A prospective randomized study to assess the clinical efficacy of gonadotrophins administered subcutaneously and intramuscularly
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1 Human Reproduction vol.13 no.4 pp , 1998 A prospective randomized study to assess the clinical efficacy of gonadotrophins administered subcutaneously and intramuscularly Lawrence Engmann 1,5, Adel Shaker 1,2, Emma White 1, Jinan S.Bekir 1, Howard S.Jacobs 1,3 and Seang Lin Tan 1,4 1 The London Women s Clinic, 115 Harley Street, London W1, 2 BMI Ross Hall Hospital, Glasgow, 3 Department of Reproductive Endocrinology, University College London Medical School, The Middlesex Hospital, London, W1, UK and 4 Department of Obstetrics and Gynecology, Royal Victoria Hospital, McGill University, Montreal, Canada 5 To whom correspondence should be addressed The purpose of this study was to compare the clinical efficacy of gonadotrophins administered s.c. or i.m., in a prospective randomized study of women undergoing invitro fertilization (IVF) treatment at a tertiary referral centre. In all, 71 patients undergoing a total of 162 IVF treatment cycles were randomized to receive either s.c. (n 41) or i.m. (n 30) administration of gonadotrophins. Up to three cycles of IVF were assessed for each patient. The main outcome measures were the number of oocytes retrieved, the total amount of gonadotrophins used, the number of follicles recruited and the cumulative pregnancy and live birth rates. The mean number of oocytes retrieved was 10.5 for each group. The number of days of stimulation was significantly shorter for the s.c. group ( days, mean SD) than the i.m. group ( days). The cumulative conception and live birth rates after three cycles of treatment were similar between the two groups. Our results suggest that the clinical efficacy of s.c. and i.m. administration of gonadotrophins is comparable. Both routes are well tolerated by patients. Key words: clinical efficacy/gonadotrophins/intramuscular/invitro fertilization/subcutaneous Introduction Although in-vitro fertilization (IVF) is a successful treatment for many forms of infertility (Tan et al., 1990b; Hull et al., 1992), it is physically and emotionally stressful. Improvements in IVF treatment protocols have led to its simplification, making it less demanding on patients and thereby encouraging more patients to undertake multiple treatments (Tan, 1994). Self-administration of medications is more convenient and less time-consuming since it allows the patient to make fewer visits to the clinic or hospital for injections. Gonadotrophinreleasing hormone (GnRH) agonists are administered either as nasal spray or s.c. injection which makes self-administration feasible. Urinary-derived gonadotrophin preparations are generally recommended to be given i.m. because of the presence of non-specific urinary proteins (Guidice et al., 1994) which may lead to unacceptable local side-effects if administered s.c. Although s.c. administration of gonadotrophins has been reported to be safe and effective (Nakamura et al., 1989; Saal et al., 1991; Jones and Darne, 1993; Howles et al., 1994; Wikland et al., 1994), previous studies have largely been in men with hypogonadotrophic hypogonadism (Saal et al., 1991; Jones and Darne, 1993) or involved the use of highly purified urinary preparations (Howles et al., 1994; Wikland et al., 1994). There are few data about the use of conventional urinary gonadotrophins administered s.c. in women undergoing IVF. The objective of the study was to investigate the efficacy of s.c. administration of urinary gonadotrophins as compared with i.m. administration. Materials and methods Patients The study was a single-centre prospective randomized trial. The subjects were recruited between June 1994 and October The last patient completed her third cycle of IVF in August Patients attending the Assisted Conception Clinic at The London Women s Clinic for IVF and fulfilling specific inclusion criteria (see below) were recruited into the study. Patients were recruited to undergo at least one stimulation cycle with a maximum of three cycles of treatment within a year. Ethical approval was obtained from the Research Ethics committee of the clinic, and each subject gave written informed consent before participating in the study. Eligible patients were randomly allocated to the s.c. and i.m. groups in a ratio 3:2 after consultation with the statistician. The urinary gonadotrophin used was Normegon (Organon, Cambridge, UK), which was supplied as a lyophilized powder in ampoules, each containing 75 IU of follicle stimulating hormone (FSH) and 25 IU luteinizing hormone (LH) activity. Up to 5 ampoules of Normegon were dissolved in 1 ml of solvent. The reconstituted solution was administered i.m. into the buttocks or s.c. into the thigh. Inclusion criteria were as follows: patients aged years at the time of screening, cause of infertility treatable by IVF, duration of infertility of at least a year, normal early follicular phase serum FSH concentrations ( 10 IU/l) and good physical and mental health. Exclusion criteria were: male factor infertility according to the World Health Organization guidelines, known contraindications to the use of GnRH agonists, human menopausal gonadotrophin (HMG) and human chorionic gonadotrophin (HCG); and previous administration of HMG and/or HCG within 3 months of screening. Treatment protocol All patients had s.c. administration of the GnRH agonist, buserelin acetate (Suprefact, Hoechst, Hounslow, UK), in a dose of 500 µg/ day, starting from day 2 of the menstrual cycle until pituitary 836 European Society for Human Reproduction and Embryology
2 Clinical efficacy of i.m. and s.c. use of urinary gonadotrophins suppression was achieved. An ultrasound scan was performed on day 15 to confirm that pituitary suppression had occurred, as shown by the absence of follicular activity and endometrial thickness 5 mm. Once pituitary suppression was achieved, the administration of Normegon was commenced and the dose of buserelin reduced to 200 µg/day. The latter was continued until, and including, the day of HCG (Pregnyl; Organon) administration. The standard starting dose of Normegon was 2 5 ampoules ( IU FSH activity) per day depending on the patient s age, previous response, basal serum FSH levels and presence or absence of polycystic ovaries (PCO) on ultrasound assessment. A nurse co-ordinator gave all the injections in the first cycle, but in subsequent cycles the s.c. patients administered the injections themselves. Monitoring of follicular growth was achieved with serial ultrasound scans and the dose of HMG adjusted according to follicular response. When two or three leading follicles were 18 mm in diameter, HCG in a dose of IU was administered as a single i.m. injection. Transvaginal ultrasound-directed oocyte retrieval was performed ~36 h after HCG administration and embryo transfer took place 48 h after oocyte retrieval. The methods for oocyte retrieval and embryo transfer have been described previously (Tan et al., 1990a). Progesterone pessaries, 400 mg twice daily (Cyclogest; Hoechst, Hounslow, UK) were given as luteal support, starting from the day of embryo transfer until 16 days thereafter. Fresh embryo transfer was not offered to patients who had serum oestradiol levels pmol/l on the day of HCG administration, or oestradiol between and pmol/l with 15 oocytes retrieved because of the increased risk of ovarian hyperstimulation syndrome (OHSS). All embryos for these patients were cryopreserved and transferred in a subsequent cycle. Efficacy endpoints Patient characteristics such as age, number of previous IVF attempts, duration and cause of infertility were recorded. The primary efficacy endpoint was the number of oocytes retrieved. Additional efficiency endpoints were the total number of ampoules of Normegon administered and the duration of treatment. Secondary efficacy endpoints were number of follicles, number of transferable embryos, cumulative embryo score and cumulative pregnancy and live birth rates. Cumulative embryo score was calculated by assessing the number of blastomeres and morphological grade of each embryo. The morphological grade of the embryo was multiplied by the number of blastomeres to produce a quality score for each embryo. The scores of all embryos transferred per patient were added to obtain the cumulative embryo score (Steer et al., 1992). Implantation rate was defined as the number of viable fetuses, as assessed by ultrasound at 6 weeks gestation, divided by the number of embryos transferred for each subject. Local tolerance assessment Patients were asked to record daily, on a diary and tolerance card, any local side-effects experienced during the preceding period after the last injection. The local side-effects, redness, itching, swelling, pain and bruising were scored as none, mild, moderate or severe. The duration of gonadotrophin administration was also noted. Patients understood that they could withdraw from the study at any stage of their treatment according to how they perceived the severity of their symptoms and signs without compromising their chances of successful outcome. If they felt they could no longer carry on with s.c. administration, patients were allowed to drop out of the study and cross over to the i.m. route of administration during the treatment or in the subsequent cycle. Statistical analysis All data were entered into a computer using an SPSS statistical package for data analysis. Data presented are mean SD and range. The Mann Whitney U-test, χ 2 -analysis were used, as appropriate. A value of P 0.05 was considered significant. Cumulative conception and live birth rates were calculated by the life-table method (Kaplan and Meier, 1958; Cramer et al., 1979). Therefore, analysis of the cumulative conception rate included only cycles up to the first pregnancy while analysis of the cumulative live birth rate was performed on all treatment cycles leading to the first live birth. The rates were expressed as percentage probabilities with 95% confidence intervals (CI). The rate of side-effects was determined as a percentage for each patient by dividing the number of injections that produced sideeffects by the total number of injections received by the patient. The rate and severity of each local side-effect between the i.m. and s.c. groups were compared using Mann Whitney U-test. Results A total of 74 subjects were initially randomized to receive s.c. Normegon and i.m. Normegon in a 3:2 ratio. However, 71 subjects actually entered the study and were treated for a total of 164 cycles. Three patients withdrew from the study before commencing treatment. In total, 41 subjects were allocated to s.c. Normegon and 30 to i.m. Normegon. A total of 96 cycles was undertaken by patients in the s.c. group and 66 cycles for the i.m. group. Two patients used a different HMG instead of Normegon in the third cycle and were omitted from the analysis of the third cycle. Analyses of efficacy were therefore based on the 71 patients recruited and 162 cycles. Five patients failed to complete all three cycles. Two of these patients achieved spontaneous pregnancy after the first and second cycles respectively, while three patients did not undertake their third cycles because of social reasons. Analyses of local sideeffect were based on 70 patients and a total of 154 cycles. Eight cards were incompletely filled and so were excluded from the analyses of side-effects. The s.c. and i.m. groups were comparable with respect to age (35 and 34.9 years respectively), duration of infertility (4.7 and 3.7 years respectively), baseline FSH level (5.5 U/l both groups), body mass index (23.7 and 22.4 kg/m 2 respectively) and cause of infertility. There were no cycles abandoned in the s.c. group while one first cycle and one second cycle were abandoned in the i.m. group because of poor ovarian response. Since there were no significant differences between the two groups of patients in the second and third cycles of treatment, only the efficacy parameters of the first cycle and overall data are presented in Tables I and II. There was no significant difference in the mean total number of ampoules of Normegon used for ovarian stimulation in all the three cycles for the s.c. (39.8, 46.6 and 55.6 ampoules) and i.m. groups (43.9, 49.9 and 58 ampoules). There was also no significant difference in the duration of ovarian stimulation in the three cycles for women receiving i.m. gonadotrophins (13.1, 12.1 and 12 days) compared with s.c. gonadotrophins (11.8, 11.5 and 11.7 days). However, when the results of all the three cycles were analysed together, the duration of ovarian stimulation was significantly 837
3 L.Engmann et al. Table I. Efficacy parameters (first cycle) a,b Parameter Subcutaneous Intramuscular (n 41) (n 30) Total no. of ampoules (12 86) (15 109) Days of Normegon administration (8 17) (9 19) Total no. of follicles (3 37) (3 31) No. of follicles 14 mm in diameter (2 17) (3 14) No. of follicles mm in diameter (0 12) (0 10) Oestradiol level on day of HCG (pmol/l) ( ) ( ) No. of oocytes retrieved (1 26) (2 20) No. of viable oocytes (1 21) (0 16) Endometrial thickness on day of HCG (mm) ( ) ( ) Fertilization rate (%) (0 100) (0 100) Cleavage rate (%) (50 100) (0 100) Total no. of embryos produced (0 11) (0 14) No. of embryos transferred (0 3) (0 3) No. of embryos frozen (0 5) (0 6) Cumulative embryo score (10 66) (12 44) a Values are means SD with ranges in parentheses. b No significant difference in any result. HCG human chorionic gonadotrophin. Table II. Efficacy parameters (all cycles) a Parameter Subcutaneous Intramuscular (n 96) (n 66) Total no. of ampoules (12 112) (12 118) Days of Normegon administration (8 17) b (8 19) Total no. of follicles (3 37) (3 31) No. of follicles 14 mm in diameter (2 19) (1 14) No. of follicles mm in diameter (0 12) (0 11) Oestradiol level on day of HCG (pmol/l) ( ) ( ) No. of oocytes retrieved (1 26) (2 22) No. of viable oocytes retrieved (1 23) (0 16) Endometrial thickness on day of HCG (mm) ( ) (6.8 19) Fertilization rate (%) (0 100) (0 100) Cleavage rate (%) (25 100) (0 100) Total no. of embryos produced (1 16) (1 14) No. of embryos transferred (0 3) (0 3) No. of embryos frozen (0 10) (0 6) Cumulative embryo score (4 66) (6 51) a Values are means SD with ranges in parentheses. b P HCG human chorionic gonadotrophin. longer in the women receiving i.m. gonadotrophins ( days) compared with those receiving s.c. gonadotrophins ( days) (P 0.05). Overall, the mean numbers of oocytes retrieved and embryos produced were similar in both groups. There were no significant differences in the cumulative conception or live birth rates between the two groups of patients (Table III). There were no significant differences in the implantation rates between the s.c. and i.m. groups (11, 10 and 8% versus 20, 15 and 10%) in all the three cycles respectively. Overall, the least commonly reported side-effect was itching, although there was a significantly higher incidence (P 0.01) of mild itching in the s.c. group (10.9%) compared with the i.m. group (0.8%). Pain was the most commonly reported sideeffect (70.6% s.c. and 52.9% i.m.), and there were significant differences in the incidence of moderate and severe pain (both P 0.01) between the s.c. and i.m. groups. The rate of redness and swelling were higher (both P 0.01) for women who 838 Table III. Cumulative conception and live birth rates a,b Parameter Cycle Subcutaneous Intramuscular (n 96) (n 66) Cumulative conception rate 1st 24.7 ( ) 35.1 ( ) per cycle started (%) 2nd 35.5 ( ) 50.4 ( ) 3rd 59.3 ( ) 64.5 ( ) Cumulative live birth rate 1st 20.0 ( ) 24.6 ( ) per cycle started (%) 2nd 31.0 ( ) 39.7 ( ) 3rd 47.0 ( ) 53.9 ( ) a Values are percentage probabilities with 95% confidence intervals in parentheses. b No significant difference between the two groups. had s.c. injection (73.7 and 56.6% respectively) compared with those who had i.m. injection (17.9 and 6.5% respectively). There were no significant differences in the incidence of bruising between the two groups. Most of the symptoms were
4 Clinical efficacy of i.m. and s.c. use of urinary gonadotrophins classified as mild. None of the patients dropped out of the study because of side-effects and those who had three cycles of treatment continued with the same route of administration in all the cycles. Discussion Ovarian stimulation with gonadotrophins has been used successfully for 30 years. However, one disadvantage of most of the currently available urinary gonadotrophins apart from the highly purified urinary products is the recommendation that they should be administered i.m. Subcutaneous administration of medications during IVF treatment cycles allows selfadministration which is much more convenient to the patient and simplifies treatment. Other clinical developments have allowed the simplification of IVF treatment procedures (Abdalla et al., 1989; Tan et al., 1992a; Tan, 1994). Although the use of s.c. gonadotrophins has been reported in the literature, most of these studies were not randomized. The administration of s.c. gonadotrophins in male patients with hypogonadotrophic hypogonadism was found to be effective in stimulation of steroidogenesis without adverse effects (Saal et al., 1991; Jones and Darne, 1993). Previous studies of ovulation induction by the administration of s.c. pulsatile gonadotrophins has shown successful ovulation and good pregnancy rates (Nakamura et al., 1989). In a retrospective analysis, Shomoutziguer et al. (1996) assessed 524 patients who had 1276 cycles of IVF using s.c. urinary gonadotrophins. The study showed that s.c. administration was safe and effective and clinical pregnancy rates per cycle of 18.2% were achieved. A number of other studies, which were not randomized, have shown that highly purified urinary gonadotrophins are as effective when given s.c. in ovarian stimulation for IVF treatment (Howles et al., 1994; Wikland et al., 1994). This present study is the first randomized study, as far as we are aware, to compare the efficacy of s.c. and i.m. administration of human urinary gonadotrophins. The results suggest that gonadotrophins produce comparable results whether they are administered s.c. or i.m. Several studies have shown that the main pharmacokinetic variables are bioequivalent regardless of the route of administration (Le Cotonnec et al., 1993; Huisman et al., 1997). However, Dobbs et al. (1994) found a shorter time interval between administration and peak serum hormone levels after i.m. administration of gonadotrophin. This is contrary to the clinical efficacy observations made in this study. A significantly shorter duration of stimulation was required for ovarian stimulation in patients using the s.c. route of administration. Nevertheless, serum oestradiol levels on the day of HCG administration and the number of oocytes retrieved were similar in the two groups. This is in accordance with the findings of a recent study using recombinant FSH (Out et al., 1997). The conflicting bioequivalence reports and the findings in clinical efficacy studies may be the result of the fact that the bioequivalence studies were performed after single administration of gonadotrophins. Such studies, although useful, do not provide adequate information about the cumulative effect of serial administration of gonadotrophins upon pharmacokinetic properties as well as ovarian response. The cumulative embryo score, implantation rates and cumulative pregnancy rates, which are the main outcome variables, were similar in the two groups. The cumulative embryo score is one of the methods used for selecting embryos for transfer and may be related to the outcome of a cycle (Steer et al., 1992). The cumulative conception and live birth rates are useful in assessing results following multiple treatment cycles and account for the entire cohort of patients thereby providing a good measure of ultimate success (Tan et al., 1992b). Cumulative conception and live birth rates between the two groups were comparable and the results compare favourably with other published results of cumulative conception and live birth rates (Tan et al., 1992b, 1994). The rates of some of the local side-effects were higher after s.c. gonadotrophins compared with i.m. gonadotrophins. However, most of these were classified as mild. A high incidence of post-injection pain was reported by patients in both the s.c. and i.m. groups. The relatively high incidence of pain reported in the i.m. group in this study is in accordance with a recent study performed by Verhoeff et al. (1997). They reported that the incidence of pain after i.m. injection was 45 49%, which is comparable with that of this study of 52.9%. It is interesting to note that none of the patients withdrew from the study because of side-effects and even those women who had local side-effects in the first cycle continued with the same route of administration in subsequent cycles. This further suggests that the symptoms were well tolerated. In conclusion, s.c. administration of gonadotrophins is as efficacious as the i.m. route of administration. Although it may be associated with more local side-effects it is well tolerated by patients. The s.c. route of administration of most urinary gonadotrophins is not licensed. Nevertheless, in view of the ease and possibility of self-administration as well as the fact that it is clinically as efficacious, the s.c. route should be considered for wider clinical usage. Acknowledgements The authors wish to acknowledge Ms Patricia Doyle for her help with calculation of the cumulative conception rates, Dr Povilas Sladkevicius for his comments on the manuscript and the doctors and nurses at the London Women s Clinic for their help with recruitment of patients. We also wish to thank Mr Tim Garnett and Mr Douglas Gibb of Organon, UK for supplying the Normegon for the study and financial support for the research nurse coordinator. References Abdalla, H.I., Baker, R., Leonard, T. et al. (1989) Timed oocyte collection in an assisted conception program using GnRH analogue. Hum. Reprod., 4, Cramer, D.W., Walker, A.M. and Schiff, I. (1979) Statistical methods in evaluating the outcome of infertility therapy. Fertil. Steril., 32, Dobbs, K.E., Dumesic, D.A., Dumesic, J.A. and Shapiro, S.S. (1994) Differences in serum follicle-stimulating hormone uptake after intramuscular and subcutaneous human menopausal gonadotropin injection. Fertil. Steril., 62, Giudice, E., Crisci, C., Eshkol, A. and Papoian, R. (1994) Composition of commercial gonadotropin preparations extracted from human post- 839
5 L.Engmann et al. menopausal urine: characterization of non-gonadotropin proteins. Hum. Reprod., 9, Howles, C.M., Loumaye, E., Giroud, D. and Luyet, G. (1994) Multiple follicular development and ovarian steroidogenesis following subcutaneous administration of a highly purified urinary FSH preparation in pituitary desensitized women undergoing IVF: a multicentre European phase III study. Hum. Reprod., 9, Huisman, J.A.M., Paulussen, R.J.A. and Geurts, T.B.P. (1997) Assessment of bioequivalence after subcutaneous and intramuscular administration of urinary gonadotrophins. Hum. Reprod., 12, Hull, M.G.R., Eddowes, H.A., Fahy, U. et al. (1992) Expectations of assisted conception for infertility. Br. Med. J., 304, Jones, T.H. and Darne, J.F. (1993) Self-administered subcutaneous human menopausal gonadotropin for the stimulation of testicular growth and the initiation of spermatogenesis in hypogonadotropic hypogonadism. Clin. Endocrinol., 38, Kaplan, E.L. and Meier, P. (1958) Non parametric estimation from incomplete observations. J. Am. Statist. Assoc., 53, Le Cotonnec, J-Y., Porchet, H.C., Beltrami, V. and Howles, C. (1993) Comparative pharmacokinetics of two urinary human follicle stimulating hormone preparations in healthy female and male volunteers. Hum. Reprod., 8, Nakamura, Y., Yoshimura, Y., Yamada, H. et al. (1989) Clinical experience in the induction of ovulation and pregnancy with pulsatile subcutaneous administration of human menopausal gonadotropin: a low incidence of multiple pregnancy. Fertil. Steril., 51, Out, H.J., Reimitz, P.E. and Coelingh Bennik, H.J.T. (1997) A prospective, randomized study to assess the tolerance and efficacy of intramuscular and subcutaneous administration of recombinant follicle-stimulating hormone (Puregon). Fertil. Steril., 67, Saal, W., Happ, J., Cordes, U. et al. (1991) Subcutaneous gonadotropin therapy in male patients with hypogonadotropic hypogonadism. Fertil. Steril., 56, Schmoutziguer, A.P.E., Van Kooy, R.J., Koudstaal, J. et al. (1996) Subcutaneous administration of urinary gonadotropins efficacy and safety in in-vitro fertilization. J. Obstet. Gynecol., 16, Steer, C.V., Mills, C.L., Tan, S.L. et al. (1992) The cumulative embryo score: a predictive embryo scoring technique to select the optimal number of embryos to transfer in an in-vitro fertilization and embryo transfer program. Hum. Reprod., 7, Tan, S.L. (1994) Simplifying in vitro fertilization therapy. Curr. Opin. Obstet. Gynecol., 6, Tan, S.L., Bennet, S. and Parsons, J. (1990a) Surgical techniques for oocyte recovery and embryo transfer. Br. Med. Bull., 46, Tan, S.L, Steer, C., Royton, P. et al. (1990b) Conception rates and in vitro fertilization. Lancet, 335, 299. Tan, S.L., Balen, A., El-Hussein, E. et al. (1992a) A prospective randomized study of the optimum timing of human chorionic gonadotropin administration after pituitary desensitization in in vitro fertilization. Fertil. Steril., 57, Tan, S.L., Royton, P., Campbell, S. et al. (1992b) Cumulative conception and live birth rates after in vitro fertilization. Lancet, 339, Tan, S.L., Maconochie, N., Doyle, P. et al. (1994) Cumulative conception and live birth rates after in vitro fertilization with, and without, the use of the long, short and ultrashort regimens of the luteinizing releasing hormone agonist, buserelin. Am. J. Obstet. Gynecol., 171, Verhoeff, A., Schmoutziguer, A.P.E. and Doesburg, W.H. (1997) A randomized study on the effects of intramuscular injections with urinary gonadotrophins (Humegon or Pergonal) on pain, local redness and fever in infertile women opting for in-vitro fertilization. Hum. Reprod., 12, Wikland, M., Borg, J., Hamberg, L. and Svalander, P. (1994) Simplification of IVF: minimal monitoring and the use of subcutaneous highly purified FSH administration for ovulation induction. Hum. Reprod., 9, Received on August 1, 1997; accepted on January 13,
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