THE RELATION BETWEEN PLASMA TESTOSTERONE LEVELS AND THE LENGTHS OF PHASES OF THE MENSTRUAL CYCLE*
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1 FERTILITY AND STERILITY Copyright 1979 The American Fertility Society Vol. 32, No.4, October 1979 Printed in U.s.A. THE RELATION BETWEEN PLASMA TESTOSTERONE LEVELS AND THE LENGTHS OF PHASES OF THE MENSTRUAL CYCLE* KEITH D. SMITH, M.D. LUIS J. RODRIGUEZ-RIGAU, M.D. ROBERT K. TCHOLAKIAN, PH.D. EMIL STEINBERGER, M.D.t Department of Reproductive Medicine and Biology, University of Texas Medical School at Houston, Houston, Texas Plasma testosterone levels were measured in 331 women of reproductive age. The incidence of clinical signs of hyperandrogenism (hirsutism, acne) was recorded. Ovulatory activity was evaluated clinically by basal body temperature and frequent observation of changes in the appearance of the cervical os and cervical mucus. Plasma testosterone levels were abnormally elevated in patients with clinical signs of hyperandrogenism. The highest mean testosterone levels were noted in the group of hyperandrogenic women with amenorrhea. Significant prolongation of the follicular phase and shortening of the luteal phase were demonstrated to be associated with clinical signs of hyperandrogenism and elevated plasma testosterone levels. Statistically significant correlations between plasma testosterone levels and duration of phases of the menstrual cycle were observed. Testosterone levels were directly related to the length of the follicular phase and inversely related to the length of the luteal phase. A significant inverse correlation between the lengths of the two phases of the menstrual cycle was also demonstrated. These results suggest an association between hyperandrogenism and prolongation of the follicular phase and shortening of the luteal phase of the menstrual cycle, possibly related to the high incidence of infertility and menstrual irregularity reported for hyperandrogenic women. Fertil Steril 32:403,1979 Amenorrhea, oligomenorrhea, irregular menstrual cycles, and infertility are frequently associated with hyperandrogenism in women. I - 4 The mechanisms underlying this association are unclear _ Abnormally high plasma androgen levels are generally found in patients with clinical signs of hyperandrogenism and disturbed ovarian function_ 2-6 It has been suggested by several investigators that the central nervous system is Received February 5, 1979; revised May 10, 1979; accepted May 14, * Presented at the Thirty-Fifth Annual Meeting of The American Fertility Society, February 3 to 7, 1979, San Francisco, Calif. treprint requests: Emil Steinberger, M.D., Professor and Chairman, Department of Reproductive Medicine and Biology, University of Texas Medical School at Houston, P.O. Box 20708, Houston, Tex influenced by elevated circulating androgens, leading to a functional discordance of the hypothalamic-pituitary-ovarian axis. 6,7 Possibly, tonic rather than cyclic gonadotropin stimulation of the ovaries is associated with anovulation and polycystic ovarian disease. 7 This is supported by studies reporting resumption of ovulatory menstrual cycles in hyperandrogenic anovulatory patients after reduction of circulating androgen levels by glucocorticoid treatment or wedge resection of the ovaries. 3, 4, 7,8 Ovulation does occur in some infertile hyperandrogenic patients and in some patients with polycystic ovarian disease. 1, 4, 9, 10 Treatment with glucocorticoids or clomiphene citrate often results in pregnancy in these patients.!. 4, 7, 10, 11 We recently reported a significant correlation between percentage suppression of plasma tes- 403
2 404 SMITHETAL. tosterone levels and pregnancy rates in infertile ovulatory women.4 Ovulatory dysfunction, secondary to hyperandrogenism, was suggested to be responsible for the infertility of these patients. Suppression of plasma testosterone levels by prednisone therapy in hyper androgenic women was associated with significant shortening of the follicular phase and lengthening of the luteal phase of the menstrual cycle. 8 Consequently, this study was conducted to investigate the possibility of a relation between hyperandrogenism, delayed ovulation (long follicular phase), and short luteal phase. To our knowledge, the relation of plasma testosterone levels to duration of phases of the menstrual cycle in ovulatory women has not been previously reported. MATERIALS AND METHODS The patient population utilized in this study comprised 331 women of reproductive age seen consecutively in our office. The most frequent presenting complaints of these women were as follows: infertility (49.8%), irregular menstrual cycles (13.3%), hirsutism (12.7%), amenorrhea (10.0%), acne (6.0%), and miscellaneous reasons (dysmenorrhea, premenstrual tension, cyclic mastodynia, sexual dysfunction, migraine headaches, etc.) (8.1%). The 165 patients with a presenting complaint of infertility include 109 patients reported previously in a preliminary study of the relation of plasma testosterone levels to infertility.4 Plasma testosterone levels were measured prior to any therapy in all patients. The method for radioimmunoassay of plasma testosterone was previously reported.12, 13 Ovulatory activity was evaluated clinically by means of basal body temperature and daily or alternate-day observation of changes in the cervical os and cervical mucus The follicular phase of the cycle was considered to commence with the 1st day of menstruation and terminate with the closure of the cervical os associated with elevation of basal body temperature. The luteal phase was measured at the time between the closure of the cervical os associated with a shift in basal body temperature and the 1st day of menstruation. If closure of the cervical os and change in the cervical mucus did not coincide with elevation of basal body temperature, ovulation was judged to have occurred the day preceding the closure of the cervical os. The patient population was divided into October 1979 women classified as amenorrheic, anovulatory, or ovulatory. Amenorrheic patients were those with the absence of vaginal bleeding for a minimum of 3 months. Anovulatory patients were those with periodic vaginal bleeding associated with a monophasic basal temperature chart and the absence of changes in the cervical os and cervical mucus suggestive of ovulation. Ovulatory patients demonstrated a biphasic basal temperature chart and typical changes in the cervical os and cervical mucus. The groups were further divided into those patients with and without clinical signs of hyperandrogenism (acne, hirsutism). Differences in plasma testosterone levels between the groups were compared. In ovulatory patients, correlations between plasma testosterone levels and duration of phases of the menstrual cycle were investigated. Results were analyzed for statistical significance by one-way analysis of variance and Duncan's multiple range test or linear regression analysis. As a control group, plasma testosterone levels were measured in 22 women selected from our donor artificial insemination population on the basis of absence of clinical signs of hypernadrogenism, biphasic basal temperature charts, typical temporal changes in the cervical os and cervical mucus suggesting ovulation, a follicular phase no greater than 17 days, a luteal phase no shorter than 12 days, and the occurrence of pregnancy in the first or second cycle of donor artificial insemination. The mean menstrual cycle length (± standard error) in these women was 27.9 ± 0.5 days, with a mean follicular phase length of 14.2 ± 0.5 days and a mean luteal phase length of 13.7 ± 0.2 days. RESULTS The mean plasma testosterone level (± standard error) for the entire group of 331 patients was 56.2 ± 1.3 ng/loo ml, significantly higher than that found in the control group of 22 women (29.3 ± 1.5 ng/100 ml, P < 0.01) (Table 1). Clinical signs of hyperandrogenism (hirsutism, acne) were present in 229 (69.2%) of these patients. Plasma testosterone levels in clinically hyperandrogenic women were significantly higher than those in women without these signs (P < 0.01). Mean levels in the latter group were not significantly different from those in the control group. Of the 331 patients, 65 were amenorrheic (19.6%), 40 were anovulatory
3 Vol. 32, No.4 PLASMA TESTOSTERONE AND PHASES OF THE MENSTRUAL CYCLE 405 TABLE 1. Plasma Testosterone Levels in 331 Consecutive Patients in Relation to Clinical Signs of Hyperandrogenism (Hirsutism, Acne) and Ovarian Function Androgen state Testosterone level" Amenorrheic subjects Anovulatory subjects Ovulatory subjects Total nglloo ml Hyperandrogenism 75.0 ± 4.7 (43)' 59.9 ± 3.8 (34)" 64.2 ± 1.6 (152)" 65.6 ± 1.4 (229) No hyperandrogenism 32.5 ± 2.5 (22)b 31.8 ± 4.9 (6)b 36.1 ± 1.5 (74)b 35.1 ± 1.2 (102)b Total SO.6 ± 2.9 (65) 55.7 ± 3.1 (40) 55.0 ± 1.1 (226) 56.2 ± 1.3 (331) Values are means ± standard error. Numbers in parentheses are numbers of patients. Control group: 29.3 ± 1.5 ng/loo ml (22 subjects). bp < 0.01, 1 > 2P < (12.1%), and 226 were ovulatory (68.3%). Mean plasma testosterone levels in the three groups were significantly elevated above normal, but were not significantly different from each other. If only patients with clinical signs of hyperandrogenism were considered (229), amenorrheic patients had significantly higher levels (P < 0.01) than either anovulatory or ovulatory patients (Table 1), a relation not found in the group of patients without clinical signs of hyperandrogenism. Evaluation of the 28 amenorrheic or anovulatory patients without hyperandrogenism suggested the diagnoses of primary ovarian failure in four patients, postpill amenorrhea in two, postpartum amenorrhea in two, hypothyroidism in two, hypogonadotropic hypogonadism in one, anorexia nervosa in one, and amenorrhea galactorrhea in one. In the remaining 15 patients, no etiology for the condition could be established. The duration of both phases of the menstrual cycle was evaluated in the ovulatory patients (Table 2). Mean follicular phase and luteal phase lengths (± standard error) for the entire group of 226 patients were 19.0 ± 0.4 days and 12.0 ± 0.2 days, respectively. Significant prolongation of the follicular phase and shortening of the luteal phase were demonstrated in clinically hyperandrogenic women when compared with either the control or the non-hyperandrogenic groups (J> < 0.01). The possible relation of plasma testosterone levels to prolongation of the follicular phase or shortening of the luteal phase was analyzed (Table 3), and highly significant correlations were observed (P < 0.001). Plasma testosterone levels were directly related to the length of the follicular phase and inversely related to the length of the luteal phase. Linear regression analysis demonstrated the significance of these correlations (Fig. 1). A significant correlation between the duration of the two phases of the menstrual cycle was demonstrated also. The longest follicular phases were found in patients with short luteal phases and vice versa (P < 0.001) (Fig. Ie; Table 4). DISCUSSION The duration of the phases of the menstrual cycle in normal ovulatory women has been studied by many authors.15-1s The mean follicular and luteal phase lengths of the 22 control women reported here (14.2 ± 2.3 days and 13.7 ± 0.8 days) were similar to those published by other investigators.15. 1S Ovulatory dysfunction characterized by delayed ovulation (long follicular phase) or a shortened luteal phase are frequently associated with infertility and menstrual disorders The pathophysiology of abnormalities in the duration of phases of the menstrual cycle is still poorly understood. Stress TABLE 2. Plasma Testosterone Levels and Duration of Phases of the Menstrual Cycles of 226 Ovulatory Patients" Androgen state No. of patients Plasma testosterone Follicular phase length Luteal phase length Hyperandrogenism No hyperandrogenism nglloo ml 64.2 ± ± 1.5b days days 20.1 ± 11.4 ± ± 0.5b 13.2 ± 0.2b Total ± ± ± 0.2 Control group "Values are means ± standard error. bp < ± 1.5b 14.2 ± 0.5b 13.7 ± 0.2b
4 406 SMITHET AL. TABLE 3. Relation of Plasma Testosterone Levels to Duration of Phases of the Menstrual Cycles of 226 Ovulatory Patients No. of Follicular Luteal phase Plasma testosterone patients phase length" length" ng!100 ml ooys ooys < ± ± ± ± l.0 ± l.7 ± 0.25 > ± l ± 0.55 Total ± ± 0.2 "Values are means ± standard error. Over-all correlationsp < 0.001, by one-way analysis of variance and Duncan's multiple range test; 1 < 2 P < 0.01; 3 > 4 > 5 P < 0.0l. or environmental changes may cause prolongation of the follicular phase The association of the long follicular phase with the short luteal phase has been reported to be common Inadequate follicular development or an inadequate luteinizing hormone surge have been suggested as possible mechanisms for this disorder.2o. 25 In this study significant prolongation of the follicular phase and shortening of the luteal phase were shown to be associated with hyperandrogenism. To our knowledge, this association has not been previously demonstrated. This study further suggests that hyperandrogenism may not be the only cause of prolongation of the follicular phase. The mean follicular phase of the non-hyperandrogenic group was significantly longer than the mean follicular phase of the control group (P < 0.01). The reason for this difference was not apparent from this study. Suppression of plasma testosterone levels by chronic glucocorticoid treatment in hyperandrogenic women with amenorrhea or anovulation 90 ;;60 3IJ A p(o.ooi 10 2e 3IJ 40 Follicular phue length (dq's) i l2 ill 90 ;;60 3IJ B,... p<o.ool 1 "'-_ 111<0_.00_'..._-;,-_"111- Follicular pmse length (dqs), 1 luteal phase length (dilys) FIG. l. Correlations between plasma testosterone (T) levels and lengths of the follicular phase and luteal phase of the menstrual cycles of 226 women (A and B), and correlation of follicular phase length to luteal phase length (C). October 1979 TABLE 4. Relation between Plasma Testosterone Levels and Duration of Phases of the Menstrual Cycle 226 Ovulatory Patients Follicular phase No. of Luteal phase Plasma length subjects length testosterone days ooys ng!100 m ± ± ± 0.2 5l.9 ± ± ± l.8 ± ± l.2 ± ± ± ± 3.9 Total ± ± l.1 Luteal phase No. of Follicular Plasma length subjects phase length testosterone ooys ooys nglloo ml ± ± l ± l ± l.0 ± l ± ± ± ± l ± 4.9 Total ± ± l.1 results in initiation of ovulatory activity in a significant number of patients In patients with a prolonged follicular phase and a shortened luteal phase, reduction of plasma testosterone levels is associated with significant shortening of the follicular phase and lengthening of the luteal phase.8 In infertile patients, we have reported a significant correlation between incidence of pregnancy and percentage suppression of plasma testosterone during chronic prednisone treatment.4 Possibly, elevated plasma androgen levels could be responsible for a functional discordance of the hypothalamic-pituitary-ovarian axis, resulting in inadequate follicular development or an inadequate luteinizing hormone surge. 7 This would lead to delayed ovulation and luteal phase deficiency, whereas higher androgen levels would result in anovulation or amenorrhea. Indeed, in this as well as in previous studies,4.8 the highest plasma tesosterone levels were observed in clinically hyperandrogenic patients with amenorrhea. Mean plasma testosterone levels were abnormally elevated in patients with clinical signs of hyperandrogenism. This is in agreement with the findings of other investigators Although it has been reported that plasma testosterone levels in normal women are highest during the peri ovulatory period,26.28 it has been acknowledged by most authors that these variations are within a narrow range, permitting a valid evaluation of testosterone levels in blood
5 Vol. 32, No.4 PLASMA TESTOSTERONE AND PHASES OF THE MENSTRUAL CYCLE 407 samples obtained during any phase of the menstrual cycle. 28 No attempt was made in this study to regulate the time of the cycle at which blood samples were obtained. In spite of this, significant correlations between plasma testosterone levels, clinical signs of hyper an drogenism, and ovarian dysfunction were demonstrated. Analysis of the data revealed that approximately 90% of the blood samples were obtained during the early or midfollicular phase of the cycle. Elimination of values obtained during the late follicular phase or periovulatory period did not alter the results significantly. In conclusion, this study demonstrates a high incidence of hyperandrogenism in patients with amenorrhea, anovulation, and ovulatory dysfunction. An association between prolongation of the follicular phase, shortening of the luteal phase, elevated plasma testosterone levels, and clinical signs of hyperandrogenism was demonstrated. It must be emphasized, however, that no cause-and-effect conclusions between hyperandrogenism and the long follicular phase or the shortened luteal phase can be drawn from these data. Further studies will be required to clarify the pathophysiology of ovulatory dysfunction associated with hyperandrogenism in women. Acknowledgment. The authors wish to thank Mrs. Carol M. Rodriguez-Rigau for her assistance in the statistical evaluation of the results. REFERENCES 1. Ferriman D, Purdie A W: Association of oligomenorrhoea, hirsutism and infertility. Br Med J 2:69, Hosseinian AH, Kim MH, Rosenfield RL: Obesity and oligomenorrhea are associated with hyperandrogenism independent of hirsutism. J Clin Endocrinol Metab 42:765, Paulson JD, Keller DW, Wiest WG, Warren JC: Free testosterone concentrations in serum: elevation is the hallmark of hirsutism. Am J Obstet Gynecol 128:851, Steinberger E, Smith KD, Tcholakian RK, Rodriguez Rigau LJ: Testosterone levels in female partners of infertile couples. Relationship between androgen levels in the woman, the male factor and the incidence of pregnancy. Am J Obstet Gynecol 133:133, Bardin CW, Hembree WC, Lipsett MB: Suppression of testosterone and androstenedione production rates with dexamethasone in women with idiopathic hirsutism and polycystic ovaries. J Clin Endocrinol Metab 28:1300, Abraham GE, Chakmakjian ZH, Buster JE, Marshall JR: Ovarian and adrenal contributions to peripheral androgens in hirsute women. Obstet Gynecol 46:169, Greenblatt RB, Mahesh VB: The androgenic polycystic ovary. Am J Obstet Gynecol 125:712, Rodriguez-Rigau LJ, Smith KD, Tcholakian RK, Steinberger E: Effect of prednisone on plasma testosterone levels and on duration of phases of the menstrual cycle in hyperandrogenic women. Fertil Steril 32:408, Goldzieher JW, Axelrod LR: Clinical and biochemical features of polycystic ovarian disease. Fertil Steril 14:631, Smith KD, Steinberger E, Perloff WH: Polycystic ovarian disease. A report of 301 patients. Am J Obstet Gynecol 93:994, Perloff WH, Smith KD, Steinberger E: Effect of prednisone on female infertility. Int J Fertil 10:31, Rao PN, Moore PH, Peterson DM, Tcholakian RK: Synthesis of new steroid haptens for radioimmunoassay Part V Carboxymethyl ether derivative of testosterone. A highly specific antiserum for immunoassay of testosterone from both male and female plasma without chromatography. J Steroid Biochem 9:539, Smith KD, Tcholakian RK, Chowdhury M, Steinberger E: Rapid oscillations in plasma levels of testosterone, LH and FSH in men. Fertil Steril 25:965, Perloff WH, Steinberger E: In vivo survival of spermatozoa.in cervical mucus. Am J Obstet Gynecol 88: 439, Moghissi KS, Syner FN, Evans TN: A composite picture of the menstrual cycle. Am J Obstet Gynecol 114:405, Punnonen R, Nummi S, Ylikorkala 0, Alapiessa U, Karvonen P, Viinikka L: A composite picture of the normal menstrual cycle. Acta Obstet Gynecol Scand [Suppl] 51:63, Strott CA, Cargille CM, Ross GT, Lipsett MB: The short luteal phase. J Clin Endocrinol Metab 30:246, Jolivet A, Gautray JP: Clinical investigation of the menstrual cycle. I. Diagram of the normal menstrual cycle. Fertil Steril 29:40, Coutts JRT, Dodson K, MacNaughton MC: Hormone profiles in normally menstruating and infertile women. Eur J Obstet Gynecol Reprod BioI [Suppl] 4:S159, Jones GS: The luteal phase defect. Fertil Steril 27:35, Smith KD, Rodriguez-Rigau LJ, Steinberger E: Relation between indices of semen analysis and pregnancy rate in infertile couples. Fertil Steril 28:1314, Matsumoto S, Igarashi M, Nagaoka Y: Environmental anovulatory cycles. Int J Fertil 13:15, Preston FS, Bateman SC, Short RV, Wilkinson RT: Effects of flying and time changes on menstrual cycle length and on performance in airline stewardesses. Aerospace Med 44:438, Maathuis JB, Van Look PFA, Michie EA: Changes in volume, total protein and ovarian steroid concentrations of peritoneal fluid throughout the human menstrual cycle. J Endocrinol 76:123, Soules MR, Wiebe RH, Aksel S, Hammond CB: The diagnosis and therapy of luteal phase deficiency. Fertil Steril 28:1033, Abraham GE: Ovarian and adrenal contribution to peripheral androgens during the menstrual cycle. J Clin Endocrinol Metab 39:340, Kim MH, Rosenfield RL, Dupon C: The effects of dexamethasone on plasma free androgens during the normal menstrual cycle. J Clin Endocrinol Metab 39:340, Dawood MY, Saxena BB: Plasma testosterone and dihydrotestosterone in ovulatory cycles. Am J Obstet Gynecol 126:430, 1976
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