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Androgen Deprivation Therapy and Estrogen Deficiency Induced Adverse Effects in the Treatment of Prostate Cancer

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Androgen Deprivation Therapy and Estrogen Deficiency Induced Adverse Effects in the Treatment of Prostate Cancer Prostate Cancer and Prostatic Diseases (2009) 12, 333–338 & 2009 Nature Publishing Group All rights reserved 1365-7852/09 $32.00 www.nature.com/pcan REVIEW Androgen deprivation therapy and estrogen deficiency induced adverse effects in the treatment of prostate cancer SJ Freedland1, J Eastham2 and N Shore3 1Departments of Surgery (Urology) and Pathology, Durham VA Medical Center and Duke Prostate Center, Duke University School of Medicine, Durham, NC, USA; 2Memorial Sloan-Kettering Cancer Center—Urology, New York, NY, USA and 3Atlantic Urology Clinics/Carolina Urologic Research Center, Myrtle Beach, SC, USA Androgen deprivation therapy (ADT) is the standard of care for metastatic prostate cancer and is increasingly used to treat asymptomatic patients with prostate-specific antigen recurrence after failed primary therapy. Although effective, ADT is associated with multiple adverse effects, many of which are related to the estrogen deficiency that occurs as a result of treatment. These include increased fracture risk, hot flashes, gynecomastia, serum lipid changes and memory loss. By providing clinicians with a greater awareness of the estrogen deficiency induced adverse effects from ADT, they can proactively intervene on the physical and psychological impact these effects have on patients. Prostate Cancer and Prostatic Diseases (2009) 12, 333–338; doi:10.1038/pcan.2009.35; published online 1 September 2009 Keywords: adverse effects; androgen deprivation; estrogen; side effects; testosterone Introduction number of patients receiving ADT is likely to see an increase. In 2008, prostate cancer was estimated to account for 25% Androgen deprivation therapy is typically performed of all new cancer cases and 10% of all cancer deaths through medical castration and, less frequently, surgical in men.1 Common treatment options for localized castration. Although there are several methods of prostate cancer include active surveillance, radical medical castration (Table 1), it is most commonly prostatectomy, radiation therapy and cryosurgery.2 achieved through the use of gonadotropin-releasing Some patients may experience an eventual increase in hormone (GnRH) agonists (for example, leuprolide, PSA or biochemical failure necessitating additional goserelin and triptorelin).7 GnRH is secreted by the treatment. hypothalamus and leads to the pulsatile release of Androgens and the functional status of androgen follicle-stimulating hormone and luteinizing hormone receptors are considered integral to both normal prostate by the pituitary gland. The release of follicle-stimulating development and prostate cancer progression;3 con- hormone and luteinizing hormone promotes testosterone sequently, androgen deprivation therapy (ADT) is a secretion by Leydig cells of the testes. High continuous common treatment for prostate cancer. Although ADT is exposure to GnRH, such as that which occurs through the standard of care for symptomatic and metastatic treatment with GnRH agonists, causes downregulation disease,4 its use has expanded to include patients who of receptors in the pituitary gland, leading to decreased show evidence of increased PSA recurrence or biochem- pituitary hormone production and ultimately a decrease ical failure.5 Although the mortality rates for prostate in the production of testosterone.8 cancer have been steadily decreasing since 1994 (whether Although ADT is effective in treating prostate cancer, it a result of improved screening, diagnosis or therapy), the is associated with adverse effects, some of which are due fact that the aging male population is increasing along- to a deficiency in testosterone levels (Figure 1). However, side a longer duration of survival is estimated to result in because estrogens are derived in men through the an increase in the number of men with prostate cancer by aromatization of testosterone, the reduction in testoster- more than 50% over the next 20 years.6 Consequently, the one due to ADT also decreases the levels of estrogen.9 This can lead to a number of estrogen deficiency induced side effects, including increased fracture risk, hot flashes, Correspondence: Dr SJ Freedland, Departments of Surgery (Urology) gynecomastia, serum lipid changes and memory loss and Pathology, Duke University School of Medicine, Box 2626 DUMC, (Figure 1). Although some of these estrogen related ADT 551 Research Drive, Room 475, Durham, NC 27710, USA. 10 E-mail: [email protected] side effects have been reviewed previously, it is Received 28 April 2009; revised 22 June 2009; accepted 25 June 2009; important to revisit and update the issue given the published online 1 September 2009 projected increase in the number of patients with Estrogen deficiency induced effects of ADT SJ Freedland et al 334 Table 1 Common methods of chemical androgen deprivation therapy Treatment type Example(s) Mechanism of action Estrogen Diethylstilbestrol Inhibits hypothalamic–pituitary axis7 GnRH agonist Leuprolide Goserelin Triptorelin Suppresses GnRH secretion47 GnRH antagonist Degarelix Antagonizes GnRH receptor47 Antiandrogen Flutamide Nilutamide Bicalutamide Blocks the effects of testosterone at the androgen receptor7 Abbreviation: GnRH, gonadotropin-releasing hormone. Sex hormone receptor types and localization Side effects of ADT of activity Estrogen Deficiency Estradiol Estrogen • Increased fracture risk receptors • Gynecomastia • Hot flashes • Adipose tissue • Lipid changes CYP19 • Bone • Memory loss Aromatase • Central nervous system Testosterone Deficiency Androgen • Erectile dysfunction Testosterone receptors • Diabetes • Muscle weakness • 2° Sex • Body composition characteristics • Skeletal muscle • Erythropoiesis Figure 1 Androgen deprivation therapy: estrogen versus testosterone deficiency adverse effects.48,49 prostate cancer who are receiving ADT. By potentially compared with those who did not receive ADT (12.6%; improving treatment through increased awareness of Po0.001). This risk began early in the course of these adverse effects and their mechanism of action, ADT administration and increased with the number of urologists can enhance overall patient care. doses of GnRH agonist administered within the first year. Patients who received 1–4 doses were at a 7% higher risk (95% CI, À2 to 16%) and those who received X9 doses were at a 45% higher risk (95% CI, Estrogen deficiency induced adverse 36–56%). A comparable pattern was seen with fractures effects of ADT that required hospitalization: 5.2% of patients receiving ADT required hospitalization compared with 2.4% of Increased fracture risk patients who did not receive ADT (Po0.001). Estrogens have a fundamental role in regulating Similar results were found in a population-based, bone integrity in men. In general, estrogen deficiency epidemiologic, case–control study in Denmark of 15 716 appears to accelerate bone remodeling by prolonging the men with fractures compared with 47 149 age-matched lifespan of osteoclasts,11 with converse effects on controls.17 Prostate cancer had been previously diag- osteoblasts and osteocytes.12,13 This disproportionate nosed in 2.5% of men in the fracture group (20% of lifespan between osteoclasts and osteoblasts/osteocytes whom received ADT) and 1.3% of men in the control leads to greater bone resorption than formation and group (15% of whom received ADT). Men with prostate contributes to the development of osteoporosis and an cancer were at an increased risk for any fracture (odds increased fracture risk.12 Although many men experience ratio ¼ 1.8), particularly hip fracture (odds ratio ¼ 3.7). both age-related hypogonadism14 and decreases in More importantly, ADT (once adjusted for prostate bone mineral density (BMD),15 the changes associated cancer, age and previous fracture) was also associated with ADT are far more severe. The result is reflected in a with an increased risk of any fracture with an odds ratio higher prevalence of fractures in men receiving ADT, of 1.7 and hip fracture with an odds ratio of 1.9. who show an average rate of fractures of 5–8% per year Finally, a Medicare claims-based cohort study of 11 661 of ADT therapy.10 eligible patients with nonmetastatic prostate cancer (3887 Several recent large studies have established a strong who received GnRH agonists and 7774 who did not) association between ADT and increased fracture examined the effect of ADT therapy on specific fractures, risk.16–18 One was a US study of the National Cancer including vertebral, hip and femur.18 On the basis of Institute’s Surveillance, Epidemiology, and End Results these results, there was a significant increase in the risk program and Medicare databases in a period from 1992 of fracture in men receiving ADT compared with control through 1997 that examined data from 50 613 men with patients: specifically, there was increased risk of any prostate cancer, 31% of whom received ADT.16 In the 12– fracture (21% higher risk; Po0.001), vertebral fracture 60 months after diagnosis, a significantly higher percen- (45% higher risk; Po0.001) and hip/femur fracture (30% tage of patients in the ADT group had a fracture (19.4%) higher risk; P ¼ 0.002). Prostate Cancer and Prostatic Diseases Estrogen deficiency induced effects of ADT SJ Freedland et al Several recent studies have also established that ADT receiving ADT, 43 (68%) reported experiencing hot 335 is associated with a significant decrease in BMD.19,20 In flashes at some point during treatment.24 Further- an analysis of prospective 12-month data from 65 men, more, nearly 50% of these patients
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