A comparison of methods to interpret the basal body temperature graph*

FERTllJTY AND STERILITY Copyright c 1983 The American Fertility Society Vol. 39, No.5, May 1983 Printed in U.SA. A comparison of methods to interpret the basal body temperature graph* John J. McCarthy, Jr., M.D.t Howard E. Rockette, Ph.D.* University of Pittsburgh School of Medicine and University of Pittsburgh Graduate School of Public Health, Pittsburgh, Pennsylvania Specific criteria are given for several methods of determining the basal body temperature shift. The specific criteria selected have been coded for a uniform interpretation by computer, and interpretations have been compared for 8496 charts. Our results indicate that the method that defines the temperature shift as 0.3~ For more above the running low average for at least 3 consecutive days provides the best concurrent chart interpretation method. A method that creates a smoothed curve that transects the average of all temperatures on a completed graph provides a good retrospective method for identifying the temperature shift. Both the temperature averaging technique and curve smoothing technique identified a temperature shift in more than 95% of the charts with complete temperature readings. Fertil Steril 39:640, 1983 The basal body temperature (BBT) graph has been used extensively in clinical practice and as a comparative parameter with other methods for detecting ovulation. Recently Moghissi, l Hilgers and Bailey,2 and Bauman 3 reported results indicating the unreliability of the BBT graph. In all three reports, hormonal analysis was used to identify the approximate time of ovulation in a small number of cycles (30, 74, and 98, respectively), and this was compared with an interpretation of the BBT graph. Only Hilgers and Bailey2 attempted to define the methods of interpreting the Received August 23, 1982; revised and accepted December 16,1982. *Supported in part by funds from the National Institute of Child Health and Human Development and the Office for Family Planning. treprint requests: John J. McCarthy, Jr., M.D., Department of Obstetrics and Gynecology, University of Pittsburgh School of Medicine, Magee-Women's Hospital, Forbes and Halket Streets, Pittsburgh, Pennsylvania 15213. :j:department of Biostatistics, University of Pittsburgh Graduate School of Public Health. BBT graph and to compare the presumptive day of ovulation (PDO) with the hormonal estimation of the day of ovulation. Bauman 3 utilized the expertise of "six experienced physicians with backgrounds in gynecology and/or reproductive endocrinology" to interpret the BBT graphs for a PDO. The diversity of interpretations from these experienced physicians suggests a lack of any uniform method of interpreting these graphs. Although Moghissi 1 found 20% monophasic charts in apparently ovulatory cycles by hormonal criteria, a single graph from each of 30 subjects is not sufficient to establish the incidence of monophasic BBT graphs. In addition, there is no stated criterion or method for interpreting the graphs. Hilgers and Bailey2 identify four single-point methods defined in their report (dip, nadir, first day of the BBT rise, and coverline). Only the coverline (COV) is a widely used method of interpreting the BBT graph. While the dip and the nadir are referred to commonly, they have been shown to be weak criteria.2,4 640 McCarthy and Rockette Interpretation of the BBT graph Fertility and Sterility

99.0.9.7.6 ~ :~ ~ 98.0 C.9 4; 0..7 E.6 2 ::.".1 97.0 t COVERLINE Figure 1 COV. Draw a "coverline" 0.10 F above the highest of the first n temperatures. A shift is identified when the (n + l)th temperature is above the coverline and the next two consecutive temperatures are on or above the coverline. These articles demonstrate the fact that there is no well-accepted method for interpreting the BBT graph. It is with this perception of the literature that we have undertaken a study to compare various suggested techniques for interpreting the BBT graph. Although this study does not have the hormonal parameters for comparison, it has the advantage of a large volume of charts. These numbers are sufficient to enable us to compare several precisely defined methods of interpreting the BBT graph. The elimination of poor or vague methods and the delineation of precise criteria categorizing the better methods of chart interpretation would seem to be a necessary prerequisite for comparing the BBT graph with other methods of determining ovulation. MATERIAItS AND METHODS The data base upon which comparisons were made consisted of 8496 temperature charts submitted by 1376 clients to the CM-BBT Program of Southwestern Pennsylvania during the period 1973 to 1979. The CM-BBT Program provides a form of natural family planning where the principle elements are cervical mucus (CM) and BBT observations. The average age of clients was 26 years, with a range of 16 to 46 years. The present analysis includes only charts with cycle lengths < 40 days. This restriction excluded less than 2% of the charts and would have little effect on the analysis. It is emphasized that in the formation of the data base of 8496 charts there was no preselection of charts based on quality or completeness. A subset of charts (5210) with more complete information was selected from the original 8496 charts. Charts with an even distribution of temperatures throughout the cycle and few missing readings, or readings identified as taken under "disturbed conditions" or when the client was ill, were placed into this subset. This subset was formed to study those methods requiring more complete chart information. The data from each chart were keypunched and verified for computer interpretation. A computer program written in Fortran was developed for chart analysis. The program is capable of interpreting each BBT graph, using a variety of interpretation techniques. The techniques of chart interpretation that have been computerized include temperature averaging (AVE), COV, and a smoothed curve (SMC) technique, which is a modification of a method proposed by Vollman. 5 The computerization of the chart interpretation assures that a uniform algorithm is being applied to all charts. INTERPRETATION 0)<' THE BBT GRAPH The interpretation of the BBT graph usually entails an initial determination of whether the curve is biphasic or monophasic. The biphasic curve is one that demonstrates a shift in the BBT from a lower phase to a higher phase. Once this shift is identified, a presumptive day of ovulation is related to the shift from the low to the high phase. If no temperature shift can be determined, the graph is classified as monophasic. This could be the result of an anovulatory cycle or a failure of a technique to identify a temperature shift. Monophasic curves are suggestive of a failure to ovulate but are by no means diagnostic. 99.0.".7.6 ~ '".".1 ~ 98.0 Q) Q..9 E.7 ~.".1 97.0 ~om 97 97.6 X t MEAN Figure 2 SMC. A smoothed curve is obtained by replacing the temperature at the ith point with the average of the three temperatures (triplets) at points i-i, i, and i + 1. A shift is identified where the smoothed curve transects the average of all temperatures (mean). Vol. 39, No.5, May 1983 McCarthy and Rockette Interpretation of the BBT graph 641

.J.2.1.0. 1. 7.s ~.5 :::J.4 ~ :: 8..1 E '".0 ~ ::. 7 t.s JF-~~~ffff~~[[ff~LO~W~A~V~E~R~AG~E~~J~1 not Figure 3 AYE. The average of the first n temperatures is computed. A shift is identified as soon as consecutive temperatures are a specified amount above this temperature average for a specified number of days. The techniques used to identify the thermal shift may be divided into two general categories. The first relates the thermal shift to a single point of change. The most widely used single-point criterion is COY. This procedure uses the highest of the normal temperatures in the low phase as the reference point. The thermal shift is determined once three consecutive temperatures are a specified number of degrees above this point. The COY technique used in this article can be summarized as follows (Fig. 1): (1) A COy is drawn 0.10 F above the highest of the first n temperatures; (2) a shift is identified when the (n + l)th temperature is above the COY and the next two consecutive temperatures are on or above the COY; and (3) once the temperature shift is identified, the day before the shift (the nth temperature) is the PDO. If the procedure is applied successively for temperatures on the first n days through the entire cycle and no rise is identified, the chart is classified as monophasic. The second general method of determining the thermal shift, AVE, has several variations. Vollman 5 suggests that the thermal shift can be identified where the BBT curve transects the mean of all temperatures on the graph. This procedure can only be used retrospectively and requires relatively complete charts if it is to be properly utilized. In this article we have modified this technique by "smoothing" the temperature curve (SMC) (Fig. 2). This "smoothed" curve is obtained by replacing the temperature at the ith point, with the average ofthe three temperatures at the points i-i, i, and i + 1. The thermal shift is located where the "smoothed" curve transects the average of all temperatures, and all points on the curve remain above this average. To declare a chart biphasic, we have required at least seven points in the postovulatory phase. The SMC technique utilizes the average of all temperatures in the cycle. An alternate technique is to use the average of the first n temperatures to establish the low temperature phase from which the shift to the higher phase can be measured. This provides a method that can be used prospectively. The World Health Organization definition relates the shift to 0.20 C (0.40 F) above the average of the previous six temperatures. In this article the prospective method of chart interpretation using an AVE is defined as follows (Fig. 3): (1) The average of the first n temperatures is computed; (2) the thermal shift is identified as soon as consecutive temperatures are a specified amount above this temperature average for a specified number of days; and (3) if no shift is identified, the chart is identified as monophasic. For a biphasic chart, the PDO is the day before the temperature shift. In the present study we have evaluated a change of 0.20 F (A VE/2), 0.30 F (A VE/3), and 0.40 F (AVE/4) sustained for time intervals of both 3 and 4 consecutive days. These methods of interpreting the BBT graph exclude any temperatures taken on the first 4 days of menstruation. In addition, temperatures taken where the chart indicated illness or unusual basal conditions were excluded from the analysis. RESULTS A model of the "normal" menstrual cycle in a population of women during the reproductive years might be expected to have certain charac- Table 1. Percentage of Charts by Temperature Interpretation for Selected Methods (8496 Chartsr Chart interpretation AVE/2 AVE/3 AVE/4 cov Biphasic 93.5 88.7 78.1 64.9 Postovulatory phase 17.7 24.0 29.5 18.4 Postovulatory phase 66 60.5 46.4 38 Postovulatory phase 9.1 4.2 2.2 3 Monophasic 6.5 11.3 21.9 35.1 Ten or more tem- 4.0 8.4 18.4 31.9 peratures Less than ten tem- 2.5 2.9 3.5 3.2 per~tures athermal shift based on 3 days' rise. 642 McCarthy and Rockette Interpretation of the BBT graph Fertility and Sterility

Table 2. Percentage of Charts by Temperature Interpretation for Methods Employing Only the Last Six Temperatures to Determine the Shift (8496 Chartsr AVE/3 COY Chart interpretation Oast six) (last six) Biphasic 86.9 76.2 Postovulatory phase 20.3 20.0 Postovulatory phase 62.1 51.7 Postovulatory phase 4.4 4.5 Monophasic 13.1 23 Ten or more tem- 10.2 20.6 peratures Less than ten tem- 2.9 3.2 peratures athermal shift based on 3 days' rise. teristics in relation to ovulation. The number of days from ovulation to the next menstrual flow should usually be in a range of 11 to 16 days, regardless of the overall cycle length. Although there may be a reasonable number of cycles where the evidence suggests that the luteal phase is shorter than 11 days, it would not be expected to find many nonpregnant women with a luteal phase over 16 days. Likewise, during the reproductive years, women with cycles < 40 days in length would be expected to have few true anovulatory cycles. This model should be kept in mind as the techniques to interpret the BBT grl;lph are reviewed. Table 1 shows the percentage of charts classified into different temperature categories for the selected methods of interpreting the BBT graph when these methods are applied to the total group of 8496 charts. The most biphasic graphs occur when the AVE technique is used, with 0.20 F difference as the criterion for identifying the temperature shift (93.5%). A definition of a 0.4 F thermal shift produces only 78.1% biphasic curves. The larger percentage of monophasic curves at 0.4 0 F (21.9%) would seem to eliminate any possibility for close agreement between the monophasic chart and an anovulatory cycle, because at the mean age represented by this group of charts the frequency of anovulatory cycles should be less than 5%.6. 7 Although the criterion of a 0.20 F thermal shift does produce more biphasic charts than a 0.3 0 F thermal shift, it also produces a significantly greater proportion of charts with a long postovulatory phase (9.1% versus 4.2%) (Table 1). The long postovulatory phase without evidence of pregnancy should Qe infrequent. The criterion of 0.3 0 F appears to provide the distribution of charts that most closely resembles the expected distribution in a population of this composition. Of the 11.3% monophasic charts that resulted when this method was used, more than 25% had less than ten temperatures for analysis. Also included in Table 1 is the percentage of charts in each category as identified by the COY criteria. The percentage of biphasic charts (64.9%) is lower than the percentage occurring for any of the A VE techniques. For the COY procedure, the existence of one aberrant high temperature (other than those temperatures for which illness or disturbed basal conditions were indicated) may result in a failure to detect a temperature shift. The effect of an unusually high temperature when using COY may be modified by basing the COY on only the last six temperatures. Table 2 compares COY with A VE/3 for 3 days when only the last six temperatures preceding the thermal shift are considered. The ratio of biphasic charts improves significantly for COY (last six) over COY (76.2% versus 64.9%) but still does not approach the 88.7% of the A VE/3 technique. On the other hand, there is no significant difference between A VE/3 using all temperatures and A VE/3 when only the last six temperatures are used to determine the average in the low phase. It was not possible to investigate the effect of requiring 4 days of sustained temperature rise Table 3. Comparison of Methods Requiring 4 Days of Rise with Those Requiring 3 Days of Rise (Percentage) (5210 Charts) Temperature interpretation AVE/2 AVE/3 AVE/4 For 3 days For 4 days For 3 days For 4 days For 3 days For 4 days Biphasic 98.1 95.9 95.1 91.4 86.7 78.9 Postovulatory phase 17.6 17.9 28.6 25.4 34.0 30.2 Postovulatory phase 70 71.1 62.3 62.7 50.4 47.1 PostovuJatory phase 9.7 6.9 4.2 3.3 2.3 1.6 Monophasic 2.1 4.1 4.9 8.7 13.3 21.1 Vol. 39, No.5, May 1983 McCarthy and Rockette Interpretation of the BBT graph 643

Table 4. Comparison of Presumed Day of Ovulation as Determined by Coverline and as Determined by CM (5210 Chartsya All No. of charts 4048 PDO by CM and BBT 72.4% ± 2 days PD~ by CM and BBT 54.1% ± 1 day Median difference in PD~ 0.026 acharts are biphasic and have the CM peak recorded. AVE/3 COV Last six All Last six 3917 2914 3433 74.2% 69.3% 72.7% 56.2% 51.5% 55.3% 0.285-0.108 0.129 with the use of the total group of charts. Since the CM-BBT Program of Southwestern Pennsylvania requires only 3 days of rise, many of the clients that have experience with the method do not continue to take temperatures after the first 3 days of rise have been identified. For this reason, comparisons of methods requiring 4 days of temperature rise were made only on the subset of 5210 charts with more complete information. Table 3 compares the effect of requiring 4 days of temperature rise instead of 3 days of rise for methods requiring a rise of 0.20 F, 0.30 F, and 0.40 F, respectively. This subgroup of charts with more complete temperatures results in a greater percentage of biphasic charts than was observed for the total group of charts with the use of the same methods of interpretation. The requirement of an additional day of temperature rise increased the percentage of monophasic charts, but less than requiring an additional tenth of a degree in the definition of the rise. Although there are similarities in the distribution of charts with A VE/2 for 4 days and A VE/3 for 3 days, the earlier detection of a PDO is evident for the criteria of A VE/2 for 4 days. The women submitting this group of charts also had identified their patterns of CM. Hilgers and Bailey2 have indicated a close correlation of endocrine parameters with vulvar observation of mucus discharge. In this article we make no attempt to evaluate the reliability of CM in predicting ovulation, but rather use it as an independent estimate to which the PDO by the selected BBT methods can be compared. Table 4 shows the relationship of the PDO by CM and by various methods of interpreting the temperature graph. Since the distribution of the difference in PDO by CM and BBT was skewed, the sample median rather than the sample mean was used as a summary statistic. On the basis of a comparison with the CM pattern, there is no reason to prefer the COY methods rather than an AVE technique requiring a 0.30 F rise for 3 days. Furthermore, more than 600 charts with a CM peak were monophasic when the COY (last six) technique was used and were biphasic with the A VE/3 technique. Table 5 compares the A VE/3 technique with SMC. The SMC technique requires a completed chart with most temperatures recorded and acceptable for interpretation, because it employs the mean of all temperatures in the cycle. It is apparent that the requirement for a complete chart with an even distribution of acceptable temperatures results in a high proportion of biphasic charts (95.1% and 96.9%). Under these conditions, the SMC technique produces a small proportion of charts distributed either to the monophasic or long postovulatory category (3.1% and 1.3%, respectively). The technique using A VE/3 as the thermal shift results in only 4.9% monophasic charts and 4.2% judged to have a long postovulatory phase. Thus, the AVE technique based on a 0.30 F rise for 3 days, which can be used concurrently to interpret the graph, compares favorably with the strictly retrospective SMC technique. The identification of a rise of 0.30 F for 3 days as the desirable criterion for identifying the temperature shift may result in the incorrect assumption that the actual shift is close to this magnitude. Table 6 shows. the difference between the low average and the completed high average Table 5. Comparison of AVEI3 with SMC (5210 Charts)a Temperature criteria classification AVE/3 SMC Biphasic 95.1 96.9 Postovulatory phase 28.6 19.0 Postovulatory phase 62.3 76.6 Postovulatory phase 4.2 1.3 Monophasic 4.9 3.1 ~hermal shift based on 3 days' rise. 644 McCarthy and Rockette Interpretation of the BBT graph Fertility and Sterility

Table 6. Difference Between Complete High and Low Average Determined by 0.3 0 F for 3 Days (AVEI3) Difference 0.3 0 F 0.4 0 F 0.5 0 F 0.6 0 F 0.7 0 F 0 0 F 0.9 0 F 1.0 0 F Total group of biphasic charts (7537) 2.5 7.3 17.0 25.3 23.3 14.9 6.5 3.1 Biphasic charts from subgroup with complete temperatures (4954) 2.7 6 16.2 24.2 24.2 16.3 6:8 2.9 after the shift is identified using 0.3 F for 3 consecutive days as the criterion. The biphasic na 0 ture of the graph is clearly seen with a difference of 0.5 0 F or more in over 90% of the biphasic charts. Only 2.5% that were determined to be biphasic had a difference between the high and low average of 0.3 0 F or less. When the distribution of the difference of the high and low average is restricted to the subset of charts with more complete temperature graphs, we obtain a remarkably symmetric distribution about the average value of 0.65 0 F. DISCUSSION The BBT graph is often used as an aid in identification of the ovulatory menstrual cycle. It is also advocated as a method of identifying the postovulatory nonfertile phase of the menstrual cycle. Couples trying to conceive have laboriously kept the BBT graph as an aid to conception. In spite of this extensive use and experience, there still exists a sense of frustration over interpretation of the graph. One of the major reasons for this frustration is the lack of any generally accepted criteria for interpreting the BBT graph. This lack of a precisely defined, well-accepted method has also limited the ability to generalize results of the investigations comparing the BBT graph with hormonal criteria as a method ofidentifying ovulation. This analysis of 8496 graphs has identified several issues. The first issue relates to the need for concurrent criteria versus interpretation of the completed graph. For concurrent interpretation, a decision must be made from the graph as to when the postovulatory infertile phase begins or when a more direct test such as endometrial biopsy or serum progesterone level for documentation of ovulation should be performed. Concurrent BBT graph interpretation requires a reasonable degree of confidence that a shift in the temperature has occurred and will be sustained. It has been shown that a single-point criterion such as COY fails to identify the thermal shift on one third of the graphs when all temperatures were used and one fourth when only the most recent six temperatures were considered. The dip before the rise and the nadir have been shown by others to be unreliable. 2, 4 A running average presents a more stable point from which to measure change. We have shown that while a minimal change of 0.20 F for 3 consecutive days results in more biphasic graphs, there is a distinct bias toward earlier detection of a shift. A more strict change of 0.4 0 F for 3 consecutive days produces a shift in the other direction, i.e., failure to detect a change or later detection of a change. The criterion of change of 0.3 0 F for 3 consecutive days seems to place the greater number of temperature graphs in a more physiologically expected range. The close agreement of this technique with the predicted day of ovulation as identified by CM adds further credibility to these findings. The observation that 97.3% of the biphasic curves maintain a difference between the final high and low average of> 0.3 0 F indicates the ability of A VE/3 to identify what will be a sustained temperature rise. While the above criterion also lends itself to retrospective interpretation, the method described by Vollman 5 and modified by us to smooth the curve for computer analysis shows excellent results in interpretation of the BBT graph retrospectively. The criteria for the SMC technique are rather demanding, in that at least the last seven points must remain above the mean of all temperatures. Nevertheless, when a BBT graph is complete, with most temperature readings acceptable, this technique results in 97% biphasic curves, with an ideal distribution of the PDO. There is also excellent correlation with the subjective CM observations. The SMC tends to erase the day-to-day variability of the BBT graph. Most clinical situations where concurrent chart interpretation is needed can be accommodated by the use of the AVE technique with at least a 0.3 0 F rise of temperature for 3 or more consecutive days. This technique may also be applied retrospectively; however, the SMC technique appears to be ideal for such applications, particularly in research. Vol. 39, No.5, May 1983 McCarthy and Rockette Interpretation of the BBT graph 645

REFERENCES 1. Moghissi KS: Accuracy of basal body temperature for ovulation detection. Fertil Steril 27:1415, 1976 2. Hilgers TW, Bailey A: Natural family planning. II. Basal body temperature and estimated time of ovulation. Obstet Gynecol 55:333, 1980 3. Bauman JE: Basal body temperature: unreliable method of ovulation detection. Fertil Steril 36:729, 1981 4. Marshall J: The Infertile Period, Principles and Practice. Baltimore, Helicon Press, 1963, p 35 5. Vollman RF: The Menstrual Cycle. Philadelphia, W. B. Saunders Co., 1977, p 80 6. Hartman CG: Science and the Safe Period. Baltimore, Williams & Wilkins Co., 1963, p 123 7. Rogers J: Endocrine and Metabolic Aspects of Gynecology. Philadelphia and London, W. B. Saunders Co., 1964, p 61 646 McCarthy and Rockette Interpretation of the BBT graph Fertility and Sterility