Abstract
 
          Objective: To determine whether the basal body temperature
          (BBT) is a reliable or not a reliable method for prediction
          and detection of ovulation the literature was searched on
          the procedure of obtaining the BBT in correspondence with
          the new data in sleep medicine.
          Results: The BBT tends to rise according to its circadian
          rhythm at the time of awakening. Measuring the BBT at that
          time will show not only the progesterone effect but also the
          circadian effect.This can explain its "unreliability".
          However, the lowest circadian thermogenic point during a
          nocturnal sleep is at the 5th hour after sleep onset.
          Measuring the temperature at this hour will show the
          progesterone effect without the masking of the circadian
          effect. This can make the BBT a reliable method for
          ovulation prediction and detection.
          Conclusions: A new basal body temperature measured at the
          5th hour of a nocturnal sleep can pinpoint the rise at the
          ovulation day without the masking effects of the circadian
          rhythm, expressed in the old BBT recordings.
          Key Words: Basal body temperature,progesterone,
          norepinephrine, sleep, circadian rhythm.
 
 
 
 
          It is almost eight years since the last publication
          concerning basal body temperature (BBT) and ovulation
          detection, in its title, appeared and listed in MEDLINE (1).
          The question is whether this "unreliable" (2) method of
          ovulation detection has still a place three years before the
          year 2000 ?
          Moghissi (3) examined in 30 normally menstruating women
          their basal body temperature recordings and correlated it
          with serum LH, progesterone and estradiol. In approximately
          20% of ovulatory cycles the BBT failed to demonstrate
          ovulation. Such poor reliability has been reported also by
          Bauman (2) who found that only 22% of BBT assessments
          corresponded to within 1 day of the biologic phenomena, and
          by Buxton and Engle (4) who found at laparoscopies performed
          on the first day of the BBT rise that in one third of cases
          ovulation had already occurred more than 24 hours earlier.
          A simple, reliable method to predict and detect ovulation in
          women is still needed.
 
          Introduction
 
          Deep body temperature shows a strong circadian rhythm. It
          varies in response to a variety of behavioral and external
          stimuli, including sleep, physical activity, postural
          changes, ambient temperature and meals. The menstrual cycle
          of women also affects their temperature rhythm, with the
          post-ovulatory temperature rise increasing the overall mean.
          The relationship between the basal body temperature recorded
          at awakening and the circadian temperature rhythm during
          nocturnal sleep were evaluated in order to find the best
          hour of basal body temperature recording that will reflect
          mostly the peri-ovulatory temperature rise. Review of
          relevant articles since 1838 reflected on one side the basal
          body temperature`s way of recording and on the other side
          the point that there is no exact determination of the best
          hour of temperature recording after onset of a nocturnal
          sleep. Review of articles on sleep revealed certain points
          considering the basal body temperature with a suggestion for
          the best hour of measuring the basal body temperature for
          prediction and detection of ovulation.
 
          Materials and methods
 
          In order to review the literature concerning the basal body
          temperature and temperature measurements during nocturnal
          sleep the Medline was searched for any article mentioning
          these items in its title or abstract. The references given
          in each article were looked for articles that were published
          before 1966, and are not included in the Medline. Articles
          as late as 1838 were searched for any information on the
          subject that can illustrate the technique of basal body
          temperature recording. The relevant data was gathered to be
          included in this review. The information on temperature
          measurements during sleep was taken mainly from the journal
          Sleep, and the references mentioned in its relevant
          articles. By citing the various techniques used to measure
          the basal body temperature and the temperature recordings
          during sleep, the best time for basal body temperature
          measurement was searched in order to exclude the other
          circadian factors influencing it besides the progesterone
          rise at the peri-ovulatory period.
          The data was arranged by three main sections: basal body
          temperature, progesterone and sleep. The connections between
          these three factors seems essential to the evaluation of the
          subject.
 
          Basal body temperature
 
          The basal body temperature graph is probably the most widely
          used aid in the identification of the day of ovulation (3).
          Von Fricke (5) studied in 1838 the axillary, vaginal and
          uterine temperatures. His observations were made eight days
          before the menses, four days before, and during the period.
          He concluded that the vagina has a higher temperature than
          either the axilla or the uterus, and that menstruation have
          no influence upon the temperature. However, daily
          observations were not made throughout the cycle.
          Jacobi (6) studied in 1876 on six women, over a period of
          two to three months, the oral, axillary, vaginal and rectal
          temperatures. She confirmed the temperature rise before
          menstruation and the fall during the flow to a level which
          was lower than that of the intermenstrual period.
          Rabuteau (7) reported in 1870 his study of a 28 year old
          healthy woman with regular menstrual periods. He stated that
          a drop in temperature occurred two days before menstruation
          and disappeared several days after the cessation of the
          flow.
          Van de Velde (8) studied in 1905 the axillary temperature
          in women, the number not stated. The typical curve showed a
          premenstrual rise maintained for a short time, then a fall
          before the onset of menstruation, and a continued drop
          during and after menstruation to reach the lowest point
          about ten days after cessation. He regarded the fall in the
          temperature as the actual cause of menstruation. He said,
          "it seems to me without doubt that an inner association
          exists between the two facts - the beginning of the lowering
          of the curve and the appearance of the menstrual bleeding -
          an association indeed in the relationship of cause and
          effect".
          Flaskamp (9) postulated in 1928 that a double wave
          temperature rhythm occuring during a day. The daily rhythm
          showed a maximum between 5 and 8 P.M., and a minimum between
          2 and 6 A.M.; a rise from 6 A.M. to noon; from 12 to 2 a
          fall; the secondary rise from 2 to 6 P.M.; and a second fall
          up to 6 A.M.
          Tompkins (10) in 1944 stated the following procedure
          utilizing temperature method for determining the date of
          ovulation: "Take the temperature rectally with a blunt tip
          rectal thermometer for five minutes by the clock immediately
          after waking in the morning and before arising, eating,
          drinking or smoking (!)" (the exclamation mark appeared in
          the original article).Then he added that "some investigators
          advise that the temperature be taken at the same hour each
          morning. I myself would prefer to have the temperature
          recorded when the patient wakes up in the belief that a more
          significant figure is recorded at 10 a.m. on a Sunday
          morning after a gay evening than at 7 a.m. when the patient
          has only had three or four hours` sleep".
          Barton and Wiesner (11) in their article on waking
          temperature wrote that "a reading must be taken every
          morning throughout the cycle, immediately on waking, before
          rising, moving or taking food or drink".
          Despite utilizing this procedure a discrepancy of up to 4
          days between basal body temperature rise and ovulation time,
          estimated by corpus luteum dating, was found (4,12,13).
          Buxton and Engle (4) wrote in 1950 that "since only basal
          body temperatures are indicative of the change produced by
          ovulation it would theoretically be necessary to keep a
          patient at complete basal rest and to take hourly
          temperature readings to narrow down the ovulatory
          temperature change more accurately".
          Moghissi (14) in his review on prediction and detection of
          ovulation, published in 1980, wrote that "a period of 6 to 8
          hours of uninterrupted rest is deemed to be necessary before
          the temperature reading is made".
          Basal body temperature charts from menstrual cycles of 98
          women were evaluated by six experienced physicians. The time
          of ovulation was estimated from the charts by a consensus of
          at least five of the evaluators coincided with the
          luteinizing hormone peak ñ 1 day in only 17 (22.1%) of the
          77 cycles that were determined by endocrine profiles to be
          ovulatory and to have adequate luteal phases. Bauman (4),
          from the Masters & Johnson Institute, St. Louis, Missouri,
          who conducted this study concluded that the basal body
          temperature was an "unreliable method of ovulation
          detection".
          McCarthy and Rockette (15) stated that "the prediction of
          ovulation solely with the basal body temperature graph is
          not useful because of the day-to-day variability of
          temperature readings, cycle variability and the effects of
          illness, medication, diet and changes in sleeping patterns".
          Wetzels et al. (16), in 1982, compared the basal body
          temperature with ultrasonographical findings for ovulation
          detection in 47 cycles."Volunteers and patients were
          carefully instructed to measure rectal temperature before
          getting up each morning". They concluded that ovulation
          detection and timing by basal body temperature were "not
          reliable".
          Weinberg and Cohen (17) from the IBM Thomas J. Watson
          Research Center, Yorktown Heights, NY, published in 1983
          their article on ovulation detection by monitoring
          temperature during sleep. To measure the temperature they
          used a stainless steel capped thermistor probe attached to a
          feminine hygiene pad which was worn in the usual way as
          during menstruation. The probe was resting against the skin
          and no adhesives or pastes were used to improve thermal
          contact. The probe had a long cable to a digital
          thermometer. The thermometer was interfaced to a
          microcomputer which recorded the data every 6 min during
          sleeping hours. It took 2-3 hours for the temperature to
          rise and stabilize. Following this period, gradual
          temperature changes and abrupt fluctuations of about 0.6øC
          (peak-to-peak) were observed.
          Deep body temperature shows a strong circadian rhythm. It
          has been suggested that this is due, at least in part, to an
          endogenous variation of the thermoregulatory set point (18).
          It also varies in response to a variety of behavioral and
          external stimuli, including sleep (19), physical activity
          (20), postural changes (21), ambient temperature (22) and
          meals (23). The menstrual cycle of women also affects their
          temperature rhythm, with the post-ovulatory temperature rise
          increasing the overall mean (24), thus confounding
          comparison of temperature rhythms recorded at different
          menstrual cycle phases.
          The CNS regulator of body temperature resides in the
          hypothalamus, and the temperature of the hypothalamus is a
          major feedback signal to the regulator (25,26). The midcycle
          rise of temperature is believed to be caused by elevation of
          progesterone and catecholamine levels (27).
          For comparison, menopausal hot flashes are thought to be a
          disorder of thermoregulation initiated centrally within the
          medial preoptic area of the hypothalamus (28).The medial
          preoptic area is innervated by ascending noradrenergic
          neurons, and increased norepinephrine turnover in the
          hypothalamus is believed responsible for the LHRH release
          and the thermoregulatory changes composing menopausal hot
          flashes (29,30). Peripheral circulating levels of plasma
          catecholamines do not change before or during hot flashes,
          but alterations in central catecholamines do occur (31-33).
          Levels of plasma 3-methoxy-4-hydroxyphenylglycol (MHPG), the
          major metabolite of brain norepinephrine, are significantly
          higher in women experiencing hot flashes than in those who
          are not, and these levels increase further during the hot
          flash itself (33). In addition, clonidine, an à2-adrenergic
          agonist has been shown to reduce hot flashes and also
          decrease central noradrenergic activity (34,35). Conversely,
          yohimbine, an à2-adrenergic antagonist that increases
          central noradrenergic activity, provokes hot flashes
          (35,36).
          Despite the fact that 158 years passed since Von Fricke`s
          study on vaginal temperature this basal body temperature is
          still probably the most widely used aid in the
          identification of the ovulation day. However, it seems that
          there was not much attention paid to the best hour of
          temperature recording after the onset of a nocturnal sleep.
          Based on recent studies it seems that 5 hours after
          nocturnal sleep onset can give a better basal body
          temperature recording that will more reflect the ovulatory
          effects upon the other factors.
 
          Progesterone
 
          Increased progesterone synthesis begins before ovulation
          (37,38). Yussman et al. (37) reported a preovulatory rise in
          progesterone 24 to 48 hours prior to ovulation in human
          subjects. Goebelsmann et al. (38) found that pregnanediol
          excretion rose on the day preceding the LH and FSH peaks.
          Moghissi et al. (24) confirmed that serum progesterone
          begins to rise two days before the LH surge.They found that
          serum progesterone rose from a level of 0.49 ñ 0.38
          nanograms/ml two days before LH surge to a level of 1.16 ñ
          0.92 nanograms/ml at the LH surge, and to 4.52 ñ 0.22
          nanograms/ml at two days after the LH surge.
          Progesterone is secreted by the adrenal cortex and accounts
          for the low plasma concentrations of 1 mg/day. Luteinization
          of the granulosa cells in the ovary results in additional
          synthesis of progesterone during the ovulatory and luteal
          phases of the menstrual cycle. Production of progesterone
          reaches 25 mg/day at its peak during the midluteal phase
          (39). The thermogenic effect of progesterone allows women to
          utilize basal body temperatures as an indicator of ovulation
          (40,41). Progesterone has been attributed with anesthetic
          properties. A natural metabolite of progesterone,
          allopregnanolone (3à-OH-DHP), is an effective modulator of
          Cl~ flux on the ç-aminobutyric acid (GABA)/ benzodiazepine
          receptor Cl~ channel complex (42), thus increasing the
          effectiveness of GABA, which leads to sedation and
          anxiolytic properties (43). Zuspan and Rao (44) postulated
          that progesterone causes an increased excretion and
          production of norepinephrine, which is responsible for the
          increased thermogenesis after ovulation. They concluded that
          the basic mechanism for thermogenesis is norepinephrine and
          not progesterone.
          Despite these facts it seems that progesterone plays a major
          role in the basal body temperature rise during ovulation and
          afterwards.
 
          Sleep
 
          Human body temperature characteristically rises during
          wakefulness and falls during sleep. This daily temperature
          fluctuation and the sleep-wake cycle are considered to be
          rhythmic functions normally synchronized to the 24 hr solar
          day. Subjects living in isolation from environmental time
          cues, however, have shown temperature and sleep-wake cycles
          that are almost invariably longer than 24 hr and not
          necessarily synchronized to each other (45,46).
          Kreider et al. (47) made simultaneous measurements of oxygen
          consumption, rectal temperature and mean weighted skin
          temperature on nine young men ( 32 man-nights ), who slept
          at night in a "comfortable" ambient environment
          (25.5-27.8øC). Significant decreases in oxygen consumption,
          rectal temperature and weighted skin temperature during the
          night were found. On the average, oxygen consumption
          decreased gradually during the night and reached a low value
          at 5.1 hours after retiring. Rectal temperature decreased
          1.2øC during the night. This low point occurred 5.6 hours
          after retiring and was followed by a slight but significant
          elevation.
          Nocturnal sleep is associated with a lowering of body
          temperature. Several studies have attributed this to
          negative or passive factors (48), such as absence of the
          specific dynamic action of food (47,49) and muscular
          relaxation (50), which would diminish metabolic activity
          (47). The association of sweating with sleep suggests that
          the nocturnal body temperature reduction may, in fact, be a
          regulated response. In 1941, sleep-sweat studies led Day
          (51) to suggest that a reduction of the thermostatic set
          point occurs with sleep.
          Shortly after Askerinsky and Kleitman (52) described rapid
          eye movement (REM) sleep as distinct from non-rapid eye
          movement sleep (NREM), Dement and Kleitman (53)
          characterized the REM-NREM cycle and reported that the
          duration of REM episodes progressively increased throughout
          the night in normal subjects. The timing of REM sleep is
          controlled, at least in part, by an endogenous circadian
          oscillator which is coupled to the one generating the body
          temperature cycle (54).
          Many studies have demonstrated that some people naturally
          have very short daily sleep requirements (55), while others
          have very long sleep needs (56). Patkai et al. (57) found
          that the duration of night sleep was longest during
          premenses and shortest at ovulation. The actual recorded
          temperature minimum in narcoleptics appeared 1 hr after
          sleep onset, independent of the occurrence of sleep-onset
          REM, compared with 4-5 hr after sleep onset in control
          subjects (58).
          Six healthy male subjects were exposed to seven different
          bedtime conditions, one per week (59). Bedtimes were
          scheduled in 4-hr intervals, resulting in times without
          sleep ranging from 16 hr to 40 hr. Rectal temperature was
          measured continuously and showed a circadian rhythm during
          both sleeping and waking. A fall in temperature immediately
          after sleep onset was noted at all bedtimes except at 0700
          and 1900 hr. In the majority of cases temperature rose
          toward the end of sleep, i.e., awakenings tended to occur
          during the rising phase of the circadian temperature rhythm.
          Slow wave sleep (SWS) is most heavily concentrated during
          the first third of nocturnal sleep, whereas the percent of
          rapid eye movement (REM) sleep gradually increases
          throughout the course of nocturnal sleep, reaching a plateau
          during the last third of the night (53,60).
          Barrett et al. (61) examined eight adult subjects (five
          males and three females), who were reportedly good sleepers.
          Rectal temperature was recorded at 1-minute intervals.
          Following sleep onset, body temperature dropped more rapidly
          and remained lower than when wakefulness continued over the
          same time, resulting in a mean sleep-evoked decrease of
          0.31 ñ 0.09øC. At the sixth hour after sleep onset the body
          temperature began to rise.
          In conclusion, during a normal nocturnal sleep the
          thermogenic circadian rhythm shows a tendency to rise at the
          sixth hour after sleep onset. So, approximately at the 5th
          hour after sleep onset the basal body temperature is at its
          lowest level. On the day of ovulation the progesterone and
          the subsequent hypothalamic norepinephrine cause the basal
          body temperature to rise. This rise in the basal body
          temperature at the ovulation day can be best noticed at the
          lowest circadian thermogenic point, which is at the 5th hour
          of the nocturnal sleep, so avoiding the masking of the BBT
          by the other regulatory factors, especially its circadian
          rise at awakening.
          However, until more sleep studies are performed in women in
          a controlled manner, it will be difficult if not impossible
          to make any conclusive remarks about the appropriate time
          for BBT measurement.
 
 
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