A Review of the Population-Based Studies, The

Menopause and Sexual Functioning: A Review of the Population-Based Studies, The

Dennerstein, Lorraine

Sexual problems are among the most frequently presented health concerns of women attending menopause clinics. We examine rigorous observational studies of the menopausal transition to determine whether there are changes in sexual functioning associated with the menopausal transition and the relative roles of aging and hormonal factors. We detail the methodological limitations of menopause research. We then review studies documenting the effects of aging on women’s sexual functioning prior to reviewing studies that document both aging and menopausal status. These latter studies are divided into both cross– sectional and longitudinal studies. In summary, there is an age-related decline in sexual functioning but an added incremental decline associated with the menopausal transition. There have been relatively few studies that have been prospective, population-based, utilised a validated measure of sexual functioning, and carried out concurrent hormonal sampling. The Melbourne Women’s Midlife Health Project is a prospective, observational study of a community– based sample of Australian born women aged 45-55 at baseline. There were eight annual assessments using a self-report questionnaire based on the McCoy Female Sexuality Questionnaire and blood sampling for hormone levels. From early to late menopausal transition, the percentage of women with scores indicating sexual dysfunction rose from 42% to 88%. Decreasing scores correlated with decreasing estradiol but not with androgens. By the postmenopausal phase there was a significant decline in sexual arousal and interest, frequency of sexual activities, and the Total Score. There was a significant increase in vaginal dryness and dyspareunia and women’s reports of their partner’s problems in sexual performance. Women with low scores of sexual functioning were more likely to be distressed on the Female Sexual Distress Scale. In conclusion, there is a dramatic decline in female sexual functioning with the natural menopausal transition.

Key Words: aging, estradiol, female sexual dysfunction, hormones, menopause, sexuality.

The research issue addressed in this review is the relationship of the menopausal transition and underlying hormonal changes to female sexual functioning. Clinicians have long been concerned about the effect of menopause on female sexual functioning as sexual complaints are amongst the most frequently reported health concerns by women attending menopause clinics (Sarrel & Whitehead, 1985). This indicates that menopausal status (and underlying hormonal change) may be linked to adverse effects on sexuality. Clinical experience, however, is known to be based on a small proportion of self-selecting women who may not be representative of most women’s experience (Morse et al., 1994). There are a number of other possible explanations for deteriorating sexual functioning at this phase of life. Major confounders include length of relationship, chronologic aging, other physical health problems, loss of partner, partner’s health and medication usage, and the many psychosocial stressors associated with midlife.

Research strategies include those of surveys and clinical trials. Surveys can provide information on the prevalence and types of sexual complaints and the relationship to menopause and other possible determinants. Clinical trials provide evidence of hormonal effects on specific parameters of sexual functioning in the groups studied. These methods are complimentary but have limitations.

Population-based studies enable the study of women in their own naturalistic setting. These investigations also allow assessment of the effect of factors other than hormonal change. The results are then generalisable to the ethnic group and location studied. In evaluating cohort studies, determine the derivation of the sample (look for a randomized sampling technique rather than a convenience sample such as a clinic sample) and sample size. In studies with large sample sizes, often fewer questions are asked, with less assurance of a reliable answer, than in smaller studies, in which investigators may be able to collect more detailed data. Based on our own experience of longitudinal studies of changes in health outcomes with the menopausal transition (see Dennerstein, Lehert, Dudley, & Guthrie, 2001), a minimum of 400 subjects are needed at the outset to provide enough power to detect change. The age of subjects at baseline should be young enough so that measures are obtained before major change in hypothalamic-pituitary-ovarian axis. During the study, documentation is needed of the use of any hormonal therapies (including hormonal replacement therapy [HRT] and oral contraceptives) and of surgery, such as hysterectomy, which may compromise ovarian functioning. Also crucial to the inferences that can be drawn are the type of study (cross-sectional vs. longitudinal), use of validated measures, and statistical techniques that can unravel the complex interrelationships between outcomes and determinants.

In relatively few of the population studies of the menopausal transition have women been asked about sexual functioning. In even fewer has a validated questionnaire to assess the different aspects of sexual functioning been used. A major problem has been to disentangle the effects of aging from that of menopause. The hormonal changes of menopause take place over a variable period of time known as the menopausal transition, so that aging and menopause are inevitably confounded. In most epidemiological studies, hormonal status of the women surveyed, using menstrual status as a proxy for hormonal status, has not been directly measured. In a recent study from the Melbourne Women’s Midlife Health Project, we compared reports by women based on retrospective recall of their menstrual frequency and flow over the prior year with information from prospectively recorded menstrual diaries (Taffe & Dennerstein, 2000). We found that self-report of change in menstrual frequency and flow had low sensitivity compared with measures based on the prospectively kept diaries. Yet, in most surveys of the effects of menopause on health outcomes, retrospective recall of menstrual change has been relied on in order to classify women into menopausal stages. A major advantage of longitudinal studies is that of less reliance on retrospective data, providing that the recall period enquired about is kept short. In longitudinal studies of samples derived from the general population, we are in the best position to sort out whether there is a change in sexual functioning associated with the menopausal transition and, if so, whether this reflects aging, health status, hormonal, or psychosocial factors. A major advantage of longitudinal studies is the ability to control for the effect of prior level of sexual functioning.

For longitudinal studies, the length of prospective follow-up is crucial. For example, after 9 years of follow-up of our population-based Melbourne Women’s Midlife Health Project cohort of women aged 45-55 at baseline (mean age = 48 years), 8% were still menstruating, and 51% of the women had reached documented final menstrual period without medical intervention. Twenty-one percent had taken up HRT before reaching final menstruation, and 8% had undergone surgical menopause (see Figure 1) (Guthrie & Dennerstein, 2003).

Most studies of the relationship between menopause and sexual functioning were carried out before recent interest in refining classifications for both sexual dysfunction (Basson et al., 2000) and for reproductive aging (Soules et al., 2001). Important components of the classification systems for sexual dysfunction are the separation of desire, arousal, orgasmic, and pain disorders, and the requirement that the person should express distress. The majority of scales developed to measure sexual functioning prior to the consensus conference had not included any measure of distress. The international consensus classification paper does indicate that a composite score may be useful (Basson et al., 2000).

New definitions for the latter part of reproductive functioning, including menopause, were reached at The Staging of Reproductive Aging Conference in Park City in 2001. The workshop had been convened to address the absence of a relevant staging system for female reproductive aging and to discuss the confusing current nomenclature for the years prior to reaching final menstruation. Changes in menstrual cyclicity, endocrinology, pelvic anatomy, symptoms, and fertility were considered. It was noted that although there was a well-established system for staging puberty (Tanner/Marshall system), a similar staging system for the dynamic period approaching final menstruation was lacking. Consensus was reached for a 7-stage model (Soules et al., 2001). This consists of early, peak, and late reproductive phases, early and late menopausal transition (MT) phases, and early and late postmenopause phases. Features of early menopausal transition are the onset of variable cycle length, with increasing follicle-stimulating hormone (FSH), whereas late menopausal transition is characterized by at least two skipped menstruations, with elevated FSH and increased likelihood of vasomotor symptoms. Final menstrual period, which marks the transition to postmenopause, is recognised after 12 months amenorrhoea. The early postmenopausal phase comprises the first 5 years after final menstrual period. Women continue to be at risk for vasomotor symptoms. FSH continues to be elevated through this phase and the subsequent late phase of postmenopause. These proposed definitions still await validation using prospectively acquired population– based data.

Clinical trials of the effects of sex steroid hormones on female sexual functioning have also been limited by methodological factors. The designation of the randomized double-blind placebo-controlled trial as that on which evidence of clinical efficacy must be based sets out to remove subject expectancy and observer bias. But even randomized double– blind placebo-controlled trials are subject to a number of biases that limit greatly the generalisability of their findings. These biases include selection bias due to inclusion and exclusion criteria. The effects of selection bias are to create a homogenous group of individuals who may bear little resemblance to the majority of those who would approach their general practitioner about a particular health problem. For example, inclusion and exclusion criteria may lead to selection of a group of individuals whose sexual functioning is not typical of the majority of midaged women. Only a limited number of hypotheses and endpoints can be explored in any one randomized controlled trial. Trials also depend on the use of validated rating scales to measure the outcome of sexual functioning. The development of validated scales to measure female sexual functioning has undergone rapid expansion over the last 8 years. Other selection factors include the failure to specify the hormonal state of women at baseline or to limit the study to a particular category. Most of the studies of androgens have been based on women who had undergone surgical menopause.

Thus, with these considerations in mind, the mode of observational epidemiological and, where possible, population-based studies was chosen to investigate the relationship between the menopausal transition and women’s sexual functioning. As menopausal transition and aging are inevitably confounded, we first document the effects of aging on sexual functioning. We then review those population-based studies that specifically examine menopausal phase or hormone level effects.

Effects of Aging

Aging and length of the relationship are known to affect sexual functioning of both men and women, and these variables are often confounded. For example, James (1983) used cross-sectional and longitudinal data to show that coital rate halved over the first year of marriage and then took another 20 years to halve again. A number of investigators have reported that an additional decrement in aspects of sexual functioning occurs in mid-age. In their early work, Pfeiffer and Davis (1972), using cross-sectional data from the Duke University study, found a pattern of declining sexual activity in both men and women, but the decrement was larger for women than for men of the same age, and the sharpest decline in sexual interest for women occurred around the mean of age of menopause (Pfeiffer, Verwoerdt, & Davis, 1972). In the Swedish cross-sectional and longitudinal studies, Hallstrom (1977) and Hallstrom and Samuelsson (1990) found a dramatic decline in sexual interest, capacity for orgasm, and coital frequency with increasing age. The number reporting an increase in interest or orgasmic capacity was small and less likely with rising age. In the Oxford studies it was found that, among women aged 35 to 59, the older women had less frequent intercourse, orgasm, and enjoyment of sexual activity (Hawton, Gath, & Day, 1994) and increased sexual dysfunction (Osborn, Hawton, & Gath, 1988).

In the Melbourne Women’s Midlife Health Project longitudinal study, we used a detailed sexuality questionnaire, the Personal Experiences Questionnaire. This was adapted from the McCoy Female Sexuality Questionnaire (McCoy & Matyas, 1996). Using a cross-sectional analysis of data from the 4th year of the longitudinal study, we found adequate internal consistency as measured by Cronbach’s alpha, (0.71) (Dennerstein, Dudley, Hopper, & Burger, 1997). Six factors were found using a principal components factor analysis. Of the six factors, three are considered as determinants of sexual functioning: Factor 1, Feelings for Partner; Factor 5, Partner Problems; and Factor 6, Vaginal Dryness/Dyspareunia. The remaining three factors are considered as dependent or outcome variables: Factor 2, Sexual Responsivity; Factor 3, Frequency of Sexual Activities; and Factor 4, Libido. Using data collected annually for 6 years we found the following factors significantly diminished (p

Aging Versus Menopausal Status

In this section, we focus on community-based studies for generalisability of findings and studies with sample sizes of a minimum of 200 in order that there is sufficient power in the statistical analyses. Although power calculations have often been based on univariate tests, from our experience these calculations are adequate to extend to examining associations using more sophisticated analytical methods. The majority of analytical methods described are concerned with taking account of the repeated nature of the data (time series analysis, nested and random effects models, and generalised estimating equations), and current power calculations sufficiently cover these methods. In terms of multi– variate analysis, we calculate that power will decrease by around 1% with the addition of each additional covariate to the regression models. For example, we found that adjusting for baseline level of the variable, with a sample size of 267 we were able to detect with less than 5% alpha and beta errors a difference as large as .1 on the health outcome (positive mood scale; Dennerstein, Lehert, Dudley, & Guthrie, 2001).

Studies are divided into cross-sectional and longitudinal studies, and methodology and findings are summarized in Tables 1 and 2. The major problem with the studies reported is the failure by most investigators to use validated questionnaires of sexual functioning or to adequately measure hormonal or menopausal status. Nevertheless, in most of the cross-sectional population surveys in which this issue was addressed, it was found that there was an additional adverse effect of menopausal status on sexual functioning over that of aging per se. In the Swedish study of 800 women, the investigator was in a better position than in most cross-sectional studies to disentangle the effect of age on women’s sexuality as it was age stratified instead of having age groups (Hallstrom, 1977). Within each age group of women aged 38, 46, 50, and 54 were women of differing menopausal status (then termed pre- peri- and postmenopausal). When age was controlled, the relationship between menopausal status and decreased sexual functioning remained highly significant, but when menopausal status phase was held constant the relationship between age and sexual functioning was not significant. These findings indicate a contribution from the phase of menopausal transition independent of that of chronological aging.

In the Oxford community-based studies of Hawton et al. (1994) and Osborn et al. (1988) they reportedly found no relationship between women’s sexual functioning and menopausal status. The wide age range may have meant the studies did not have the power to detect differences.

We reported cross-sectional data from the Melbourne Women’s Midlife Health Project from the initial baseline study of a population sample of 2,001 randomly selected Australian-born women aged between 45 and 55 years (Dennerstein, Smith, Morse, & Burger, 1994). The major outcome variables (responses were obtained in a telephone interview) were responses to questions relating to changes in sexual interest over the prior 12 months, reasons for any changes, occurrence of sexual intercourse, and unusual pain on intercourse. Although the majority of women (62%) reported no change in sexual interest, 31% reported a decrease. We found that reduction in sexual interest was significantly associated with natural menopause rather than age, decreased wellbeing, lower education, lack of paid employment, and increased symptoms. Our initial study was limited by using only four questions about sexual functioning rather than a valid, reliable measure of sexual functioning. The analysis related to sexual interest included women who did not have a current partner. Hormone levels were not assessed at baseline but were introduced into the longitudinal study. These aspects influenced us to introduce into the longitudinal phase a validated rating scale, the Personal Experiences Questionnaire (Dennerstein et al., 1997), based on the McCoy Female Sexuality Questionnaire (McCoy & Matyas, 1996).

The results of the longitudinal phase of the Melbourne Women’s Midlife Health Project are described in some detail as there is no other study using a validated measure of female sexual functioning with the length of follow-up, concurrent hormonal data, and prospectively kept menstrual diaries for accurate estimation of menopausal phase. The Personal Experiences Questionnaire (PEQ) was handed to each woman annually at the time of interview. Each woman completed the questionnaire and handed it back to the fieldworker. The PEQ was modified (Dennerstein et al., 1997) and shortened to retain each sexual functioning domain with the minimal number of items (Dennerstein, Lehert, & Dudley, 2001). The shortened version of the PEQ (Shortened PEQ; SPEQ) was then subjected to validation externally utilising clinic samples (Dennerstein, Anderson-Hunt, & Dudley, 2002). The items in the SPEQ are shown in Table 3. Items are averaged within each SPEQ factor, and a total score is calculated as the sum of SPEQ Factor 2 (Sexual Responsivity), SPEQ Factor 3 (Frequency of Sexual Activities), and SPEQ Factor 4 (Libido). Based on the clinical evaluative study of the SPEQ, an SPEQ total score of 7 or less is considered indicative of sexual dysfunction (Dennerstein, Anderson-Hunt & Dudley, 2002). In this study, satisfactory external criterion validity, concurrent validity, reliability on retest, and validation of the composite score were established (Dennerstein, Anderson-Hunt & Dudley, 2002)

Menopausal status was determined from change in menstrual status asked at each annual interview for those women who were not taking hormone therapy. Early menopausal transition status was assigned to women who had menstruated in the prior 3 months. Late menopausal transition status was assigned when women reported at least 3 months of amenorrhea but less than 12 months amenorrhea. Women were deemed to be postmenopausal when there had been amenorrhea for at least 12 months. Reports of 3 or more months of amenorrhea and the date of the final menstrual period were verified by fieldworkers from prospectively kept daily menstrual diaries.

Once a year, fasting morning blood samples for hormone measures were taken between days 4 and 8 of the menstrual cycle for those still cycling, or after 3 months of amenorrhea as previously described (Burger et al., 1999). FSH, estradiol (E2), testosterone, and sex hormone binding globulin (SHBG) were measured as described previously (Dennerstein, Randolph, Taffe, Dudley, & Burger, 2002). Free testosterone index (FTI) was calculated as the ratio of the measured testosterone to measured SHBG x 100. The free estradiol index (FEI) was calculated as measured estradiol to measured SHBG x 100.

We have previously demonstrated by longitudinal analysis the timing of changes in estradiol, FSH (Burger et al., 1999), and the androgens (Burger, Dudley, Dennerstein, & Harper, 2000) associated with the menopausal transition. No significant change in total testosterone (T) or in DHEAS occurred with the menopausal transition, although aging itself had a significant effect on Dehydroepiandrosterone sulphate (DHEAS). The free testosterone index (FTI) increased significantly as women passed through the menopausal transition due to a significant decline in SHBG levels reflecting declining estradiol. The phase of maximum change in FSH, E2, and FTI levels was that of the late menopausal transition.

We found that as women passed through the menopausal transition there was a significant decline in SPEQ total scores, and in Sexual Responsivity, Frequency of Sexual Activities, Libido, and in Feelings for Partner (Dennerstein, Dudley, & Burger, 2001). A significant increase occurred in Vaginal Dyspareunia and Partner’s Problems (see Figures 2 and 3, adapted with permission, from Dennerstein, Randolph, et al., 2002).

In the early menopausal transition phase, we found 63 women (42%) had SPEQ total scores of 7 or less, whereas 86 women had scores greater than 7. In the 8th year of observation, utilizing women who are now postmenopausal, 88% of the women (n = 137) now had SPEQ total scores of 7 or below (Dennerstein, Randolph, et al., 2002). Repeated measures regression found that for the total SPEQ score, there was a significant effect of age (B = 0.2, p

Nevertheless it should be noted that androgen levels in this population of midaged women are already low. At the time the testosterone assay was established there was no diagnostic interest in low testosterone levels, and there is an acknowledged lack of testosterone assays with the necessary sensitivity and precision to define the lower end of the normal female range reliably. It is, therefore, possible that assay insensitivity has contributed to the difficulty in establishing a correlation of androgens and sexual functioning. Study results are also limited by the floor effect in the estradiol assay used.

Does Dysfunction Cause Distress?

Bancroft, Loftus, and Long (2003), in a cross-sectional national probability sample survey of American women aged 20 to 65 years, found that 25% reported marked distress about their sexual relationship and/or their own sexuality. These authors reported that although “sexual problems” tended to be more common in older women, it was younger women who were more likely to be troubled by them.

In the 11th year of the Melbourne Women’s Midlife Health Project (2002), the SPEQ and the Female Sexual Distress Scale were administered to participants (Dennerstein, Randolph, Taffe, & Clark, 2003). In a preliminary analysis of 48 women who had current sexual partners, we found that 81.2% of women had sexual dysfunction as determined by a PEQ score of less than, or equal to, 7. Sexual Distress was reported in 16.7% of the group as defined as a score of greater than 15 on the Female Sexual Distress Scale (FSDS), whilst 25% of the group had scores of zero. The Spearman’s correlation coefficient between the sexual distress (FSDS) and sexual function (SPEQ scores) was -0.44 (p = .01) demonstrating that there is an inverse relationship between scores on the SPEQ and scores on the Female Sexual Distress Scale. However, not all women with low sexual functioning scores were distressed. This may reflect the women’s changing feelings towards their partners as they progress through the menopausal transition (Dennerstein, Randolph, et al., 2002). A qualitative content analysis was conducted, based on comments made by women in the study (Dennerstein, Lehert, Burger, Garamszegi, & Dudley, 1999). The following statements were illustrative of the group of women who reported decreased sexual interest:

“The last five years have been quieter in the sex department than were the previous years.”

“We seldom have sex. Our relationship is good but not sexual these days.”

“Sexual intercourse is less exciting now than earlier years and I seem to find other things take [from the] time [my] partner & I spend together e.g., children, friends, work. [And we seem to] put less effort into making it fun.”

“At 47 I don’t feel like instigating sex.”

Summary

Population-based studies find a decline in several aspects of female sexual functioning associated with the midlife years. There is growing evidence that this reflects hormonal changes of the menopausal transition and specifically declining estradiol levels. The research is still pending on the impact of lowered testosterone levels on the population as a whole versus that of selected clinical trial populations (Bachmann et al., 2002; Burger, Hailes, Nelson, & Menelaus, 1987; Davis, McCloud, Strauss, & Burger, 1995; Floter, Nathorst-Boos, Carlstrom, & von Schoultz, 2002; Sherwin, Gelfand, & Brender, 1985). However, hormonal change is only one aspect of the many factors that impact on sexual functioning. These include the woman’s own premorbid level of sexual functioning, her personality, educational level, stress, physical and psychological health status, and changes in partner status, as well as the woman’s feelings towards the partner.

Given the range of factors affecting sexual functioning and the variability of the impact of those factors on each individual woman, it is important to recognise that a hormonal prescription alone may not be sufficient to change sexual function.

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Lorraine Dennerstein

Department of Psychiatry

The University of Melbourne

Jeanne L. Alexander

The Alexander Foundation for Women’s Health

Krista Kotz

Kotz Health Policy Consulting

Lorraine Dennerstein, AO, MBBS, PhD, DPM, FRANZCP, is director of the Office for Gender and Health, Department of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia. Jeanne L. Alexander, MD, FABPN, FRCPC, is affiliated with the Alexander Foundation for Women’s Health, Berkeley, California and Northern California Kaiser Permanente. Krista Kotz PhD, MPH, is affiliated with Kotz Health Policy Consulting, Orinda, California. Requests for reprints should be sent to Lorraine Dennerstein, Office for Gender and Health, 6th Floor, Charles Connibere Building, Royal Melbourne Hospital, Victoria 3050, Australia. (ldenn@unimelb.edu.au)

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