BASAL BODY TEMPERATURE: UNRELIABLE METHOD OF OVULATION DETECTION

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1 FERTILITY AND STERILITY Copyright c 1981 The American Fertility Society Vol. 36, No. 6, December 1981 Printed in U.SA. BASAL BODY TEMPERATURE: UNRELIABLE METHOD OF OVULATION DETECTION JOAN E. BAUMAN, PH.D. Masters & Johnson.lnstitute, St. Louis, Missouri Basal body temperature (BBT) charts from menstrual cycles of 98 women were evaluated by six experienced physicians. The time of ovulation as estimated from the charts by a consensus of at least five of the evaluators coincided with the luteinizing hormone (LH) peak ± 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. An additional22.1% of these cycles were thought to have monophasic patterns by a consensus of the physicians. Extreme caution in interpretation is urged when BBT is used for clinical or research evaluations of ovulation or menstrual cycle dynamics. Fertil Steril 36:729, 1981 Basal body temperature (BBT) charts have long been used as a simple, inexpensive method to determine whether ovulation has occurred and to estimate its timing in the menstrual cycle. The BBT is considered by many to be a reliable ovulatory index, since most women have a sustained rise in the luteal phase of the cycle, presumably due to the thermogenic properties of progesterone.1 Several recent reports have indicated, however, that some women do not show a thermal shift during endocrinologically normal cycles 2 4 and that when a shift is present, the BBT chart may be difficult to interpret or inaccurate in indicating the time of ovulation. 5_ 9 In spite of such studies, BBT records are commonly used by clinicians in the diagnosis and treatment of infertility,10 11 by scientists researching various aspects of the menstrual cycle/ 2 13 and by tens of thousands of couples as an important element of family planning practice This study was planned to assess how closely BBT charts matched detailed endocrine data in distinguishing ovulatory from anovulatory cycles, detecting short or inadequate luteal phase cycles, and determining the time of ovulation. In Received June 8, 1981; revised and accepted August 10, Reprint requests: Joan E. Bauman, Ph.D., Masters & Johnson Institute, 4910 Forest Park Boulevard, St. Louis, Missouri addition, the use of a panel of six expert evaluators provided a measure of possible variability in individual interpretation of identical BBT charts. METHODS Six experienced physicians with backgrounds in gynecology and/or reproductive endocrinology were asked to separately evaluate 104 BBT charts. The charts, identified only by three-digit code numbers, were taken from four separate studies conducted in our laboratory for other purposes over a period of several years. Each study involved detailed daily serum hormone analyses of the menstrual cycle in addition to the keeping of BBT charts; follicle-stimulating hormone (FSH), luteinizing hormone (LH), 17j3-estradiol, and progesterone were among the hormones analyzed by standard radioimmunoassay methods Reagents for assay of FSH and LH were generously provided by the National Institute of Arthritis, Metabolism and Digestive Diseases. All subjects were between the ages of 18 and 30, were in good general health, and had no history of infertility or endocrine disease. The subjects were provided with and carefully instructed in the use of standard BBT charts and thermometers graduated to the nearest 0.1 o F. The study groups were largely recruited from populations of nursing and medical students, university students, and hospital employees; the subjects were judged reliable on the basis of personal

2 730 BAUMAN December 1981 TABLE 1. Luteal Phase and Endocrine Parameters of Cycles during Which Basal Body Temperature Charts Were Obtained Group I ± 1.1" Group II ± 1.6 Group III 3 "Values are means ± standard deviation. brange. n Luteal Phase days (11-16)b (5--10) Luteinizing hormone peak mlu!ml Progesterone peak ngldl ± 31.5 ( ) 1270 ± 483 ( ) 92.9 ± 29.9 ( ) 632 ± 339 ( ) 5.9 ± 1.1 ( ) 37 ± 23 (11-52) interview, cooperation in the keeping of records other than BBT, and adherence to laboratory scheduling. The cycles were chosen for inclusion in this study on the basis of completeness and lack of ambiguity of the endocrine data and without reference to the BBT charts, which were stored in a separate file during the selection process. The charts given to the physicians included the following information: group I, 77 apparently ovulatory cycles with normal luteal phase length(~ 11 days); group II, 18 apparently ovulatory cycles with short luteal phases(~ 10 days); and group III, 3 apparently anovulatory cycles. The endocrine data from these cycles are summarized in Table 1. Duplicates of six of the 77 group I BBT charts, with separate code numbers, were also included in the set of 104 charts. Absolute certainty of the occurrence of ovulation-defined as the release of an ovum from a mature ovarian follicle-requires either subsequent verification of pregnancy or invasive procedures such as recovery of an ovum from the fallopian tubes or direct observation of follicular rupture at the time oflaparotomy, but most authorities accept as presumptive evidence of ovulation the detection of a gonadotropin surge (LH greater than 40 miu/ml) followed by a progesterone rise from normal follicular levels of less than 100 ng/ dl to greater than 500 ng/dl. 2 These criteria were used in this study to classify the group I cycles as ovulatory. Since cycles with short luteal phases are also often deficient in steroid production, cycles were classified as ovulatory, group II, if the LH peak was followed by a progesterone rise to greater than 100 ng/dl, and if the next menses followed the LH peak by no more than 10 days. Cycles were classified as group III, presumably anovulatory, if no LH level greater than 40 miu/ ml and no progesterone greater than 100 ng/dl was detected throughout the cycle. The physicians were asked to evaluate each chart for the presence or absence of a biphasic pattern and to estimate the day of ovulation for each chart that they thought showed a biphasic BBT curve. Accuracy of estimation was judged by comparison with the day of the LH peak, since ovulation is known to occur within approximately 16 hours following the LH surge Although the timing of ovulation in regard to the LH peak is well established, no such agreement exists in deducing the time of ovulation from the BBT pattern: some investigators use the BBT nadir; others, the thermal shift or other indicators. This matter will be addressed more fully in the discussion. Since one method has never been established as clearly more accurate than the others, and since this study was directed at assessing the success of the BBT method of ovulation detection as it is actually practiced, the physicians were instructed to interpret the BBT patterns as they routinely did, rather than follow a standardized method. RESULTS The physicians' evaluations of the 77 group I BBT charts are summarized in Table 2. Chart analysis by each physician was consistent: the six pairs of duplicate group I cycles were assigned the same ovulation days in 91.7% of the evaluations. The number of charts for which each physician correctly estimated the time of ovulation ± 1 day of the LH peak ranged from 24 to 34. There was no significant difference between physicians when the number of BBT patterns assessed correctly was compared with the total number not assessed correctly (those judged not biphasic or with an error of 2 or more days) by x 2 analysis. Although each physician correctly estimated the time of ovulation from an average of 38.1% of the BBT charts, only nine of the individual charts were correctly assessed by all six of the physicians, with five of six agreeing on the correct time of ovulation in an additional eight of the 77 cycles. This 22.1% of cycles on which the expert evaluators were able to reach a consensus may be considered the subset of the sample in which a clear, biphasic BBT pattern accurately reflects ovulation. 'I

3 Vol. 36, No. 6 BASAL BODY TEMPERATURE 731 TABLE 2. Evaluation of 77 Group I (Ovulatory) Basal Body Temperature Charts Physician A B c D E F Mean % Correcta Not biphasicb Incorrectc aoay of ovulation estimated within ± 1 day of luteinizing hormone (LH) peak. bpattern monophasic or too complex to allow estimation of ovulation day. coay of ovulation estimated as ± 2 or more days from LH peak. An additional 22.1% of the group I cycles were described as not biphasic by at least five of the six evaluators. Luteal progesterone levels were similar in the 17 cycles found to be monophasic by a consensus of the evaluators and in the 17 cycles in which the BBT pattern allowed accurate estimation of the time of ovulation: 1175 ± 478 ng/dl (mean ± standard deviation) versus 1331 ± 520 ng/dl, respectively (not significant). Thirty-seven, or 48%, ofthe group I charts drew a mixed response from the evaluators, whose judgments differed regarding the presence of hiphasic patterns or the correct day of ovulation, or both. In addition, 7.8% of the ovulatory group I cycles received a consensus on a time of ovulation that was more than two days before or after the LH peak. These ambiguous or misleading patterns pose a clear danger to the would-be interpreter of BBT charts, whether researcher, clinician, or patient. Correct evaluation of the 18 group II short luteal phase cycles proved even more elusive (Table 3). The day of ovulation was assessed correctly in only one cycle by two of the six physicians, while in the majority of the evaluations the cycles were judged as not showing a biphasic pattern. This result was not unexpected, since the rise in BBT is dependent on progesterone, 1 and the maximal progesterone levels reached were significantly lower in the short luteal phase cycles than in the group I cycles: 632 ± 339 versus 1207 ± 483 (mean ± standard deviation), t = 5.29, df = 93, P < When the short luteal phase cycles showed a biphasic pattern but the day of ovulation was incorrectly estimated, the mean magnitude of the error was greater than in the group I cycles: 5.0 ± 2.2 days from the LH peak versus 2.9 ± 1.2 days, t = 6.41, df = 142, P < In both groups more errors were made that placed the estimated ovulation date before, rather than after, the LH peak, but this tendency was stronger in the short luteal phase group than in the group with luteal phases of 11 or more days: 88.9% of errors (group II) versus 64.8% (group I) estimated ovulation early, rather than late, in the cycle Cx 2 = 9.4, df = 1, P < 0.01). The probable explanation for this is the use of the day of onset of the next menses as an aid to BBT interpretation with the expectation that ovulation occurs approximately two weeks before the end of the cycle. The bias introduced by this method is fairly one-sided: an earlier study in our laboratory demonstrated that when ovulation did not occur on reverse cycle days 13 to 15 (as it did in 48.2% of cycles), it was more likely to occur on reverse cycles days 10 to 12 (27% of cycles) than on reverse cycle days 16 to 18 (5% of cycles). In 19.8% of cycles, ovulation occurred on reverse cycle days,;;; 9.21 The group III, or probable anovulatory, cycles were uniformly found to have monophasic patterns by all evaluators. DISCUSSION The finding that 22.1% of the group I hormonally normal cycles were described as monophasic by a consensus of the evaluators did not come as a TABLE 3. Evaluation of 18 Group II (Short Luteal Phase) Basal Body Temperature Charts Physician A B c D Correct a Not biphasicb Incorrectc aday of ovulation estimated within ± 1 day of luteinizing hormone (LH) peak. bpattern monophasic or too complex to allow estimation of ovulation day. coay of ovulation estimated as ± 2 or more days from LH peak. E F Mean %

4 732 BAUMAN surprise: the percentage was similar to that described by other investigators. Monophasic patterns were found in 20% of ovulatory cycles studied by Moghissi 2 and by Lenton and colleagues, 7 while Johansson and co-workers 3 reported the same finding in 12% of their sample. Whitelaw observed that monophasic BBT curves can sometimes occur concurrently with normal, secretory endometria as assessed by biopsy. 4 The reason that some women do not show a thermogenic response to normal postovulatory progesterone levels is not known. 1 For those normal cycles that did exhibit a hiphasic BBT pattern in this study, the pattern proved to be a poor predictor of the time of the LH peak (known to be closely associated in time with actual ovulation ): the evaluators agreed on a time of ovulation consistent with endocrine evidence (LH peak> 40 miu/ml, followed by a progesterone peak> 500 ng/dl) in only a minority of the BBT patterns evaluated. Cycles with biphasic BBT patterns can be misleading, since the temperature rise may be abrupt, gradual, or stepwise. 5 The abrupt rise is probably the easiest to identify, but such a rise occurred in only 26% ofbiphasic BBT charts studied by Durkan. 6 Lenton and her colleagues found that only 80% of the cycles they studied could be correctly predicted as ovulatory or anovulatory on the basis of the BBT pattern; of this number, only 34% predicted a time of ovulation that correlated with the LH peak. 7 Buxton and Engle 8 and Morris et al. 9 found BBT unsatisfactory and inaccurate for the purpose of determining the day of ovulation. Different rates of progesterone production were found by Buxton and Engle to lead to as much as a 4-day variation between ovulation time as predicted by BBT rise and as determined by direct visual examination of the corpus luteum at operation. 8 Further confusion has resulted from disagreement among investigators concerning the correct interpretation ofbbt charts 22 : some use the thermal nadir, others use the thermal shift, and at least one investigator 23 preferred the intercept between the mean temperature for the cycle and the BBT curve. The nadir, or low point before the rise in temperature begins, is preferred by many workers, but Marshall found such a nadir in only 10% of the series he studied. 5 Some investigators use the time of the onset of the next menses to aid in the estimation of ovulation day from BBT charts, 12 but the assumption that ovulation occurs 13 to 15 days before menstruation was found December 1981 to be correct in less than half of 146 cycles studied in our laboratory. 21 Hilgers and Bailey 24 attempted to correlate four commonly used points on the BBT curve (BBT dip, BBT nadir, first day of BBT rise, and BBT coverline) with the time of ovulation as estimated from hormonal parameters, and concluded that none of the points tested was sufficiently precise to indicate the day of ovulation for either research or clinical purposes. The classic dip, often pictured in publications and referred to as "day of ovulation," occurred in only 10 of 66 hormonally normal cycles studied by Hilgers and Bailey, and coincided with the endocrinologically estimated time of ovulation in only a single cycle. The use of these different methods of interpretation may explain the fact that individual evaluators in the present study averaged 38.1% of hi phasic cycles correctly identified as to time of ovulation, while consensus was reached on only 22.1 %. In some individual cycles, estimates of time of ovulation given by the six evaluators ranged from 5 days before to 4 days after the LH peak. The failure of BBT to identify short luteal phase cycles is striking, with a total of 98.1% of the evaluations indicating monophasic patterns or erroneous ovulation days. Space was provided for comments on each BBT chart given to the physicians: the comment that the cycle might have had a short or inadequate luteal phase was made on only 2. 7% of group II charts and also appeared on 3.0% of group I charts. Some of the group II cycles were hormonally deficient and almost certainly infertile (i.e., luteal phase length 5 days with maximum progesterone 140 ng/dl) while others probably were fertile (luteal phase 10 days with maximum progesterone 1169 ng/dl). This uncertainty, coupled with the bias toward preovulatory rather than postovulatory estimates of ovulation day in both the normal and short luteal phase groups, makes the use of BBT patterns for contraception extremely hazardous, since the method assumes that intercourse is safe after the thermal shift has occurred in any cycle. 14 Mounting evidence presented in this and other studies indicates that BBT patterns are inaccurate in the majority of women; yet there is considerable resistance to abandoning this method. Many recent research and clinical records assume the usefulness of the thermal shift as an indicator of time of ovulation and luteal phase length when a clear-cut shift is present. 10, u, 13, 14

5 Vol. 36, No. 6 BASAL BODY TEMPERATURE 733 At best, BBT should be considered an adjunct to other methods of ovulation monitoring in those women shown to have a clear, biphasic pattern. BBT should be interpreted with caution in all cases and never solely relied on in situations where the potential consequences of error are serious. Finally, much research in which BBT was used to correlate ovulation with various behavioral or physiologic parameters needs to be critically reevaluated. REFERENCES 1. Moghissi KS: Prediction and detection of ovulation. Fertil Steril 34:89, Moghissi KS: Accuracy of basal body temperature for ovulation detection. Fertil Steril 27:1415, Johansson EDB, Larsson-Cohn U, Gemzell C: Monophasic basal body temperature in ovulatory menstrual cycles. Am J Obstet Gynecol 113:933, Whitelaw MJ: Ovulation after unilateral oophorectomy as determined by endometrial biopsy and basal body temperature. Surg Gynecol Obstet 92:747, Marshall J: Thermal changes in the normal menstrual cycle. Br Med J 1:102, Durkan JP: Clinical experience with basal temperature rhythm. Fertil Steril 21:322, Lenton EA, Weston GA, Cooke ID: Problems in using basal body temperature recordings in an infertility clinic. Br Med J 1:803, Buxton CL, Engle ET: Time of ovulation: a correlation between basal temperature, the appearance of the endometrium, and the appearance of the ovary. Am J Obstet Gynecol 60:539, Morris NM, Underwood LE. Easterling W: Temporal relationship between basal body temperature nadir and luteinizing hormone surge in normal women. Fertil Steril 27:780, Pfeffer WH, Wallach EE, Beck WW, Barrett ATM: Artificial insemination with husband's semen: prognostic factors. Fertil Steril 34:356, Kredentser 'JV, Hoskins CF, Scott JZ: Hyperprolactinemia: A significant factor in female infertility. Am JObstet Gynecol 139:264, Preti G, Huggins GR, Silverberg GD: Alterations in the organic compounds of vaginal secretions caused by sexual arousal. Fertil Steril 32:47, Gautray JP, DeBrux J, Tajchner G, Robel P, Mouren M: Clinical investigation of the IJ)enstrual cycle: III. Clinical, endometrial, and endocrine aspects ofluteal defect. Fertil Steril 35:296, Abrams RM, Royston JP: Some properties of rectum and vagina as sites for basal body temperature measurement. Fertil Steril 35:313, Marshall J: The Infertile Period: Principles and Practice. Baltimore, Helicon Press, 1967, p Saxena BB, Dermura H, Gandy HM, Peterson RE: Radioimmunoassay of human follicle stimulating and luteinizing hormones in plasma. J Clin Endocrinol Metab 28:519, Wu CH, Lundy LE: Radioimmunoassay of plasma estrogens. Steroids 18:91, Niswender GD: Influence of the site of conjugation on the specificity of antibodies to progesterone. Steroids 22:413, Yussman MA, Taymor ML: Serum levels of follicle stimulating hormone and luteinizing hormone and of plasma progesterone related to ovulation by corpus luteum biopsy. J Clin Endocrinol Metab 30:396, Moghissi KS, Syner FN, Evans TN: A composite picture of the menstrual cycle. Am J Obstet Gynecol 114:405, Kolodny RC, Bauman JE: Letter: Female sexual activity at ovulation. N Engl J Med 300:626, Abraham GE: The normal menstrual cycle. In Endocrine Causes of Menstrual Disorders, Edited by JR Givens. Chicago, Year Book Medical Publishers, 1978, p Vollman RF: The Menstrual Cycle. Philadelphia, W. B. Saunders Co, Hilgers TW, Bailey AJ: Natural family planning: II. Basal body temperature and estimated time of ovulation. Obstet Gynecol 55:333, Rakoft' AE: Ovulatory failure: clinical aspects. In Modern Trends in Infertility and Conception Control, Edited by EE Wallach, RD Kempers. Baltimore, Williams & Wilkins Co, 1979, p 159