Circadian rhythms, sleep, and the menstrual cycle.

Women with ovulatory menstrual cycles have a circadian rhythm superimposed on the menstrual-associated rhythm; in turn, menstrual events affect the circadian rhythm. In this paper, we review circadian rhythms in temperature, selected hormone profiles, and sleep-wake behavior in healthy women at different phases of the menstrual cycle. The effects on menstrual cycle rhythmicity of disrupted circadian rhythms, for example, with shiftwork and altered circadian rhythms in women with menstrual-related mood disturbances, are discussed. Compared to the follicular phase, in the post-ovulation luteal phase, body temperature is elevated, but the amplitude of the temperature rhythm is reduced. Evidence indicates that the amplitude of other rhythms, such as melatonin and cortisol, may also be blunted in the luteal phase. Subjective sleep quality is lowest around menses, but the timing and composition of sleep remains relatively stable across the menstrual cycle in healthy women, apart from an increase in spindle frequency activity and a minor decrease in rapid eye movement (REM) sleep during the luteal phase. Disruption of circadian rhythms is associated with disturbances in menstrual function. Female shiftworkers compared to non-shiftworkers are more likely to report menstrual irregularity and longer menstrual cycles. There also is accumulating evidence that circadian disruption increases the risk of breast cancer in women, possibly due to altered light exposure and reduced melatonin secretion. Further investigations into the biological consequences of circadian disruption in women will offer insight into some menstrual-associated disorders, including mood changes, as well as reproductive function and possible links with breast cancer.

[1]  R. Hauger,et al.  Circadian rhythms of prolactin and thyroid-stimulating hormone during the menstrual cycle and early versus late sleep deprivation in premenstrual dysphoric disorder , 1996, Psychiatry Research.

[2]  M. Rousseau.  Women's midlife health. Reframing menopause. , 1998, Journal of nurse-midwifery.

[3]  C. Pollak,et al.  High nocturnal body temperature in premenstrual syndrome and late luteal phase dysphoric disorder. , 1991, The American journal of psychiatry.

[4]  S. Berga,et al.  Circadian pattern of plasma melatonin concentrations during four phases of the human menstrual cycle. , 1990, Neuroendocrinology.

[5]  Derk-Jan Dijk,et al.  Getting Through to Circadian Oscillators: Why Use Constant Routines? , 2002, Journal of biological rhythms.

[6]  C. Eastman,et al.  Effect of Sex, Menstrual Cycle Phase, and Oral Contraceptive Use on Circadian Temperature Rhythms , 1995 .

[7]  J. Gillin,et al.  Sleep EEG studies during early and late partial sleep deprivation in premenstrual dysphoric disorder and normal control subjects , 1999, Psychiatry Research.

[8]  A. Cagnacci,et al.  Regulation of the 24-hour rhythm of body temperature in menstrual cycles with spontaneous and gonadotropin-induced ovulation. , 1997, Fertility and sterility.

[9]  Kathryn A. Lee,et al.  Sleep patterns related to menstrual cycle phase and premenstrual affective symptoms. , 1990, Sleep.

[10]  A. Paoletti,et al.  REGULATION OF THE 24H BODY TEMPERATURE RHYTHM OF WOMEN IN LUTEAL PHASE: ROLE OF GONADAL STEROIDS AND PROSTAGLANDINS , 2002, Chronobiology international.

[11]  Geoffrey C Kabat,et al.  Shift work, light at night, and breast cancer on Long Island, New York. , 2006, American journal of epidemiology.

[12]  C. Pollak,et al.  Sleep spindle frequency changes during the menstrual cycle , 1994, Journal of Sleep Research.

[13]  R. Hauger,et al.  Neuroendocrine effects of light therapy in late luteal phase dysphoric disorder , 1994, Biological Psychiatry.

[14]  R. Stevens,et al.  Inverse association between breast cancer incidence and degree of visual impairment in Finland , 1999, British Journal of Cancer.

[15]  Richard G. Stevens,et al.  Circadian Disruption and Breast Cancer: From Melatonin to Clock Genes , 2005, Epidemiology.

[16]  L. Lack,et al.  The Effect of Sleep/Wake State on Nocturnal Melatonin Excretion , 1990, Journal of pineal research.

[17]  G. Guyatt,et al.  The effect of bright light therapy on depression associated with premenstrual dysphoric disorder. , 2005, American journal of obstetrics and gynecology.

[18]  R. Wurtman,et al.  The circadian rhythm of plasma melatonin during the normal menstrual cycle and in amenorrheic women. , 1988, The Journal of clinical endocrinology and metabolism.

[19]  I. Rothchild,et al.  The effects of dosage, and of estrogen, androgen or salicylate administration on the degree of body temperature elevation induced by progesterone. , 1952, Endocrinology.

[20]  G. Richardson,et al.  Brief wake episodes modulate sleep-inhibited luteinizing hormone secretion in the early follicular phase. , 2005, The Journal of clinical endocrinology and metabolism.

[21]  K. Lushington,et al.  The rhythms of human sleep propensity and core body temperature , 1996, Journal of sleep research.

[22]  Kathryn A. Lee,et al.  Self-reported sleep disturbances in employed women. , 1992, Sleep.

[23]  L. Wetterberg,et al.  Human serum melatonin changes during the menstrual cycle. , 1976, The Journal of clinical endocrinology and metabolism.

[24]  S. Berga,et al.  Plasma Melatonin Circadian Rhythms during the Menstrual Cycle and after Light Therapy in Premenstrual Dysphoric Disorder and Normal Control Subjects , 1997, Journal of biological rhythms.

[25]  T Uehata,et al.  The fatigue and maternity disturbances of night workwomen. , 1982, Journal of human ergology.

[26]  I. Janssen,et al.  Relationship of day-to-day reproductive hormone levels to sleep in midlife women. , 2005, Archives of internal medicine.

[27]  I. Halbrecht.  Ovarian function and body temperature. , 1945, Lancet.

[28]  S. Honma,et al.  Effects of Menstrual Cycle on Plasma Melatonin Level and Sleep Characteristics , 1993, The Japanese journal of psychiatry and neurology.

[29]  I. Fentiman,et al.  Melatonin and breast cancer: a prospective study. , 2004, Journal of the National Cancer Institute.

[30]  J. Gillin,et al.  Early versus late partial sleep deprivation in patients with premenstrual dysphoric disorder and normal comparison subjects. , 1995, The American journal of psychiatry.

[31]  D. O. Walter,et al.  Changes in sleep-wakefulness in female rats during circadian and estrous cycles. , 1968, Brain research.

[32]  A. Borbély.  A two process model of sleep regulation. , 1982, Human neurobiology.

[33]  I. Tobler,et al.  Influence of estrus cycle and ageing on activity patterns in two inbred mouse strains , 2006, Behavioural Brain Research.

[34]  B. Claustrat,et al.  Urinary melatonin, LH, oestradiol, progesterone excretion during the menstrual cycle or in women taking oral contraceptives. , 1987, Acta endocrinologica.

[35]  M. Wheeler,et al.  Neurohypophysial hormone and melatonin secretion over the natural and suppressed menstrual cycle in premenopausal women , 1998, Clinical endocrinology.

[36]  U. Halbreich.  The etiology, biology, and evolving pathology of premenstrual syndromes , 2003, Psychoneuroendocrinology.

[37]  T. Shimazoe,et al.  Estrogen differentially regulates expression of Per1 and Per2 genes between central and peripheral clocks and between reproductive and nonreproductive tissues in female rats , 2005, Journal of neuroscience research.

[38]  W. Mendelson,et al.  Longitudinal sleep EEG, temperature, and activity measurements across the menstrual cycle in patients with premenstrual depression and in age-matched controls , 1989, Psychiatry Research.

[39]  I. Karacan,et al.  Sleep pattern changes in menstrual cycles of women with premenstrual syndrome: a preliminary study. , 1997, American journal of obstetrics and gynecology.

[40]  Kathryn A. Lee.  Circadian Temperature Rhythms in Relation to Menstrual Cycle Phase , 1988 .

[41]  [Changes in circadian sleep-wake and rest-activity rhythms during different phases of menstrual cycle]. , 2005, Sheng li xue bao : [Acta physiologica Sinica].

[42]  K. Lee,et al.  REM sleep and mood state in childbearing women: sleepy or weepy? , 2000, Sleep.

[43]  J. Bruce,et al.  Human pineal physiology and functional significance of melatonin , 2004, Frontiers in Neuroendocrinology.

[44]  K. Lee,et al.  Prevalence of perimenstrual symptoms in employed women. , 1991, Women & health.

[45]  K. Messing,et al.  Menstrual-cycle characteristics and work conditions of workers in poultry slaughterhouses and canneries. , 1992, Scandinavian journal of work, environment & health.

[46]  Anna Wirz-Justice,et al.  Sleep deprivation in depression: what do we know, where do we go? , 1999, Biological Psychiatry.

[47]  D. Skene,et al.  6‐Sulphatoxymelatonin Production in Breast Cancer Patients , 1990, Journal of pineal research.

[48]  L A Stephenson,et al.  Circadian rhythm changes in core temperature over the menstrual cycle: method for noninvasive monitoring. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[49]  M. Moline,et al.  Sleep in women across the life cycle from adulthood through menopause. , 2003, The Medical clinics of North America.

[50]  F. Baker,et al.  Self-reported sleep across the menstrual cycle in young, healthy women. , 2004, Journal of psychosomatic research.

[51]  Sheila R. Taylor,et al.  Sleep and 24 hour body temperatures: a comparison in young men, naturally cycling women and women taking hormonal contraceptives , 2001, The Journal of physiology.

[52]  Mary A. Ho.  Sex Hormones and the Sleep of Women , 1972 .

[53]  D. Fuller,et al.  Comparison of oral and infrared auditory canal thermometry in sports participants , 1998 .

[54]  T. Porkka-Heiskanen,et al.  Women's sleep in health and disease. , 2005, Journal of psychiatric research.

[55]  Anna Wirz-Justice,et al.  Biological rhythm disturbances in mood disorders , 2006, International clinical psychopharmacology.

[56]  A. Winfree.  Book reviewThe clocks that time us : Martin Moore-Ede, Frank Sulzman, and Charles Fuller Harvard University Press, Cambridge, 1982, 448 pp., $25.00 , 1983 .

[57]  F. Baker,et al.  Oral contraceptives alter sleep and raise body temperature in young women , 2001, Pflügers Archiv.

[58]  The Thermogenic Property of Progesterone , 1950 .

[59]  Johnni Hansen,et al.  Increased Breast Cancer Risk among Women Who Work Predominantly at Night , 2001, Epidemiology.

[60]  G. Rogers,et al.  Acetaminophen does not affect 24-h body temperature or sleep in the luteal phase of the menstrual cycle. , 2002, Journal of applied physiology.

[61]  P. Badia,et al.  Effects of menstrual cycle phase and oral contraceptives on alertness, cognitive performance, and circadian rhythms during sleep deprivation , 1999, Behavioural Brain Research.

[62]  M. Uchiyama,et al.  Long‐term rectal temperature measurements in a patient with menstrual‐associated sleep disorder , 2002, Psychiatry and Clinical Neurosciences.

[63]  Wehr Ta,et al.  Therapeutic effect of sleep deprivation in patients with premenstrual syndrome. , 1987 .

[64]  M. Uchiyama,et al.  Diurnal fluctuation of sleep propensity and hormonal secretion across the menstrual cycle , 2000, Biological Psychiatry.

[65]  D. Swaab,et al.  Sex Hormone Receptors Are Present in the Human Suprachiasmatic Nucleus , 2002, Neuroendocrinology.

[66]  M. Mauri.  Sleep and the reproductive cycle: a review. , 1990, Health care for women international.

[67]  R. Kronauer,et al.  Bright light induction of strong (type 0) resetting of the human circadian pacemaker. , 1989, Science.

[68]  D. Kripke,et al.  Melatonin and phototherapy in premenstrual depression. , 1990, Progress in clinical and biological research.

[69]  R. Reid,et al.  Menopausal-like hot flashes reported in women of reproductive age. , 1998, Fertility and sterility.

[70]  A. Borbély,et al.  Sleep homeostasis in the female rat during the estrous cycle , 1998, Brain Research.

[71]  T. Nakayama,et al.  Action of progesterone on preoptic thermosensitive neurones , 1975, Nature.

[72]  J. Derr,et al.  Chronic hormone replacement therapy alters thermoregulatory and vasomotor function in postmenopausal women. , 1997, Journal of applied physiology.

[73]  G. Rogers,et al.  High nocturnal body temperatures and disturbed sleep in women with primary dysmenorrhea. , 1999, American journal of physiology. Endocrinology and metabolism.

[74]  M. Lippman,et al.  ROLE OF PINEAL GLAND IN ÆTIOLOGY AND TREATMENT OF BREAST CANCER , 1978, The Lancet.

[75]  F. Leidenberger,et al.  The circadian pattern of melatonin and its positive relationship with progesterone in women. , 1986, The Journal of clinical endocrinology and metabolism.

[76]  B. Saletu,et al.  Influence of partial sleep deprivation on the secretion of thyrotropin, thyroid hormones, growth hormone, prolactin, luteinizing hormone, follicle stimulating hormone, and estradiol in healthy young women , 1993, Psychiatry Research.

[77]  F. Baker,et al.  Menstrual factors in sleep. , 1998, Sleep medicine reviews.

[78]  M. Lippman,et al.  Decreased nocturnal plasma melatonin peak in patients with estrogen receptor positive breast cancer. , 1982, Science.

[79]  R. Hauger,et al.  Cortisol circadian rhythms during the menstrual cycle and with sleep deprivation in premenstrual dysphoric disorder and normal control subjects , 2000, Biological Psychiatry.

[80]  G. Laughlin,et al.  Modification of circadian body temperature rhythm during the luteal menstrual phase: role of melatonin. , 1996, Journal of applied physiology.

[81]  Charles A. Czeisler,et al.  INFLUENCE OF LIGHT ON CIRCADIAN RHYTHMICITY IN HUMANS , 1999 .

[82]  P. Zee,et al.  EFFECTS OF SHIFTWORK ON SLEEP AND MENSTRUAL FUNCTION IN NURSES , 2002, Health care for women international.

[83]  J. Marshall.  Thermal Changes in the Normal Menstrual Cycle , 1963, British medical journal.

[84]  Short Rv,et al.  Effects of flying and of time changes on menstrual cycle length and on performance in airline stewardesses. , 1973 .

[85]  A A Borbély,et al.  Sleep and the sleep electroencephalogram across the menstrual cycle in young healthy women. , 1996, The Journal of clinical endocrinology and metabolism.

[86]  D. Deaver,et al.  Estrogen replacement in middle-aged women: thermoregulatory responses to exercise in the heat. , 1992, Journal of applied physiology.

[87]  R. Stevens,et al.  Night shift work, light at night, and risk of breast cancer. , 2001, Journal of the National Cancer Institute.

[88]  R. Rylander,et al.  Outcome of pregnancy in relation to irregular and inconvenient work schedules. , 1989, British journal of industrial medicine.

[89]  Cantab Ma.  John Crighton Bramwell. , 1976 .

[90]  P. Clopton,et al.  Temperature Circadian Rhythms during the Menstrual Cycle and Sleep Deprivation in Premenstrual Dysphoric Disorder and Normal Comparison Subjects , 1997, Journal of biological rhythms.

[91]  Elizabeth B. Klerman,et al.  Clinical Aspects of Human Circadian Rhythms , 2005, Journal of biological rhythms.

[92]  R. Armitage,et al.  Short note: oral contraceptives and sleep in depressed and healthy women. , 2002, Sleep.

[93]  R. Frydman,et al.  Time relationships between basal body temperature and ovulation or plasma progestins. , 1984, Fertility and sterility.

[94]  R. Bootzin,et al.  Sleep and the menstrual cycle. , 1997, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[95]  Peter W. Jones,et al.  Efficacy of selective serotonin-reuptake inhibitors in premenstrual syndrome: a systematic review , 2000, The Lancet.

[96]  Susan E Hankinson,et al.  Urinary melatonin levels and breast cancer risk. , 2005, Journal of the National Cancer Institute.

[97]  S. Berga,et al.  Blunted Phase-Shift Responses to Morning Bright Light in Premenstrual Dysphoric Disorder , 1997, Journal of biological rhythms.

[98]  B. Kinon,et al.  Prevalence of hyperprolactinemia in schizophrenic patients treated with conventional antipsychotic medications or risperidone 1 1 This work was sponsored by Eli Lilly and Company. , 2003, Psychoneuroendocrinology.