The basal body t.emperature chart in artificial insemination by donor pregnancy cycles*

Transcription

1 FERTLTY AND STERLTY Copyright 1982 The American Fertility Society Vol. 38 No.4 October 1982 Printed in U.SA. The basal body t.emperature chart in artificial insemination by donor pregnancy cycles* Robert G. D. Newill M.D. M.R.e.G.p. t Maurice Katz F.e.p. (SA) M.R.e.p.* University College Hospital Medical School and School of Medicine University College London England The basal body temperature (BBT) charts in pregnancy cycles of 110 consecutive women who became pregnant by a single heterologous insemination were studied. The occurrence of ovulation was proven by the pregnancies in each case. All of these pregnancy charts showed a biphasic pattern and most followed one of three stated types. The charts of 10 pregnancies that ended in miscarriage were no different from those 100 charts of pregnancies that proceeded to live births. No pregnancies occurred when artificial insemination by donor (AD) was performed before day 11 of the cycle or 2 or more days after the temperature elevation. Of 94 singleton pregnancies 56 (60%) were male and 38 (40%) were female. This male predominance had not been noted previously. Knowledge of the appearance of a typical pregnancy chart is useful not only in the diagnosis of certain Clluses of infertility but also in the accurate timing of artificial insemination. Previous work on the association between the BBT chart and ovulation compared the chart with variolls tests of presumptive ovulation. n this series the charts were studied in ovulatory cycles proven by pregnancy. Fertil Steril38: As long ago as 1904 the pioneer sexologist Van de Velde suggested a relationship between ovarian function and the daily recording of the body temperature. 1 This observation was given a more scientific basis in 1945 by Halbrecht 2 in srael and by Barton and Wiesner 3 in London who described the patterns of the basal body temperature (BBT) in ovulatory anovulatory and pregnancy cycles. Received March ; revised and accepted June *Supported in part by a grant to Dr. Newill from the Rockefeller Fund of University College Hospital Medical School. treprint requests: Robert G. D. Newill M.D. M.R.C.G.P. Clinical Lecturer Department of Obstetrics and Gynaecology University College Hospital Medical School London WCE 6JJ England. tconsultant Endocrinologist Department of Obstetrics and Gynaecology School of Medicine University College. Vol. 38 No.4 October 1982 Since then the BBT recording has become a recognized part of an infertility investigation although some have questioned its value. The doubts have arisen largely because the exact criteria for a normal BBT chart have never been positively laid down and possibly cannot be so that the interpretation of any particular monthly chart depends on the knowledge and experience of the doctor who studies it. As a result one possibly inexperienced doctor will confidently diagnose a chart as normal while another doctor may diagnose it as clearly abnormal. Because of the inability of the BBT chart to accurately indicate the exact time of ovulation other workers have tried combining it with other suggested methods for determining the occurrence of ovulation. Moghissi 4 studied the BBT in apparently normal healthy women. He used the luteal serum progesterone (P) level and endometrial biopsy as Newill and Katz BBT chart in AD pregnancy cycles 431

2 criteria of ovulation and concluded that ovulation had occurred in 20% of cycles showing monophasic BBT charts. Morris et al. 5 showed that the luteinizing hormone (LH) peak generally coincided with the slight nadir in the BBT that frequently precedes the temperature rise but they concluded that the BBT chart is an unsatisfactory method of determining the exact time of ovulation. Yussman and Taymor 6 reported the occurrence of ovulation 12 to 24 hours after the serum LH peak and this observation combined with the findings of Morris et al. 5 would suggest that ovulation actually occurs after the rise in temperature. n 1972 Johanssen et al. 7 compared the BBT with the midluteal plasma P and urinary excretion of estrogens in regularly menstruating young women. They found monophasic cycles in 12% of women in whom other parameters were considered to be within ovulatory levels. They also concluded that a monophasic BBT can occur in an ovulatory cycle. More recently Lenton et al. B presented 60 varied BBT charts to selected doctors some presumed to be experts because they were practicing gynecologists and others assumed to be nonexperts (general practitioners and junior hospital physicians and surgeons) and asked for their interpretation of these charts stating if and when ovulation had occurred. Their results showed that the experts were only slightly better than the nonexperts. A criticism of this paper was that the doctors were not asked to state their diagnostic criteria so that their answers were in fact only guesses. Magyar et al. 9 emphasized that all tests for ovulation are indirect and rely on the secretion of P by the corpus luteum (CL). They studied 40 normal healthy women over several menstrual cycles and compared the usual tests for ovulation the BBT chart midluteal serum P and histologic study of the endometrium with the regularity of menstrual cycles and the occurrence or absence of cyclical molimina i.e. cervical mucorrhea premenstrual breast tenderness abdominal bloating dysmenorrhea etc. They concluded that regularity of menstruation and the presence of molimina were as accurate a guide to the occurrence of ovulation as the usual tests. Most previous work suggests that ovulation in fact does occur immediately before the rise in temperature but it is also frequently asserted that ovulation can occur in the presence of a monophasic basal temperature with no rise in 432 Newill and Katz BBT chart in AD pregnancy cycles temperature during the luteal phase. These assertions were based on the assumption of ovulation based on criteria other than the occurrence of pregnancy. The present study was undertaken to assess the BBT charts of women who achieved pregnancy through a single heterologous insemination at the time of expected ovulation with a view to help interpret charts indicating pregnancy. MATERALS AND METHODS One hundred ten consecutive BBT charts of women who achieved pregnancy through a single heterologous insemination at the time of expected ovulation were analyzed. All the women were satisfied that pregnancy had resulted from the single insemination and not from their husbands-all of whom were sterile or grossly subfertile-or from other consorts. Most patients by previous investigations had been shown to have regular menstrual cycles ovulatory levels of P (more than 35 nmole/l i.e. 11 ng/ml) during the midluteal phase and patent fallopian tubes; but some whose husbands were azoospermic had little preliminary investigation prior to insemination since their histories initially gave no reason to suspect any infertility factors on their side. nseminations were intracervical 1 ml of fresh semen being instilled directly into the cervical canal through a special metal insemination cannula. Because the insemination was intracervical the patient was required to remain in a supine position for only 5 or 6 minutes afterwards. Because of the large number of patients attending the clinic for artificial insemination by donor (AD) we could not administer more than one insemination per month. Therefore the insemination was planned for the expected day of ovulation or just before. Women whose cycles were slightly irregular were given a small dose of clomiphene (50 mg daily for 3 days) from day 3 of their cycles in an attempt to program ovulation to occur on the same day each month. n some cases an injection of human chorionic gonadotropin (hcg) (5000 to U) was also given at the time of the insemination. RESULTS n a study of the BBT charts the first fact noted was that they were all clearly biphasic. One chart Fertility and Sterility

3 DAY OF CYCLE B :'2 TREATMENT ( ( ( H ( G t':enstruatlg 37.0 C -+--: 'H--+--L H--l t-+--1H-t-t-+++--H-' H C ! H-' -t-++-t---t--h-+rt-+--irhf--!.ol.r-+-!' +-i-+-i!--+--t-+ ii!' i l! ' C--hd-l++H-'! j-+-JH-++-l-j-+-H--lrll-'-t-H Hf-+-j-H ).n 1'1'F ''. l ' 36.4 C+-+--;--fl\j-++-H-+-+-l-++--'-++-H++-l-+-H-++-H+-H H ' 1 36'2 0 c++--!r+! !--+-j--l' !+.-Hi-+'+H' H-+++-i--H 36'0.cl_...LL..L...L.11L.L..l...JL.L..l...Ji-Li..L..!-L..L..!;1 i-l.l.l...l...l.j...l...l.j...l...l...j...ll..l...l-.-..l...l-.-..l.j...j Figure 1 Pregnancy chart showing a minimal temperature shift after ovulation. The arrow indicates the day of insemination. C clomiphene citrate 50 mg; hcg human chorionic gonadotropin. (Fig. 1) demonstrated only a minimal rise after the insemination but one still could see it as being biphasic. One hundred pregnancies ended in live births and ten miscarried during the first trimester-a spontaneous abortion rate of 10% which is similar to the spontaneous abortion rate in normally fertile couples. The pregnancies were proof that ovulation had taken place and certainly in those that carried through to term that the hormonal milieu was adequate for the maintenance ofpregnancy. Figure 2 is a typical BBT chart from this series. t shows a noticeable dip before the rise. Eightytwo charts (74%) showed this pattern which was the commonest seen in ovulatory cycles and the temperature rise after the dip. was fairly steep (type 1). Seventeen charts (16%) showed a more gradual stepwise rise (Fig. 3) but were nevertheless clearly biphasic (type 2). The remaining 11 charts (10%) although biphasic showed more than one temperature nadir during the periovulatory phase (Fig. 4) making it difficult to decide on the probable time of ovulation (type 3). Ten charts showed a temporary dramatic drop in temperature almost to preovulatory levels about 2 to 4 days after the ovulatory rise (Fig. 5). No pregnancies occurred when the insemination was done 2 or more days after the sharp rise in temperature. However four women did con- DAY OF CYCLE B TREATMENT MENSTRUAT 37.0 C. l J 36.8 C \ j ; o.j 36.6 C! ' \! r ::::! i 362 C_ i : T H C \j ' Figure 2 Type 1 pregnancy chart showing a steep temperature rise after insemination. Vol. 38 No.4 October 1982 Newill and Katz BBT chart in AD pregnancy cycles 433

4 DAY OF CYCLE i B TREATMENT T T T T 00 [ 10 MENSTRUATON 37.0 C 36.8 C 36.60( t tl} f rt \ i\i lln 36.4 C 36.2 C.J!!! 36.0 C Figure 3 Type 2 pregnancy chart showing a gradual stepwise rise after insemination. T tamoxifen 20 mg; D dienestrol 2 mg. ceive when the insemination was done on the same day as the temperature rise and the chart of one of these women is shown in Figure 6. A careful study of the ten charts of pregnancies that ended in first-trimester miscarriage revealed no difference between these charts and the charts of pregnancies that had a successful conclusion. Eight charts showed a type 1 pattern one a type 2 and one a type 3 pattern. Figure 7 shows the initial temperature pattern of one such pregnancy that terminated in spontaneous abortion at 10 weeks' gestation. No conception occurred when the insemination was done before day 11 of the cycle. Several women tended to have short cycles of 23 to 25 days with temperature charts showing a good biphasic pattern but with a short proliferative phase of 8 to 10 days. These women did not conceive when the insemination was done between days 8 to 10 but several became pregnant when the proliferative phase was extended by the administration of clomiphene in a small dose usually 50 mg daily for 3 days from the third day of the cycle. n women with short cycles due to a short proliferative phase their luteal phase length covered 12 days or more and their midluteal serum P levels were 35 nmole/l (11 ng/ml) or over indicating adequate CL function. Another interesting finding in this group of women attending for AD was that those who DAY OF CYCLE TREAT:ENT MENSTRUATON 37.0 C 36.8 C V 36.6 C n :r f 36.4C J \ J \ 11 l r'1! \.ioj 36.2 C 36.0 C.- f n t n J J Figure 4 Type 3 pregnancy chart giving no information on the probable day of ovulation. 434 Newill and Katz BBT chart in AD pregnancy cycles Fertility and Sterility

5 DAY OF (YCLE :' TREATMENT { ( ( ( MENS ( MJ 36.61: 1\ \ J 1\ ' 36.8 ( 1\. M ' 1.lr1 J 36.4 ( ( ( Figure 5 Pregnancy chart showing a marked secondary dip 3 days after the probable time of ovulation. C clomiphene citrate 50 mg. became pregnant easily tended to produce a reasonably steady temperature pattern with little daily fluctuation during the luteal phase. On the contrary an erratic or spiked BBT chart was characteristic of subfertile women or emotionally unstable women (Fig. 8) and the chart frequently reverted to a more steady pattern after treatment with a small dose of clomiphene or a suitable tranquilizer usually chlordiazepoxide 10 mg twice daily (Fig. 9). The sex of the baby when born was recorded on these charts; and the 100 successful pregnancies resulted in the births of 56 boys 38 girls and 6 sets of twins. A study of the charts revealed no clues e.g. timing of the insemination as to the subsequent sex of the baby or whether twins were forthcoming but this sex difference with a male predominance has been confirmed in analyzing a total of 607 AD pregnancies from which 371 males and 307 females have been born. DSCUSSON This study the first in which BBT charts have been analyzed during pregnancy cycles has highlighted a number of important facts. Apart from the 110 consecutive BBT charts studied in detail in this series approximately 150 other women returned their charts after they had become pregnant by AD. n every case these charts showed a biphasic pattern. This large number of biphasic pregnancy charts raises the question of whether!uy Of CYClE ) !t 2S DS TREAT1ENT HENST nol: 36.8 ( 36.61: ( 36.rc \l. J \ OC i \... 1 \j 1 ' i1-- \jll r-- Figure 6 Pregnancy chart showing insemination done after a steep rise in temperature. Vol. 38 No.4 October 1982 Newill and Katz BBT chart in AD pregnancy cycles 435

6 DAY OF CYCLE TREATMENT MENSTRUAT 37.0 C 36.8 C ' 36.6( J 36.4-C \ \-- oj f' 36.2 C \ C f ( \J ifj..j V Figure 7 Pregnancy chart of a woman in whom the pregnancy ended in spontaneous abortion at the tenth week. ovulation does in fact occur in cycles accompanied by monophasic temperature patterns or more significantly if it does occur whether pregnancy ever follows. n all previous studies ovulation was assumed by indirect tests laparoscopies were not performed and to our knowledge no pregnancy has ever been recorded in a patient with a monophasic temperature chart. All temperature charts could be categorized into one of three major patterns. The greatest number of pregnancies occurred when insemination was performed on the day before the temperature rise while some pregnancies occurred following insemination performed 1 or 2 days before the temperature nadir; no conception occurred if the insemination was performed before day 11 of the cycle suggesting that the follicle and its contents require maturation beyond a certain critical phase before fertile ovulation occurs. Patients with short follicular phases (10 days or less) did not conceive even when the insemination was performed at the temperature nadir and despite an adequate CL as defined by a luteal phase length of 12 days or more and a plasma P level of 35 nmole/l or more. This phenomenon of follicular inadequacy is commonly seen during the perimenopause and may explain in part why the fertility of such women in this phase of their reproductive life is reduced. n considering charts like Figure 5 it could be argued that there is no proof that ovulation did occur at the time of the insemination; that it DAY OF CYCLE J TREATMENT ( MENSTRUAT C 36.8 C 36.6( 36.4 C 36.2C 36.0 C i a 1 ' r r '\ \' l 11 \! Figure 8 Erratic spiked BBT chart of a young woman showing the effect of anxiety. 436 Newill and Katz BBT chart in AD pregnancy cycles Fertility and Sterility

7 DAY OF CYClE t B :ro TR::.A.HENT (!C (.;ENSTRlJATiON ? C : i! i! 368'C 11/ /! ' i!! 36.6( 36.4'C i! 1: i \h i 1/! J V ' '(' ''''''' V 36.2'( l' 36.0 C y r' \ 1 Figure 9 Pregnancy chart of the same young woman as in Figure 8 after treatment with chlordiazepoxide 10 mg twice daily. C clomiphene citrate 50 mg. could have occurred at the time of the secondary dip and that the sperm survived for some days after the insemination. However comparison of these pregnancy charts with the charts kept by the same women in the months prior to becoming pregnant showed that this secondary dip tended to occur in most cycles and was rarely as pronounced as the first nadir. Furthermore the first nadir almost invariably occurred 13 or 14 days before the onset of menstruation suggesting that they ovulated at this time. So in charts showing a secondary dip ovulation is most likely to occur at the time of the initial dip preceding the temperature rise. Marik and Hulka10 described the recovery of ova from unruptured luteinized follicles and demonstrated that a follicle can degenerate into a CL secreting P without actually rupturing and releasing its ovum. Recently several studies have confirmed this entity11-13 so it remains true that the only proof that ovulation has occurred in any particular cycle is pregnancy at the end of it. t would appear therefore that a biphasic chart is consistent either with true ovulation or with nonovulation associated with luteinization of an unruptured follicle and ovum entrapment. t only requires a small blood level of P to produce a rise in BBT. Moghissi4 showed that a biphasic chart can occur with a luteal peak P as little as 6.4 nmole/l. A possible cause of an inaccurate BBT chart is the inability of the patient to read a thermometer and keep an accurate temperature record. There was no evidence of this in our series. The intelligence of the women who kept these charts covered a wide spectrum; but all Vol. 38 No.4 October 1982 with one exception returned charts that were clear and easily legible. The exception was an immigrant women who spoke little English and whose charts were always bizarre but even her pregnancy chart showed an elevated temperature after the insemination; therefore we believe that a monophasic temperature pattern indicates anovulation. Women attending for AD are under considerable emotional strain and this shows itself in several ways. Menstruation may become irregular.14 Women may have raised blood prolactin levels or the midluteal P level may be depressed.15 The stress effect we believe is frequently apparent in the BBT chart which becomes erratic with wide swings of temperature from day to day. Figures 8 and 9 show the charts of one woman before and after the administration of chlordiazepoxide. Young women under the age of 25 are more prone to these effects of anxiety than older and more mature women. REFERENCES 1. Van de Velde TH: Uber den Zusammenhang zwischen ovarialfunktion. Wellenbewegung Haarlem The Netherlands Halbrecht : Ovarian function and body temperature. Lancet 2: Barton M Wiesner BP: Waking temperature in relation to female fecundity. Lancet 2: Moghissi KS: Accuracy of basal body temperature for ovulation detection. Fertil Steril 27: Morris NM UnderwoodLE Easterling W: Temporal relationship between basal body temperature nadir and luteinizing hormone surge in normal women. Fertil Steril 27: Newill and Katz BBT chart in AD pregnancy cycles 437.

8 6. Yussman MA Taymor ML: Serum levels offsh and LH and plasma progesterone related to ovulation by corpus luteum biopsy. J Clin Endocrinol Metab 30: JohanssenEDBLarsson-Cohn U Gemzell CA: Monophasic basal body temperature in ovulatory menstrual cycles. Am J Obstet Gynecol 113: Lenton EA Weston GA Cooke D: Problems in using basal body temperature recordings in an infertility clinic. Br Med J 1: Magyar DM Boyes SP Marshall JR Abraham GE: Regular menstrual cycles and premenstrual molimina as indications of ovulation. Obstet Gynecol 53: Marik J Hulka J: Luteinized unruptured follicle syndrome: a subtle cause of infertility. Fertil Steril 29: Koninckx P Heyns WJ Corvelyn PA Brosens A: Delayed onset ofluteinization as a cause of infertility. Fertil Steril 29: Brosens la Koninckx PR Corvelyn P A: A study of plasma progesterone oestradiol 1713 prolactin and LH levels and the luteal phase appearance of the ovaries in patients with endometriosis and infertility. Br J Obstet Gynaecol 85: Dmowski WP Rao R Scommegna A: The luteinized unruptured follicle syndrome and endometriosis. Fertil Steril 33: Newill RGD: A..D.-A review of 200 cases. Br J Urol 48: Vere MF Joyce DN: Luteal function in patients seeking A..D. Br Med J 2: Newill and Katz BBT chart in AD pregnancy cycles Fertility and Sterility