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1 RBMOnline - Vol 6. No Reproductive BioMedicine Online; on web 13 March 2003 Article Pregnancy after administration of high dose recombinant human LH alone to support final stages of follicular maturation in a woman with long-standing hypogonadotrophic hypogonadism Professor Juan Balasch Juan Balasch obtained his MD degree (1974) and the speciality degree in Obstetrics and Gynaecology (1977) at the Faculty of Medicine-Hospital Clínic, University of Barcelona in Spain. The PhD degree was granted to him at the same University in At present he is full professor in Obstetrics and Gynaecology and Head of the Fertility Unit at the Faculty of Medicine-Hospital Clinic, University of Barcelona. Professor Balasch is Past President of the Spanish Fertility Society and has more than 150 publications in international journals and books; in a series of studies he and his team developed a new hypothesis on the pathogenesis of the ovarian hyperstimulation syndrome. He serves as ad-hoc reviewer or is in the Editorial Board of different international journals dealing with fertility, gynaecological endocrinology, and human reproduction. Professor Balasch s current research interests include assisted reproduction, repeated abortion, implantation failure, and ovarian (hyper)stimulation. Dr Francisco Fábregues was born in Amposta (Tarragona), Spain in In 1983 obtained his medical degree and in 1998 his PhD at the Faculty of Medicine, University of Barcelona in Spain. He received the qualification in Obstetrics and Gynaecology in After completing his obstetrics/gynaecology residency in the Hospital Clínic of Barcelona in 1992, he joined the Fertility and Assisted Reproduction unit where he is currently senior specialist. Current clinical research interests include studies on ovulation induction and ovarian hyperstimulation. He has in excess of 60 publications to his name in international journals. Dr Francisco Fábregues Juan Balasch 1,2, Francisco Fábregues 1 1 Institut Clínic of Gynecology, Obstetrics and Neonatology, Faculty of Medicine-University of Barcelona, Hospital Clínic-Institut d Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain 2 Correspondence: Institut Clínic of Gynecology, Obstetrics and Neonatology, Hospital Clínic, C/Casanova 143, Barcelona, Spain. Fax: ; jbalasch@medicina.ub.es Abstract Traditionally, the roles of LH in folliculogenesis have been considered to be limited to stimulating theca cells androgen production, triggering ovulation and supporting the corpus luteum. However, in the late stages of follicle development, granulosa cells become receptive to LH stimulation and LH becomes capable of exerting its actions on both theca cells and granulosa cells. Thus, it has been postulated that once an appropriate (i.e. LH-responsive) stage of follicular development has been achieved in response to treatment with FSH, there are theoretical grounds for reducing or completely withdrawing FSH and maintaining tonic stimulation of the dominant follicle with exogenous LH. This hypothesis was tested in a woman with long-standing hypogonadotrophic hypogonadism, which is the best and only true model to investigate correctly any LH hypothesis. Ovulation induction treatment was carried out with daily s.c. injections of 150 IU recombinant human FSH (rhfsh) (increased to 225 IU daily on stimulation day 15) and 375 IU recombinant human LH (rhlh). When a 14-mm follicle was identified on stimulation day 26, rhfsh was discontinued and from treatment days 26 to 29 the patient was given only rhlh at the above-mentioned dose of 375 IU/day. On treatment day 30, the single dominant follicle measured 22 mm in diameter and oestradiol serum concentration was 148 pg/ml. Thus, an injection of 10,000 IU i.m. human chorionic gonadotrophin was given and sexual intercourse was advised. The patient conceived and a viable singleton intrauterine pregnancy was obtained. Keywords: follicular maturation, FSH, LH, ovulation induction, recombinant gonadotrophins 427

2 428 Introduction The most important principle in ovulation induction is to provide as close as possible physiological restoration of cyclical ovarian function. In particular, the aim should be to achieve the ovulation of a single follicle. Multifollicular development, however, has been a frequent complication of ovulation induction with urinary human menopausal gonaodotropin (HMG), the most widely used exogenous gonadotrophin preparation since its introduction in the early 1970s (Fauser and Van Heusden, 1997). The use of HMG [theoretically containing similar amounts (75 IU) of FSH and LH] has been based on classic experiments in hypophysectomized rats treated with more or less pure forms of FSH and LH obtained from animal pituitary glands and suggesting that both hormones were necessary to stimulate pre-ovulatory follicular development and synthesis of oestrogen (Fevold, 1941; Greep et al., 1942; Short, 1962). Thus it has been generally accepted that satisfactory clinical results may be obtained irrespective of the LH content of the preparation, provided that adequate FSH is administered. This means that clinicians usually rely on the use of urinary gonadotrophin extracts containing FSH with varying amounts of LH, making it difficult to alter selectively the dose of either gonadotrophin, while experimentalists resorted to scarce and expensive pituitary preparations of varying purity (Hillier, 2001). The breakthrough came with the recent availability of recombinant human FSH (rhfsh) and LH (rhlh), which are truly monohormonal products and hence provided powerful new tools in experimental endocrinology, thus allowing a clear definition of the individual roles of FSH and LH on follicular development in humans (Hillier, 1994, 2001). The importance of FSH in control of ovarian function during the early- through mid-follicular phase of the menstrual cycle is beyond question. FSH provides the primary stimulus for growth and differentiation of the granulosa layer in the preovulatory follicle (Hillier, 1994; Zeleznik, 2001). This is consistent with current clinical experience with the use of FSH-only products in ovulation induction regimens (Balasch and Fábregues, 2002; Shoham, 2002). By mid-follicular phase, however, there is a gradual increase in oestradiol serum concentrations in association with a progressive fall in FSH concentrations; this notwithstanding, the developing follicle continues to mature. This indicates that there are specific functional changes in the FSH-stimulated follicle that render it less dependent on FSH while follicular dependence on LH is increasing. Thus, LH activity administration in the mid- to late-follicular phase during ovarian stimulation for assisted reproduction has been proposed to enhance ovarian response and optimize treatment in patients having a profound LH down-regulation or requirement for excessive exogenous FSH (Lisi et al., 2002), or even in a general assisted reproduction treatment population (Commenges-Ducos et al., 2002; Filicori et al., 2002). A hallmark action of FSH during pre-ovulatory follicular development is the induction of LH receptors on granulosa cells (Hillier, 1994; Zeleznik, 2001). Thus, while granulosa cells from early antral follicles are only responsive to FSH, granulosa cells from FSH-stimulated follicles are responsive to either FSH or LH. It has therefore been stressed that once an appropriate (i.e. LH-responsive) stage of follicular development has been achieved in response to treatment with FSH, there are theoretical grounds for reducing or completely withdrawing FSH and maintaining tonic stimulation of the dominant follicle with exogenous LH (Hillier, 1994, 2000). A recent pilot study (Sullivan et al., 1999) conducted in humans using rhfsh and rhlh supports this possibility. However, this previous study was carried out in normal ovulatory women undergoing pituitary suppression with s.c. leuprolide acetate. In addition, rhlh was given only for a 2-day period once rhfsh treatment was terminated when a 14-mm follicle was identified by ultrasound (Sullivan et al., 1999). It is well accepted that the best and only true model to investigate any LH hypothesis correctly is the hypogonadotrophic woman who may be totally LH deficient, in contrast with down-regulated women with s.c. gonadotrophin-releasing hormone (GnRH) agonist, where LH is not completely absent (Balasch and Fábregues, 2002; Shoham, 2002). This report describes a patient with longstanding hypogonadotrophic hypogonadism who became pregnant during an ovulation induction cycle with rhfsh and rhlh where rhlh alone was administered during the last 4 days of follicular maturation. Materials and methods A healthy female aged 34 years was referred to the infertility unit because of a wish for a child. She was first seen at another institution at the age of 18 years and the clinical presentation strongly suggested the diagnosis of Kallmann s syndrome in that she had primary amenorrhoea with hypogonadotrophic hypogonadism and anosmia. There were no other congenital defects, and plain skull X-rays and computed tomography of the pituitary gland were normal. Chromosomal analysis showed a normal female karyotype. Following diagnosis, the patient commenced oestrogen and progestagen replacement therapy. Six months before being referred to the clinic, the patient underwent an ovulation induction treatment cycle with i.m. HMG but the cycle was cancelled because of no ultrasound evidence (i.e. no follicle >10 mm in diameter) of ovarian response after 28 days of gonadotrophin administration at the following daily dose: 150 IU on days 1 14 of ovarian stimulation, 225 IU on days and 300 IU on days After this failed ovulation induction cycle the patient restarted hormone replacement treatment. At the time of her presentation to the centre, a physical examination revealed mild obesity (body mass index 26.8 kg/m 2 ) and normal general physical examination. Anosmia was confirmed. General medical history, routine urine/serum laboratory evaluation (including haematology, liver and kidney function) and the following tests were normal: hysterosalpingogram (normal uterine configuration but reduced uterine volume and patent Fallopian tubes) and serum thyroid hormone, growth hormone, prolactin, and adrenal hormone concentrations. A semen analysis of the patient s partner was normal. Transvaginal ultrasound scanning revealed the presence of small inactive ovaries (right ovarian volume 2.45 cm 3, left ovarian volume 1.88 cm 3 ). Ovulation induction was thus indicated. The treatment protocol with rhfsh and rhlh was approved by the Investigation and Ethics Committee of the hospital, and the patient gave informed consent.

3 For the specific purpose of this study, two serum aliquots were obtained from each blood sample. Oestradiol was measured daily in one of the serum aliquots for clinical monitoring, and the second aliquot was stored at 20ºC for later measurements of FSH, LH, inhibin A, inhibin B and androstenedione. Frozen serum samples were examined in one run. Hormones were measured using commercially available kits as reported previously (Balasch et al., 1998, 2001; Peñarrubia et al., 2000). Ultrasound scans were performed using a 5 mhz vaginal transducer attached to an Aloka sector scanner (Model SSD-620; Aloka Co., Tokyo, Japan). Results The patient stopped hormonal replacement therapy 3 months before undergoing ovulation induction in the infertility clinic. Three months later, the serum FSH concentration was 1.0 IU/l, the LH concentration was 0.9 IU/l and the oestradiol concentration was <10 pg/ml. Ovulation induction treatment was started with daily s.c. injections of 150 IU rhfsh (Gonalf; Serono S.A., Madrid, Spain) and 375 IU rhlh (Luveris; Serono S.A.). The dose of rhlh was chosen according to the advice of Hillier (2000). Treatment was monitored with transvaginal pelvic ultrasound and blood samples for the determination of oestradiol, FSH, LH, inhibin A, inhibin B, and androstenedione (Figure 1). As on stimulation day 15 no ovarian response could be seen, the daily dose of rhfsh was increased to 225 IU (Figure 1). On stimulation day 21, a growing follicle measuring 11 mm in diameter was observed on ultrasonography and the dose of rhfsh and rhlh was continued until a 14-mm follicle was identified on stimulation day 26. At this time, rhfsh was discontinued and from treatment days 26 to 29 the patient was given only rhlh at the above-mentioned dose of 375 IU/day (Figure 1). On treatment day 30, the single dominant follicle measured 22 mm in diameter and oestradiol serum concentration was 148 pg/ml. Thus, an injection of 10,000 IU i.m. human chorionic gonadotrophin (HCG) (Profasi; Serono S.A.) was administered and the patient was advised to have sexual intercourse on the evening of the HCG injection and on the following day. Micronized vaginal progesterone (300 mg/day; Progeffik, Laboratorios Effik, Madrid, Spain) was given for luteal phase support. rhfsh and rhlh are available, it is possible to develop improved clinical strategies for stimulating ovarian function. The challenge is to tailor therapy with FSH and LH, alone or in combination. Traditionally, the roles of LH in folliculogenesis have been considered to be limited to stimulating theca cells androgen production, triggering ovulation, and supporting the corpus luteum. However, in the late stages of follicle development granulosa cells become receptive to LH stimulation and LH becomes capable of exerting its actions on both theca cells and granulosa cells (Hillier, 1994, 2001). Recent findings indicate that the process of pre-ovulatory follicular development may be regulated by a single intracellular message (camp), which, The patient conceived and a pregnancy test performed 20 days later was positive. Subsequent ultrasound examination confirmed a viable singleton intrauterine pregnancy. The pregnancy is, at the time of writing, at 33 weeks gestation and it is progressing uneventfully. Discussion According to current concepts of the roles of FSH and LH in folliculogenesis, follicular responsiveness to FSH and LH is developmentally regulated (Hillier, 1994, 2001). Although it is a continuum, the life-cycle of a pre-ovulatory follicle can be broken down into three successive phases: (i) initiation, which occurs from birth to senescence independent of gonadotrophic support; (ii) FSH-dependent progression, requiring tonic stimulation by FSH; and (iii) LH-responsive maturation, when FSH-induced genes fall under LH control, leading to final follicular maturation and ovulation (Hillier, 2001). Therefore, on the basis of physiology, now that pharmaceutically pure Figure 1. rhfsh and rhlh dose regimens administered, serum FSH and LH concentrations, follicular development and serum ovarian hormone concentrations. 429

4 430 in turn, is controlled in succession by two different messengers, FSH and LH (Zeleznik, 2001). In fact, most of the physiological actions of FSH on granulosa cells, including stimulation of the aromatase system, can be exerted by LH once its receptors are expressed (Hillier, 1994, 2001; Zeleznik, 2001). As would be predicted by the common intracellular camp pathway, granulosa cells from FSH-stimulated follicles respond similarly to both FSH and LH, and moreover, at nonsaturating concentrations of FSH and LH, the responses are additive (Zeleznik, 2001). The overall significance of these findings is that while granulosa cells from early antral follicles are only responsive to FSH, granulosa cells from FSHstimulated follicles are responsive to either FSH or LH. Thus, it is possible that the maturing follicle reduces its dependence on FSH by acquiring LH receptors (Hillier, 2001; Zeleznik, 2001). The latter hypothesis was recently tested in 24 reproductive aged women using rhfsh and rhlh after pituitary downregulation with leuprolide acetate (Sullivan et al., 1999). Follicular growth was stimulated with rhfsh until a 14-mm follicle was identified by ultrasound. The women were then randomized to one of four groups (n = 6/group) for a 2-day period: continued rhfsh treatment, substitution of rhfsh with saline, low dose rhlh (150 IU, twice daily), or high dose rhlh (375 IU, twice daily). Two days after randomization (24 h after the final saline or recombinant gonadotrophin injection), subjects received 10,000 IU HCG. Although pregnancies occurred in each of the gonadotrophin treatment groups, no data on final follicular development were provided in that study. Serum oestradiol concentrations in the women receiving saline declined by the end of the 2-day randomization period. In contrast, serum oestradiol concentrations continued to rise in women receiving either rhfsh or rhlh compared with those in the saline-treated group. Therefore, the results of Sullivan s study demonstrated that LH sustains follicular oestradiol production in the presence of falling serum FSH concentrations. However, the serum oestradiol concentrations of women in the groups receiving either rhfsh or rhlh rose throughout the study period, thus indicating that the residual low serum LH concentrations existing after pituitary downregulation in normally ovulating women are sufficient to maintain oestrogen production during ovarian stimulation with rhfsh. This is in keeping with a recent report by us (Balasch et al., 2001). On the other hand, it has been shown that follicles do not decrease in size or collapse 1 2 days after FSH withdrawal (Schoot et al., 1992; Sullivan et al., 1999), but inhibin and oestradiol serum concentrations rapidly decline when FSH concentrations decrease (Porchet et al., 1994) after stopping rhfsh treatment alone. Therefore, features of the present report were that: (i) a long-standing hypogonadotrophic hypogonadism woman rather than pituitary-suppressed women was used and (ii) the LH coast was maintained for 4 days. This study adds new data to the scanty evidence suggesting that rhlh may be a useful tool for supporting the final stages of follicular maturation. Remarkably, the decline in FSH concentrations seen after rhfsh discontinuation and during rhlh-only treatment in the patient presented was in agreement with that observed in the only previous study on the subject, and similar to the decline in FSH concentrations existing during the spontaneous follicular phase (Sullivan et al., 1999). Remarkably, there was a minimal increase in serum LH concentrations throughout the study period, in spite of daily high doses of rhlh administered. This can be explained on the basis that both endogenous LH and exogenously administered LH (either urinary or recombinant) have a short terminal halflife of around h (le Cotonnec et al., 1998). In spite of that FSH decline, androstenedione serum concentrations were maintained and the endocrine markers of follicular maturation and function such as oestradiol, inhibin A and inhibin B in the patient reported here had the normal pattern reported in spontaneous and gonadotrophin-induced ovulatory cycles (Groome et al., 1996; Eldar-Geva et al., 2000). Finally and most important, a normal pregnancy was obtained. Further studies are necessary to establish the precise stage of follicular development when LH can sustain follicular development in the presence of declining serum FSH concentrations as well as which dose, frequency and duration of LH administration are adequate to sustain the development of a single pre-ovulatory follicle without exceeding the ceiling beyond which LH induces premature luteinization or disordered oocyte development (Hillier, 2000). Although a monofollicular cycle was obtained in this patient, the proposed dual advantage of high dose rhlh of promoting the terminal maturation of a single pre-ovulatory follicle and simultaneously arresting the development of multiple less mature follicles that would otherwise occur in response to treatment with FSH (Hillier, 2000) also warrants further investigation. References Balasch J, Fábregues F 2002 Is luteinizing hormone needed for optimal ovulation induction? Current Opinion in Obstetrics and Gynecology 14, Balasch J, Fábregues F, Peñarrubia J et al Follicular development and hormonal levels following highly purified or recombinant follicle-stimulating hormone administration in ovulatory women and WHO group II anovulatory infertile patients. Journal of Assisted Reproduction and Genetics 15, Balasch J, Vidal E, Peñarrubia J et al Suppression of LH during ovarian stimulation: analysing threshold values and effects on ovarian response and the outcome of assisted reproduction in down-regulated women stimulated with recombinant FSH. Human Reproduction 16, Commenges-Ducos M, Piault S, Papaxanthos A et al Recombinant follicle-stimulating hormone versus human menopausal gonadotropin in the late follicular phase during ovarian hyperstimulation for in vitro fertilization. Fertility and Sterility 78, Eldar-Geva T, Robertson DM, Cahir N et al Relationship between serum inhibin A and B and ovarian follicle development after a daily fixed dose administration of recombinant folliclestimulating hormone. Journal of Clinical Endocrinology and Metabolism 85, Fauser BCJM, Van Heusden AMV 1997 Manipulation of human ovarian function: physiological concepts and clinical consequences. Endocrine Reviews 18, Fevold HL 1941 Synergism of follicle stimulating and luteinizing hormone in producing estrogen secretion. Endocrinology 28, Filicori M, Cognigni GE, Samara A et al The use of LH activity to drive folliculogenesis: exploring uncharted territories in ovulation induction. Human Reproduction Update 8, Greep RO, Van Dyke HB, Chow BF 1942 Gonadotropins of the swine pituitary. I. Various biological effects of purified

5 thylakentrin (FSH) and metakentrin (ICSH). Endocrinology 30, Groome NP, Illingworth PJ, O Brien M et al Measurement of dimeric inhibin B throughout the human menstrual cycle. Journal of Clinical Endocrinology and Metabolism 81, Hillier SG 1994 Current concepts of the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Human Reproduction 9, Hillier SG 2000 Controlled ovarian stimulation in women. Journal of Reproduction and Fertility 120, Hillier SG 2001 Gonadotropic control of ovarian follicular growth and development. Molecular and Cellular Endocrinology 179, le Cotonnec JY, Porchet HC, Beltrami V, Munafo A 1998 Clinical pharmacology of recombinant human luteinizing hormone: Part I. Pharmacokinetics after intravenous administration to healthy female volunteers and comparison with urinary human luteinizing hormone. Fertility and Sterility 69, Lisi F, Rinaldi L, Fishel S et al Use of recombinant LH in a group of unselected IVF patients. Reproductive BioMedicine Online 5, Peñarrubia J, Balasch J, Fábregues F et al Day 5 inhibin B serum concentrations as predictors of assisted reproductive technology outcome in cycles stimulated with gonadotrophinreleasing hormone agonist gonadotrophin treatment. Human Reproduction 15, Porchet HC, le Cotonnec JY, Loumaye E 1994 Clinical pharmacology of recombinant human follicle stimulating hormone. III. Pharmacokinetic pharmacodynamic modeling after repeated subcutaneous administration. Fertility and Sterility 61, Schoot DC, Coelingh Bennink HJT, Mannaerts BMJL et al Human recombinant follicle-stimulating hormone induces growth of preovulatory follicles without concomitant increase in androgen and estrogen biosynthesis in a woman with isolated gonadotropin deficiency. Journal of Clinical Endocrinology and Metabolism 74, Shoham Z 2002 The clinical therapeutic window for luteinizing hormone in controlled ovarian stimulation. Fertility and Sterility 77, Short RV 1962 Steroids in the follicular fluid and the corpus luteum of the mare: a two-cell type theory of ovarin steroid synthesis. Journal of Endocrinology 24, Sullivan MW, Stewart-Akers A, Krasnow JS et al Ovarian responses in women to recombinant follicle-stimulating hormone and luteinizing hormone (LH): a role for LH in the final stages of follicular maturation. Journal of Clinical Endocrinology and Metabolism 84, Zeleznik AJ 2001 Follicle selection in primates: Many are called but few are chosen. Biology of Reproduction 65, Received 20 January 2003; refereed 7 February 2003; accepted 10 February

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