were reported to be extremely active in stimulating the release of gonadotropins in animals4
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1 FERTILITY AND STERILITY Copyright ~ 1977 The American Fertility Society Vol. 28, No.3, Mareh 1977 Printed in U.SA. STIMULATION OF LUTEINIZING HORMONE (LH) AND FOLLICLE-STIMULATING HORMONE BY [D-LEU6,DES-GLYIO-NH 21-LH-RELEASING HORMONE ETHYLAMIDE AFTER SUBCUTANEOUS, INTRAVAGINAL, AND INTRARECTAL ADMINISTRATION TO WOMEN MOTOI SAITO, M.D.* TAKAHIRO KUMASAKI, M.D.* YOSHIMASA YAOI, M.D.* NOZOMU NISHI, M.D.* AKIRA ARIMURA, M.D.t DAVID H. COY, PH.D.t ANDREW V. SCHALLY, PH.D.t Department of Obstetrics and Gynecology, Tokyo Medical and Dental University, Tokyo, Japan, Department of Medicine, Tulane University School of Medicine, and Endocrine and Polypeptide Laboratories, Veterans Administration Hospital, New Orleans, Louisiana Women, most of whom had regular menstrual cycles, were administered f.d-leu 6,des GlylO-NH 21-1uteinizing hormone-releasing hormone (LH-RH) ethylamide (D-Leu 6 -LH RH-EA) via different routes during the early or midfollicular phase of the cycle. Plasma LH, follicle-stimulating hormone (FSH), and estrogen levels were determined by radioimmunoassay before and after administration ofd-leu 6 -LH-RH-EA. Plasma LH and FSH increased and reached peak levels 3 to 4 hours and 3 to 6 hours, respectively, after subcutaneous injection of25 pg of the analog oflh-rh. Intravaginal or intrarectal application of2 mg ofd-leu 6 -LH-RH-EA also increased plasmalh andfsh levels in most of the women, but the magnitude of the rise, the time of initiation of response, and the peak level varied among the women. The plasma estrogen level also rose after administration via either route. After luteinizing hormone-releasing hormone (LH-RH) was characterized and synthesized,!' 2 various potent agonists were synthesized. 3 A mong these, [D-Ala6,des-Glylo-NH21-LH-RH ethylamide and [D-Leu6,des-Glylo-NH21-LH-RH ethylamide were reported to be extremely active in stimulating the release of gonadotropins in animals4 5 and humans These analogs were active even when administered orally or intravaginally to animals, although a larger dose was required to induce a release of gonadotropins by these routes than by the parenteral route. 8 Accepted October 25, *Department of Obstetrics and Gynecology, Tokyo Medical and Dental University. tdepartment of Medicine, Tulane University School of Medicine, and Veterans Administration Hospital, New Orleans, La. 240 In the present study, we investigated the effect of [D-Leu 6,des-GlylO-NH 21-LH-RH ethylamide (D-Leu 6 -LH-RH-EA) administered by subcutaneous, vaginal, or rectal routes on plasma luteinizing hormone (LH), plasma follicle-stimulating hormone (FSH), plasma estrogens, and the menstrual cycles of women with regular menstrual cycles. MATERIALS AND METHODS Preparation for Subcutaneous Injection. D-Leu6- LH-RH-EA was synthesized by using solid-phase methods described elsewhere. 5 The analog was dissolved in 0.9% Nael solution in a concentration of 25 JLg/ml and sterilized by heat, ultraviolet light, and ultrafiltration by a Millipore filter. Samples of the solution (1.2 ml) were then placed
2 Vol. 28, No.3 VAGINAL AND RECTAL ADMINISTRATION OF D-LEU"-LH-RH-EA 241 in ampules, and the ampules were sealed aseptically. They were stored at 4 C until used. Preparation of Vaginal and Rectal Suppositories. Vaginal suppositories were made by mixing 2 mg of the analog with mg of lactose and solidified by adding mg of starch and 9 mg of magnesium stearate. These suppositories were also initially used rectally, but later the rectal suppositories, containing 2 mg of analog, were made of carbowax (polyethylene glycols: 400,0.19 gm; 1500, 0.75 gm; 4000, 0.93 gm). The suppositories were stored at 4 C until used. All experiments were performed between days 5 and 10 of the menstrual cycle in women 21 to 40 years of age. Most of the women had regular menstrual cycles (24 to 34 days), but four women had prolonged cycles (36 to 46 days). The analogs were administered at 9:00 A.M. For subcutaneous administration, 25 ILg of analog in 1 ml of saline were injected into the deltoid region in eight women. Vaginal administration was carried out in 10 women by inserting a suppository containing 2 mg of the analog into the posterior fornix of the vagina and then inserting a cotton tampon to prevent the suppository from slipping out. The tampon was removed at 6 P.M. on the same day. Rectal administration was carried out in seven women using the lactose-stearate suppository, and in eight others using carbowax suppositories. After the rectum was emptied by defecation, the suppository containing 2 mg of analog was inserted. Defecation was not permitted for 12 hours thereafter. Suppositories melted within 30 to 60 minutes after insertion in the vagina, but the rectal suppositories were only partially melted 4 to 5 hours after insertion. Determination oflh andfsh in Plasma. Blood was collected in a heparinized syringe from the antecubital vein 30 minutes before, immediately before, and 15 minutes, 30 minutes, and 1,2, 3, 4, 6, 24, and 48 hours after administration of the analog. Plasma was separated by centrifugation and stored at - 20 C until assayed for LH and FSH. Plasma LH and FSH were determined by radioimmunoassay (RIA) using a human LH RIA kit and human FSH-RIA kit (Daiichi Seiyaku C., Tokyo). Second International Reference Preparation human menopausal gonadotropin (2nd IRP-HMG) was used as the standard reference preparation for both LH and FSH. One milliinternational unit of LH and FSH in terms of 2nd IRP-HMG corresponded to 2.6 ng and 27.4 ng of LER-907, respectively. The minimal detectable dose in this RIA system is 1.95 miu/ml for both LH and FSH. Coefficients of intra-assay and interassay variation of RIA for LH were 6.8% and 7.5%, respectively, and those for FSH were 7.4% and 8.6%, respectively. Some of the plasma samples were assayed for estrogen by RIA as described by Hotchkiss et al.9 Basal body temperature CBBT) was recorded in each woman. RESULTS Subcutaneous Injection of D-Leu 6 -LH-RH-EA. After subcutaneous injection of25 ILg of this analog, the plasma LH level started to rise within 15 minutes after injection in all but one woman, and reached a peak level 3 to 4 hours after injection. The mean peak LH level was about 21 times greater than the preinjection level. Twenty-four hours after injection, the mean LH values were still above the preinjection levels, but had returned to this level 48 hours after injection (Table 1). Plasma FSH started to rise more slowly than LH and reached a peak level, which was 7 times greater than the preinjection level, 3 to 6 hours after the injection. As was the case with LH, the FSH level was still slightly elevated at 24 hours but after 48 hours it had returned to the preinjection level (Table 2). TABLE 1. Plasma LH Levels after Subcutaneous, Intravaginal, and Intrarectal Administration of D-Leu 6-LH-RH-EA a No. of Route of administration Dose women Time after administration -30 min o min 15 min 30 min Ihr 2hr 3hr 4hr 6hr 24 hr 48hr mlu/ml Subcutaneous 25ILg b 65.0c 89.0c 155.7c 244.7c 248.3c 169.1c ±3.2 ±3.1 ±13.6 ±12.4 ±21.4 ±20.8 ±25.2 ±31.4 ±40.4 ±25.0 ±2.1 Intravaginal 2mg b b ±3.7 ±3.5 ±2.1 ±4.9 ±7.6 ±21.0 ±32.9 :t36.5 ±41.8 ±11.7 ±30.6 Intrarectal Lactose-stearate 2mg suppository ±5.8 ±5.7 ±5.7 ±8.8 ±17.1 ±21.0 ±21.7 ±23.7 ±11.2 ±2.3 ±1.6 Carbowax suppository 2mg ±1.6 ±1.1 ±1.5 ±1.8 ±8.4 ±53.0 ±58.2 ±45.7 ±24.8 ±4.0 ±1.0 avalues are means ± standard error of the mean, in terms of 2nd IRP-HMG. b. CSignificantly different from the preadministration levels (0 min) at P < 0.05 and P < 0.01, respectively (Student's t-test).
3 242 SAITOETAL. March 1977 TABLE 2. Mean Plasma FSH Levels after Subcutaneous, Intavaginal, and Intrarectal Administration of D-Leu 6 -LH-RH-EA No. of Time after administration Route of administration Dose women -30 min o min 15 min 30 min Ihr 2hr 3hr 4hr 6hr 24 hr 48hr mju/ml Subcutaneous 25ILg b 24.4b 41.3c 47.1" 40.4c 12.1b 9.1 ±1.5 ±1.6 ±1.1 ±2.2 ±2.0 ±6.0 ±6.7 ±6.4 ±6.1 ±1.8 ±2.2 Intravaginal 2mg ±2.2 ±2.2 ±2.2 ±2.1 ±1.8 ±2.0 ±6.2 ±13.0 ±8.3 ±2.9 ±5.4 Intrarectal Lactose-stearate 2mg suppository ±1.7 ±1.7 ±2.4 ±3.1 ±3.9 ±4.3 ±4.9 ±5.6 ±4.7 ±3.7 ±3.0 Carbowax suppository 2mg b 23.8b 25.5b 25.3b ±0.7 ±0.8 ±0.7 ±1.1 ±2.2 ± 4.8 ±5.2 ±5.4 ±5.6 ±2.9 ±1.5 Values are means ± standard error of the mean, in terms of 2nd IRP-HMG. b. csignificantly different from the preadministration levels (0 min) at P < 0.05 and P < 0.01, respectively (Student's t-test). Vaginal Administration of D-Leu 6 -LH-RH-EA. Vaginal administration of suppositories containing 2 mg of n-leu 6 -LH-RH-EA raised the plasma LH level within 6 hours in all of the women tested, but the magnitude of the LH response, the time of initiation of the response, and the peak LH level varied considerably among the women. The mean peak level was reached 4 to 6 hours after vaginal application, as was the case for subcutaneous injection. The mean peak level was lower than that for subcutaneous injection of 25 t-tg of the analog. However, in contrast to the subcutaneous route, the mean LH levels at both 24 and 48 hours were higher than the preinjection levels (Table 1). The plasma FSH level showed a pattern similar to that of LH, rising gradually and reaching a peak level 4 to 6 hours after vaginal administration. The mean peak FSH level increased to 3 times the preinjecti(m level. FSH levels were still elevated at 48 hours in most of the women (Table 2). Rectal Administration of D-Leu 6 -LH-RH-EA. Rectal administration of 2 mg of the analog in lactose-stearate suppositories resulted in a rise in plasma LH levels in five of seven women. In one of these women, the plasma LH level started to rise at 30 minutes and reached a peak at 4 hours. The peak LH level was about 4 times the preinjection level. In the other four women, the magnitude of the LH response was small. However, because of the great variation in response, the mean peak LH level was not significantly different from the preinjection level (Table 1). The LH level returned to the preinjection level at 24 hours. The plasma FSH level approximately doubled after rectal administration in the women who showed a considerable LH response. Two other women showed a slight increase, and the remaining four failed to show FSH responses (Table 2). When n-leu 6 -LH-RH-EA suppositories made of carbowax were administered by rectum, plasma LH levels increased in all of the women tested. In one subject, the LH level increased from 6.7 to 500 miu/ml within 3 hours. In five of eight women, LH levels were still elevated at 24 hours. However, again because of the large variation in response, mean postadministration values were not significantly different from pre administration values (Table 1). The plasma FSH level also increased after rectal administration of the analog in carbowax suppositories in seven of eight women tested. The peak levels were reached between 3 and 6 hours after administration and were 2 to 3 times the preinjection level (Table 2). Plasma estrogen levels were also determined after subcutaneous, vaginal, and rectal Oactosestearate suppository only) administration of the analog. The results are illustrated in Figure 1. The mean estrogen level rose in all seven women at 6 hours and remained elevated in five of the seven at 24 hours after subcutaneous injection, but these results were insignificant statistically owing Vaginal Route (2mg) ---- Subcutaneous (25 fl9) &--& Rectal Route (2mg) Time (hours) FIG. 1. Mean plasma estrogen levels after subcutaneous, vaginal, and rectal (lactose-stearate suppository) administration ofd-leu 6 -LH-RH-EA in women. Seven to ten women were treated in each group. Vertical bars indicate standard error of the mean.
4 Vol. 28, No.3 VAGINAL AND RECTAL ADMINISTRATION OF D-LEU6-LH-RH-EA 243 TABLE 3. Influence of Subcutaneous, Intravaginal, and Intrarectal Administration of D-Leu 6 -LH-RH-EA on Menstrual Periods Route of administration Subject Age Preceding Present Day of Last day of Last day of menstrual menstrual administration low BBT phase low BBT phase cycle cycle in cycle preceding cycle of present cycle Subcutaneous (7 women) K.K. 29 M.Y. 27 Y.N. 31 Ch. S. 23 N.A. T.M J. U. 35 Intravaginal (10 women) M.G. 26 T. o. 28 R. o. 30 Ch. S. 27 T. S. 29 Ch. K. 31 T. S. 31 Ch. H. 29 Y. K. 31 K.K. 29 Intrarectal: lactose-stearate suppository H. Ch. 33 (7 women) M.Y. 27 T.M. 31 H.O. 25 Ch. K. 31 M.F. 29 T.M. 28 Intrarectal: carbowax suppository N.S. 28 (8 women) K. H. 26 T.H. 29 T. S. 27 S.H. 40 Y.A. 27 Y.H. 21 T. S. 28 days days No rise in BBT No rise in BBT Pregnancy to a large variation in absolute values among individuals. In contrast, the level of plasma estrogen was elevated (more than 2-fold) at 24 and 48 hours after vaginal administration in eight of ten women, and also increased in two of seven women at 6 and 24 hours and in six of seven women at 48 hours after rectal administration Oactosestearate suppositories). Influence of Administration of D-Leu 6 -LH-RH EA on BBT and Menstrual Cycles. The results of subcutaneous administration are summarized in Table 3. Subcutaneous administration of 25 I-tg of D-Leu 6 -LH-RH-EA during the follicular phase blocked the expected rise in BBT (and probably ovulation) in two of seven women. Both of these women showed excellent LH and FSH responses to the analog. In other women, the low BBT phase tended to be prolonged after administration of the analog, as compared with the preceding cycle. The menstrual cycle was shortened in two women, prolonged in two others, and remained unchanged in three. Vaginal administration of 2 mg of the analog prolonged the low BBT phase in five of ten women, shortened it in two, and had no effect in three. In most of the women, the luteal phase (high BBT phase) was not affected. Rectal administration of the analog in lactosestearate suppositories also prolonged the low BBT phase in one woman and shortened it in two. Rectal administration of 2 mg of the analog in carbowax suppositories considerably prolonged the low BBT phase in four of eight women, slightly delayed it in one, and shortened it in three. These treatments did not affect the duration ofthe luteal phase in most of the women. DISCUSSION The present study indicates that an extremely active LH-RH analog, D-Leu 6 -LH-RH-EA, administered via subcutaneous, vaginal, and rectal routes stimulates the release of gonadotropins
5 244 SAITOET AL. in women. Although oral and vaginal administration oflh-rh itself has been found to stimulate gonadotropin release in animals, a considerably larger dose of LH-RH is needed to induce a response as compared with parenteral administration. This is also the case for potent LH RH agonists, but the absolute dose of an analog such as n-leu 6 -LH-RH-EA or n-ala 6 -LH-RH-EA necessary to induce a significant response is relatively small,s indicating that it is feasible to give these analogs via nonparenteral routes. Although the peak LH level was reached 6 hours after vaginal administration of n-leu 6 -LH-RH-EA, as observed for subcutaneous injection, LH levels were still elevated at 48 hours. Subcutaneous injection induced a greater increase in LH at 3 to 4 hours than did vaginal administration, but the plasma LH returned to the control level at 48 hours. Vaginal administration of n-leu 6 - LH-RH-EA may induce a lower but more prolonged response than that induced by subcutaneous injection. Therefore, the vaginal route may be better when a low but long-lasting release of gonadotropins is required, such as for stimulating follicular maturation and estrogen secretion. The mean plasma estrogen level 24 hours after subcutaneous injection of the analog was higher than the preinjection level, but returned to the control level at 48 hours. In contrast, after vaginal administration, plasma estrogen remained elevated at both 24 hours and 48 hours. Rectal administration of the analog in a lactosestearate suppository appears to be less effective than vaginal application. The analog in a carbowax suppository is better than in the lactosestearate suppository for stimulating gonadotropin but is still less effective than vaginal application. Differences among many of the factors which affect absorption and inactivation of the analog could account for the difference between stearate and carbowax suppositories. A response following rectal administration smaller than that following vaginal administration could be accounted for by better absorption of the analog through the vaginal mucous membrane than the rectal mucous membrane and/or lesser inactivation in the vagina that in the rectum. When the peak plasma LH level was used as an index for the magnitude of response, the subcutaneous injection of 25 J1-g of n-leu 6 -LH-RH EA induced a response twice as great as that induced by vaginal administration of2 mg of analog. This poor level of efficacy indicated that only a small portion of the analog in the suppository had been absorbed into the body. Nevertheless, the March 1977 dose of the drug, such as 2 mg, is not large in view of convenience and practicality of administration. None of the women tested complained of any local or general discomfort after. administration of the analog via either route. Improvement of the suppository vehicle may further increase the efficacy of the analog. Rectal administration of the analog may also be useful for stimulating the pituitarygonadal axis in some hypogonadal men and in children with delayed puberty. These results extend our work on the oral 12 and intranasap3 administration of this analog. The intravaginal and rectal routes are clearly more effective than the oral route, since the oral administration of 2 mg of this analog was not effective in raising LH and FSH levels. Only doses of 10 mg were active. The expected rise in BBT usually following ovulation was blocked by the subcutaneous injection of the analog in two women, and ovulation tended to be delayed in many other women after administration of the analog via any route. It is possible that the analog, when given during the follicular phase, blocked expected ovulation in some women and delayed it in others. Yamaji et al. 14 reported that the LH release induced by the administration of estrogen during the early follicular phase resulted in delayed ovulation in rhesus monkeys. 14 Similar events could have occurred in these women, who showed an excellent LH response to the analog and in whom ovulation was delayed or blocked by this treatment. It is difficult to explain why the analog prolonged the low BBT phase. Stimulation of progestin secretion as well as estrogen could have delayed ovulation, as reflected by prolonged low BBT, but this problem remains to be clarified. Acknowledgments. The authors are greatly indebted to Dr. William Locke, Miss Georgianne Farley, and Miss Alice Conradi for their editorial help. REFERENCES 1. Matsuo H, Baba Y, Nair RMG, Arimura A, Schally AV: Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem Biophys Res Commun 43:1334, Schally AV, Arimura A, Kastin AJ, Matsuo H, Baba Y, Redding TW, Nair RMG, Debeljuk L, White WF: Gonadotropin-releasing hormone: one hypothalamic polypeptide regulates secretion of both luteinizing and folliclestimulating hormones. Science 173:1036, Schally AV, Kastin AJ, Coy DH: LH-releasing hormone and its analogues: recent basic and clinical investigation. Int J Ferlil 21:1, 1976
6 Vol. 28, No.3 VAGINAL AND RECTAL ADMINISTRATION OF D-LEU6 -LH-RH-EA Arimura A, Vilchez-Martinez JA, Coy DH, Coy EJ, Hirotsu y, Schally A V: [D-Ala6,Des-Gly-NH2,oJ-LH-RHethylamide: a new analogue with unusually high LH RHlFSH-RH activity. Endocrinology 95:1174, Vilchez-Martinez JA, Coy DH, Arimura A, Coy EJ, Hirotsu Y, Schally AV: Synthesis and biological properties of [Leu-6J-LH-RH and [D-Leu-6,desGly-NH.lOJ-LH-RH ethylamide. Biochem Biophys Res Commun 59:1226, Soria J, Zarate A, Canales ES, Ayala A, Schally AV, Coy DH, Coy EJ, Kastin AJ: Increased and prolonged LH RHIFSH-RH activity of synthetic D-Ala6,des-Gly-NH2'O LH-RH ethylamide in normal women. Am J Obstet Gynecol 123:145, Zimartu J, Rosner JM, Guiloff E, Ibarra-Polo AA, Croxatto HD, Croxatto HB, Aguilera E, Coy DH, Schally AV: Attempts to programme ovulation with exogenous oestrogens and LH-RH analog. Br Med J 2:527, Nishi N, Arimura A, Coy DH, Vilchez-Martinez JA, Schally A V: The effect of oral and vaginal administration of synthetic LH-RH and [D-Ala 6,DesGly'O-NH.J-LH-RH ethylamide on serum LH levels in ovariectomized steroid blocked rats. Proc Soc Exp BioI Med 148:1009, Hotchkiss J, Atkinson LE, Knobil E: Time course of serum estrogen and luteinizing hormone (LH) concentrations during the menstrual cycle of the rhesus monkey. Endocrinology 89:177, Amoss M, Rivier J, Guillemin R: Release of gonadotropins by oral administration of synthetic LRF or a tripeptide fragment of LRF. J Clin Endocrinol Metab 35:175, Humphrey RR, Dermody WC, Brink HO, Bousley FG, Schottin NH, Sakowski R, Vaitkus JW, Veloso HT, Reel JR: Induction ofluteinizing hormone (LH) release and ovulation in rats, hamsters and rabbits by synthetic luteinizing hormone-releasing factor (LRF). Endocrinology 92: 1515, Gonzalez.:Barcena D, Kastin AJ, Miller MC III, Schalch DS, Coy DH, SchallyAV, Escalante-Herrera A: Stimulation of luteinizing hormone (LH) release after oral administration of an analogue of LH-releasing hormone. Lancet 2:1126, Gonzalez-Barcena D, Kastin AJ, Schalch DS, Coy DH, Schally AV: Prolonged elevation of luteinizing hormone (LH) after intranasal administration of an analog of LHreleasing hormone. Fertil Steril 27:1246, Yamaji T, Dierschke DJ, Hotchkiss J, Bhattacharya AN, Surve AH, Knobil E: Estrogen induction of LH release in the rhesus monkey. Endocrinology 89:1034, 1971
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