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Evidence-based management of endometriosis-associated infertility Hassan N. Sallam, MD, FRCOG, PhD (London) Professor in Obstetrics and Gynaecology The University of Alexandria, and Clinical and Scientific Director, Alexandria Fertility Center, Alexandria, Egypt 3rd Congress of Society of Reproductive Medicine, 5 – 9 October 2011, Antalya / Turkey The old Alexandria medical school The uterus (after Soranos of Ephesus) Karl, baron von Rokitansky (1804-1878) Does endometriosis affect infertility? YES 1. More commonly found in infertility patients (Mahmoud and Templeton, 1991) 2. Pregnancy rates are higher in treated patients (Marcoux et al, 1997) 3. Pregnancy with AID is lower with endometriosis (Jansen, 1986) 4. Pregnancy with IVF is lower with endometriosis (Barnhart et al, 2002) Prevalence of endometriosis (Mahmoud and Templeton, 1991) (OS) 25 25% 20 21% 15 15% 10 5 6% 0 Sterilization Infertility Pain DUB/TAH Mahmoud and Templeton, Hum Reprod 6(4): 544-9, 1991 Laparoscopic surgery v/s no surgery (RCT) (Canadian Collaborative Group, Marcoux et al, 1997) Surgery (n=172) No surgery (n= 169) P value CPR 30.7% 17.7% 0.006 Fecundity 4.7% 2.4% <0.05 Marcoux et al, N Engl J Med 337(4):217-22, 1997 AID in minimal endometriosis (Fecundity rates per month of exposure) 1 0.9 0.8 0.7 0.6 Normal pelvis Endometriosis 0.5 0.4 0.3 0.2 0.1 0 1 3 5 7 9 11 13 15 Jansen RP, Fertil Steril 46 (1): 141-3, 1986 IVF in endometriosis versus tubal infertility (CPR) Barnhart et al, Fertil Steril 77(6): 1148-55, 2002 How does endometriosis affect infertility? 1. Tubal adhesions 2. Impaired gamete interaction 3. Impaired implantation Cross-over oocyte donation study (Pellicer et al, 2001) Oocytes from normal controls to endometriosis patients Oocytes from endometriosis patients to normal controls Similar implantation rates Reduced implantation rates i.e. Endometrial receptivity does not play a role in diminished pregnancy rates in endometriosis Causes of diminished pregnancy and implantation rates in IVF for endometriosis Poor quality of oocytes (Hull et al, 1998; Norenstedt et al, 2001) Lower quality embryos with a reduced ability to implant (Simon et al, 1994; Arici et al, 1996) The poor quality of the oocytes is probably due to the altered follicular environment: • Increased progesterone concentration in FF (Pellicer et al, 1998) • Increased concentration of IL-6 in FF (Pellicer et al, 1998) • Lower levels of cortisol in FF (Smith et al, 2002) • Lower concentrations of IGFBP-1 in FF (Cunha-Filho et al, 2003) The poor quality of the oocytes is probably due to the altered follicular environment (cont…) • Increased expression of the TNF-α in the cultured granulosa cells (Carlberg et al, 2000) • Increased rate of apoptosis (cell death) in the granulosa cells mediated by elevated concentrations of soluble Fas ligand in serum and peritoneal fluid (GarciaVelasco et al, 2002) Effect of GnRHa on the endometrium in endometriosis (CCT) Frozen cycles Fresh cycles P value LBR 16.9 % 11.9 % <0.05 CPR 18.2 % 12.7 % <0.05 Mohamed et al, Eur J Obstet Gynecol Reprod Biol 156(2):177-80 , 2011 Management of endometriosisassociated infertility 1. Surgical treatment 2. Medical treatment 3. Combined medical and surgical therapy 4. Controlled ovarian hyperstimulation +/- IUI 5. Assisted reproductive techniques Evidence-based medicine • Level A – The recommendation based on good and consistent scientific evidence (RCT) • Level B – The recommendation is based on limited or inconsistent scientific evidence (CT, cohort, case control) • Level C – The recommendation is based primarily on consensus and expert opinion Problems in the evaluation of management options 1. Any management option should be compared to expectant management 2. The monthly fecundity rate (MFR) is more meaningful than the pregnancy rate (PR) Expectant management in endometriosis (Prospective cohort study PCS) Degree of endometriosis Cumulative Monthly pregnancy rate fecundity rate (CPR) (MFR) Mild 52.9% 5.7% Moderate 25% 3.2% Severe 0% 0% All cases 24.4% 3.1% Olive et al, Fertil Steril 44(1):35-41, 1985 Expectant management of stage I and II endometriosis (CCT) Miscarriage rate No treatment Cumulative pregnancy rate 55% MPA 71% 6.3% Danazol 46% 11% P value NS NS Hull et al, Fertil Steril 47(1):40-4, 1987 14.3% Management of endometriosisassociated infertility 1. Surgical treatment 2. Medical treatment 3. Combined medical and surgical therapy 4. Controlled ovarian hyperstimulation +/IUI 5. Assisted reproductive techniques Problems in evaluating surgical management of endometriosis 1. Few studies are controlled 2. Few studies report the fecundity rate 3. Techniques/skills differ 4. Recognition of “atypical” lesions 5. Use of adhesion prevention agents White endometriosis, clear endometriosis, red endometriosis and powder burn lesions. Powder burns on the right uterosacral ligament causing painful intercourse Surgical treatment of endometriosis 1. Ablation and/or resection of laparoscopic lesions 2. Drainage +/excision/ablation of endometriomas Surgical treatment of endometriosis 1. Ablation and/or resection of laparoscopic lesions 2. Drainage +/excision/ablation of endometriomas Power sources in endoscopic surgery (Sutton, 1995) 1. Electrocautery (mono or bipolar) 2. CO2 Laser 3. Fibre lasers (KTP, argon, contact Nd:YAG, tunable dye or diode laser) 4. Harmonic scalpel 5. Helica thermal coagulator Resection or ablation for minimal or mild endometriosis - Canadian Collaborative Group (RCT) Clinical pregnancy rate Fecundity rate Miscarriage rate Resection Diagnostic or ablation laparoscopy P value (n = 172) (n = 169) 30.7% 17.7% <0.01 4.7% 2.4% <0.05 20.6% 21.6% 0.91 Marcoux et al, N Engl J Med 337(4):217-22, 1997 Resection or ablation for minimal or mild endometriosis (RCT) Clinical pregnancy rate Birth rate Miscarriage rate Resection Diagnostic or ablation laparoscopy P value (n = 54) (n = 47) 24% 29% NS 19.6% 22.2% NS 16.7% 23.1% NS Parazzini et al, Hum Reprod 14:1332-4, 1999 Resection or ablation versus no surgery for minimal or mild endometriosis (MA) Clinical pregnancy rate OR = 1.613 (95% CI = 1.04 – 2.50)* P = 0.042 Sallam et al, submitted for publication Resection or ablation for moderate and severe endometriosis (stages III and IV) Cumulative Fecundity pregnancy rate rate Luciano et al, 1992 (OS) 70% 6.7% Busacca et al, 1999 (OS) 57.5% 2.4% Surgical treatment of endometriosis 1. Ablation and/or resection of laparoscopic lesions 2. Drainage +/excision/ablation of endometriomas. Simple drainage of endometriomas leads to recurrence in 50-100% of cases (Nezhat et al, 1988; Vercillini et al, 1992; Olive, 1989) Excision of endometriomas Drainage + resection/ablation of cyst wall Study n Technique CPR Daniell et al, 1991 32 Laser + stripping 38% Marrs et al, 1991 23 KTP laser ablation 30.4% Wood et al, 1992 52 Cyst stripping 50% Bateman et al, 1994 21 Cyst stripping 42.8% Montanino et al, 1996 11 Stripping + GnRHa Donnez et al, 1996 814 CO2Laser + GnRHa 45% 51% Drainage + resection/ablation of cyst wall (cont…) Study n Technique CPR Sutton et al, 1997 66 CO2 Laser + KTP 45% Hemings et al, 1998 84 Cyst stripping 50% Beretta et al, 1998 64 Cyst stripping 66.7% Busacca et al, 1999 57 Cyst stripping 57.5% Milingos et al, 1999 32 Cyst stripping 53% Jones & Sutton, 2002 39 KTP laser/diathermy 39.5% Surgical versus non-surgical therapy Adamson and Pasta, Am J Obstet Gynecol 171:1488-504, 1994 Laparoscopic excision versus electrocoagulation in mild endometriosis (CCT) Pregnacy rate Miscarriage rate Duration to pregnancy Electrocoagulation (n = 48) 57.1% Excision (n = 53) P value 53.5% NS 12.5% 17.4% NS 10.7 months 13.3 months Tulandi and Al-Took, Fertil Steril 69(2):229-31, 1998 Laparoscopy versus laparotomy (Cumulative pregnancy rates – CCT) Laparoscopy Laparotomy P value Stage I & II 67.4% 74.3% NS Stage III & IV 62.2% 44.4% <0.05 Adamson et al, Fertil Steril 59(1): 35-44, 1993 Laparoscopy versus laparotomy in severe endometriosis – (CCT) Laparoscopy Laparotomy P value (n = 67) (n = 149) 44.9% 62.7% NS CPR Recurrence of dysmenorrhoa Recurrence of dyspareunia 16.4% 20.3% NS 33.3% 15.4 NS Crosignani et al, Fertil Steril 66(5): 706-11, 1996 Management of endometriosisassociated infertility 1. Surgical treatment 2. Medical treatment 3. Combined medical and surgical therapy 4. Controlled ovarian hyperstimulation +/- IUI 5. Assisted reproductive techniques Medical treatment of endometriosis (A) Ovarian suppression - Medroxyprogesterone (MPA) - Gestrinone - GnRH agonists - Danazol (B) Aromatase inhibitors - Letrozole (C) Novel approaches Ovarian suppression for endometriosis (CPR) No therapy Thomas et al, 1987 (RCT) (Gestrinone) Bayer et al, 1988 (RCT) (Danazol) Telimaa et al, 1988 (RCT) (Danazol) Telimaa et al, 1988 (RCT) (MPA) Fedele et al, 1992 (RCT) (Buserelin) Ovarian P suppression value 24% 25% NS 57.4% 37.2% NS 46% 33% NS 46% 42% NS 61% 37% NS Ovarian suppression for endometriosis (Hughes et al, 2007) (Odds ratio for pregnancy) Ovarian suppression v/s no treatment or placebo OR = 0.79 (95% CI = 0.54 – 1.14) Ovarian suppression v/s danazol OR = 1.37 (95% CI = 0.94 – 1.99) Hughes et al, Cochrane Database Syst Rev. 2007 Jul 18;(3):CD000155 Effect of letrozole on the ASRM score (OS) Ailawadi et al, Fertil Steril 81(2): 290-6, 2004 Letrozole for the treatment of endometriosis (RCT) Letrozole Triptorelin Controls P (n = 47) (n = 40) (n = 57) value CPR after 12 months Recurrence 23.4% 27.5% 28.1% NS 6.4% 5% 5.3% NS Alborzi et al, Arch Gynecol Obstet 284: 105-10, 2011 Novel medical therapies 1. Antiangiogenic agents (Dabrosin et al, 2002) 2. SPRMs (e.g. J867) (Chwalisz et al, 2002) 3. GnRH antagonists (e.g. ganirelix and cetrorelix) (Kupker et al, 2002) 4. Mifepristone (Murphy et al, 2002) 5. Local therapy (e.g. methotrexate) (Mesogitsis et al, 2000) Management of endometriosisassociated infertility 1. Surgical treatment 2. Medical treatment 3. Combined medical and surgical therapy 4. Controlled ovarian hyperstimulation +/- IUI 5. Assisted reproductive techniques Pre-operative medical treatment for endometriosis (CCT) Danazol Gestrinone Buserelin Regression of endometriosis 30% 34% 73% * Cumulative pregnancy rate 45% 47% 58% * Donnez et al, Int J Fertil 35(5): 297-301, 1990 Post-operative GnRHa for endometriosis (Cumulative pregnancy rates - CPR) Parazzini et al, 1994 (RCT) Vercellini et al, 1999 (RCT) Surgery with GnRHa 19% Surgery without GnRHa 18% P value 11.6% 18.4% NS NS Pre and post operative medical therapy for endometriosis surgery (Cochrane review) • Pre-surgical medical therapy showed a significant improvement in AFS scores • Post-surgical hormonal suppression showed no benefit for the outcomes of pain or pregnancy rates but a significant improvement in disease recurrence Yap et al, Cochrane Database Syst 2004;(3):CD003678 Management of endometriosisassociated infertility 1. Surgical treatment 2. Medical treatment 3. Combined medical and surgical therapy 4. Controlled ovarian hyperstimulation +/- IUI 5. Assisted reproductive techniques COH in stages I & II endometriosis Intervention Simpson et Clomiphene al, 1992 citrate (CCT) Fedele et al, HMG 1992 (RCT) No therapy COH P value 9% 22% <0.05 24% 37.4% NS COH + IUI in stages I & II endometriosis No therapy COH + IUI Deaton et al, 1990 (RCT) Tummon et al, 1997 (RCT) Serta et al, 1992 (CCT) Peterson et al, 1994 (CCT) P value 3.3% 9.5% <0.05 2% 11% <0.005 32% 32% NS 1.4% 15% <0.005 COH + IUI in endometriosis (Meta-analysis) Number of Number of Mean cycle studies cycles fecundity (SD) Stage I & II 5 783 0.14 * Stage III & IV 3 179 0.08 Peterson et al, Fertil Steril 62(3):535-44, 1994 Management of endometriosisassociated infertility 1. Surgical treatment 2. Medical treatment 3. Combined medical and surgical therapy 4. Controlled ovarian hyperstimulation +/- IUI 5. Assisted reproductive techniques Intracytoplasmic sperm injection (ICSI) IVF in endometriosis versus tubal infertility (CPR) Barnhart et al, Fertil Steril 77(6): 1148-55, 2002 Surgical approaches to treat endometriosis before IVF and ICSI 1. Surgical removal of endometriomas appears to diminish the success rate of IVF/ICSI (Aboulghar et al, 2003) 2. Laparoscopic cystectomy has no effect (Canis et al, 2001; Marconi 2002) Surgical approaches to treat endometriosis before IVF and ICSI (cont…) 3. LASER vaporization of the internal wall of endometriomas did not affect the outcome (Donnez et al, 2001; Wyns et al, 2003) 4. Ultrasound-directed cyst aspiration is associated with mixed results (Dicker et al, 1991; Suganuma et al, 2002) and an increased incidence of infection (Nargund and Parsons, 1995) Medical approaches to treat endometriosis before IVF and ICSI 1. Corticosteroids (Kim et al, 1997) (RCT but small and not repeated) 2. Danazol (Tei et al, 1998) (RCT but small and not repeated) 3. GnRH agonists (Oehninger et al, 1989; Dicker et al, 1990; Dale et al, 1990; Nakamura et al, 1992; Curtis et al, 1993; Marcus et al, 1994; Chedid et al, 1995; Ruiz-Velasco and Allende, 1998) Corticosteroids before IVF in endometriosis (RCT) CPR Miscarriage rate Multiple pregnancy rate Corticosteroids Controls P value (n = 54) (n = 57) 42.6% 22.8% <0.05 21.7% 15.4% NS 17.4% 15.4% NS Kim et al, J Obstet Gynaecol Res 23(5): 463-70, 1997 Danazol before IVF in repeated IVF failures (RCT) Number CPR Danazol (400 Controls P value mg/d for 12 wks) 41 41 40% 19.5% Tei et al, J Reprod Med 43(6): 541-6, 1998 <0.05 Sallam et al, Cochrane Database Syst Rev 25;(1):CD004635, 2006 GnRH agonist v/s no agonist before IVF (Clinical pregnancy rate per woman) Sallam et al, Cochrane Database Syst Rev 25;(1):CD004635, 2006 GnRH agonist v/s no agonist before IVF (Ongoing pregnancy rate per woman) Sallam et al, Cochrane Database Syst Rev 25;(1):CD004635, 2006 GnRH agonist v/s no agonist before IVF (Number of oocytes retrieved) Sallam et al, Cochrane Database Syst Rev 25;(1):CD004635, 2006 GnRH agonist v/s no agonist before IVF (Dose of HMG or FSH required) Sallam et al, Cochrane Database Syst Rev 25;(1):CD004635, 2006 Effect of GnRHa on adenomyosis (CCT) Fertilization Adenomyosis Control P cycles (n=20) cycles (n=54) value 48.0 % 42.0 % NS Implantation 31.0 % 28.2 % NS Miscarriage 19.0 % 26.1 % NS Preg >12 wks 35.0 % 30.0 % NS Mijatovic et al, Eur J Obstet Gynecol Reprod Biol 151(1):62-5 , 2010 Conclusions 1. In endometriosis-associated infertility, expectant management is associated with ~ 50% CPR in stages I and II, while patients with stages III and IV rarely become pregnant (B) 2. In general, surgical management is associated with a significantly higher pregnancy rate compared to medical or no treatment (B) 3. Simple cyst aspiration results in recurrence in ~ 50% of instances (B) Conclusions (cont…) 4. Drainage of endometriomas + ablation or resection of their walls results in a higher pregnancy rate compared to no therapy (B) 5. Laparoscopic ablation and/or resection in stages I & II is associated with a significantly higher pregnancy rate compared to diagnostic laparoscopy (A) 6. Danazol, gestrinone, MPA, letrozole and GnRH agonists do not improve pregnancy rates over placebo or no therapy (A) Conclusions (cont…) 7. Combining laparoscopic surgery and medical therapy does not improve pregnancy rates over surgery alone (A) 8. COH+IUI improves the pregnancy rates significantly compared to no therapy in stages I and II endometriosis (A) 9. Women with endometriosis treated with IVF have significantly lower pregnancy rates compared to tubal infertility (B) 10. Long-term GnRHa before IVF improves the pregnancy rates significantly (A) Bibliotheca Alexandrina Evidence-based management of endometriosis-associated infertility Hassan N. Sallam, MD, FRCOG, PhD (London) Professor in Obstetrics and Gynaecology The University of Alexandria, and Clinical and Scientific Director, Alexandria Fertility Center, Alexandria, Egypt 3rd Congress of Society of Reproductive Medicine, 5 – 9 October 2011, Antalya / Turkey GIFT versus COH+IUI in endometriosis (CCT) (Delivery rate per cycle) GIFT COH+IUI P value Stages I & II 28.1% 14.7% <0.05 Stages III & IV 40.9% 12.5% NS Lodhi et al, Gynecol Endocrinol 19(3):152-9, 2004 Effect of GnRHa on stage III and IV endometriosis Long term GnRH agonist Control cycles Ma et al, Int J Gynaecol Obstet 100(2):167-70, 2008 P value -Mohamed et al, Eur J Obstet Gynecol Reprod Biol. 2011 Jun;156(2):177-80 - Mijatovic et al, Eur J Obstet Gynecol Reprod Biol. 2010 Jul;151(1):62-5 - Tavmergen et al, Curr Opin Obstet Gynecol. 2007 Jun;19(3):284-8 - Gong et al, Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2009 Mar;34(3):185-9 - Ma et al, Int J Gynaecol Obstet. 2008 Feb;100(2):167-70 - Tokushige et al. Discovery of a novel biomarker in the urine in women with endometriosis Fertility and Sterility 95(1): 46-49, 2011