Interpersonal Influences on Female Reproductive Endocrinology
Copyright ©1987 Clinical Practices in Sexuality, (3:8:24-28, 1987)
Winnifred B. Cutler, Ph.D.
Athena Institute for Women's Wellness
Onset of coital behavior, coital regularity and olfactory cues appear
to influence female fertility.
Studies of animals and humans have created a body of evidence suggesting a role for pheromones in human sexuality. The earlier studies of pheromones in lower mammals coupled to the more recent demonstrations of relationships between heterosexual behavior and reproductive endocrine response in humans combined to form the basis for subsequent research showing human pheromonal effects. Heterosexual coital frequency and olfactory cues from men and other women appear to affect menstrual cycles and fertility status.
Menstrual Cycle Lengths Reflect Endocrine Milieu
In 1971, Treloar and colleagues provided quantitative information on the menstrual cycle throughout life, based on 25,000 years of prospectively gathered data. There appear to be three distinct stages of menstrual cycling throughout the life of women: adolescent, reproductively viable, and premenopausal. Cycles of about 26 to 33 days are common during the reproductively viable years, although some women regularly have shorter and longer cycles. In contrast, the first seven (adolescent) and last seven (premenopausal) years are characterized by a very high incidence of long and short menstrual cycles, in addition to cycles of 26 to 33 days. Subsequent studies by Vollman and others indicate that cycle lengths frequently reflect endocrine milieu and consequent fertility status. Cycles of about 29.5 +/- 3 days characterize a fertile, biophasic endocrine milieu while shorter or longer cycles have an increased incidence of infertile patterns.
Synchronized Reproductive Cycles
McClintock (1971) found that female college students who live together for several months begin to cycle together. Subsequently, several investigators replicated that phenomenon. Earlier work in small mammals had shown that exposure of females to the odors of urine or cage bedding of males will alter cycles to promote estrus or stimulate ovulation. In some infrahuman primates, males were also shown to influence cycle lengths. Female baboons denied mating show significantly longer cycles. Rhesus monkeys show a summer amenorrhea two to four months after a male decrease in sexual potency.1
Sexual Behavior Affects Female Reproductive Endocrinology
From 1979 through 1986 a series of studies were published which provided evidence for a role of heterosexual behavior in the development and maintenance of a fertile endocrine system in women. One study investigated the first coital age of a private patient practice predominantly composed of women with infertility problems who had sought help at a specialty clinic at the University of Pennsylvania.2 Women who were routine gynecological patients had the earliest first coital age (18.3 years). Women with increasingly greater degrees of infertility pathology showed increasingly later first coital ages. Women with primary infertility (with and without detectable pathology) had a mean age at first coitus that was 2.3 years older (20.6).
The results were the same whether one considered the chronologic or the gynecologic age (years since menarche) of the groups. Moreover, women who postponed their first coital experience more than seven years after the menarche were significantly more likely to be among the primary infertility group. This seven year "threshold" was particularly noteworthy in light of Treloar's demonstration of a seven year interval from menarche to the onset of regular fertile-type cycling. It was suggested that there might be a critical period for the onset of first coitus to optimize the likelihood of fertility.2
In other studies, sexual behavior frequency was examined in five sets of women, in Philadelphia, PA and in Stanford, CA. All the studies showed a similar phenomenon. When one separated the groups into women who engaged in weekly (never missing a nonmenstruating week of coitus) or less than weekly (either celibate or sporadic activity), those women who have regular weekly intercourse showed substantially higher incidences of fertile patterns of menstrual cyclicity.
The fertility patterns were revealed in cycle length. A menstrual cycle of less than 26 days was never observed among weekly active women while sexually less active women often showed short cycles. Furthermore, cycles longer than 33 days were substantially less common among the weekly active women. 3-6 Furthermore, women who had weekly intercourse had significantly higher levels of estrogen as well.6-8 In the Stanford Menopause Study, perimenopausal women who showed weekly sexual behavior had average estradiol concentration of 78+8.08 pg/ml whereas those with less sexual activity had lower estradiol levels of 57.65+7.53 pg/ml. Among a younger group of women, in Philadelphia, luteal phase levels of estradiol for women who were sexually active at least weekly centered at 120 pg/ml; levels of only half that - 60 pg/ml - were found in those who were either sporadically active or celibate.6
Analysis of basal body temperature data revealed similar relationships between regular weekly coital activity and an increased incidence of a normal ovulatory endocrine milieu. Among weekly sexually active women, 90% showed normal biphasic, adequately long luteal phases; this contrasted with a lower incidence of fertile BBT's among sporadically sexually active women (55%) and celibate women (44%).3,5
Further studies showed luteal phase lengths indicative of deficiencies (hyperthermic phase length <12 days) associated with sporadic sexual behavior, and particularly with infrequent or absent sexual activity in the luteal phase.3 Sporadic sexual behavior was further investigated in a sample of young college women who had prospectively recorded sexual behavior and cycle lengths. Women who where sporadically active (they did not have a regular weekly stable pattern of coital behavior), but who did have increased quantities of coital behavior in sporadic patterns, were more likely to show aberrant length menstrual cycles than those sporadically active women who showed lower amounts of coital exposure. When sexual behavior was weekly or more, increased quantities did not alter the cycle length. When behavior was sporadic, increased quantities of behavior tended to disrupt the cycle.4 In fact, a separate study revealed that half of the sporadically active young women (average age 23) had average luteal phase estradiol levels lower than 45 pg/ml.6
In composite, the studies have shown that sex with men occurring in a consistent and regular pattern is associated with an increased incidence of fertile-type endocrine milieu. That regular sexual behavior leads to a fertile milieu can be inferred from published data indicating that women with a pattern of weekly heterosexual behavior consistently showed a high incidence of “normal” (29.5+ 3 day) length cycles, fertile-type basal body temperature rhythm and higher post-ovulatory estrogen levels. However, the association does not hold in the reverse situation - a normal cycle length, a normal biphasic basal body temperature rhythm or higher post-ovulatory estrogen levels do not necessarily indicate which pattern of sexual behavior exists. 1, 3-6
Questions that emerge from these tentative conclusions are: What constitutes adequate sexual behavior? Is masturbation sufficient? Is intercourse necessary? What about homosexual behavior?
Tentative answers can be inferred from the data. Masturbation was shown in two separate studies not to be an adequate associate of the above-described fertile patterns of cycling; however, the presence of a man, either during noncoital genital stimulation or as a participant in sexual intercourse, was associated with the above-describe fertile endocrine patterns. Until 1987, there were no data about the possible role of homosexual behavior on these phenomena, but the Kinsey Institute Group recently reported that lesbian sexual activity which occurs at least 3 times per week is also associated with cycle lengths of 29.5 days (Society for Menstrual Cycle Research, 1987).
Because it was found that regular weekly patterns of heterosexual activity might influence menstrual cycle length, that women who lived together tended to cycle together, and because nonhuman studies suggested that chemical signals from other animals of the same species might be involved, an investigation was undertaken to evaluate whether an extract from the axillary region of men and women could offer a sufficient stimulus to induce changes in the menstrual cycle pattern of recipient women. The preliminary studies provided evidence indicating that axillary extracts from both sexes are effective.
To determine if olfactory cues are responsible for the influence of other people on womens' menstrual cycles and fertility status, studies were designed to determine if male essence makes aberrant length menstrual cycles less so and if female essence stimulates synchronization of normal cycles.
Among women with 29.5+1 day cycle lengths, there is a tendency to menstruate at or around the full moon. This phenomenon has now been demonstrated with peak levels in the autumn. 10,11 Therefore, in order to minimize the potential influences of either of these geophysical effects on the experiment, extracts of axillary secretions were collected in the autumn of one year, frozen, and applied (after thawing) in the autumn of the following year.
Axillary secretions were collected with underarm cotton pads from four female volunteer donors and five male donors, recruited from among co-workers and members of the community.12-14 All donors were engaged in a heterosexual relationship, had large numbers of lipophilic diptheroids in their axillary region, and for the duration of the experiment they did not shave or use deodorant, deodorant soaps, or perfumes in the axillary region. They washed each morning with only Ivory soap. The odor donors were picked for their ability to produce the complete spectrum of axillary odorants, having both the lipophilic diptheroids (a pungent odor similar to certain androgens) and the micrococcaceae. The dominant constituents of both are thought to be volatile acids and steroids. The male extracts were pooled together and female extracts were similarly batched, but here according to time of cycle.
Twenty-nine women, 19 to 30 years of age, were enrolled in this study. All met the following criteria: "gynecological maturity" (menstruating for at least 7 years), nulliparous, unmarried, not currently (nor within the last 3 months) using oral contraceptives or an I.U.D., and a willingness to make a daily entry of basal body temperature (BBT) and sexual behavior. A complete history and physical exam failed to find pathologies which might influence length of menstrual cycle. Women who believed themselves to generally cycle within the 26 to 32 day range were assigned to the female extract experiment to test for menstrual synchrony; women who believed themselves to have aberrant length menstrual cycles (<26 or >32 days) were assigned to the male extract experiment to test for the influence of male essence. Subjects came to the laboratory three times per week for 12.5 to 14.5 weeks to have the stimuli in an ethanol base rubbed on the upper lip. Neither of the experimenters handling the extracts on a routine basis could distinguish a difference in odor between the blank and potent extracts.
Among the group of women who began the experiment with aberrant length menstrual cycles, within the 14 weeks of the experiment male essence was effective in reducing the incidence of aberrant menstrual cycling. Both short and long cycles tended to become more normal in length. Four of the women receiving placebo had cycles more aberrant than any of the women receiving male extract, and all of the women receiving male extract appeared to be more bound in towards the fertile length cycle band. In this small sample, there were no apparent differences in testosterone, progesterone, or estradiol levels among women who received different treatments.
Female essence was found to bring recipients' cycles into synchrony with the donors while placebo did not influence the cycles of recipients.13
Exogeneous influences on the fertility of women have now been demonstrated in a variety of ways. It appears that regular, stable patterns of sexual behavior are conducive to optimal fertility. The timing of sexual behavior, both via an adequately early onset and an ongoing regular pattern, appear to enhance and promote the fertile endocrine milieu of women. Likewise, regular sexual behavior also reduces perimenopausal symptomatology.7,8,9,15,16 In addition, olfactory cues appear to influence female reproductive endocrinology.
1. Cutler WB, Garcia CR, Krieger AM. Sexual Behavior Frequency and Menstrual Cycle Length in Mature Premenopausal Women. Psychoneuroendocrinology 4: 297-309, 1979.
2. Cutler WB, Garcia CR, Krieger AM. Infertility and Age at First Coitus: A Possible Association. J. Biosoc Sci 11:425-432, 1979.
3. Cutler WB, Garcia CR, Krieger AM. Luteal Phase Defects: A Possible Relationship Between Short Hyperthermic Phase and Sporadic Sexual Behavior and Menstrual Cycle Length in Women. Hormones and Behavior 13:; 214-218, 1979.
4. Cutler WB, Garcia CR, Krieger AM. Sporadic Sexual Behavior and Menstrual Cycle Length in Women. Hormones and Behavior 14: 163-172, 1980.
5. Cutler WB, Preti G, Huggins G, Erickson B, Garcia CR. Sexual Behavior Frequency and Fertile-type Menstrual Cycle. Physiology and Behavior 34: 805-810, 1985.
6. Cutler WB, Garcia CR, Huggins GR, Preti G. Sexual Behavior and Steroid Levels Among Gynecologically Mature Premenopausal Women. Fertil Steril 45(4):496-502, 1986.
7. Cutler WB, Davidson JM, McCoy N. Sexual Behavior, Steroids and Hot Flashes are Associated During the Perimenopause. Neuroendo. L 5(3): 185, 1983.
8. McCoy N, Cutler W, Davidson JM. Relationships Among Sexual Behavior, Hot Flashes, and Hormone Levels in Perimenopausal Women. Arch Sexual Behavior 14(5) 385-394, 1985.
9.Cutler WB and Garcia CR. The Medical Management of the Menopause and Premenopause: Their Endocrinologic Basis. Lippincott Co., Philadelphia, PA, 1984.
10. Cutler WB. Lunar and Menstrual Phase Locking. Am J Obstet Gynecol 137: 834-839, 1980.
11. Cutler WB , Schleidt WM, Friedmann E, Preti G, Stine R.(1987) Lunar Influences on the Reproductive Cycle in Women. Human Biology, 59 (6) 959-972.
12. Cutler WB, Preti G, Krieger A, Huggins GR, Garcia CR, Lawley RJ (1986) Human Axillary Secretions Influence Women's Menstrual Cycles: The Role of Donor Extract from Men. Hormones and Behavior 20:463-470.
13. Preti G, Cutler WB, Krieger A, Huggins GR, Garcia CR, Lawley RJ (1986) Human Axillary Secretions Influence Women's Menstrual Cycles: The Role of Donor Extract from Women. Hormones and Behavior 20:474-482.
14. Preti G., Cutler WB. (1987) Human Axiallary Extracts: An Analysis of Compounds from Samples Which Influence Menstrual Timing. J. Chem Ecol 13:717-731
15. Cutler WB, Garcia CR, McCoy N. (1987) Perimenopausal Sexuality. Archives of Sex Behavior: 16:3:225-234.1987.
16. Cutler WB, Garcia CR, Edwards DA. Menopause: A Guide for Women and the Men Who Love Them. W.W. Norton & Co., Inc., New York, 1983. Updated paperback, 1985.