health

University of Pittsburgh

Essay Reader:

Faith Selzer, PhD ______________________________________

Research Assistant Professor

Department of Epidemiology

Graduate School of Public Health

University of Pittsburgh

Essay Reader:

Charity Moore, PhD, MSPH ______________________________________

Professor

Department of Medicine

Graduate School of Medicine

University of Pittsburgh

Copyright © by Yiting Wang

2014

Samar R. El Khoudary, PhD, MPH

PHYSICAL FUNCTIONING AND MENOPAUSE IN MIDDLE AGED WOMEN

Yiting Wang, MPH

University of Pittsburgh, 2014

Search 1

Figure 1 Flow chart of searching process

N=17,867

N=17,084

53 independent variables not qualified

16 outcome variables not qualified

9 review articles

5 no full text accessible

Search 2

Search 3

Table 1. Physical Functioning and Menopausal Status (continued)

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