Roy Homburg. Ovulation Induction and Controlled Ovarian Stimulation A Practical Guide Second Edition

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1 Roy Homburg Ovulation Induction and Controlled Ovarian Stimulation A Practical Guide Second Edition 123

2 Ovulation Induction and Controlled Ovarian Stimulation

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4 Roy Homburg Ovulation Induction and Controlled Ovarian Stimulation A Practical Guide Second Edition

5 Roy Homburg Homerton Fertility Centre Homerton University Hospital London United Kingdom ISBN ISBN (ebook) DOI / Springer Cham Heidelberg New York Dordrecht London Library of Congress Control Number: Springer International Publishing Switzerland 2014 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. Exempted from this legal reservation are brief excerpts in connection with reviews or scholarly analysis or material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Duplication of this publication or parts thereof is permitted only under the provisions of the Copyright Law of the Publisher's location, in its current version, and permission for use must always be obtained from Springer. Permissions for use may be obtained through RightsLink at the Copyright Clearance Center. Violations are liable to prosecution under the respective Copyright Law. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. While the advice and information in this book are believed to be true and accurate at the date of publication, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein. Printed on acid-free paper Springer is part of Springer Science+Business Media (

6 Contents 1 A Potted History of Ovulation Induction References Physiology of Ovulation Hypothalamic-Pituitary-Ovarian Axis Gonadotrophin Releasing Hormone (GnRH) FSH LH Two Cells: Two Gonadotrophins Oestradiol Progesterone Ovarian Morphology Selection of the Dominant Follicle Ovulation Fine Tuning Inhibin Activin and Follistatin Growth Factors Anti-Mullerian Hormone (AMH) Ovarian Steroidogenesis Diagnosis and Causes of Anovulation Prevalence Diagnosis Following the Diagnosis of Anovulation Causes of Anovulation v

7 vi Contents Hypothalamic-Pituitary Failure (WHO Group I) Hypothalamic-Pituitary Dysfunction (WHO Group II) Ovarian Failure (WHO Group III) Hyperprolactinaemia (WHO Group IV) Diagnostic Schemes Conclusions General Factors Influencing Ovarian Function and the Prognosis for Ovulation Induction Influence of Female Age Ovarian Reserve Prognosis for Conception Influence of Obesity and Weight Loss References Assessment of Ovarian Reserve Female Age Day 3 FSH Antral Follicle Count Anti-Mullerian Hormone (AMH) Other Methods References Management of Hypogonadotrophic- Hypogonadism Pulsatile Gonadotrophin-Releasing Hormone Therapy Gonadotrophin Therapy References Understanding the Problems of Treating PCOS Definition Pathophysiology Management Weight Loss

8 Contents vii 7.4 Anti-oestrogens Insulin Sensitisers Gonadotrophin Therapy Laparoscopic Ovarian Drilling In-Vitro Fertilization (IVF) Long-Term Health Implications of PCOS References Anti-oestrogens Clomifene Citrate Mode of Action Dose Results Monitoring Possible Adjuvants to Clomifene Treatment Unexplained Infertilty Aromatase Inhibitors Mode of Action Possible Advantages of Letrozole Results Use of Letrozole in Controlled Ovarian Hyperstimulation Questions Remaining Safety References Low-Dose Gonadotrophin Therapy for Ovulation Induction Rationale Chronic Low-Dose Regimen Results Variations on a Theme Starting Dose Incremental Dose Rise Patience Is a Virtue Gonadotrophin Preparations Summary References

9 viii Contents 10 Insulin Lowering Agents Weight Loss Metformin Restoration of Ovulation Metformin Alone Metformin + Clomiphene Metformin + Low-Dose FSH Metformin in IVF Metformin During Pregnancy The Treatment of PCOS in Adolescence Other Insulin Lowering Drugs References Laparoscopic Ovarian Drilling Surgical Methods Results Patient Selection and Mechanism of Action How Does It Work? The Order of Treatment Options References Management of Hyperprolactinaemia Aetiology Diagnosis Indications for Treatment Treatment Results of Treatment Gonadotrophins for Ovulation Induction Principles Preparations Urinary vs Recombinant: Safety Urinary FSH vs Recombinant FSH: Efficacy FSH vs hmg Treatment Protocols for Ovulation Induction References

10 Contents ix 14 Unexplained Infertility Diagnostic Tests Definition When to Intervene Treatment Options References Controlled Ovarian Stimulation for Intra-uterine Insemination Principles Treatment Regimes for IUI Conclusions References Controlled Ovarian Stimulation for IVF/ICSI Principles Gonadotrophins in COH The Choice of Gonadotrophin Preparation LH Content Starting Doses Patient Comfort Triggering Ovulation GnRH Agonists Protocols Oral Contraceptives and the Long GnRH Protocol Doses GnRH Antagonists Principles Protocols Single or Multiple Doses, Fixed Day or Flexible? References Management of Poor Responders Definition Aetiology

11 x Contents 17.3 Predictive Markers Proposed Therapeutic Options High Dose Gonadotrophins GnRH Agonist GnRH Antagonist Natural Cycles Adjuvant Therapies Conclusions References Management of High Responders Prediction of the High Responder Preference of an Antagonist Protocol Starting Dose for Stimulation Agonist Trigger Oral Contraceptive Pre-treatment Metformin Carbergoline In-Vitro Maturation (IVM) References Mild Stimulation Protocols Natural Cycles Modified Natural Cycles Delayed Low-Dose FSH with GnRH Antagonist Clomifene Combined with Gonadotrophins Aromatase Inhibitors Combined with Gonadotrophins Summary References Ovarian Hyperstimulation Syndrome Aetiology and Pathophysiology Risk Factors

12 Contents xi 20.3 Prevention (See Also Chap. 18) Ovulation Induction and COH for IUI IVF Treatment Conclusions References Multiple Pregnancies Incidence of Multiple Pregnancies Preventative Methods In Ovulation Induction In Ovarian Stimulation Preceding Intra-uterine Insemination (IUI) (See Also Chap. 15) IVF/Embryo Transfer Foetal Reduction Conclusions References Future Perspectives Patient Comfort Drug Delivery Systems Less Injections Less Complications Better Results Improved Protocols Time-Lapse Imaging Less Optimistic Predictions Utopia Suggested Further Reading on Time-Lapse Imaging

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14 Introduction Ovulation induction and controlled ovarian stimulation lie at the very heart of the treatment for infertility. Ovulation induction for the anovulatory infertile woman is arguably the most successful treatment for infertility, boasting high pregnancy rates, while controlled ovarian stimulation has become an integral part of protocols in preparation for in vitro fertilization and intra-uterine insemination. This has been a rapidly advancing science and there are many variations on a theme, often confusing, and new ideas for improvements, not always scientifically sound, are proffered with startling regularity. This book puts some order into the field. It is neither a standard textbook nor an encyclopaedia of infertility but, as the title says, it is a practical guide to ovulation induction and controlled ovarian stimulation. The book is written as a concise, no-nonsense, accurate practical guide to these complicated topics which can only be made simple by clearly written, logical, evidence- and experience- based solutions. As such, it is aimed at the general gynaecologist, fertility specialist whether established or in training, health worker and student. An understanding of the basic physiology and anatomy of the ovary, the most dynamically changing organ in the body, last to become active and first to lose its basic functions, is an essential start to this guide. A scheme for the diagnosis of the aetiology of anovulation, once this has been established, is presented in a way which is treatment orientated. That is to say that once the aetiological diagnosis is cubby-holed, the therapeutic possibilities automatically open up. If anovulation xiii

15 xiv Introduction is not the problem causing the infertility or additional factors are involved, a simple algorithm for making the diagnosis and the consequent treatment is suggested. The titles of ovulation induction and controlled ovarian stimulation should not be confused. The terms are often used interchangeably, and mistakenly, but they are distinctly different entities with different aims. The object of ovulation induction is to restore the ovulatory state and restore fertility potential. This should ideally produce one ovulatory follicle. Controlled ovarian stimulation is applied to already ovulating women to boost their ovulatory capacity, i.e. to produce multiple ovulating follicles. These different aims demand a completely different approach to how the ovary is stimulated. The pros and cons of all the applicable methods are considered herein. The ovary is not an island. It is strongly influenced by what is happening in the hinterland of the rest of the body. The prime example of this is age, the most important single factor affecting female fertility potential. An assessment of ovarian reserve and consequent fertility potential is becoming an integral part of the work-up in these modern days of a desire for pregnancy in the more advanced fertile age groups. Overweight and frank obesity may have a devastating effect on fertility potential, both for conception and the prevalence of miscarriage. This health curse of modern society is a matter of too much flesh preceding the way of all flesh. While its disturbing effect on fertility may not be its most catastrophic medical effect, it still gives the fertility specialist a headache. While advancing age cannot be treated, the knowledge of its possible effects on the ovary and conception capabilities must be made more widely known to the general public. Similarly, the problem of obesity is an educational topic, the difference being that it is most definitely correctable by a change of lifestyle. A discussion of these two impeders precedes details of ovulation inducing agents. Both ovulation induction and controlled (sometimes uncontrolled) ovarian stimulation have two major complications multiple pregnancies and ovarian hyperstimulation

16 Introduction xv syndrome. Both are iatrogenic, both can be limited far better than is being done today. Relatively few multiple pregnancies will result from a low dose gonadotrophin protocol and virtually no ovarian hyperstimulation syndrome. The replacement of one embryo following IVF is not going to produce many multiple pregnancies, and softer protocols required to produce embryos from which a good quality single embryo can be chosen and replaced is the direction of the future. Sandwiched between an enlightening look at the history of ovulation induction and stimulation and some crystal-ball gazing at future perspectives is the meat of the book which is replete with algorithms and explanatory tables. This guide is not over-referenced but relies on evidenced based medicine wherever this is available and, in particular, on almost 50 years of my own experience in this, surely the most fascinating and satisfying of medical sciences, the creation of a new life. Since writing the first edition of this book, Robert ( Bob ) Edwards has passed away. This gentle giant of a man changed history and not just in our profession. A stubborn Yorkshireman (as I am by birth), I found him incisive but polite, generous with praise and a kind man. One of Bob s greatest attributes was his ability to foresee the next step before anyone else and to set about achieving it doggedly. Our conversations, rarely about medicine, revealed his indepth knowledge of Yorkshire cricket, English rugby and the plight of Leeds United. Belatedly receiving the Nobel Prize and sparingly credited in his own country, he can rest assured that he will be fondly remembered.

17 Chapter 1 A Potted History of Ovulation Induction Abstract Since the early 1960s we have been privileged to witness one of the most amazing evolutions in modern medical practice, that of infertility treatment. Up to that time we could do little to help the infertile couple and a consultation usually consisted of some wise nodding of the head and an explanation of the frequency and timing of intercourse. The 1960s, most famous for the introduction and widespread use of the oral contraceptive pill, paradoxically also brought about the possibility to treat anovulation and cure infertility emanating from this cause. Clomiphene citrate was the first agent to restore ovulation and this was soon followed by the extraction and purification of human menopausal gonadotrophins from urine. Today LH and FSH are produced by recombinant technology, shorn of impurities and very safe. The missing link connecting the hypothalamus and the pituitary, gonadotrophin-releasing hormone (GnRH) was elucidated in the 1970s eventually leading to today s widespread use of GnRH agonists and antagonists. All the milestones in ovulation induction have been accompanied by brilliant technological advances. The advent of IVF, due to the foresight and stubborness of Steptoe and Edwards, and the ensuing technique of intra-cytoplasmic sperm injection (ICSI) have been incredible steps forward. In the last 50 years or so, we have progressed from helplessness to hopefulness for all infertile couples, only few of whom cannot conceive with R. Homburg, Ovulation Induction and Controlled Ovarian Stimulation, DOI / _1, Springer International Publishing Switzerland

18 2 Chapter 1. A Potted History of Ovulation Induction today s knowledge and facilities. Can the next 50 years possibly be as exciting for reproductive physicians? Keywords Ovulation Induction Infertility Anovulation Clomiphene citrate Anti-oestrogen FSH Gonadotrophins Amenorrheic women Ovarian stimulation IVF ICSI IUI GnRH Prolactin Bromocryptine Hyperprolactinaemia hmg LH From the time I was a medical student in the early 1960s up to the present moment, I have been priviliged to witness one of the most amazing evolutions in modern medical practice, that of infertility treatment. Up to the beginning of the 1960s we could do little to help the infertile couple and a consultation usually consisted of some wise nodding of the head and an explanation of the frequency and timing of intercourse. The 1960s, most famous for the introduction and widespread use of the oral contraceptive pill, paradoxically also brought about the possibility to treat anovulation and cure infertility emanating from this cause. Clomiphene citrate was tested by Greenblatt et al. [ 1 ] in 1961 and found to be a safe and efficient way to induce ovulation. Since then an enormous number have benefitted from the unusual mode of action of this anti-oestrogen in indirectly releasing a spurt of FSH discharge and putting the ovulatory cycle back in correct order. The simplicity and inexpensive nature of this treatment have retained clomiphene citrate until today in its position as the first line treatment for anovulation associated with normal concentrations of endogenous oestrogens. Around this exiting time, the importance of being able to administer FSH in order to induce ovulation was being realised. This was first achieved in 1958 using human pituitary gonadotrophins by Gemzell [ 2 ] and the first resulting pregnancy was reported in 1960 [ 3 ]. The classical indication for this treatment was, of course, for those lacking gonadotrophins. Subsequently pregnancies were achieved in

19 Chapter 1. A Potted History of Ovulation Induction 3 hypophysectomized patients, using human pituitary gonadotrophins [ 4, 5 ]. This enormous breakthrough sparked the challenge to find a more amenable source for these valuable human gonadotrophins. Menopausal women were known to be excreting them in plenty in their urine and it was Lunenfeld and his group that succeeded in extracting them and inducing pregnancies in large series of amenorrheic women, reported by Lunenfeld [ 6 ] and Insler [ 7 ] in On a personal note, I am very proud that both these outstanding researchers were my teachers and instilled in me the enthusiasm for this most fascinating of subjects. Urinary human menopausal gonadotrophins (hmg) have been very widely used up to the present day with extraordinary success, not only for ovulation induction, but also for ovarian stimulation for both IVF and IUI, It is hard to imagine where fertility treatment would be today without them. The missing link in the hypothalamic-pituitary ovarian axis, gonadotrophin releasing hormone (GnRH), was isolated and its structure established in the 1970s [ 8 10 ]. As the structure was a relatively simple decapeptide, a synthetic GnRH soon became available for research and clinical purposes. The synthesis of GnRH may have been relatively simple, but discovering its mode of action and efficient clinical uses took some unravelling. It was Knobil, who in the seventies [ 11 ], discovered that GnRH was released from the hypothalamus in a pulsatile fashion and, in order to be effective as replacement therapy, had to be administered in a similar way. This has since been used as the classical treatment for hypothalamic hypogonadotrophic hypogonadism with outstanding success [ 12, 13 ]. However, paradoxically, it was the early failed experiments, showing that GnRH, when given continuously, actually suppressed pituitary secretion of gonadotrophins, that led to the widespread use of GnRH agonists and later GnRH antagonists, in so-called controlled ovarian stimulation, in order to prevent premature luteinisation. Another corner of ovulation induction developed in the early 1970s, when prolactin was purified by Hwang et al. [ 14 ] and a specific assay was made available [ 15 ]. The discovery that

20 4 Chapter 1. A Potted History of Ovulation Induction high concentrations of prolactin secreted by the anterior pituitary could cause anovulation, prompted the successful search for a prolactin lowering drug. Bromocryptine proved to be very efficient in lowering prolactin concentrations and subsequently allowing the resumption of ovulation [ ]. Since then several other prolactin lowering medications have been developed. They also have the remarkable ability to reduce the size, and often eliminate, micro- and macroadenomata of the pituitary, a common cause of hyperprolactinaemia. Highly purified urinary hmg is now available and highly purified urinary FSH has also been relatively regularly used. The logistics of urine collection and the suspicion (so far thankfully unsubstantiated) that potentially harmful impurities may exist in urinary preparations, prompted the now widespread use of recombinant human FSH (r-hfsh), produced by recombinant DNA technology. Because of their lack of impurities, these pure FSH preparations can be selfadministered subcutaneously and, in addition to their safety, this is a logistically important advantage. It did not take long, using the same technology, before recombinant human LH and hcg became available. All these milestones in ovulation induction have been accompanied by brilliant technological advances. The advent of IVF, due to the foresight and stubborness of Steptoe and Edwards [ 19 ], and the ensuing technique of ICSI [ 20 ] have been incredible steps forward. In the last 50 years or so, we have progressed from helplessness to hopefulness for all infertile couples, only few of whom cannot conceive with today s knowledge and facilities. Can the next 50 years possibly be as exciting for reproductive physicians? References 1. Greenblatt RB, Barfield WE, Jungck EC, Ray AW. Induction of ovulation with MRL/41. JAMA. 1961;178: Gemzell CA, Diczfalusy E, Tillinger KG. Clinical effects of human pituitary follicle stimulating hormone (FSH). J Clin Endocrinol Metab. 1958;18:

21 References 5 3. Gemzell CA, Diczfalusy E, Tillinger KG. Human pituitary follicle stimulating hormone. 1. Clinical effects of partly purified preparation. Ciba Foundation Colloqia Endocrinol. 1960;13: Bettendorf G. Human hypophyseal gonadotropins in hypophysectomized women. Int J Fertil. 1963;8: Gemzell CA. Treatment of infertility after partial hypophysectomy with human pituitary gonadotropins. Lancet. 1964;1: Lunenfeld B, Insler V, Rabau E. Die Prinzipien der Gonadotropintherapie. Acta Endocrinol Suppl. 1970;148: Insler V, Rabau E, Lunenfeld B. Comparison of ovarian response to different treatment schedules of human gonadotrophins. In: Butler JK, editor. Developments in the pharmacology and clinical uses of human gonadotrophins. High Wycombe: GD Searle; p Matsuo H, Baba Y, Nair RMG, Arimura A, Schally AV. Structure of the porcine LH and FSH releasing factor: 1. The proposed amino acid sequence. Biochem Biophys Res Commun. 1971;43: Gullemin R. Peptides in the brain: the new endocrinology of the neuron. Science. 1978;202: Schally AV, Coy DH, Meyers CA. Hypothalamic regulatory hormones. Ann Rev Biochem. 1978;47: Knobil E. Neuroendocrine control of the menstrual cycle. Recent Prog Horm Res. 1980;36: Crowley WF, McArthur JW. Stimulation of the normal menstrual cycle in Kallman s syndrome by pulsatile administration of luteinizing hormone releasing hormone. J Clin Endocrinol Metab. 1980;51: Leyendecker G, Wildt L, Hansmann M. Pregnancies following chronic intermittent (pulsatile) of GnRH by means of a portable pump a new approach to the treatment of infertility in hypothalamic amenorrhea. J Clin Endocrinol Metab. 1980;51: Hwang P, Guyda H, Friesen HG. Purification of human prolactin. J Biol Chem. 1972;247: Friesen H, Belanger C, Guyda H, Hwang P. The synthesis and secretion of placental lactogen and pituitary prolactin. In: Wolstenholme GEW, Knight J, editors. Lactogenic hormones. Edinburgh/London: Churchill Livingstone; p Del Pozo E, Varga L, Wyss H, et al. Clinical and hormonal response to bromocryptine (CB 154) in the galactorrhea syndromes. J Clin Endocrinol Metab. 1974;39:18 26.

22 6 Chapter 1. A Potted History of Ovulation Induction 17. Thorner MO, McNeilly AS, Hagan C, Besser GM. Long term treatment of galactorrhea and hypogonadism with bromocryptine. Br Med J. 1974;2: Jacobs HS, Franks S, Murray MAF, Hull MGR, Steele SJ, Nabarro JDN. Clinical and endocrine features of hyperprolactinaemic amenorrhea. Clin Endocrinol (Oxf). 1976;5: Steptoe PC, Edwards RG. Birth after reimplantation of a human embryo. Lancet. 1978;2: Palermo G, Joris H, Devroey P, van Steirteghem AC. Pregnacies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet. 1992;340:17 8.

23 Chapter 2 Physiology of Ovulation Abstract The release of a mature, fertilizable egg from the dominant follicle is the culmination of a wonderfully integrated and synchronized succession of hormonal actions and morphological changes involving the hypothalamus, pituitary and ovaries. The major players in this system are gonadotrophin releasing-hormone (GnRH), FSH, LH, oestrogen and progesterone but essential fine-tuning is provided by a large number of other factors. The steps involved in the process of ovulation, necessitating the exact sequence of so many events, leaves one in awe of the ingenuity of the system and a little surprised that its breakdown, i.e. anovulation, does not occur much more frequently. Normal functioning of this axis is dependent on the correct synchronization of release and quantity of the hormones involved. These change dramatically throughout the cycle according to the stimulatory or inhibitory signals received. The ovary is a veritable production line for a vast number of steroid hormones but also, arguably, the most dynamically, constantly changing organ in the female body during the reproductive life span. Of the millions of primordial follicles that started life in the ovary, only about 400 will actually achieve ovulation. The key to being chosen as the month s ovulatory follicle is sensitivity to FSH as only the most sensitive can survive, thrive and produce the most oestrogen and LH receptors. The others, starved of the possibility of FSH stimulation, become R. Homburg, Ovulation Induction and Controlled Ovarian Stimulation, DOI / _2, Springer International Publishing Switzerland

24 8 Chapter 2. Physiology of Ovulation atretic. The mid-cycle LH surge is the trigger for ovulation itself, activating a cascade of inflammatory responses in the dominant follicle leading to the breakdown of the follicular boundary wall and the escape of the oocyte with its cumulus oophorus. Keywords Ovulation Ovulation induction Oocyte Dominant follicle Hormones Gonadotrophin releasing hormone GnRH FSH LH Oestrogen Progesterone Ovarian hyperstimulation IVF Corpus luteum Antral follicles Androstendione Testosterone Oestradiol Inhibin B Granulosa cell Follicular rupture Luteinization Inhibin Activin Follistatin Insulin-like growth factors IGF Anti- Mullerian hormone AMH Ovarian steroidogenesis In order to appreciate the niceties of ovulation induction, a basic understanding of the mechanism of ovulation is essential. In the normal course of events, ovulation occurs once a month between the time of menarche and menopause. The release of a mature, fertilizable oocyte from the dominant follicle is the culmination of a wonderfully integrated and synchronized succession of hormonal actions and morphological changes involving principally the anterior hypothalamus, anterior pituitary and ovaries. The major players in this system are gonadotrophin releasing-hormone (GnRH), FSH, LH, oestrogen and progesterone but essential fine-tuning is provided by a large number of other factors including inhibin, activin and growth factors. An appreciation of the steps involved in the process of ovulation, necessitating the exact sequence of so many events, leaves one in awe of the ingenuity of the system and a little surprised that its breakdown, i.e. anovulation, does not occur much more frequently than is actually seen. 2.1 Hypothalamic-Pituitary-Ovarian Axis The normal functioning of this axis is dependent on the correct synchronization of the timing of release and the quantity of the hormones involved. These change dramatically

25 2.1 Hypothalamic-Pituitary-Ovarian Axis 9 HYPOTHALAMUS + GnRH PITUITARY LH + FSH OVARIES Estradiol Progesterone Figure 2.1 A diagrammatic representation of the origin, target organ and feedback mechanisms of the principal hormones involved in the hypothalamus-pituitary-ovarian axis throughout the cycle as a result of the various feedback mechanisms involved. Firstly, we will consider the individual hormones involved, their target organs and actions, before piecing together the mosaic of the feedback mechanisms to complete the hormonal profile of the normal ovulatory cycle. Figure 2.1 provides a very simple representation of the origin, target organ and feedback mechanisms of the principal hormones involved in this axis Gonadotrophin Releasing Hormone (GnRH) GnRH is a decapeptide which is synthesized and released by specific neuronal endings in the anterior and mediobasal

26 10 Chapter 2. Physiology of Ovulation hypothalamus. It is secreted into the portal vessels which run a very short course to the anterior pituitary. It is the compactness of the portal system which allows small quantities of GnRH to be concentrated enough to exert its action of gonadotrophin release from the pitiuitary and explains why GnRH is undetectable in the peripheral circulation. The discharge of the gonadotrophins, FSH and LH, induces the production of oestradiol and progesterone from the ovary which, in turn, through a feedback mechanism, influence the pattern of release of GnRH from the hypothalamus. GnRH is released in a pulsatile fashion and it is the frequency and amplitude of these pulses, in addition to the sensitivity of the pituitary gonadotrophs, that dictate the pattern of the release of the two gonadotrophins. The GnRH pacemaker is principally influenced by the ovarian steroids but many other factors, including opiates, catecholamines, neuropeptide Y, also play a role. If GnRH is released in a constant, non-pulsatile fashion, gonadotrophin release is suppressed due to an apparent desensitization of the pituitary GnRH receptors. Pulsatile release of GnRH and fluctuations in the pattern of this pulsatility are thus integral features in the normal functioning of the ovulatory cycle. As GnRH cannot be detected in human peripheral circulation, we have relied on the correlation with LH pulsatile release for our information on variations of pulsatility through the ovulatory cycle and in pathological conditions. Pulses of FSH are much more difficult to detect due to its longer half-life. In the follicular phase of a normal cycle, pulses of LH (reflecting GnRH) can be detected every min. Immediately preceding the pre-ovulatory LH surge, there is an enormous release of GnRH and following ovulation, under the influence of rising progesterone concentrations, the frequency of these pulses gradually decreases from one every 2 4 h in the early luteal phase to every 8 12 h towards the end of the cycle. The amplitude of LH pulses in the luteal phase is significantly greater than in the follicular phase. The fluctuations in the frequency and amplitude of GnRH

27 2.1 Hypothalamic-Pituitary-Ovarian Axis 11 pulsatile release are central in dictating the pattern of release of FSH and LH and, in turn, the triggering of the ovulatory process and ovarian steroid production. This knowledge of the basic physiology of the pattern of release and action of GnRH has brought with it many clinical implications. Induction of ovulation for women who have hypothalamic hypogonadrophic hypogonadism is very successful when GnRH is administered in a pulsatile fashion with one pulse every min. This is an ideal example of pure substitution therapy. The search for an agonist to boost GnRH action proved to have exactly the opposite eventual effect due to desensitization of GnRH receptors. These compounds are now very widely used before and during ovarian hyperstimulation for IVF to prevent premature LH surges. The use of GnRH antagonists is now gradually taking the lead over the agonist during controlled ovarian stimulation for IVF as they do not induce an initial, fleeting gonadotrophin release as do the agonists, but an immediate decrease in their concentrations. The comparison of the properties and clinical uses of GnRH agonists and antagonist is made in detail in a future chapter FSH The amount and timing of FSH release by the anterior pituitary changes throughout the ovulatory cycle. This mechanism is influenced by many factors. With the sudden demise of the corpus luteum which immediately precedes menstruation, the negative feedback effects of oestradiol, progesterone and inhibin A on FSH secretion are suddenly lost so that FSH is secreted in relatively large quantities during menstruation itself. This rise in FSH concentrations stimulates the growth of antral follicles, granulosa cell proliferation and differentiation. It also encourages the action of the enzyme aromatase in the conversion of the basic androgens, androstendione and testosterone to oestrogens. The sum total of these actions results in increasing oestradiol and inhibin B concentrations, feedback

28 12 Chapter 2. Physiology of Ovulation mechanisms come into play and there is a consequent reduction of FSH concentrations. At mid-cycle, in tandem with the LH surge, there is a temporary increase in FSH secretion, more like a blip, whose significance is not clear. It may be a mere bi-product of the GnRH surge or may have a function in preparing a cohort of antral follicles for the next cycle. With the formation of the corpus luteum and the outpouring of both oestradiol and progesterone, the negative feedback mechanism comes into play and continues its suppression of FSH release until just before the next menstruation. FSH is a hormone of many roles. It is a promotor of: 1. Granulosa cell proliferation and differentiation 2. Antral follicle development 3. Oestrogen production 4. Induction of LH receptors on the dominant follicle 5. Inhibin synthesis In addition to these functions, the decrease in FSH concentrations with rising oestrogen concentrations is thought to play an important part in the selection of the dominant follicle. The declining secretion of FSH prevents multiple follicular development, as only the largest of the developing follicles stays above the FSH threshold, has the most FSH receptors, remains most sensitive to FSH and produces most oestrogen. It is then less affected by the declining FSH concentrations and can continue to develop while others fade into atresia due to lack of enough FSH stimulation. The induction of LH receptors on the largest developing follicle(s) enables LH to take a part in the development of the dominant follicle in the late follicular phase and prepare it for the oncoming LH surge. This basic knowledge of the mode of action of FSH, particularly regarding the FSH threshold for follicular growth, has influenced a change in ovulation induction regimes. This has become particularly important in the development of a chronic low- dose regimen for the induction of mono- follicular ovulation and the avoidance of multiple pregnancies and ovarian hyperstimulation syndrome.

29 2.1 Hypothalamic-Pituitary-Ovarian Axis 13 FSH LH Granulosa cell Theca cell Oestrogen Androgen Androgen Cholesterol Aromatase Figure 2.2 The two-cell, two-gonadotrophin hypothesis LH During the early and mid-follicular phase, the secretion of LH is relatively quiet with pulses every min and a fairly constant low concentration of circulating LH. However, this is the calm before the storm. An enormous climax is reached with the onset of the LH surge in the late follicular phase, the central event of the ovulatory cycle (Fig. 2.2 ). Concentrations of LH rise to times their resting level during the rest of the cycle. The duration of the surge is h. The LH surge, without which ovulation does not occur, is brought about by a combination of circumstances. Principally, there is a dramatic switch from a negative to a positive feedback action of oestradiol at both the pituitary and hypothalamic level, triggered when persistently increasing oestradiol concentrations reach a critical point. LH secreting pituitary gonadotrophs clearly become highly sensitive to GnRH stimulation, probably by increasing their numbers of GnRH receptors, a GnRH surge occurs and a small rise in progesterone levels in the late follicular phase may also have a triggering role.

30 14 Chapter 2. Physiology of Ovulation The pre-ovulatory LH surge has a number of key functions: 1. Triggering of ovulation and follicular rupture about 36 h after the surge. 2. Disruption of the cumulus-oocyte complex. 3. Induction of the resumption of oocyte meiotic maturation. 4. Luteinization of granulosa cells. Following the formation of the corpus luteum, increasing concentrations of progesterone slow down the frequency of the LH (GnRH) pulses to one every 3 then one every 4 h. Concentrations of LH once again dip down to baseline levels. It is therefore, not clear what kind of influence LH levels have on the maintenance of the corpus luteum. This structure, which produces large quantities of hormones, seems to have a mind of its own or a built-in programme which terminates in a very constant manner after 14 days. The luteal phase is thus the constant part of the ovulatory cycle whereas the follicular phase is much more likely to be prone to changes in duration Two Cells: Two Gonadotrophins Outside the tumultuous events of the mid-cycle surge, the main function of LH is to encourage the production of androgens by theca cells. The androgens, androstendione and testosterone, are then passed on to the granulosa cells. Here they meet aromatase (CYP19), whose function it is to convert them into oestrogens, mainly oestradiol but also oestrone. Aromatase action, and therefore oestrogen production, is controlled by FSH. Hence, the function of theca cells and granulosa cells are controlled by LH and FSH respectively (Fig. 2.2 ). There is some overlap however as the LH receptors expressed by FSH on the granulosa cell membranes of developing follicles of >10 mm diameter render LH capable of inducing oestradiol production and follicular growth in the mid-late follicular phase.

31 2.1 Hypothalamic-Pituitary-Ovarian Axis 15 In clinical practice, hcg has been used as an excellent substitute for the LH surge in the triggering of ovulation as it binds to the LH receptor. It has a much longer half-life than LH. The current availability of pure, recombinant LH and recombinant FSH has enabled the further investigation of the physiology of the ovulatory cycle. High doses of recombinant LH are capable of triggering ovulation. The availability of these preparations as separate entities has prompted a large number of experiments to examine what is their exact function and necessity throughout the cycle Oestradiol Oestrogens are the basic female hormones and oestradiol is the most important as far as the ovulatory cycle is concerned. The synthesis of oestradiol by granulosa cells is a function of the action of FSH. FSH stimulates the enzyme aromatase (CYP19) to convert the substrate of basic androgens, androstendione and testosterone, to oestradiol in granulosa cells. The production of this vital hormone thus requires the availability of the androgen substrate whose production in theca cells is promoted by LH, followed by the action of FSH. The key functions of oestradiol in the ovulatory cycle are: 1. As a cog in a negative feedback mechanism suppressing the secretion of FSH and so aiding in the selection of the dominant follicle and preventing multifollicular development in the mid-late follicular phase. 2. Triggering of the LH surge in mid-cycle by initiating a positive feedback mechanism when its concentrations rise to a critical level. 3. As a growth hormone for the development of the endometrium. Oestradiol concentrations are at their lowest during menstruation. The FSH induced follicular development brings about rapidly rising oestradiol production in the mid- follicular phase. When oestradiol levels attain a persistently high critical concentration in the late follicular phase, they induce the

32 16 Chapter 2. Physiology of Ovulation FSH LH Follicle Corpus luteum Progesterone Oestradiol Endometrium Day Follicular phase Ovulation Luteal phase Figure 2.3 Hormonal, follicular and endometrial changes across the phases of the ovulatory cycle LH surge. Following ovulation, oestradiol concentrations dip temporarily but are revived by corpus luteum activity. With the demise of the corpus luteum, oestradiol concentrations sink rapidly to their lowest levels and invoke the FSH rise immediately preceding menstruation (Fig. 2.3 ). A mistake of nature, hypogonadotrophic hypogonadism, in which both FSH and LH secretion is essentially missing, has provided a learning tool for the understanding of ovulatory physiology. The absence of FSH results in a lack of follicular development and oestrogen production and the absence of LH in a lack of androgen substrate production. When treatment with pulsatile GnRH is administered, pure substitution therapy, everything falls into place and ovulation can be successfully induced. If pure FSH is used to induce ovulation by direct stimulation of the ovaries, the lack of LH and therefore lack of production of androgen substrate, allows the growth of follicles but not oestradiol production. Even if ovulation can be triggered by hcg or recombinant LH when a large follicle is obtained, implantation cannot occur due to the lack of oestrogen stimulation on the endometrium.

33 2.2 Ovarian Morphology Progesterone Progesterone is produced by luteinized granulosa cells. Large quantities are synthesized by the corpus luteum following ovulation. Progesterone concentrations rise to a peak 7 8 days following ovulation and fall rapidly with the failure of the corpus luteum (Fig. 2.3 ). The main function of progesterone from the corpus luteum is to fashion a secretory endometrium, capable of hosting the implantation of an embryo and to maintain this endometrium throughout the early weeks of pregnancy until trophoblastic/placental hormones take over this role. Under the influence of progesterone the endometrial glandular structures increase greatly in numbers and become more tortuous. Progesterone also plays a role in the expression of genes needed for implantation at the level of the endometrium. Together with oestradiol, progesterone suppresses pituitary gonadotrophin release during the luteal phase. The increasing concentrations of progesterone following ovulation gradually reduce the frequency of the GnRH/LH pulses and increase their amplitude. During this phase, FSH is synthesized and stored ready for release when freed from the inhibition imposed by progesterone and oestradiol when the corpus luteum fails. The initial rise of progesterone concentrations immediately preceding the LH surge may play a role in the triggering of this surge. 2.2 Ovarian Morphology The ovary is, arguably, the most dynamically, constantly changing organ in the female body during the reproductive life span (Fig. 2.4 ). The inner, medullary or stromal section, is made up of connective tissue inundated by small capillaries and adrenergic nerves. The cortex, contains an enormous number of oocyte- containing follicles ranging from approximately 300,000 at menarche to 1,500 at menopause. There is a constant state of flux in the various stages of development of the follicles from

34 18 Chapter 2. Physiology of Ovulation Cumulus with egg Corpus luteum Ovulation Corpus albicans Cortex Hilus cells Adreneric nerve Spiral artery Primary follicle Preovulatory folicle Primordial follicles Atretric follicle Interstitial cells Early teriary follicle Medulla Secondary follicle Figure 2.4 Diagrammatic representation of ovarian morphology primordial (an oocyte with a single layer of granulosa cells around it), through primary and secondary stages with increasing numbers of layers of granulosa cells, antral stage containing follicular fluid, to a fully fledged, pre-ovulatory follicle. A corpus luteum can be seen in the luteal phase of the cycle and the picture is completed by the presence of corpora albicans (remnants of degenerate corpora lutea). Although much of this changing picture of stages of follicular development is dependent on the stage of the (gonadotrophin- dependent) ovulatory cycle, there is a constant, non-fsh dependent, progression in development of primordial to potentially ovulatory follicles being available at the start of the ovulatory cycle, a process that may take about 10 weeks. A diagrammatic representation of a pre-ovulatory follicle is illustrated in Fig. 2.5.

35 2.3 Selection of the Dominant Follicle 19 Membrana granulosa cells Theca interna Basal lamina Antrum (follicular fluid) Corona radiata granulosa cells Theca interstitial cells Capillaries Zona pellucida Loose connective tissue Theca externa Cumulus oophorus granulosa cells Figure 2.5 Morphology of the antral follicle 2.3 Selection of the Dominant Follicle Of the millions of primordial follicles that started life in the ovary, only about 400 will actually achieve ovulation during the reproductive life span. That means that more than 99.9 % of follicles become atretic. At the beginning of each cycle, a group of the most mature follicles of 2 5 mm diameter are recruited for further growth, granulosa cell differentiation and multiplication. The follicles more sensitive to FSH rather than those less mature are selected at the time of the FSH inter-cycle rise for further development (Fig. 2.6 ). The key to being chosen as the month s ovulatory follicle is sensitivity to FSH. The follicles most sensitive to FSH will utilize it to increase aromatase activity and produce oestrogens and inhibin. As FSH concentrations fall in response to rising oestrogen and inhibin B levels and become less available, only

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