Evaluation of the in vivo efficacy of a new vaginal contraceptive agent in stumptailed macaques
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1 FERTILITY AND STERILITY Copyright e 1984 The American Fertility Society Printed in U.SA. Evaluation of the in vivo efficacy of a new vaginal contraceptive agent in stumptailed macaques Lourens J. D. Zaneveld, D.V.M., Ph.D.*t James W. Burns, M.S.* Jessie C. Goodpasture, Ph.D.t Brian H. Vickery, Ph.D.t College of Medicine, University of Illinois Health Sciences Center, Chicago, Illinois, and Institute of Biological Sciences, Syntex Research, Palo Alto, California I i! The 'effect of precoital vaginal placement of three spermicidal formulations on postcoitally recovered vaginal and cervical spermatozoa was compared. Periovulatory stumptailed macaque monkeys were administered intravaginally 1 ml of Ramses Contraceptive Vaginal Jelly (C. Schmid Products Company, Little Fall, NJ), or a formulation containing 0, 0.1, or 1.0% of a new spermicidal compound, RS All spermicide-containing formulations reduced the motility of both vaginal and cervical sperm, compared with the gel containing no spermicide. The 1.0% RS formulation was particularly effective. No motile spermatozoa were recovered from either location, and only 0.5% of the numbers of cervical spermatozoa recovered in control animals were recoverable from this treatment group (P < ). The formulation containing 0.1% RS appeared to be bioequivalent to the Ramses formulation containing 5% nonoxynol-9. These in vivo results support previous in vitro comparisons in which RS was estimated to be 50 times as potent a spermatostatic agent as nonoxynol-9. Fertil Steril41 :455, '1984 Little progress has been made in the development of new vaginal contraceptives during the, past two decades in spite of the fact that they are known to be less effective than other commonly used methods such as oral contraceptives or intrauterine devices. The latter two methods have a number of undesirable side effects associated Received June 22, 1983; revised and accepted November 16, *Department of Physiology and Biophysics, College of Medicine, University of Illinois Health Sciences Center. tdepartment of Obstetrics and Gynecology, College ofmedicine, University of Illinois Health Sciences Center. :j:department of Physiology, Institute of Biological Sciences, Syntex Research. Reprint requests: Dr. Brian H. Vickery, Department of Physiology, Institute of Biological Sciences, Syntex Research, R7-241, 3401 Hillview Avenue, Palo Alto, California with their use that can be avoided by using vaginal contraception. A more potent vaginal contraceptive would be an important addition to available birth control methods. Marketed vaginal contraceptives primarily employ surfactants, particularly nonylphenoxypolyethoxyethanol (nonoxynol-9), as their active ingredient. These surfactants are mixed with a number of different base materials and are delivered to the vagina in a variety offormulations. Their lack of effectiveness is normally attributed to user error. However, under carefully controlled conditions, primate studies with a representative commercially available preparation have resulted in a 50% pregnancy rate over four menstrual cycles. 1 Such results indicate that more potent active ingredients should be sought for vaginal contraception to gain optimal efficacy. Zaneveld et ai. A new vaginal contraceptive 455
2 The active ingredient of any vaginal contraceptive should immobilize spermatozoa rapidly, because sperm penetration into the cervical mucus may be accomplished within minutes. 2 The active ingredient should also be able to penetrate the seminal coagulum because, on ejaculation, the seminal coagulum may be deposited adjacent to the external cervical os so that, as lysis takes place, the spermatozoa can enter the cervical mucus without actually contacting the vaginal contents. Recently, it was demonstrated that the nonsurfactant agent, dl-1-[2-(2,4-dichlorobenzyloxy)~ n-octyl]imidazole oxalate (RS-37367), is a very potent spermatostatic agent in vitro against rabbit, dog, cynomolgus macaque,3,4 and human spermatozoa.3-5 The compound is ~ 50-fold more active than nonoxynol-9. These in vitro data indicate that this I-substituted imidazole has excellent potential as a new vaginal contraceptive. The present study evaluates the in vivo efficacy of RS MATERIALS MATERIALS AND METHODS RS was mixed with a at two different concentrations of the drug: 1% and 0.1 %. Control experiments were performed using the only ("placebo"). Comparative studies were done with nonoxynol-9, also in gel form (Ramses Contraceptive Vaginal Jelly, C. Schmid Products Company, Little Fall, NJ), which contains 5% nonoxynol-9, 1% boric acid, and 5% ethyl alcohol as active ingredients. EXPERIMENTAL PROCEDURE The Macaca arc to ides (stumptailed macaque) was used as the primate model. Females are easy to handle, and the animals will routinely mate immediately upon placing the female with the male. Only males and females of proven fertility were employed. Previous methods l, 6 were modified so that a postcoital sample of cervical mucus could be collected and evaluated. Since cervical mucus only allows optimal penetration of spermatozoa during the ovulatory period, all experiments were carried out with females at midcycle. This was judged to be between days 9 and 14 of the menstrual cycle, because the luteinizing hormone peak in the stumptailed ma- 456 Zaneveld et al. A new vaginal contraceptive caque occurs on about day 12.7 Thus,the animals were considered for use beginning orr day 9 of their cycles but only chosen for use if the cervical mucus had the typical periovulatory characteristics of being thin, watery, and produced in copious quantities. An animal was used only once during her cycle. Each formulation was tested in six to eight different females. The study was conducted in an open fashion. To perform the experiments, 1 ml of the formulation was placed into a 1-ml tuberculin syringe. The syringe was inserted into the vagina until it reached the cervix. The formulation was expelled while the syringe was slowly withdrawn, ensuring an even distribution throughout the vagina. The female was immediately placed in the cage of the male. The coital act was normally completed within 5 minutes. Individual experiments were rejected if a longer time period elapsed. The female was separated from the male with a transfer cage. The vaginal contents were recovered by placing a 1-ml tuberculin syringe in the vagina and injecting 0.2 ml of 0.9% NaCl. The saline was used because the male stumptailed macaque ejaculates only a very small volume of semen. The vagina was rinsed several times and the vaginal contents were aspirated into the syringe. The contents were immediately examined by light microscopy for spermatozoal motility and forward progression. Usually, 5 minutes or less were required between the completion of the coital act and evaluation of the recovered vaginal spermatozoa. The spermatozoal concentration was determined at a later time. In order to prevent contamination of the cervical mucus with vaginal spermatozoa during the mucus. collection procedure, the cervix was first rinsed extensively by douching the animals three times with 50 ml of 0.9% NaCl. The female was anesthetized with 0.5 to 1.0 ml ketamine (Vetelar, Parke-Davis, Morris Plains, NJ). The cervix was exposed with a speculum, and cervical mucus collected by entering a 14-gauge, 2-inch Angiocath intravenous Teflon catheter (Deseret Company, Sandy, UT) ~ 0.5 cm into the cervical os. Mucus was withdrawn by applying suction with a 3 ml syringe attached to the catheter. The mucus was immediately examined for the presence of spermatozoa, spermatozoal motility, ~nd forward progression. The number of spermatozoa in a representative sample of mucus was also determined. Fertility and Sterility
3 Table 1. The Effect or Vaginally Applied Preparations on Vaginal and Cervical Spermatozoa Recovered Postcoitally from Primates a Preparation n Vaginal spermatozoa Cervical spermatozoa Concentration % Motile Forward pro- NO.b % Motile Forward progression. gression x lob/ml Placebo pluronic ± ± ± ± 3 3 gel 1% RS plu ± 145 o ± ± 3 o ± 0 0 ronic gel 0.1 % RS ± ± ± ± Ramses Jelly ± ± ± ± asee text for methods. Numbers represent the mean ± standard error of the mean except forward progression, for which the range is given. bnumber of spermatozoa per 25, 1-mm 2 squares of a microscope grid at x 100 magnification. To assess spermatozoal motility, 100 spermatozoa were counted in various fields, and the number of motile spermatozoa was recorded. The percentage of motility was calculated. The number of motile spermatozoa that moved in a forward direction (forward progression) was also counted and recorded on a scale of 0 to 4 (0, none of the motile spermatozoa possessed forward motion; 1, up to 25% of the motile spermatozoa possessed forward motion; 2, from 26% to 50% of the motile spermatozoa moved forward, etc.). The concentration of spermatozoa recovered from the vagina was determined by diluting the sample tenfold with a mixture of 3% polyethylene glycol in 0.4% formaldehyde and counting the spermatozoa with the use of a white blood cell hemocytometer. Due to the thickness of the cervical mucus, the hemocytometer technique could not be applied for counting the cervical spermatozoa. Therefore, a grid (100 x 1 mm 2 ) was placed in the ocular of the microscope, and the number of spermatozoa in. several representative fields under the grid was counted at a 100-fold magnification. The average number of spermatozoa per 25, 1-mm 2 squares was calculated. STATISTICAL ANALYSES For concentration of vaginal spermatozoa, percentage of motility of vaginal spermatozoa, numbers of cervical spermatozoa, and percentage of motility of spermatozoa in cervical mucus, a Kruskal-Wallis one-way layout test was performed for each parameter. Since in the three latter cases, the control (placebo gel) and treatments were shown not to be equivalent to one another (P < 0.001), Fisher's Randomization Tests 8 were made for all pairwise comparisons. The comparisons of each treatment with the control were one-tailed tests; the comparisons among all other treatments were two-tailed tests. RESULTS The concentration of spermatozoa in the vagina was not different among any of the groups. The placebo gel did not alter the motility or forward progression of the spermatozoa recovered from the vagina (Table 1), as compared with the results obtained when no test materials were placed in the stumptailed macaque vagina prior to mating. 1, 6 The cervical mucus in these animals contained a large number of highly motile spermatozoa, most of which possessed forward motion. None of the spermatozoa recovered from the vagina of animals treated with 1% RS gel were motile (Table 1). Low vaginal spermatozoal motility was found with poor forward progression of the spermatozoa following application of 0.1 % RS gel. Ramses Jelly also depressed vaginal spermatozoal motility and forward progression. The motility of the vaginal spermatozoa from placebo-treated animals was significantly higher than that of the 1.0% RS gel-, the 0.1 % RS gel-, or the Ramses Jelly-treated animals (Table 2). The vaginal spermatozoal motility also differed significantly between the 1% RS gel and the Ramses Jelly, but not between the 1% and 0.1% RS gels and between 0.1% RS gel and Ramses Jelly. Very few spermatozoa penetrated the cervical mucus when the primates were treated with 1% RS gel (Table 1), and none of these spermatozoa possessed forward progression. A much higher number of spermatozoa was present in the cervical mucus following coitus with Ramses Zaneveld et al. A new vaginal contraceptive 457
4 Table 2. Multiple Comparisons, Using Fisher's Randomization Test, of the Effect of Four Vaginally Applied Preparations on Vaginal Spermatozoal Motility, Numbers of Spermatozoa in Cervical Mucus, and Their Motility, Collected Postcoitally from Primates a Preparations compared a Levels b Vaginal Cervical Cervical sperm sperm sperm motility numbers motility C Placebo versus 1% RS in Placebo NS d versus Ramses Jelly Placebo NS versus 0.1% RS in pluronic gel Ramses Jelly versus % RS in Ramses Jelly versus NS NS NS 0.1 % RS in 1 % RS in plu- NS NS ronicgel versus 0.1 % RS in astatistical analyses performed on data shown in Table 1. See Table 1 and text for experimental detail. bsmallest level of confidence at which mean differences are detected. cnumber of spermatozoa per 25, 1-mm 2 squares of a microscope grid at x 100 magnification. dnot significant (P > 0.05). Jelly or with 0.1 % RS gel in place. During several of the experiments, the spermatozoa collected from the Ramses Jelly-treated animals possessed good motility and forward progression. The numbers of spermatozoa in cervical mucus in the placebo treatment group as compared with either the 0.1% RS gel group or Ramses Jelly group were not significantly different. On the other hand, significant differences were found for this parameter between the 1% RS gel and the other three preparations. The cervical spermatozoal motility was significantly higher in the Ramses Jelly- and the 0.1 % RS treated groups than in the 1 % RS treated animals. No significant differences were found between the Ramses Jelly-treated and 0.1% RS geltreated animals with regard to spermatozoal numbers and motility. DISCUSSION In the development of vaginal contraceptives, a number of factors need to be considered. Not only 458 Zaneveld et al. A new vaginal contraceptive should the active ingredient(s) be spermicidal! spermatostatic, but it should also be able to enter the seminal coagulum and contact the spermatozoa. RS satisfies these requirements because it is highly spermicidal3-5 and penetrates the seminal coagulum. 4 The present results show that, at least in nonhuman primates, a 1% concentration of the compound is also very active in vivo, because it caused rapid immobilization of vaginal spermatozoa and allowed almost no penetration of the spermatozoa into the cervical mucus, and none of the spermatozoa found in the cervical mucus were motile. Ramses Contraceptive Jelly (containing 5% nonoxynol-9) still allowed 23% of the spermatozoa in the vagina to be motile. This is similar to the data reported previously for Delfen Contraceptive Cream (Ortho Pharmaceutical Corporation, Raritan, NJ) which, under exactly the same conditions of vaginal insertion and mating, allowed an average of 17% vaginal spermatozoal motility.6 Delfen Contraceptive Cream also contains 5% nonoxynol-9. In vitro, nonoxynol-9 appears to be as effective in immobilizing nonhuman primate spermatozoa as it is in immobilizing human spermatozoa, because the same minimal concentration of Delfen Contraceptive Cream (5 mg/md was required for complete immobilization of both human and stumptailed macaque spermatozoa within 20 seconds.6 Therefore, the presence of motile spermatozoa in the vagina after nonoxynol-9 treatment is not due to a poor spermicidal potency of the compound toward nonhuman primate as compared with human spermatozoa, but rather to the inability of formulated nonoxynol-9 to consistently immobilize all the spermatozoa. under natural mating conditions. This conclusion is reinforced by the fact that, in the present study, many motile spermatozoa were found in the cervical mucus of animals treated with Ramses Jelly, and that these spermatozoa often possessed forward progression. When 0.1% RS gel was used, no significant differences were found in spermatozoal numbers and motility in the vagina and the cervix as compared with those observed during the use of Ramses Jelly. Since Ramses Jelly contains 5% nonoxynol-9, it can be estimated that RS is - 50-fold more potent than nonoxynol-9 in vivo. This value is similar to the relative potency found in vitro.3-5 Therefore, the present results demonstrate that the enhanced potency of RS previously seen in vitro is also found in Fertility and Sterility
5 vivo, at least in the nonhuman primate, and support further development and clinical evaluation of this compound. Acknowledgments. We thank Dr. Keith Walker, Dr. Lih Yang Lin, and Ms. Alice Tinker for compound synthesis, formulation, and statistical analyses, rerpectively. REFERENCES 1. Zaneveld LJD, Bhattacharyya AK, Kim DS, Schumacher GFB, Beluhan Z: Primate model for the evaluation of vaginal contraceptives. Am J Obstet Gynecol 129:368, Moghissi KS: Sperm migration in the female genital tract. In Vaginal Contraception: New Developments, Edited by GI Zatuchni, AJ Sobrero, JJ Speidel, JJ Sciarra. Hagerstown, Harper & Row, 1979, p Vickery BH, Walker KAM, Freymark F: Studies on the actions of a new non-surfactant spermicide. Presented at the Twenty-Ninth Annual Meeting of the Society for Gynecological Investigation, March 24 to 27, 1982, Dallas, Texas. Published by the Society for Gynecological Investigation, in the Program of Scientific Sessions, p Goodpasture JC, Bergstrom K, Vickery BH: Comparison of the spermicidal efficacy of two nonoxynol-containing preparations with that of a new agent, using a novel "no mix" assay. Contracept Deliv Syst 3:167, Overstreet JW, Katz DF, Brazil CK, Vickery BH: Assessment of a new spermicidal agent against human sperm in vitro. Contracept Deliv Syst 3:144, Zatuchni B, Hahn DW, Zaneveld LJD: Postcoital, vaginal, spermicidal potency of formulations: the Macaca arctoides (stumptailed macaque) as animal model. Fertil Steril 35:683, Wilks J: Endocrine characterization of the menstrual cycle of the stumptailed monkey (Macaca arctoides). BioI Reprod 16:474, Conover WJ: Practical Nonparametric Statistics. New York, John Wiley & Sons, 1980, p 327 Zaneveld et ai. A new vaginal contraceptive 459
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