Sleep Disturbance in Perimenopausal Women

Article information

Chronobiol Med. 2024;6(3):109-115
Publication date (electronic) : 2024 September 30
doi : https://doi.org/10.33069/cim.2024.0027
Department of Hospital Medicine, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea
Corresponding author: Kyung Mee Park, MD, PhD, Department of Hopspital Medicine, Yongin Severance Hospital, Yonsei University College of Medicine, 363 Dongbaekjukjeon-daero, Giheung-gu, Yongin 16995, Korea. Tel: 82-31-5189-8531, E-mail: kmpark87@yuhs.ac
Received 2024 August 13; Accepted 2024 September 9.

Abstract

Female sex hormones are involved in various physiological processes including sleep and the circadian cycle. During menopausal transition, various symptoms caused by hormonal changes can occur. Among various perimenopausal symptoms, sleep disturbance is one of the most common and important health issues. More than 40% of perimenopausal women report sleep problems, which not only lower quality of life but also pose substantial health risks including increased cardiovascular risk. Factors contributing to sleep disturbances during perimenopause include direct changes in sleep due to decline of female sex hormones and indirect changes resulting from perimenopausal symptoms. This article will address the influence of female sex hormones on sleep and circadian rhythm, sleep changes in perimenopausal women and their possible mechanisms, prevalent sleep disorders during perimenopause, and their treatments.

INTRODUCTION

Human sleep depends on the circadian cycle. The circadian cycle regulates the vital physiology and metabolic cycles in humans, with an approximate 24-hour periodicity [1]. The circadian cycle is driven by the suprachiasmatic nucleus (SCN), the brain’s central circadian clock, and is organized as a hierarchical multi-oscillator system that transmits signals to peripheral clocks distributed throughout the cerebral cortices and the body [2]. Another important substance mediating the circadian cycle is melatonin, a neurotransmitter secreted by the pineal gland in response to light level stimuli, providing feedback to the SCN [3]. Melatonin exerts beneficial effects on sleep through its synchronizing effects on circadian rhythms [4].

Sex hormones have a bidirectional relationship with the circadian cycle. It is known that the SCN is involved in the control of the hypothalamus, which secretes gonadotropin-releasing hormones [5], and melatonin has also been shown to influence sexual function and reproduction [6]. Changes in sex hormones also affect the circadian cycle. Paul et al. [7] reported that gonadal function has significant correlation to sex differences in the sleep-wake cycle in mice. Additionally, the fact that women have more estrogen and progesterone receptors in the SCN compared to men suggests an influence of female sex hormones on the circadian cycle [8,9]. There are also studies indicating that the effects of melatonin are modulated by gonadal steroids. Animal studies have reported that gonadal steroids might modulate melatonin receptor expression [10], and another study claimed that the degree to which melatonin affects body temperature regulation and gonadotrophin in premenopausal women depends on the menstrual cycle [11].

The most significant change in female hormones is menopause. Menopause is defined as the cessation of cyclic ovarian function. It is diagnosed after 12 months of amenorrhea resulting from the permanent cessation of ovarian function which typically occurs around the age of 51 [12]. The transitional phase leading to menopause is known as perimenopause, which can begin several years before the final menstrual period (mean age of 47 years) and is characterized by irregular menstrual cycles and fluctuations in hormone levels [13]. The pathophysiology of menopause involves a complex interplay of hormonal changes. At the beginning of perimenopause, declines in estrogen and progesterone levels occur due to dysregulated ovulation [12]. The reduction in estrogen levels disrupts the feedback mechanisms in the hypothalamus and pituitary gland, leading to increased levels of follicle-stimulating hormone (FSH). In the early phase of perimenopause, follicular phase estradiol and luteal phase progesterone levels are lower in premenopausal women, and FSH levels are elevated but variable because the majority of cycles are ovulatory [14,15]. The late menopausal transition is characterized by FSH levels ≥25 IU/L, which implies the cessation of follicular development and ovulation [16]. After menopause, FSH levels continue to rise over the first two years following the final menstrual period, after which they gradually stabilize [16].

Perimenopause is characterized by various symptoms that significantly impact a woman’s quality of life [17]. These symptoms are primarily due to hormonal fluctuations and can vary widely among individuals. Common symptoms related to perimenopause are as follows: sleep disturbance [18,19], vasomotor symptoms (hot flashes and night sweats) [18,20,21], psychiatric symptoms including depressed mood [22-24], sexual dysfunction [25,26], joint or muscle pain [21,27], and urogenital symptoms [28,29]. Among these, problems related to sleep are particularly significant. Many perimenopausal women report experiencing poor sleep quality, which significantly impacts their quality of life. In this paper, we will discuss sleep changes among perimenopausal women, prevalent sleep disorders in perimenopausal periods including insomnia and sleep-disordered breathing (SDB), and their treatments.

SLEEP CHANGES IN PERIMENOPAUSAL WOMEN AND ITS POSSIBLE MECHANISM

A high proportion of perimenopausal women report subjective sleep difficulties. A previous study examining the sleep quality of 12,603 middle-aged women aged 40–55 found that self-reported sleep difficulties ranged from 40.5% to 43.8% in the perimenopause group, which is higher compared to 31.4% in premenopausal women [19]. A meta-analysis of 24 studies on sleep disturbance in menopausal women confirmed that the prevalence of sleep disturbance is higher in perimenopausal (odds ratio [OR] 1.60), postmenopausal (OR 1.67), and surgical postmenopausal women (OR 2.17) than in premenopausal women [30]. In the Study of Women’s Health Across the Nation (SWAN), which tracked 3,045 middle-aged women for eight years, 34.3% of perimenopausal women reported sleep discomfort which is higher compared to 28.0% of premenopausal women [31]. Sleep disturbances in menopausal women are primarily characterized by subjective sleep discomfort and poor sleep quality, while polysomnography studies show controversial results. Polysomnography performed in the SWAN study revealed no significant differences between the perimenopausal and premenopausal groups [32], and the study of Wisconsin cohort also found that there were no significant polysomnographic changes associated with the transition to menopause, except for an increase in obstructive apnea in menopausal women [33,34]. However, late-perimenopausal and postmenopausal women exhibited more high-frequency beta EEG activity, suggesting greater cortical hyperarousal during sleep than premenopausal and early-perimenopausal women [32].

Some of these sleep disturbances are attributed to the hormonal changes of perimenopause. While the data on the impact of menopause on the circadian cycle is limited, some previous studies suggest hormonal changes and alterations in the circadian cycle. Animal models also suggest that alterations in reproductive hormone secretion may affect circadian rhythmicity [35]. In addition, previous study found that melatonin secretion in menopausal women is lower compared to premenopausal women [36]. Another study examining the melatonin levels and circadian regulation of 21 premenopausal and postmenopausal women revealed an advanced circadian phase in postmenopausal women, characterized by more fragmented sleep or early morning awakenings [37]. Some authors propose that the complex interaction between melatonin and the gonadal hormonal milieu depends more on the effects of melatonin rather than on its own levels [38]. Moreover, changes in melatonin levels induce significant alterations in the biological function of almost every organ, with potential implications for sleep quality [39].

Hormonal changes can directly and indirectly affect sleep quality and sleep discomfort, in addition to their effects on the circadian cycle. Previous study examining estrogen levels and sleep quality in perimenopausal women has shown that lower estradiol and higher luteinizing hormone (LH) levels are associated with poor sleep quality [40]. Replacement of estrogen in perimenopausal women could improve sleep by increasing total sleep time, and decreasing sleep latency, the number of awakenings after sleep, and the number of cyclic spontaneous arousals [41]. Polysomnography study also have shown that estrogen replacement is associated with an increase in both slow-wave sleep and REM sleep [42,43]. This could be due to increased core temperatures following peripheral vasodilation caused by a decrease in estrogen level, resulting in hot flashes [44]. Hot flashes and core temperature contribute to sleep fragmentation and reduced sleep quality [45-47]. Progesterone is known to have a stimulating effect on γ-aminobutyric acid receptors, exerting a hypnotic and sedative effect [48]. In addition, proogesterone is a potent respiratory stimulant associated with a decrease in episodes of obstructive sleep apnea (OSA) [49]. During pregnancy, when progesterone levels are high, OSA occurs less frequently, and the lower incidence of OSA in premenopausal women compared to men is also thought to be attributed to this effect [50]. Perimenopausal psychiatric symptoms including depression or anxiety related to hormone change also influence sleep [51,52].

INSOMNIA

Insomnia is the most common sleep disorder among women, and its prevalence worsens in menopausal women. In a study of 6,079 mid-life women, the prevalence of insomnia during perimenopause screened by a Pittsburgh Sleep Quality Index (PSQI) score of 5 or higher was approximately 41.7% [53]. According to the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) criteria of chronic insomnia, 26% of 982 perimenopausal women qualified for a diagnosis of insomnia lasting six months or more with difficulty maintaining sleep being the most common symptom [46]. Polysomnography findings also revealed poorer sleep efficiency, more wakefulness after sleep onset, and shorter total sleep time among perimenopausal women with the insomnia diagnosis [54].

This problem related to maintaining sleep in perimenopausal women is mainly related to hot flashes, one of the vasomotor symptoms in perimenopause. Hot flash is defined as an exaggerated heat dissipation response resulting in widespread cutaneous vasodilation and upper body sweating [55]. It lasts approximately 3–10 minutes and may be accompanied by sensations of heat, sweating, flushing, chills, anxiety, and shivering [56]. Hot flash emerges as estrogen levels decrease, but its mechanism is more complex than just estrogen withdrawal [57]. It is assumed that the involvement of central noradrenergic activity, serotonergic mechanisms, and LH secretion are correlated with hot flashes [44,58,59]. Previous studies have found that hot flash is strongly associated with a diagnosis of insomnia and that there is a correlation between an increased risk of chronic insomnia symptoms and the severity of hot flashes [46,60]. It is also found that the presence of hot flashes and the number of awakenings per hour of sleep measured by polysomnography are significantly correlated with each other [54].

Psychiatric symptoms are also known to affect perimenopausal insomnia. It has been established through previous studies that psychiatric symptoms, including depression and anxiety, are prevalent in menopausal women [61,62]. Depression and sleep are believed to have a bidirectional relationship in perimenopausal women, as well as in general population [51,63]. The correlation between depressive symptoms and vasomotor symptoms is also suggested to contribute to insomnia in perimenopausal women. Previous research has found that perimenopausal women with vasomotor symptoms are 4.39 times more likely to have depression, regardless of prior depression history [64].

Hormone replacement therapy might be effective for treating insomnia in perimenopausal women when vasomotor symptoms including hot flashes are present [14,50,65]. Hormone replacement therapies targeting insomnia symptoms in perimenopausal women recommend the application of low-dose estrogen or progesterone, which are known to improve subjective sleep quality and sleep continuity [50,65]. However, the results of previous studies are somewhat controversial. According to a review paper published in 2014, hormone replacement therapy showed significant sleep improvement effects in more than ten studies, including randomized controlled trial (RCT), while more than five studies reported no sleep improvement effects [65]. This review suggests using hormone replacement therapy to manage insomnia in perimenopausal women but recommends selecting based on dosing and formulation heterogeneity in previous studies and considering the risk/benefit of hormone replacement therapy itself. The Women’s Health Initiative showed that hormone replacement therapy decreased perimenopausal symptoms and the risk of osteoporotic fractures but found no long-term cardiovascular benefit and confirmed prior studies showing an increased risk of breast cancer [66,67]. Therefore, it is not recommended as a first-line treatment for insomnia in perimenopausal women without prominent vasomotor symptoms [50]. Additionally, the North American Menopause Society advises using hormone replacement therapy for no more than five years and at the lowest effective dose possible to minimize possible side effects [68].

Antidepressants, including fluoxetine, paroxetine, and venlafaxine, are known to help alleviate hot flashes [65,69,70], but they are not recommended for improving sleep [71]. Antidepressants are recommended to be used for perimenopausal insomnia only when accompanied by depressive symptoms. Studies have reported that escitalopram significantly improved sleep in perimenopausal women with depressive symptoms, and there are also findings of significant effects with mirtazapine and controlled-release melatonin [72,73]. Gabapentin is also known to help improve insomnia symptoms accompanied by hot flashes [74,75]. Among dietary supplements for perimenopausal women, soy isoflavones have shown significant effects in reducing hot flashes and improving sleep symptoms in RCTs [76,77]. Sedative hypnotics can be used for acute, short-term treatment as in general insomnia. Since the most prevalent sleep complaints in perimenopausal women involves difficulty in sleep maintenance, eszopiclone could be the choice of drug. Previous studies have also shown that eszopiclone improves sleep quality and vasomotor symptoms [78,79].

For non-pharmacological treatments, cognitive behavioral therapy for insomnia (CBT-I), an effective first-line treatment for chronic insomnia, can be used for perimenopausal insomnia. A study involving 106 perimenopausal women who received telephone-administered CBT-I found that CBT-I improved sleep quality regardless of the improvement in perimenopausal symptoms including hot flashes, and the treatment effect persisted for up to six months [80]. Additionally, previous studies have shown that exercise can significantly improve sleep quality. Kline et al. [81] have found a correlation between indicators such as sleep quality, PSQI, sleep efficiency, and high-intensity physical activity in a study conducted with 339 perimenopausal women. Another study, which compared low-intensity stretching and high-intensity physical activity among 173 participants, found significant improvements in sleep quality in both groups and a correlation between increased physical activity and sleep improvement [82].

SLEEP-DISORDERED BREATHING

SBD, particularly OSA, shows a gender difference in prevalence, with rates of 22% in men and 17% in women [83]. The prevalence of OSA tends to increase with age in both men and women, but there is a significant difference before and after menopause in women. Premenopausal women have about one-third the prevalence of OSA compared to men, and there is approximately a threefold difference in OSA prevalence between premenopausal and postmenopausal women [34,84,85]. It has also been found that about 20% of women with OSA develop the condition during perimenopause [86].

The reasons for the differences in OSA prevalence before and after menopause are not clearly understood but may relate to the effects of sex hormones, blood concentration of leptin, and weight gain after perimenopause [50]. Among the hormonal changes around menopause, progesterone is thought to have the most significant impact on SDB in women. Since progestogens are potent respiratory stimulants, it has been speculated that they protect women from SDB until menopause [87]. It is also suggested that the protective role of progesterone may be due to its effect on the upper-airway dilator muscles. A previous study found that the activity of upper-airway dilator muscles was greater during the luteal phase, when progesterone levels are high; less in postmenopausal women; and increased with hormone replacement therapy [88]. Hormone replacement therapy is associated with a lower prevalence of SDB, which also suggests the influence of sex hormones on the development of OSA [34,89]. Leptin, a hunger-suppressing adipokine, also stimulates breathing, and it is noted that women have a higher average blood concentration of leptin than men [90]. A previous study found that higher leptin levels were associated with a better upper airway neuromuscular response in women [91]. After menopause, blood concentration of leptin decreases in women [92]. This loss of leptin, which could cause the development of abdominal obesity, insulin resistance, and leptin resistance, might partially explain the association between menopause and OSA [50]. In addition, body weight gain after menopause might lead to a higher BMI, larger neck circumference, and higher waist-hip ratio, which could affect the prevalence of OSA [93]. Weight gain after menopause could also lead to a change in body habitus, with an accumulation of adipose tissue in the upper part of the body as well as a shift toward visceral adipose deposition, which is also a critical risk factor for OSA [34,94].

OSA is one of the major risk factors for cardiovascular disease, including hypertension, heart failure, atrial fibrillation, coronary artery disease, and stroke in the general population [95-99]. Especially in women, OSA is related to an increased risk of heart failure after adjustment for previous myocardial infarction, menopausal status, age, waist circumference, alcohol or tobacco use, and hormone replacement therapy [100]. Given the health risks associated with untreated SDB, women suspected of having the disorder should be formally evaluated and treated. However, OSA tends to be underdiagnosed in women. Among the general population with symptoms of SDB, women are significantly less likely to be diagnosed compared to men (25% vs. 14%, p<0.001), and they are also less likely to receive any treatment (17% vs. 11%, p=0.05) [101]. Considering that progression through menopausal stages is associated with SDB severity, with a 4% higher apnea-hypopnea index for every additional year since entering the menopausal transition, it is crucial to properly screen and treat OSA in perimenopausal women [102].

The gold standard treatment for OSA is continuous positive airway pressure (CPAP) [64]. Although there is evidence of a correlation between hormonal changes in menopausal women and the development and the less prevalence of OSA in groups undergoing hormone replacement therapy [34,89], studies on the actual effects of hormone replacement therapy on perimenopausal women with OSA have shown conflicting results [103]. Several studies on the therapeutic effect of exogenous hormone administration among postmenopausal women with sleep apnea showed no significant improvement in the number of apneas [103-105]. Therefore, hormone replacement therapy is not primarily recommended for the treatment of OSA in menopausal women considering the risks of hormone therapy [106].

RESTLESS LEGS SYNDROME AND PERIODIC LIMB MOVEMENT

Restless legs syndrome (RLS) and periodic limb movements (PLMs) are conditions that frequently occur during perimenopause, but their relationship with menopause is not clearly established. According to a survey study conducted with 3,501 middle-aged women, RLS showed a significant correlation with vasomotor symptoms but not with menopausal status or hormone replacement therapy [107]. The appearance of these two conditions during perimenopause may be due to their increased prevalence with age, suggesting that the overlap in timing could be coincidental [108]. Additionally, since these two are common sleep disorders, they might have been co-diagnosed alongside other sleep disorders that occur during menopause when women seek medical attention for sleep [50].

Dopamine agonists including pramipexole or ropinirole hydrochloride have been approved by the US Food and Drug Administration for treating RLS, and have been shown to be effective in reducing their symptoms [109]. However, they do not directly improve sleep, and long-term use is limited by augmentation. Alpha-2-delta ligand drugs such as gabapentin, enacarbil, and pregabalin could be another treatment option. These drugs are known to increase slow wave sleep and improve pain while having less impact on leg movements than dopamine agonists [110]. Although hormone replacement therapy has not been extensively studied in the field, it is assumed to be not particularly helpful for perimenopausal women with RLS and PLMs. An RCT conducted on perimenopausal women with RLS found that while estrogen therapy helped improve sleep quality, it did not alleviate RLS and PLMs symptoms [111]. Additionally, cyclic hormone replacement therapy has been reported to potentially worsen symptoms [50].

SUMMARY

As women transition through menopause, sleep difficulties become increasingly prevalent, significantly impacting their quality of life and daily functioning. Hormonal changes during perimenopause may lead to alterations in the circadian cycle, poor sleep quality, and an increased risk for SDB. In addition, vasomotor symptom during perimenopause is also responsible for frequent awakening and poor sleep maintenance. The complex interplay of direct and indirect influences on sleep during this period necessitates a comprehensive understanding and tailored approach to treatment.

Insomnia is prominent sleep problem in perimenopausal women. Vasomotor symptom, especially hot flash is a distinct and common contributor to perimenopausal insomnia, often disrupting sleep and contributing to prolonged wakefulness during the night. While hot flash is a significant factor, perimenopausal insomnia may also arise from hormonal fluctuations, mood disorders, and life stressors. Hormone replacement therapy for the perimenopausal insomnia with hot flash could be beneficial, but health professionals should consider the potential risks of hormone replacement therapy against its benefits. Antidepressants could also be used, particularly for those experiencing concurrent mood disturbances. Gabapentin and soy isoflavones are known to be effective in reducing insomnia symptoms related to hot flashes. Short-term use of sedative-hypnotics may also provide relief. As non-pharmacological treatment, CBT-I and exercise are found to be beneficial.

DB including OSA, which is often underestimated in women, requires increased vigilance during perimenopausal period. There is more than a threefold risk of developing OSA after postmenopause compared to premenopausal women. The development of OSA in perimenopause might be attributed to changes in sex hormones, decrease in leptin levels, weight gain, and alterations in fat disposition. Physicians must be proactive in evaluating and treating OSA in perimenopausal women, recognizing its cardiovascular implications. CPAP therapy should be considered for OSA in the population, and hormone replacement therapy is not a treatment of choice. RLS and PLMs are not directly related to perimenopause, but they also frequently occur during this period. Proper pharmacological management could be helpful in reducing symptoms.

Changes in sleep are an integral aspect of the quality of life for menopausal women. Addressing sleep disturbances in perimenopausal women demands thorough medical concern, proper diagnosis, and personalized medical treatments. By adopting a holistic approach to sleep disturbance related to perimenopause, healthcare providers can better support women through this transitional phase, fostering better sleep and overall well-being.

Notes

The author has no potential conflicts of interest to disclose.

Availability of Data and Material

Data sharing not applicable to this article as no datasets were generated or analyzed during the study.

Funding Statement

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Acknowledgements

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References

1. Hastings MH, Maywood ES, Brancaccio M. Generation of circadian rhythms in the suprachiasmatic nucleus. Nat Rev Neurosci 2018;19:453–469.
2. Honma S. The mammalian circadian system: a hierarchical multi-oscillator structure for generating circadian rhythm. J Physiol Sci 2018;68:207–219.
3. Arendt J, Aulinas A. Physiology of the pineal gland and melatonin. In: Endotext [Internet]. South Dartmouth: MDText.com, Inc.; 2000. Available at: https://www.ncbi.nlm.nih.gov/books/NBK550972. Accessed July 20, 2024.
4. Tordjman S, Chokron S, Delorme R, Charrier A, Bellissant E, Jaafari N, et al. Melatonin: pharmacology, functions and therapeutic benefits. Curr Neuropharmacol 2017;15:434–443.
5. Saper CB, Lu J, Chou TC, Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci 2005;28:152–157.
6. Acuña-Castroviejo D, Escames G, Venegas C, Díaz-Casado ME, LimaCabello E, López LC, et al. Extrapineal melatonin: sources, regulation, and potential functions. Cell Mol Life Sci 2014;71:2997–3025.
7. Paul KN, Dugovic C, Turek FW, Laposky AD. Diurnal sex differences in the sleep-wake cycle of mice are dependent on gonadal function. Sleep 2006;29:1211–1223.
8. Kruijver FP, Swaab DF. Sex hormone receptors are present in the human suprachiasmatic nucleus. Neuroendocrinology 2002;75:296–305.
9. Curran-Rauhut MA, Petersen SL. The distribution of progestin receptor mRNA in rat brainstem. Brain Res Gene Expr Patterns 2002;1:151–157.
10. Cagnacci A, Volpe A. Influence of melatonin and photoperiod on animal and human reproduction. J Endocrinol Invest 1996;19:382–411.
11. Cagnacci A. Melatonin in relation to physiology in adult humans. J Pineal Res 1996;21:200–213.
12. Greendale GA, Lee NP, Arriola ER. The menopause. Lancet 1999;353:571–580.
13. Santoro N. The menopausal transition. Am J Med 2005;118:8–13.
14. Baker FC, de Zambotti M, Colrain IM, Bei B. Sleep problems during the menopausal transition: prevalence, impact, and management challenges. Nat Sci Sleep 2018;10:73–95.
15. Hale GE, Zhao X, Hughes CL, Burger HG, Robertson DM, Fraser IS. Endocrine features of menstrual cycles in middle and late reproductive age and the menopausal transition classified according to the staging of reproductive aging workshop (STRAW) staging system. J Clin Endocrinol Metab 2007;92:3060–3067.
16. Harlow SD, Gass M, Hall JE, Lobo R, Maki P, Rebar RW, 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.
17. Woods NF, Mitchell ES. Symptoms during the perimenopause: prevalence, severity, trajectory, and significance in women’s lives. Am J Med 2005;118:14–24.
18. Dennerstein L, Dudley EC, Hopper JL, Guthrie JR, Burger HG. A prospective population-based study of menopausal symptoms. Obstet Gynecol 2000;96:351–358.
19. 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.
20. Freeman EW, Grisso JA, Berlin J, Sammel M, Garcia-Espana B, Hollander L. Symptom reports from a cohort of African American and white women in the late reproductive years. Menopause 2001;8:33–42.
21. Gold EB, Sternfeld B, Kelsey JL, Brown C, Mouton C, Reame N, et al. Relation of demographic and lifestyle factors to symptoms in a multi-racial/ethnic population of women 40-55 years of age. Am J Epidemiol 2000;152:463–473.
22. Avis NE, Crawford S, Stellato R, Longcope C. Longitudinal study of hormone levels and depression among women transitioning through menopause. Climacteric 2001;4:243–249.
23. Bromberger JT, Harlow S, Avis N, Kravitz HM, Cordal A. Racial/ethnic differences in the prevalence of depressive symptoms among middle-aged women: the study of women’s health across the nation (SWAN). Am J Public Health 2004;94:1378–1385.
24. Matthews KA, Wing RR, Kuller LH, Meilahn EN, Kelsey SF, Costello EJ, et al. Influences of natural menopause on psychological characteristics and symptoms of middle-aged healthy women. J Consult Clin Psychol 1990;58:345–351.
25. Dąbrowska-Galas M, Dąbrowska J, Michalski B. Sexual dysfunction in menopausal women. Sex Med 2019;7:472–479.
26. Heidari M, Ghodusi M, Rezaei P, Kabirian Abyaneh S, Sureshjani EH, Sheikhi RA. Sexual function and factors affecting menopause: a systematic review. J Menopausal Med 2019;25:15–27.
27. Watt FE. Musculoskeletal pain and menopause. Post Reprod Health 2018;24:34–43.
28. Calleja-Agius J, Brincat MP. The urogenital system and the menopause. Climacteric 2015;18(Suppl 1):18–22.
29. Shifren JL, Zincavage R, Cho EL, Magnavita A, Portman DJ, Krychman ML, et al. Women›s experience of vulvovaginal symptoms associated with menopause. Menopause 2019;26:341–349.
30. Xu Q, Lang CP. Examining the relationship between subjective sleep disturbance and menopause: a systematic review and meta-analysis. Menopause 2014;21:1301–1318.
31. Kravitz HM, Zhao X, Bromberger JT, Gold EB, Hall MH, Matthews KA, et al. Sleep disturbance during the menopausal transition in a multi-ethnic community sample of women. Sleep 2008;31:979–990.
32. Campbell IG, Bromberger JT, Buysse DJ, Hall MH, Hardin KA, Kravitz HM, et al. Evaluation of the association of menopausal status with delta and beta EEG activity during sleep. Sleep 2011;34:1561–1568.
33. Young T, Rabago D, Zgierska A, Austin D, Laurel F. Objective and subjective sleep quality in premenopausal, perimenopausal, and postmenopausal women in the Wisconsin sleep cohort study. Sleep 2003;26:667–672.
34. Young T, Finn L, Austin D, Peterson A. Menopausal status and sleep-disordered breathing in the Wisconsin sleep cohort study. Am J Respir Crit Care Med 2003;167:1181–1185.
35. Mong JA, Cusmano DM. Sex differences in sleep: impact of biological sex and sex steroids. Philos Trans R Soc Lond B Biol Sci 2016;371:20150110.
36. Toffol E, Kalleinen N, Haukka J, Vakkuri O, Partonen T, Polo-Kantola P. Melatonin in perimenopausal and postmenopausal women: associations with mood, sleep, climacteric symptoms, and quality of life. Menopause 2014;21:493–500.
37. Walters JF, Hampton SM, Ferns GA, Skene DJ. Effect of menopause on melatonin and alertness rhythms investigated in constant routine conditions. Chronobiol Int 2005;22:859–872.
38. Cagnacci A. Role of melatonin in circadian rhythm at menopause. Climacteric 2017;20:183.
39. Hardeland R, Cardinali DP, Srinivasan V, Spence DW, Brown GM, PandiPerumal SR. Melatonin—a pleiotropic, orchestrating regulator molecule. Prog Neurobiol 2011;93:350–384.
40. Murphy PJ, Campbell SS. Sex hormones, sleep, and core body temperature in older postmenopausal women. Sleep 2007;30:1788–1794.
41. Scharf MB, McDannold MD, Stover R, Zaretsky N, Berkowitz DV. Effects of estrogen replacement therapy on rates of cyclic alternating patterns and hot-flush events during sleep in postmenopausal women: a pilot study. Clin Ther 1997;19:304–311.
42. Carrier J, Land S, Buysse DJ, Kupfer DJ, Monk TH. The effects of age and gender on sleep EEG power spectral density in the middle years of life (ages 20-60 years old). Psychophysiology 2001;38:232–242.
43. Antonijevic IA, Stalla GK, Steiger A. Modulation of the sleep electroencephalogram by estrogen replacement in postmenopausal women. Am J Obstet Gynecol 2000;182:277–282.
44. Freedman RR. Pathophysiology and treatment of menopausal hot flashes. Semin Reprod Med 2005;23:117–125.
45. Erlik Y, Tataryn IV, Meldrum DR, Lomax P, Bajorek JG, Judd HL. Association of waking episodes with menopausal hot flushes. JAMA 1981;245:1741–1744.
46. Ohayon MM. Severe hot flashes are associated with chronic insomnia. Arch Intern Med 2006;166:1262–1268.
47. Woodward S, Freedman RR. The thermoregulatory effects of menopausal hot flashes on sleep. Sleep 1994;17:497–501.
48. Manber R, Armitage R. Sex, steroids, and sleep: a review. Sleep 1999;22:540–541.
49. Empson JA, Purdie DW. Effects of sex steroids on sleep. Ann Med 1999;31:141–145.
50. Eichling PS, Sahni J. Menopause related sleep disorders. J Clin Sleep Med 2005;1:291–300.
51. Baker A, Simpson S, Dawson D. Sleep disruption and mood changes associated with menopause. J Psychosom Res 1997;43:359–369.
52. Freeman EW, Sammel MD, Lin H, Nelson DB. Associations of hormones and menopausal status with depressed mood in women with no history of depression. Arch Gen Psychiatry 2006;63:375–382.
53. Blümel JE, Cano A, Mezones-Holguín E, Barón G, Bencosme A, Benítez Z, et al. A multinational study of sleep disorders during female mid-life. Maturitas 2012;72:359–366.
54. Baker FC, Willoughby AR, Sassoon SA, Colrain IM, de Zambotti M. Insomnia in women approaching menopause: beyond perception. Psychoneuroendocrinology 2015;60:96–104.
55. Kronenberg F. Hot flashes: epidemiology and physiology. Ann N Y Acad Sci 1990;592:52–86. discussion 123-133.
56. Kronenberg F. Menopausal hot flashes: a review of physiology and biosociocultural perspective on methods of assessment. J Nutr 2010;140:1380S1385S.
57. Freedman RR. Hot flashes: behavioral treatments, mechanisms, and relation to sleep. Am J Med 2005;118:124–130.
58. Archer DF, Sturdee DW, Baber R, de Villiers TJ, Pines A, Freedman RR, et al. Menopausal hot flushes and night sweats: where are we now? Climacteric 2011;14:515–528.
59. Rance NE, Dacks PA, Mittelman-Smith MA, Romanovsky AA, KrajewskiHall SJ. Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: a novel hypothesis on the mechanism of hot flushes. Front Neuroendocrinol 2013;34:211–227.
60. Polo-Kantola P, Erkkola R, Helenius H, Irjala K, Polo O. When does estrogen replacement therapy improve sleep quality? Am J Obstet Gynecol 1998;178:1002–1009.
61. Freeman EW, Sammel MD, Liu L, Gracia CR, Nelson DB, Hollander L. Hormones and menopausal status as predictors of depression in women in transition to menopause. Arch Gen Psychiatry 2004;61:62–70.
62. Harlow BL, Wise LA, Otto MW, Soares CN, Cohen LS. Depression and its influence on reproductive endocrine and menstrual cycle markers associated with perimenopause: the Harvard study of moods and cycles. Arch Gen Psychiatry 2003;60:29–36.
63. Fang H, Tu S, Sheng J, Shao A. Depression in sleep disturbance: a review on a bidirectional relationship, mechanisms and treatment. J Cell Mol Med 2019;23:2324–2332.
64. Joffe H, Hall JE, Soares CN, Hennen J, Reilly CJ, Carlson K, et al. Vasomotor symptoms are associated with depression in perimenopausal women seeking primary care. Menopause 2002;9:392–398.
65. Attarian H, Hachul H, Guttuso T, Phillips B. Treatment of chronic insomnia disorder in menopause: evaluation of literature. Menopause 2015;22:674–684.
66. U.S. Preventive Services Task Force. Hormone therapy for the prevention of chronic conditions in postmenopausal women: recommendations from the U.S. Preventive Services Task Force. Ann Intern Med 2005;142:855–860.
67. Rossouw JE, ANderson GL, Prentice RL, LaCroix AZ, Kooperberg C, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women. In: Liu C, Rindos N, Shainker SA, editors. 50 studies every obstetrician-gynecologist should know. New York: Oxford University Press, 2021, p.262.
68. North American Menopause Society. Recommendations for estrogen and progestogen use in peri-and postmenopausal women: October 2004 position statement of The North American Menopause Society. Menopause 2004;11(6 Pt 1):589–600.
69. Loprinzi CL, Sloan JA, Perez EA, Quella SK, Stella PJ, Mailliard JA, et al. Phase III evaluation of fluoxetine for treatment of hot flashes. J Clin Oncol 2002;20:1578–1583.
70. Loprinzi CL, Kugler JW, Sloan JA, Mailliard JA, LaVasseur BI, Barton DL, et al. Venlafaxine in management of hot flashes in survivors of breast cancer: a randomised controlled trial. Lancet 2000;356:2059–2063.
71. Nowakowski S, Meliska CJ, Martinez LF, Parry BL. Sleep and menopause. Curr Neurol Neurosci Rep 2009;9:165–172.
72. Dolev Z. Case series of perimenopausal women with insomnia treated with mirtazapine followed by prolonged-release melatonin add-on and monotherapy. Arch Womens Ment Health 2011;14:269–273.
73. Soares CN, Arsenio H, Joffe H, Bankier B, Cassano P, Petrillo LF, et al. Escitalopram versus ethinyl estradiol and norethindrone acetate for symptomatic peri- and postmenopausal women: impact on depression, vasomotor symptoms, sleep, and quality of life. Menopause 2006;13:780–786.
74. Yurcheshen ME, Guttuso T Jr, McDermott M, Holloway RG, Perlis M. Effects of gabapentin on sleep in menopausal women with hot flashes as measured by a Pittsburgh Sleep Quality Index factor scoring model. J Womens Health (Larchmt) 2009;18:1355–1360.
75. Guttuso T Jr. Nighttime awakenings responding to gabapentin therapy in late premenopausal women: a case series. J Clin Sleep Med 2012;8:187–189.
76. Mucci M, Carraro C, Mancino P, Monti M, Papadia LS, Volpini G, et al. Soy isoflavones, lactobacilli, Magnolia bark extract, vitamin D3 and calcium. Controlled clinical study in menopause. Minerva Ginecol 2006;58:323–334.
77. Hachul H, Brandão LC, D’Almeida V, Bittencourt LR, Baracat EC, Tufik S. Isoflavones decrease insomnia in postmenopause. Menopause 2011;18:178–184.
78. Soares CN, Joffe H, Rubens R, Caron J, Roth T, Cohen L. Eszopiclone in patients with insomnia during perimenopause and early postmenopause: a randomized controlled trial. Obstet Gynecol 2006;108:1402–1410.
79. Greenblatt DJ, Harmatz JS, Roth T, Singh NN, Moline ML, Harris SC, et al. Comparison of pharmacokinetic profiles of zolpidem buffered sublingual tablet and zolpidem oral immediate-release tablet: results from a singlecenter, single-dose, randomized, open-label crossover study in healthy adults. Clin Ther 2013;35:604–611.
80. McCurry SM, Guthrie KA, Morin CM, Woods NF, Landis CA, Ensrud KE, et al. Telephone-based cognitive behavioral therapy for insomnia in perimenopausal and postmenopausal women with vasomotor symptoms: a MsFLASH randomized clinical trial. JAMA Intern Med 2016;176:913–920.
81. Kline CE, Irish LA, Krafty RT, Sternfeld B, Kravitz HM, Buysse DJ, et al. Consistently high sports/exercise activity is associated with better sleep quality, continuity and depth in midlife women: the SWAN sleep study. Sleep 2013;36:1279–1288.
82. Tworoger SS, Yasui Y, Vitiello MV, Schwartz RS, Ulrich CM, Aiello EJ, et al. Effects of a yearlong moderate-intensity exercise and a stretching intervention on sleep quality in postmenopausal women. Sleep 2003;26:830–836.
83. Theorell-Haglöw J, Miller CB, Bartlett DJ, Yee BJ, Openshaw HD, Grunstein RR. Gender differences in obstructive sleep apnoea, insomnia and restless legs syndrome in adults – What do we know? A clinical update. Sleep Med Rev 2018;38:28–38.
84. Heinzer R, Marti-Soler H, Marques-Vidal P, Tobback N, Andries D, Waeber G, et al. Impact of sex and menopausal status on the prevalence, clinical presentation, and comorbidities of sleep-disordered breathing. Sleep Med 2018;51:29–36.
85. Young T, Evans L, Finn L, Palta M. Estimation of the clinically diagnosed proportion of sleep apnea syndrome in middle-aged men and women. Sleep 1997;20:705–706.
86. Hall MH, Kline CE, Nowakowski S. Insomnia and sleep apnea in midlife women: prevalence and consequences to health and functioning. F1000Prime Rep 2015;7:63.
87. Skatrud JB, Dempsey JA, Kaiser DG. Ventilatory response to medroxyprogesterone acetate in normal subjects: time course and mechanism. J Appl Physiol Respir Environ Exerc Physiol 1978;44:939–944.
88. Popovic RM, White DP. Upper airway muscle activity in normal women: influence of hormonal status. J Appl Physiol (1985) 1998;84:1055–1062.
89. Bixler EO, Vgontzas AN, Lin HM, Ten Have T, Rein J, Vela-Bueno A, et al. Prevalence of sleep-disordered breathing in women: effects of gender. Am J Respir Crit Care Med 2001;163(3 Pt 1):608–613.
90. Lubkowska A, Radecka A, Bryczkowska I, Rotter I, Laszczyńska M, Dudzińska W. Serum adiponectin and leptin concentrations in relation to body fat distribution, hematological indices and lipid profile in humans. Int J Environ Res Public Health 2015;12:11528–11548.
91. Shapiro SD, Chin CH, Kirkness JP, McGinley BM, Patil SP, Polotsky VY, et al. Leptin and the control of pharyngeal patency during sleep in severe obesity. J Appl Physiol (1985) 2014;116:1334–1341.
92. Di Carlo C, Tommaselli GA, Nappi C. Effects of sex steroid hormones and menopause on serum leptin concentrations. Gynecol Endocrinol 2002;16:479–491.
93. Jehan S, Auguste E, Zizi F, Pandi-Perumal SR, Gupta R, Attarian H, et al. Obstructive sleep apnea: women›s perspective. J Sleep Med Disord 2016;3:1064.
94. Kapsimalis F, Kryger MH. Gender and obstructive sleep apnea syndrome, part 2: mechanisms. Sleep 2002;25:499–506.
95. Kapsimalis F, Kryger M. Sleep breathing disorders in the U.S. female population. J Womens Health (Larchmt) 2009;18:1211–1219.
96. Peppard PE, Young T, Palta M, Skatrud J. Prospective study of the association between sleep-disordered breathing and hypertension. N Engl J Med 2000;342:1378–1384.
97. Chang CC, Chuang HC, Lin CL, Sung FC, Chang YJ, Hsu CY, et al. High incidence of stroke in young women with sleep apnea syndrome. Sleep Med 2014;15:410–414.
98. Otto ME, Belohlavek M, Romero-Corral A, Gami AS, Gilman G, Svatikova A, et al. Comparison of cardiac structural and functional changes in obese otherwise healthy adults with versus without obstructive sleep apnea. Am J Cardiol 2007;99:1298–1302.
99. Yeghiazarians Y, Jneid H, Tietjens JR, Redline S, Brown DL, El-Sherif N, et al. Obstructive sleep apnea and cardiovascular disease: a scientific statement from the American Heart Association. Circulation 2021;144:e56–e67.
100. Ljunggren M, Byberg L, Theorell-Haglöw J, Lindahl B, Michaëlsson K, Lindberg E. Increased risk of heart failure in women with symptoms of sleep-disordered breathing. Sleep Med 2016;17:32–37.
101. Lindberg E, Benediktsdottir B, Franklin KA, Holm M, Johannessen A, Jögi R, et al. Women with symptoms of sleep-disordered breathing are less likely to be diagnosed and treated for sleep apnea than men. Sleep Med 2017;35:17–22.
102. Mirer AG, Young T, Palta M, Benca RM, Rasmuson A, Peppard PE. Sleepdisordered breathing and the menopausal transition among participants in the sleep in midlife women study. Menopause 2017;24:157–162.
103. Polo-Kantola P, Rauhala E, Helenius H, Erkkola R, Irjala K, Polo O. Breathing during sleep in menopause: a randomized, controlled, crossover trial with estrogen therapy. Obstet Gynecol 2003;102:68–75.
104. Hensley MJ, Saunders NA, Strohl KP. Medroxyprogesterone treatment of obstructive sleep apnea. Sleep 1980;3:441–446.
105. Orr WC, Imes NK, Martin RJ. Progesterone therapy in obese patients with sleep apnea. Arch Intern Med 1979;139:109–111.
106. Mirer AG, Peppard PE, Palta M, Benca RM, Rasmuson A, Young T. Menopausal hormone therapy and sleep-disordered breathing: evidence for a healthy user bias. Ann Epidemiol 2015;25:779–784.e1.
107. Wesstrom J, Nilsson S, Sundstrom-Poromaa I, Ulfberg J. Restless legs syndrome among women: prevalence, co-morbidity and possible relationship to menopause. Climacteric 2008;11:422–428.
108. Phillips B. Movement disorders: a sleep specialist›s perspective. Neurology 2004;62(5 Suppl 2):S9–S16.
109. McCormack PL, Siddiqui MA. Pramipexole: in restless legs syndrome. CNS Drugs 2007;21:429–437. discussion 438-440.
110. Ondo WG. Restless legs syndrome: pathophysiology and treatment. Curr Treat Options Neurol 2014;16:317.
111. Polo-Kantola P, Rauhala E, Erkkola R, Irjala K, Polo O. Estrogen replacement therapy and nocturnal periodic limb movements: a randomized controlled trial. Obstet Gynecol 2001;97:548–554.

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