Management of endometrial polyps diagnosed before or during ICSI cycles

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1 Reproductive BioMedicine Online (2012) 24, ARTICLE Management of endometrial polyps diagnosed before or during ICSI cycles Bulent Tiras a, Umit Korucuoglu b, *, Mehtap Polat c, Hulusi Bulent Zeyneloglu d, Ayse Saltik c, Hakan Yarali e a Gazi University Faculty of Medicine, Ankara, Turkey; b Women and Children s Hospital, Mus, Turkey; c Anatolia IVF Center, Ankara, Turkey; d Baskent University Faculty of Medicine, Ankara, Turkey; e Hacettepe University Faculty of Medicine, Ankara, Turkey * Corresponding author. address: korucu23@yahoo.com (U Korucuoglu). Bulent Tiras graduated as a medical doctor from Ankara University s Faculty of Medicine, Turkey in Bulent Tiras continued as an obstetrician and gynecologist at Gazi University s Faculty of Medicine, Turkey, obtaining the titles of associate professor in 1997 and professor in Bulent Tiras have also conducted research on IVF, infertility and microsurgery at the University of London, on reproductive endocrinology and IVF at Johns Hopkins University Medical School and on advanced endoscopic surgery at Chattanooga, USA in Bulent Tiras was president of the Turkish Society of Gynecology and Obstetrics between 2004 and Abstract This retrospective study aimed to shed light on the management options of endometrial polyps diagnosed before or during intracytoplasmic sperm injection (ICSI) treatment. The study included all fresh ICSI cycles performed in the Anatolia IVF Center between July 2005 and January Group 1 consisted of 47 patients who were diagnosed with an endometrial polyp before their ICSI cycle. All patients diagnosed with an endometrial polyp by transvaginal ultrasonography before the ICSI cycle underwent hysteroscopic polyp resection. Group 1 was compared with 47 matched control patients without endometrial polyps who underwent standard ICSI cycles (group 2). Group 3 included 128 patients diagnosed with an endometrial polyp during stimulation in their ICSI cycles. Group 3 was compared with 128 matched control patients without endometrial polyps who underwent standard ICSI cycles (group 4). Patients diagnosed with an endometrial polyp before ICSI cycles were similar to their controls with regard to clinical pregnancy (29.8% versus 38.3%) and live-birth (25.5% versus 31.9%) rates per transfer, as were patients diagnosed with an endometrial polyp during ovarian stimulation (clinical pregnancy rates 45.3% versus 46.9%; live-birth rates 40.6% versus 39.8%). In conclusion, further studies are required to identify the most appropriate management of endometrial polyps. RBMOnline ª 2011, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. KEYWORDS: endometrial polyp, pregnancy outcome, pregnancy rate Introduction Successful pregnancy requires both good-quality embryos and appropriate uterine receptivity. Selective singleembryo transfer cycles rarely produce pregnancy rates not higher than 30%, and even using the best single blastocyst can only produce a pregnancy rate of about 50% (Wang et al., 2010). Implantation is the most important step, requiring maternal embryonic talk, complex endometrial protein synthesis and synchronized reactions for enhanced /$ - see front matter ª 2011, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. doi: /j.rbmo

2 124 B Tiras et al. receptivity (Teklenburg and Macklon, 2009). Endometrial thickness, structure and texture are crucial for uterine receptivity. Any structural pathology in the uterine cavity may lead to subfertility or implantation failure; there are abundant reports in the literature regarding decreased pregnancy rates in the presence of fibroids, polyps, intrauterine adhesions, endometritis or decreased endometrial thickness. Among all intrauterine lesions interfering with the endometrial cavity, endometrial polyps are the most common (Doldi et al., 2005). Endometrial polyps have been proven to interfere with fertility, both with natural conception (Valle, 1984; Varasteh et al.,1999; Wang et al.,1992) and intrauterine insemination (IUI; Perez-Medina et al., 2005). Their presence or appearance before or during IVF or intracytoplasmic sperm injection (ICSI) cycles are rather challenging. The possible management options are: (i) cycle cancellation and polypectomy; (ii) removal of the endometrial polyp and embryo freezing with embryo transfer after a few months; (iii) ignoring the polyp and continuing treatment; and lastly (iv) hysteroscopic polypectomy during the ICSI cycle before oocyte retrieval without cycle cancelation (Batioglu and Kaymak, 2005; Madani et al., 2009). The diversity of these management options can confuse the assisted reproduction clinician, who aims for better implantation and pregnancy rates. There are only a few reports assessing the effect of endometrial polyps on IVF/ICSI cycles. In a study by Isikoglu et al. (2006), endometrial polyps <1.5 cm discovered both before or during IVF/ICSI cycles did not seem to affect implantation and pregnancy rates. In their study investigating the effect of endometrial polyps on pregnancy outcome in an IVF programme, Lass et al. (1999) claimed that polyps <2 cm did not decrease pregnancy rates but increased miscarriage rates; thus, they proposed the possible beneficial approach of performing hysteroscopy and polypectomy immediately following oocyte retrieval, freezing all embryos and replacing them a few months later for better take-home baby rates. This study aimed to assess the impact of endometrial polyps in ICSI patients on the pregnancy rates in this retrospective analysis of 8359 cases. Materials and methods This study includes retrospective analysis of all fresh ICSI cycles performed at the Anatolia IVF Center between July 2005 and January Frozen cycles were not included in this study. Institutional Review Board approval was not obtained in this study, because it is a retrospective analysis of standard procedures included in assisted reproduction. Four patient groups were formed. Group 1 consisted of 47 patients who were diagnosed with an endometrial polyp before their ICSI cycle and underwent hysteroscopic polyp resection, subsequently followed by ICSI treatment. Group 2(n = 47) was formed from ICSI patients without endometrial polyps as a control group for group 1 matched for demographic characteristics. These 47 patients of group 2 were selected from 8359 patients in a way they would be matched with patients of group 1 with regard to age, body mass index (BMI), cause and duration of infertility, antral follicle count, number of oocytes retrieved and number and quality of embryos. Group 3 included 128 patients diagnosed with an endometrial polyp during stimulation in their ICSI cycles. Group 4 (n = 128) was formed from ICSI patients without endometrial polyps as a control group for group 3 matched for demographic characteristics. These 128 patients of group 4 were selected from 8359 patients in a way they would be matched with patients of group 3 with regard to age, BMI, cause and duration of infertility, antral follicle count, number of oocytes retrieved and number and quality of embryos. All patients diagnosed with an endometrial polyp by transvaginal ultrasonography before the ICSI cycle underwent hysteroscopic polyp resection. All hysteroscopic polyp resections were performed under general anesthesia using a 2.9-mm 30 office hysteroscope (Storz, Germany). Polyps were removed by scissors and sent for pathological examination. All pathology examinations verified the diagnosis of the endometrial polyp. As the patients were infertile, major trauma to the endometrium was avoided. Thus, dilatation and curettage were not performed for any of these patients. As a result, no other pathological results, such as endometritis or hyperplasia, were observed, but transvaginal ultrasonographic examinations of patients did not raise suspicion of any other uterine pathologies. These patients underwent ICSI treatment in the next cycle. Pituitary desensitization with gonadotrophin-releasing hormone (GnRH) agonist leuprolide acetate (Lucrin; Abbott, Illinois, USA) or cetrorelix (Cetrotide; Serono, Rockland, USA) was given to prevent premature LH surge. Gonadotrophin dose was individualized and monitored according to follicular growth and serial plasma oestradiol determinations. As at least three or more follicles reached a diameter of 17 mm, human chorionic gonadotrophin (HCG) was administered either in the form of 10,000 IU urinary HCG (Pregnyl; Organon, Whitehouse Station, USA) or 250 lg recombinant HCG (Ovitrelle; Serono) to achieve final follicular maturation and to trigger ovulation. Oocyte retrieval was carried out under general anesthesia using transvaginal ultrasound-guided puncture, 36 h after injection of HCG. Oocytes were inseminated 4 6 h after retrieval by ICSI using fresh ejaculates and cultured for 3 days. Embryo transfer was performed on day 3. Usually two or three embryos were replaced according to patient age, indication of IVF, number of previous attempts and number and quality of embryos available. The embryos were all loaded into Wallace embryo-replacement catheters (23 cm, 1816 N; Smiths Medical International, Hythe, UK). All embryo transfers were carried out under ultrasound guidance (MC12H6J3-M, 2003; Siemens sonoline, Adara) while the patient had a full bladder. One day after oocyte retrieval, all patients began to receive luteal-phase support by vaginal progesterone (Crinone gel 8%; Serono). Pregnancy was diagnosed by increasing serum concentrations of b-hcg 14 days after oocyte retrieval and a serum b-hcg concentration 45 miu/ml was considered as positive. Cases with b-hcg concentrations <45 miu/ml were considered negative for pregnancy for the statistical analysis. These patients underwent b-hcg follow-up every 2 days. Those with decreasing concentrations were considered to have biochemical pregnancies and those with increasing concentrations were closely followed because of the risk of ectopic pregnancy.

3 Endometrial polyps and IVF 125 of fetal heartbeat and biochemical pregnancy rate was also calculated. Statistical analysis Statistical analysis was performed using Statistical Package for Social Sciences (SPSS, Chicago, IL, USA) version The chi-squared test and Fisher s exact test were used to analyze nominal variables in the form of frequency tables. Normally distributed (Kolmogorov Smirnov test) parametric variables were tested by independent Student s t-test. Non-normally distributed metric variables were analysed by Mann Whitney U-test. A P-value <0.05 was considered as statistically significant. Values are expressed as mean ± SD unless stated otherwise. Figure 1 Transvaginal ultrasonographic view of an endometrial polyp. During ovarian stimulation, serial transvaginal ultrasound examinations were performed (Toshiba Medical System Corporation 1385; Shimoishigami, Japan). An endometrial polyp was diagnosed by the presence of a hyperechogenic endometrial mass confirmed by two expert ultrasonographers (Figure 1). Measurements of the endometrial polyp was always performed on two dimensions and the average was recorded as the definitive dimension of the endometrial polyp. Those patients diagnosed with endometrial polyps during ovarian stimulation underwent standard ICSI treatment. It is a well-known fact that two-dimensional ultrasonographic diagnosis of endometrial polyps may be problematic. However, in this study, the diagnosis was made by the common opinion of two expert ultrasonographers. The diagnosis of endometrial polyps in group 3 was not verified by sonohysterogram or hysteroscopy as these patients continued treatment and the embryo transfer was performed at the same cycle. Such invasive procedures might decrease IVF success. Female and male ages, BMI, length of ovulation induction, total dose of gonadotrophin used, endometrium thickness on the day of transfer, number of retrieved oocytes and number of embryos transferred were recorded for all patients in each group. The main outcome measure was clinical pregnancy rate based on ultrasound visualization Results Demographic characteristics Patients diagnosed with an endometrial polyp before ICSI cycles (group 1) were similar to their controls (group 2) with regard to demographic, stimulation and transfer characteristics (Table 1). Patients diagnosed with an endometrial polyp during ovarian stimulation (group 3) were similar to their controls (group 4) with regard to demographic, stimulation and transfer characteristics (Table 2). The impact of BMI on prevalence of endometrial polyps was also investigated in this study. BMI of patients diagnosed with an endometrial polyp before ICSI treatment was ± 5.65 kg/m 2 and BMI of patients diagnosed with an endometrial polyp during treatment was ± 4.68 kg/m 2. BMI of patients who did not have endometrial polyps was ± 5.48 kg/m 2. These three groups were similar to each other. BMI did not seem to have an effect on prevalence of endometrial polyps in this study. Impact of polyp presence Patients diagnosed with an endometrial polyp before ICSI cycles (group 1) were similar to their controls (group 2, both n = 47) with regard to pregnancy rates and pregnancy outcomes (Table 3). In groups 1 and 2, respectively, the Table 1 Demographic and cycle characteristics of patients who underwent polyp resection prior to ICSI (group 1) and matched controls with no polyps (group 2). Characteristic Group 1 (n = 47) Group 2 (n = 47) Female age (years) 32.9 ± ± 5.8 Male age (years) 36.4 ± ± 6.9 BMI (kg/m 2 ) 27.6 ± ± 5.3 Length of ovulation induction (days) 9.9 ± ± 1.5 Total dose of gonadotrophins (ampoules) 37.3 ± ± 16.9 Endometrial thickness on transfer day (mm) 11.5 ± ± 2.3 Oocytes retrieved 11.9 ± ± PN oocytes 6.9 ± ± 4.6 Embryos transferred 2.8 ± ± 1.0 Values are mean ± SD. There were no statistically significant differences between the two groups. BMI = body mass index; ICSI = intracytoplasmic sperm injection; PN = pronuclei.

4 126 B Tiras et al. Table 2 Demographic and cycle characteristics of patients diagnosed with an endometrial polyp during ovarian stimulation (group 3) and their matched controls with no polyps (group 4). Characteristic Group 3 (n=128) Group 4 (n=128) Female age (years) 33.4 ± ± 5.0 Male age (years) 36.7 ± ± 6.0 BMI (kg/m 2 ) 26.1 ± ± 4.9 Length of ovulation induction (days) 10.0 ± ± 1.8 Total dose of gonadotrophins (ampoules) 38.8 ± ± 20.0 Endometrial thickness on day of transfer (mm) 12.7 ± ± 2.3 Oocytes retrieved 11.4 ± ± 5.5 2PN oocytes 6.6 ± ± 4.2 Embryos transferred 3.0 ± ± 1.1 Values are mean ± SD. There were no statistically significant differences between the two groups. BMI = body mass index; PN = pronuclei. Table 3 Comparison of pregnancy rates and outcomes in patients who underwent polyp resection prior to ICSI (group 1) and matched controls with no polyps (group 2). Pregnancy outcome Group 1 (n =47) Group 2 (n=47) HCG 45 miu/ml 15 (31.9) 22 (46.8) Clinical pregnancies 14 (29.8) 18 (38.3) Biochemical pregnancies 1 (2.1) 4 (8.5) Miscarriages 2 (4.3) 3 (6.4) Live births 12 (25.5) 15 (31.9) Values are n (% per embryo transfer). There were no statistically significant differences between the two groups. HCG = human chorionic gonadotrophin; ICSI = intracytoplasmic sperm injection. Table 4 Comparison of pregnancy rates and outcomes in patients diagnosed with an endometrial polyp during ovarian stimulation (group 3) and their matched controls with no polyps (group 4). Pregnancy outcome Group 3 (n=128) Group 4 (n=128) HCG 45 miu/ml 62 (48.4) 62 (48.4) Clinical pregnancies 58 (45.3) 60 (46.9) Biochemical pregnancies 4 (3.1) 2 (1.6) Miscarriages 5 (3.9) 8 (6.3) Live birth rate 1 (0.8) 1 (0.8) Live birth % 52 (40.6) 51 (39.8) Values are n (% per embryo transfer). There were no statistically significant differences between the two groups. HCG = human chorionic gonadotrophin. implantation rates were 31.9% versus 46.8% and the clinical pregnancy rates were 29.8% versus 38.3%. Patients diagnosed with an endometrial polyp during ovarian stimulation (group 3) were similar to their controls (group 4) with regard to pregnancy rates and pregnancy outcomes (Table 4). Polyp localization Among all patients diagnosed with an endometrial polyp during ovarian stimulation (group 3, n = 128), localization of the endometrial polyp was recorded in 78 cases (60.9%). The polyp was located in the upper third of the uterine cavity in 36 cases (46.2%). Of these 36 patients, 16 patients (44.4%) achieved a serum b-hcg concentration 45 IU/ml after treatment. The polyp was located in the middle third in 26 cases (33.3%) and 13 (50.0%) of these achieved a serum b-hcg concentration 45 IU/ml after ICSI. The endometrial polyp was located at the lower third in 16 cases (20.5%) and eight of these achieved a serum b-hcg concentration 45 IU/ml after treatment (50.0%). Thus, localization of

5 Endometrial polyps and IVF 127 the endometrial polyp did not seem to affect pregnancy rates. Polyp size Polyp size was available in 98 cases of group 3 (76.6%). The smallest polyp was 4 mm in dimension and the biggest polyp was 14 mm in dimension. Most commonly, polyps were between 6 and 10 mm (n = 77; 78.6%). Polyps <6 mm and bigger than 10 mm were rare. Among these 98 patients of group 3 with a known polyp size, mean polyp dimension was 8.8 ± 2.3 mm for those who achieved serum b-hcg 45 IU/ml after treatment and 8.4 ± 2.0 mm for those who could not. Discussion A successful pregnancy is strongly dependent on an appropriate uterine receptivity. Any lesion leading to the distortion of the endometrial cavity, such as fibroids, synechia or polyps, may have a negative impact on uterine receptivity. The most common lesion of the endometrial cavity is an endometrial polyp (Doldi et al., 2005) defined as the overgrowth of endometrial glands and stroma covered by endometrial epithelium. The exact mechanism by which endometrial polyps cause decreased uterine receptivity and subsequent infertility is not known. Among possible mechanisms, the most emphasized is an inflammatory process caused by the polyp acting in a similar way as an intrauterine device (Ben-Nagi et al., 2009). Anatomical distortion of the endometrial cavity is another postulation and focuses mainly on the diminished volume of the endometrial cavity. Whatever the mechanism, endometrial polyps might be associated with decreased pregnancy rates both in natural conceptions (Valle, 1984; Varasteh et al.,1999; Wang et al.,1992) and in IUI cycles (Perez-Medina et al., 2005). In their study, Spiewankiewicz et al. (2003) obtained a 76% pregnancy rate in one year, after hysteroscopic removal of the endometrial polyp among 25 infertile patients. Varasteh et al. (1999) reported a similar 78% cumulative pregnancy rate after hysteroscopic polypectomy in cases of female infertility. In another study, investigating the effect of endometrial polyps on pregnancy rates in IUI cycles, Perez-Medina et al. (2005) studied subfertile women with sonographic diagnosis of endometrial polyps trying to conceive for at least 24 months and planned for IUI. The polyps were detected in 452 of 2800 (16.1%) consecutive patients scheduled for IUI and after hysteroscopic removal of endometrial polyps there was a 63% cumulative pregnancy rate compared with 28% in the control group (relative risk (RR) 2.3, 95% confidence interval (CI) ) (Perez-Medina et al., 2005). Interestingly, 65% of all pregnancies in the polypectomy group occurred before the first IUI cycle was started, resulting in a spontaneous pregnancy rate of 29% in the polypectomy group versus 3% in the control group (RR 10, 95% CI 3 30). The pregnancy rate after surgery at the uterotubal junction was significantly higher than that of other locations (Yanaihara et al., 2008). Although studies in the literature point to a negative impact of endometrial polyps in natural conceptions and IUI cycles, the impact of endometrial polyps on pregnancy rates and pregnancy outcomes in IVF/ICSI cycles is rather obscure and there are few studies on the subject. In the study of Isikoglu et al. (2006), implantation and pregnancy rates were similar for patients with endometrial polyps who proceeded with subsequent ICSI treatment without hysteroscopic polypectomy, for those patients who underwent hysteroscopic polyp removal before their ICSI cycle and for the control group. The same study revealed similar miscarriage rates for the three groups. In another study (Lass et al., 1999), 83 patients with endometrial polyps were divided into two groups. The first group did not undergo hysteroscopic polyp removal and continued the standard IVF treatment. The second group underwent hysteroscopic polypectomy just after oocyte retrieval and the embryos were freezed and transferred in a subsequent cycle. They found that the pregnancy rate of the first group was similar to the overall pregnancy rate for their clinic over the same period of time. The miscarriage rate tended to be higher but the difference was not statistically significant. As a result, they concluded that the presence of a small endometrial polyp before or through the stimulation for IVF should not alter the planned oocyte recovery and embryo transfer. In another study (Hereter et al., 1998), pregnancy rates and outcomes of 33 patients with endometrial polyps were compared with 280 controls and no difference was observed between the two groups with respect to implantation and miscarriage rates. The current study obtained similar pregnancy rates, miscarriage rates and live-birth rates in all four groups. Recently, two studies have been published suggesting that hysteroscopic polypectomy before oocyte retrieval without cycle cancellation in IVF cycles might be possible (Batioglu and Kaymak, 2005; Madani et al., 2009). Their trial proposes that hysteroscopic polypectomy during ovarian stimulation may be a harmless procedure. However, their series is too small to be conclusive, with nine patients in one study and six patients in the other. Also, the current study believes that this invasive procedure just before embryo transfer should be evaluated in detail, as recent studies fail to prove any deleterious effect of endometrial polyps <1.5 cm on pregnancy rates and pregnancy outcomes in ICSI cycles. In most cases, the endometrial polyp presents itself as a single lesion and it is mostly located close to the uterine fundus. The question whether the localization of the endometrial polyp has an effect on pregnancy rates is also challenging. The current study failed to show any effect of the endometrial polyp localization on pregnancy rates. However, the observation from non-controlled trials that pregnancy rates are higher after removal of tubocornual polyps than after removal of polyps situated in other intrauterine locations suggests that tubocornual polyps may have a different effect on reproductive function (Lee et al., 1997; Shokeir et al., 2004; Yanaihara et al., 2008). Besides, polyps in the isthmocervical part of the uterus may preferentially interfere with sperm transport. These two different mechanisms could explain the differences in conception rates after hysteroscopic removal of polyps in different locations observed in non-controlled studies. However, this finding has not been verified in the current study, which had similar pregnancy rates for endometrial polyps situated in different locations within the endometrial cavity.

6 128 B Tiras et al. The size of the endometrial polyp is also an important factor affecting pregnancy rates. Most studies investigating the effect of endometrial polyps on pregnancy rates, both in natural conceptions and in cycles using assisted reproductive technologies, deal with small endometrial polyps, usually <2 cm in diameter. Similarly, the biggest endometrial polyp was 14 mm in this study. The common endpoint of these studies (Isikoglu et al., 2006; Lass et al., 1999) and also the current study is that it is likely that polyps <2 cm will not require treatment prior to assisted reproduction treatment. However, the impact of polyps >1.5 cm on assisted reproduction outcomes does warrant further investigation. Polyp sizes in this study were <1.4 cm, probably because the study center mostly receives referred cases and patients with bigger polyps probably undergo polypectomy before they are referred to the center. This study presents data on the impact of endometrial polyps on pregnancy rates and outcomes in ICSI cycles and is unique, as far as it is known, as it involves the highest number of patients among all studies about the subject in the literature. The first finding is that endometrial polyps <1.4 cm that occurred during ovarian stimulation did not affect pregnancy rates, miscarriage rates and live-birth rates in ICSI cycles. Thus, such endometrial polyps do not seem to require any intervention and cancellation of the embryo transfer is unnecessary. As a second point, patients with an endometrial polyp detected before ICSI treatment and resected by hysteroscopy had similar pregnancy rates compared with patients with no endometrial polyps. Also, resection of an endometrial polyp <1.5 cm before oocyte retrieval without cycle cancellation or hysteroscopic polypectomy after oocyte retrieval with embryo freezing and transfer in a subsequent cycle does not seem appropriate with the available data, taking into consideration the possible harmful effect of the hysteroscopic resection on the endometrium just before embryo transfer and the relatively low pregnancy rates with frozen embryos as compared with fresh cycles. As a result, the impact of endometrial polyps on pregnancy rates and outcomes in ICSI cycles is challenging to the assisted reproduction clinician. Although several management options exist, the most appropriate method is still a subject of debate and further studies are required. As far as is known, this study involves the highest number of patients in the literature in this field and it hopes it will help all clinicians. These data may guide clinicians, in that endometrial polyps <1.5 cm occurring during ovarian stimulation do not require any intervention. Resection of such polyps before an ICSI cycle is not required and may even be harmful. References Batioglu, S., Kaymak, O., Does hysteroscopic polypectomy without cycle cancellation affect IVF? RBM online 10, Ben-Nagi, J., Miell, J., Yazbek, J., Holland, T., Jurkovic, D., The effect of hysteroscopic polypectomy on the concentrations of endometrial implantation factors in uterine flushings. Reprod. Biomed. Online 19, Doldi, N., Persico, P., Di Sebastiano, F., Marsiglio, E., De Santis, L., Rabellotti, E., et al., Pathologic findings in hysteroscopy before IVF-ET. Gynecol. Endocrinol. 21, Hereter, L., Carreras, O., Pascual, M.A., Repercusion de la presencia de polipos endometriales en un ciclo de FIV. Progressione Obstetricia y Ginecologia 41, 5 7. 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