1 Epidemiology Branch, 2 Biostatistics Branch, National Institute of Environmental Health Sciences, Durham, NC, USA, 3 Westat, Inc., Durham, NC, USA, 4 Biomonitoring and Health Assessment Branch, Division of Applied Research and Technology, National Institute for Occupational Safety and Health, Cincinnati, Ohio, USA
5 To whom correspondence should be addressed at: Epidemiology Branch, MD A3-05, P.O.Box 12233, Durham NC 27709, USA. e-mail wilcox{at}niehs.nih.gov
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Abstract |
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Key words: intercourse/ovulation
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Introduction |
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If one or more of these mechanisms act in humans, we would expect to see more frequent intercourse during a womans fertile days. We explored this possibility using prospectively collected data on intercourse and ovulation from sexually active women who were using effective non-hormonal methods of birth control.
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Materials and methods |
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We performed a supplemental analysis to address the hypothesis that intercourse is able to accelerate ovulation. Because this supplemental analysis would not be affected in any way by intentional timing of intercourse (such as could be expected among women who were trying to become pregnant), we were able to increase our sample size by including data from an additional group of 217 women (696 cycles) who were trying to conceive. These women were enrolled under the same protocol and have been extensively described (Wilcox et al., 1988, 1995).
Laboratory assays
We measured the daily excretion of estrone 3-glucuronide (a primary urinary metabolite of estradiol) and pregnanediol 3-glucuronide (a metabolite of progesterone) using competitive time-resolved fluoroimmunoassays (Kesner et al., 1994).
Defining the day of ovulation
The secretion of estrogen and progesterone undergoes rapid and distinctive changes around the time of ovulation. These changes are reflected in the urinary metabolites of these hormones. We had previously developed an algorithm to identify day of ovulation based on changes in the ratio of estrogen to progesterone metabolites throughout the several days before and after ovulation. We validated the algorithm against the surge of urinary LH (Baird et al., 1991, 1995). Subsequent studies have substantiated the relative precision of this method (Dunson et al., 2001
). A recent French study (using ultrasound monitoring of follicular rupture as the gold standard) showed the algorithm to be as accurate as urinary LH in estimating the time of ovulation (Ecochard et al., 2001
).
Statistical methods
All analyses of cycles were based on within-women averages rather than on total cycles. We included only non-bleeding days in our calculations because these couples reduced their frequency of intercourse during menstruation. We compared the frequency of intercourse during the 6 fertile days and during all other non-bleeding days, first by calculating the mean for each woman during those two time periods, and then by testing the difference with a Wilcoxon signed rank test. In estimating the distribution of ovulation across the days of the week, we calculated the proportion of ovulations occurring on each weekday for each woman, and then averaged these proportions across women.
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Results |
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Figure 1 shows the mean daily frequency of intercourse in relation to day of ovulation. The dashed line shows raw daily means, while the dark solid line represents the 3 day moving average. The overall mean frequency of intercourse on non-bleeding days was 0.29 (shown by the horizontal line, equivalent to twice a week). The frequency of intercourse was above the mean for most of the follicular phase (before ovulation) and below the mean for most of the luteal phase. The 6 consecutive days of the cycle with the highest frequency of intercourse corresponded exactly with the 6 fertile days. The mean daily frequency of intercourse was 24% higher during the fertile days than during all other non-bleeding days (0.339 compared with 0.274, P < 0.001).
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Exploring biological mechanisms
The distinctive pattern of intercourse frequency across the menstrual cycle among women not trying to conceive suggests the presence of biological mechanisms that influence intercourse. One obvious hypothesis is an increase in male or female libido with the approach of ovulation, and a decline thereafter. We did not collect information on libido and so we cannot pursue this specific question.
The increasing frequency of intercourse just before ovulation could also represent an acceleration of ovulation stimulated by intercourse. In some mammals, intercourse can accelerate the rupture and luteinization of a mature ovarian follicle by triggering a release of GnRH that sets off the LH surge (Bakker and Baum, 2000). In humans, ovulation is thought to follow the LH surge by an average of 30 h (World Health Organization Task Force, 1980
; Ecochard et al., 2001
). If intercourse in humans could affect ovulation through the same neuronal pathway as in other mammals (assuming that the time from the triggering event of intercourse to the LH surge is no more than a few hours), we would expect ovulation to follow the triggering intercourse by 12 days.
It is inherently difficult in observational data to know whether ovulation is the causeor the resultof the high frequency of intercourse just before ovulation. We addressed this question by taking advantage of a strong cultural pattern of intercourse. Couples in our study were most likely to have intercourse on the weekend (Friday, Saturday or Sunday). Ovulation, in contrast, presumably occurs without regard to day of the week. If intercourse were able to accelerate ovulation, then we would expect weekend intercourse to produce a corresponding increase of ovulation 12 days later. In order to address this question, we enlarged our sample size by adding a supplemental sample of 217 women who were trying to become pregnant. This provided a total of 285 women and 867 cycles.
Figure 2 shows the frequency of intercourse and ovulation by day of week. The peak of intercourse on FridaySaturdaySunday is followed by a small rise in the frequency of ovulation on SundayMondayTuesday (47% of all ovulations, compared with an expected 3/7 or 43%). This association is too weak to confirm the hypothesis. However, it did suggest a further test.
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Figure 3 shows the pattern of ovulation in these three groups. Among couples with no pattern of weekend intercourse, the estimated probability of ovulation on SundayMondayTuesday was 41% (slightly less than the null expectation of 43%). The percentage of post-weekend ovulations rose to 46% among couples with moderate patterns of weekend intercourse, and reached 54% for couples with the strongest pattern of weekend intercourse (test for trend, P < 0.01). This trend was similar for the two study groups (those using effective birth control and those trying to conceive).
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Discussion |
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We analysed intercourse data from 68 women who were using highly effective non-hormonal methods of birth control (either IUD or tubal ligation). These women had no reason to modify the timing of their intercourse in relation to their fertile days. Their frequency of intercourse was above the mean during the follicular phase, peaking during the 6 fertile days of the cycle, and then falling to relatively low levels during the luteal phase (Figure 1). This pattern is unlikely to be due to chance. What biological mechanisms might explain it?
There are at least three possible contributors to this pattern. One is cyclic fluctuation in womens libido. Dennerstein et al. (1994) conducted a study of female libido in which 168 women kept daily diaries and collected daily urine samples for later identification of ovulation. Self-reported sexual interest increased in the days before ovulation and declined afterward. These changes in womens libido are consistent with the pattern of intercourse in our data.
Another factor in this intercourse pattern could be a cyclic increase in the womans sexual attractiveness. An increase in intercourse initiated by the male partner has been reported to occur around ovulation (Harvey, 1987). This could reflect the mans response to subtle behavioural cues from the woman, or perhaps to the womans production of cycle-dependent pheromones. Support for a pheromone hypothesis is found in a recent clinical trial of a commercially produced pheromone (McCoy and Pitino, 2002
). Women using the active product reported more frequent sexual approaches by their male partner. Taken together, these two lines of evidence raise the possibility that cycle-specific influences on male libido contribute to the cyclic pattern of intercourse.
A third possibility is the acceleration of ovulation by intercourse. How plausible is such a mechanism in humans? While the possibility has been raised (Clark and Zarrow, 1971; Joechle, 1975
) it has been regarded with skepticism (Vollman, 1970
). Species are usually thought to be either reflex or spontaneous ovulators, with ovulation in humans being spontaneous. However, experiments on rodents have suggested that even among spontaneous ovulators, the neural circuitry needed for intercourse to stimulate ovulation may be present (Bakker and Bau, 2000
).
Our observation of a rise in ovulation following the weekend peak of intercourse supports the possibility of accelerated ovulation in humans. However, this could also reflect weekend changes in other factors (perhaps sleep patterns, exercise, or stress) that might affect ovulation. A simple randomized trial could test the hypothesis definitively. Such a randomized trial could be conducted among volunteer couples using non-hormonal methods of birth control. Couples would have to agree to ultrasound surveillance of follicle development and then to the random assignment of intercourse (or no intercourse) from the time the dominant follicle approaches its maximum size until after ovulation. A cross-over design in successive cycles would provide statistical power with relatively modest sample size.
In conclusion, our data from 68 women using effective methods of birth control show that intercourse is most likely to occur during the 6 fertile days of the menstrual cycle. It is remarkable that the biological forces shaping this intimate aspect of human behaviour have gone largely unrecognized, perhaps because the effect is modest in absolute terms. For couples who wish to conceive, these biological mechanisms act as a silent partner that facilitates the optimum timing of intercourse. Women who do not wish to become pregnant should be informed that occasional unprotected intercourse may be more risky than chance alone would predict (Wilcox et al., 2001).
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References |
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Submitted on December 16, 2003; resubmitted on April 14, 2004; accepted on April 16, 2004.