Syndrome in Clinical Practice

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1 Focus on CME at the University of British Columbia Polycystic Ovarian Syndrome in Clinical Practice Although polycystic ovarian syndrome was first recognized and described more than 60 years ago, the primary cause remains unknown. An endocrine work-up should exclude other endocrine problems that may be confused with it. By Sheila M. Pride MD, FRCSC; and Anthony P. Cheung MBBS MPH, FRACOG, FRCSC Presented at the 6th Annual Update in Office Gynecology and Women s Health, University of British Columbia, June Polycystic ovary syndrome (PCOS) is the most frequent cause of clinical hyperandrogenism, with an estimated prevalence of 5% in premenopausal women. 1 This chronic endocrine disorder is commonly described as heterogenous a reference to the wide variability observed in its clinical and biochemical presentation. No single feature is pathognomonic of PCOS, and for years, investigators have used different criteria to establish the diagnosis. Dr. Pride is clinical assistant professor, division of reproductive endocrinology and infertility, department of obstetrics and gynecology, University of British Columbia, Vancouver. Her areas of particular interest include PCOS and menopause. Dr. Cheung is assistant professor, division of reproductive endocrinology and infertility, department of obstetrics and gynecology, and medical director, In Vitro Fertilization Program, University of British Columbia, Vancouver. His areas of interest are PCOS, infertility and menopause. The Canadian Journal of CME / December

2 Summary Polycystic Ovarian Syndrome in Clinical Practice The heterogeneity of PCOS suggests the existence of subgroups with differing modulators and/or etiologies. All theories incorporate mechanisms for increased ovarian androgen production, although about 50% also have elevated adrenal androgen output. Symptom onset is usually peripubertal, but a delay in onset is not unusual, and is sometimes precipitated by weight gain. Obesity is observed in 50% to 65% of patients. Obesity tends to be central (e.g., increased waist-hip ratio) and exacerbates the severity of most PCOS features (e.g., hirsutism, infertility and metabolic abnormalities). The emphasis of the endocrine work-up is to exclude other endocrine problems that may be confused with PCOS. A basic laboratory evaluation includes measuring serum androgen (e.g., total or free testosterone and dehydroepiandrosterone sulfate [DHEAS]), thryoid stimulating hormone (TSH) and prolactin levels. Therapeutic combinations may be required to manage more than one symptom or to achieve a better effect when a single agent falls short. In 1990, the National Institutes of Health- National Institute of Child Health and Human Development (NIH-NICHD) convened a conference on PCOS and three diagnostic criteria were supported by the majority of experts in this field: Hyperandrogenism, a reference to either clinical or biochemical evidence of androgen excess; Chronic infrequent or absent ovulation; and The exclusion of other endocrinopathies that might share similar features (e.g., adult onset congenital adrenal hyperplasia [CAH], Cushing s syndrome, androgen-secreting tumor of the adrenal gland or ovary, hypothyroidism and hyperprolactinemia). 2 Other clinical findings commonly observed in PCOS, including the typical ultrasound appearance of ovaries, were not required to make the diagnosis (Table 1). Etiology Although PCOS was first recognized and described more than 60 years ago, the primary cause remains unknown. No single, unifying pathogenic theory can explain the broad clinical and biochemical spectrum observed in clinical practice. Such heterogeneity suggests the existence of subgroups with differing modulators and/or etiologies. All theories incorporate mechanisms for increased ovarian androgen production, although about 50% also have elevated adrenal androgen output. 3 Neuroendocrine, intra-ovarian, adrenal, and insulin resistance have all been proposed as possible mechanisms. Recent evidence suggests intrauterine growth retardation might also be a risk factor. 4 Some patients may have a genetic predisposition, as suggested by the frequency with which PCOS occurs in families. 1 Clinical Presentation Symptom onset is usually peripubertal, but a delay in onset is not unusual and is sometimes precipitated by weight gain (Table 1). 142 The Canadian Journal of CME / December 2001

3 Table 1 Features of PCOS Feature Estimated Prevalence Hirsutism 75% Acne 25% to 30% Alopecia 8% Insulin resistance Lean: 6% to 25% Obese: 50% to 75% Acanthosis nigricans 1% to 3% Glucose intolerance 40% Type 2 diabetes 10% to 16% Hypertension? Obesity-related Dyslipidemia Increased Hirsutism and acne. Common signs of hyperandrogenism in PCOS are acne (17%) and hirsutism (75%). The hirsutism tends to be slowly progressive. Rapid progression or signs of virilization (e.g., male pattern balding, alopecia, increased muscle mass, deepening voice or clitoromegaly) are unusual and should raise the possibility of an androgen-producing tumor or ovarian hyperthecosis. 3 Anovulation. Using the 1990 inclusion criteria discussed earlier, all patients with PCOS will have infrequent or absent ovulation clinically recognized as oligomenorrhea, amenorrhea, or irregular dysfunctional uterine bleeding. Some report regular cycles at first, but subsequently experience menstrual irregularity with weight gain. 5 Total estrogen production is increased in PCOS. Serum estradiol levels fall within the early- to mid-follicular range, but estrone levels are elevated, due to peripheral conversion of circulating androgens in the adipose stroma and skin. Such chronic, acyclic estrogen production disturbs feedback relationships within the hypothalamic-pituitary-ovarian axis and contributes to anovulation. Chronic unopposed estrogen stimulation of the endometrium increases the risk of endometrial hyperplasia, dysfunctional bleeding and neoplasia a risk that can be minimized by exposure to progesterone or progestin. 5 Obesity. Patients with PCOS are prone to weight gain, and obesity is observed in 50% to 65% of patients. 3 Obesity tends to be central (e.g., increased waist-hip ratio) and exacerbates the severity of most PCOS features (e.g., hirsutism, infertility, and metabolic abnormalities). 3 It may also exert a negative impact on treatment success (e.g., ovulation induction, pregnancy outcome). Infertility. PCOS-related infertility is due to anovulation. When conception does occur, some investigators have reported an increased spontaneous pregnancy loss, the cause of which was unclear. 6 If the patient is obese, weight loss is encouraged. A loss of as little as 5% can improve reproductive potential. 7 The Canadian Journal of CME / December

4 Insulin resistance and metabolic abnormalities in PCOS. The prevalence of insulin resistance and compensatory hyperinsulinemia has been reported in 30% of lean, and up to 75% of obese, patients with PCOS. 8 Post receptor defects (e.g., serine phosphorylation of insulin receptors and/or insulin receptor-substrates [IRS], polymorphisms of IRS), and impaired insulin clearance are some of the mechanisms proposed for PCOS-related insulin resistance. 2,9,10 Obesity aggravates insulin resistance in PCOS by superimposing additional mechanisms for insulin resistance. Obesity increases fat tissue levels of tumor necrosis factor alpha (TNF) (causing serine phosphorylation of IRS), reduces glucose transport protein (GLUT-4) in muscle and fat and increases free fatty acid, which impairs insulin signalling. 11,12 Hyperinsulinemia stimulates ovarian androgen production, through a synergistic interaction with luteinizing hormone (LH) on theca cells, and enhances testosterone bioavailability by reducing the hepatic production of sex hormonebinding globulin (SHBG). 2 Insulin working in synergy with LH may also be involved in the premature follicular arrest, which is so typical of PCOS. 13 Comorbidities In PCOS, insulin resistance increases the risk of impaired glucose tolerance (20%), Type 2 diabetes (10%) and dyslipidemias. 1 Retrospective studies suggest an increased prevalence of hypertension, but this also could be a result of obesity. 1 Nevertheless, a significant number of women with PCOS appear to fulfill the World Health Organization (WHO) criteria for Metabolic Syndrome X. 14 More recently, studies suggest an increased risk of obstructive sleep apnea in PCOS when compared to weightmatched controls. 15 The higher risk of endometrial hyperplasia and neoplasia is well recognized, but the question of an increased risk of ovarian cancer or breast cancer remains unresolved. 1 The prevalence of these comorbidities increases with age, family history and obesity, and may be associated with short-term (e.g., gestational diabetes, pregnancy-induced hypertension) and long-term (e.g., cardiovascular) health risks. 1 Investigation A careful and detailed history and physical examination often will help direct investigations. The emphasis of the endocrine work-up is to exclude other endocrine problems that may be confused with PCOS. A basic laboratory evaluation will include measuring serum androgen (e.g., total or free testosterone and dehydroepiandrosterone sulfate [DHEAS]), thryoid stimulating hormone (TSH) and prolactin levels. Androgen-secreting tumors of adrenal or ovarian origin are suggested by serum DHEAS levels of > 21 nmol/l and total testosterone levels of > 7 nmol/l, and warrant further assessment and referral. An early morning serum 17a-hydroxyprogesterone < 3nmol/L excludes adult onset CAH, and if there are features suggestive of Cushing s syndrome, a 24-hour urinary free cortisol or overnight dexamethasone suppression test (1 mg taken at 11 p.m.) is indicated. The latter is more convenient, but has a higher falsepositive rate. Pelvic ultrasound is useful in measuring endometrial thickness and assessing pelvic structures, particularly in obese or virgin patients, where clinical examination can be difficult. If appropriate, an endovaginal scan is preferred, as transabdominal scans are less sensitive, particularly if the patient is obese. An endometrial biopsy is prudent in this high-risk 144 The Canadian Journal of CME / December 2001

5 group when intermenstrual intervals exceed three months and endometrial thickness exceeds 7 mm. 10 The biopsy is also indicated in older or very obese (e.g., > 90 kg) patients who have had no recent exposure to progestins or oral contraceptives (OCs). 16,17 Screening for glucose intolerance and Type 2 diabetes is reasonable, due to their high prevalence in PCOS patients. The gold standard for evaluating insulin resistance is the euglycemic hyperinsulinemic clamp, however, it is impractical in the clinical setting. A number of clinically feasible methods have been used by investigators, but a uniform screening method has yet to be agreed upon. A 1997 consensus development conference on insulin resistance could not recommend routine screening for insulin resistance with fasting insulin and glucose levels. Reasons given for this position included difficulty in establishing normal cut-off values, a wide variability of the assay and the absence of data to show a benefit in treating insulin resistance to delay the onset of overt diabetes. 18 The clinical objective for treating insulin resistance in PCOS is clearly different, however, where a cause-andeffect relationship is thought to exist between the hyperinsulinemia and ovarian hyperandrogenemia. 2 Finally, judicious assessment of lipoproteins also may be warranted for this population. 1 Pre-treatment Considerations PCOS is a lifelong condition and its natural history is not clear. It is uncertain whether the increased prevalence of comorbidities requires long-term surveillance of these women. Available therapies are directed toward symptom management, rather than curing PCOS. When treatments cease, patients usually revert to their Screening for glucose intolerance and Type 2 diabetes is reasonable, due to their high prevalence in PCOS. pretreatment state. In making treatment decisions, it is often necessary to prioritize symptom management. For example, therapy for hirsutism is postponed until infertility is dealt with, and infertility treatment is postponed until endometrial hyperplasia with atypia is resolved. In obese patients, weight loss should form an integral part of the management plan. The Canadian Journal of CME / December

6 Treatment Therapeutic combinations may be required to manage more than one symptom or to achieve a better effect when a single agent falls short. Progestins and oral contraceptives. Exposure to progestins reduces the risk of endometrial hyperplasia or cancer. 20 This may be achieved by using medroxyprogesterone acetate (MPA) 10 mg for 12 to 14 days monthly or OCs. Ethinyl estradiol/cyproterone acetate (CPA) has been released in Canada for the treatment of acne. CPA is both a potent progestin and moderate antiandrogen, preventing the binding of androgen. Both OCs and ethinyl estradiol/cyproterone acetate also can improve mild acne and hirsutism by reducing LH and increasing SHBG Laparoscopic ovarian drilling with electrocautery is a final option and has been shown to reduce androgen levels, post-operative, allowing recovery of ovulation (up to 80% in small studies) and conception (50%). levels. OCs, however, are less effective in obese patients and may have a negative impact on insulin resistance, glucose intolerance and dyslipidemia. 19,20 Antiandrogens. Antiandrogens are effective in treating hirsutism, acne, or alopecia, but have not been specifically approved for this indication. The diuretic spironolactone is an effective antiandrogen at higher doses (75 mg to 200 mg daily). Although its strongest effect is as a receptor blocker, it also impedes androgen synthesis by decreasing 17a-hydroxylase activity and perhaps 5a-reductase activity, which converts testosterone to the more potent dihydrotestosterone. Although the drug is well-tolerated, irregular uterine bleeding may develop at higher doses. This can be controlled by either lowering the dose or adding an OC. Flutamide 250 mg daily is also an androgen receptor blocker, but is not more effective than spironolactone. Rare reports of fatal liver toxicity give this drug a less favorable risk profile. Finasteride (5 mg daily), a 5a-reductase inhibitor, has no advantage over spironolactone, and is well-tolerated. Antiandrogens are contraindicated in pregnancy because of the potential risk of feminization of male offspring. Improvement of hirsutism (or alopecia) with any medication is usually not apparent until four to six months, with a maximal effect seen by 12 months. Insulin sensitizers. Hyperinsulinemia has been implicated in both increased androgen production and, possibly, the premature arrest of follicular maturation. 13 This provides the rationale for using metformin and other insulin sensitizers. Metformin (up to 2.5 g daily) was initially used in women wishing to conceive. Studies reported ovulation in 50% to 80% of patients, while other patients had an improved response to clomiphene. 21 In our infertility practice, spontaneous ovulation rates following metformin have been disappointing. Obese women with PCOS have a better ovulatory response than lean patients (88% versus 36%). 20 Metformin also has been used to treat symptoms of hyperandrogenism, but results are mixed. Long-term use has been associated with lower vitamin B12 and folate levels. The rare occurrence of lactic acidosis (with a 50% mortality) becomes a greater risk when used in conditions where lactic acid production is increased or elimination is impaired. Metformin, therefore, should be avoided in patients with significant impairment of respiratory, cardiac, hepatic or 148 The Canadian Journal of CME / December 2001

7 renal function. Metformin, a class B drug, has not been associated with any human teratogenesis. Two newer agents, rosiglitazone maleate and pioglitazone, are available in Canada and their use in PCOS is under investigation. Their insulin-sensitizing action differs from that of metformin (peroxisome proliferator activated receptor [PPAR] g agonists), however, two potential drawbacks to their use in PCOS are weight gain and little or no improvement in lipid profiles. Ovulation induction. Clomiphene citrate successfully induces ovulation in 80% of women with PCOS, however the cumulative conception rate is lower (50%). 7 Failure to conceive after four to six ovulatory cycles is an indication to exclude other coexistent causes of infertility before continuing. With clomiphene, there is an increased risk of twins (5% to 10%). A few studies have raised the concern of an increased risk of ovarian cancer with extended use of clomiphene (> 12 months), but this remains unresolved. Failure to ovulate or conceive after an adequate trial is an indication for other therapy. Injectable exogenous gonadotropins require the expertise and intensive monitoring available at an infertility center. The treatment is effective, but expensive, with a greater risk of complications (e.g., higher rate and order of multiple births, ovarian hyperstimulation syndrome). 7,22 Laparoscopic ovarian drilling with electrocautery is a final option and has been shown to reduce androgen levels, post-operative, allowing recovery of ovulation (up to 80% in small studies) and conception (50%). Improvement tends to be temporary, however, and there is a risk of periovarian adhesions, albeit much less than observed with the older wedge resections. 7,22 This risk becomes acceptable when there are no other options. Natural History The natural history of PCOS is sketchy and its co-morbidities infer a negative impact on longterm health, but solid information is lacking. Other questions about the progress of PCOS remain unresolved. When does PCOS actually begin? Is there a benefit to early intervention? What happens at menopause? What are the true cancer risks? Prospective epidemiological data are clearly needed, and we are currently in the process of developing a voluntary registry as a means to this end. CME References: 1. Solomon CG: The epidemiology of the polycystic ovary syndrome: Prevalence and associated disease risk. Endocrinol Metabol Clin NA 1999; 28(2): Dunaif A: Insulin action in the polycystic ovary syndrome. Endocriol Metab Clin NA 1999; 28 (2): Chang RJ, Katz S: Diagnosis of polycystic ovary syndrome. Endocrinol Metabol Clin NA 1999; 28(2): Ibanez L, Valls C, Potau N, et al: Sensitization to insulin in adolescent girls to normalize hirsutism, hyperandrogenism, oligomenorrhea, dyslipidemia, and hyperinsulinism after precocious pubarche. J Clin Endocrinol Metab 2000; 85 (10): Taylor AE: Polycystic ovary syndrome. Endocrinol Metab Clin N A 1998; 27(4): Sagle M, Bishop K, Ridley N, et al: Recurrent early miscarriage and polycystic ovaries. Brit Med J 1988; 297(6655): Phipps WR: Polycystic ovarian syndrome and ovulation induction Obstet Gynecol 2001; 28(1): Prelevic GM Insulin Resistance in polycystic ovary syndrome. Curr Opin Obstet Gynecol 1997; 9(3): El Mkadem S, Lautier C, Molinari N, et al: Role of allelic variants Gly972Arg of IRS-1 and Gly1057Asp of IRS-2 in moderate to severe insulin resistance of women with polycystic ovary syndrome Diabetes 2001; 50(9): Morin-Papunen LC, Vauhkonen I, Koivunen RM, et al: Insulin sensitivity, insulin secretion, and metabolic and hormonal parameters in healthy women and women with polycystic ovarian syndrome. Hum Reprod 2000; 15(6): Hunter S, Garvey T: Insulin action and insulin resistance: Diseases involving defects in insulin receptors, signal transduction, and glucose transport effector system. Am J Med 1998; 105: The Canadian Journal of CME / December

8 12. Schmitz-Peiffer C: Signalling aspects of insulin resistance in skeletal muscle: Mechanisms induced by lipid oversupply. Cell Signal 200; 12(9-10): Frank S, Gilling-Smith C, Watson H, et al: Insulin action in the normal and polycystic ovary. Endocrinol Metab Clin NA 1999; 28(2): Groop L, Orho-Melander M: The dysmetabolic syndrome. J Intern Med 2001; 250(2): Vgontzas A, Legros R, Bixler E, et al: Polycystic ovary syndrome is associated with obstructive sleep apnea and daytime sleepiness: Role of insulin resistance. J Clin Endocrinol Metab 2001; 86(2): Cheung AP: Ultrasound and menstrual history in predicting endometrial hyperplasia in polycystic ovary syndrome. Obstet Gynecol 2001; 98(2): Farquhar CM, Lethaby A, Sowter M, et al: An evaluation of risk factors for endometrial hyperplasia in premenopausal women with abnormal menstrual bleeding. Am J Obstet Gynecol 1999; 181(3): American Diabetes Association: Consensus Development Conference on Insulin Resistance. Diabetes Care 1997; 21(2): Cibula D, Hill M, Fanta M, et al: Does obesity diminish the positive effect of oral contraceptive treatment on hyperandrogenism in women with polycystic ovarian syndrome? Hum Reprod 2001;16(5): Moghetti P, Castello R, Negri C, et al: Metformin effects on clinical geatures, endocrine and metabolic profiles, and insulin sensitivity in polycystic ovary syndrome: A randomized, double-blind, placebo-controlled 6-month trial, followed by open, long-term clinical evaluation. J Clin Endocrinol Metab 2000; 85(1): Nestler JE, Jakubowicz DJ, Evans WS, et al: Effects of metformin on spontaneous and clomiphene-induced ovulation in the polycystic ovary syndrome. N Engl J Med 1998; 338(26): Taylor AE, Dunaif A: The Polycystic Ovary Syndrome and Hyperandrogenism. In: Ryan K, Berkowitz R, Barbieri M, et al (eds.) Kistner s Gynecology & Women s Health, Seventh Ed. Mosby Inc., St Louis, 1999, pp

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