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doi:10.1111/jog.12529
J. Obstet. Gynaecol. Res. Vol. 41, No. 2: 264–268, February 2015
Pathological assessment of follicular loss in laparoscopic endometrioma excision: Effects of cyst size and surgeon’s experience Pinar Caglar Aytac1, Huriye Ayse Parlakgumus1, Filiz Aka Bolat2, Tayfun Cok1, Bulent Haydardedeoglu1 and Esra Bulgan Kilicdag1 Departments of 1Obstetrics and Gynecology and 2Pathology, Baskent University Faculty of Medicine, Adana, Turkey
Abstract Aim: We planned to histologically demonstrate unintentional ovarian harm caused by excision of endometriomas. Methods: One hundred and seven patients with 135 endometriomas had laparoscopic excision of endometriomas at a tertiary health-care clinic over a 6-year period. Records were obtained retrospectively and pathological specimens were reevaluated to demonstrate follicular loss. Tissue damage was scored morphologically and compared according to surgeons’ experience and endometrioma size. Results: Ovarian follicles were detected in 80% of endometrioma specimens near the cyst wall. Morphological scores of ovarian follicles were not affected by the surgeon’s experience or endometrioma size. Conclusion: Surgical excision of endometriomas causes inevitable ovarian follicular loss. As observed in our study, this loss rate could not be traced to surgical experience or ovarian size. Key words: endometrioma, excision, follicular loss, stripping, surgeon’s experience.
Introduction Endometriosis is defined as the presence of endometrial glandular structures outside of the uterine cavity; its prevalence is approximately 10–15% at reproductive age.1 As it can settle in extrapelvic locations, it usually manifests itself in the ovary as a cystic mass, which is clinically known as an endometrioma. Because medical treatment is an option that requires constant practice, it is not suitable for patients who cannot use regular medication. Laparoscopic cyst excision is currently considered as the best surgical option for endometriomas. Due to the complexity in distinguishing the cleavage plane of an endometrioma from the surrounding ovarian tissue, dissection and excision of the cyst capsule may result in uninten-
tional removal of some healthy ovarian tissue. Studies concerning endometrioma excision suggest that ovarian follicular tissue was detected in pathological specimens of 50% of the cases.2,3 Even in some patients, this ratio can reach 90% with the increased size of the endometrioma.4,5 When endometriomas and other ovarian cysts were compared in terms of excised ovarian tissue ratios, they were seen to be similar; however, morphological observations demonstrated that excised ovarian tissues were denser in endometriomas.6 Acquiring the skills necessary to perform laparoscopic surgery requires a long learning curve, along with years of experience. Muzii et al. suggested that the surgeon’s experience is an important factor in endometrioma surgery, so as to preclude damage to the ovarian reserve.7,8
Received: April 7 2014. Accepted: June 27 2014. Reprint request to: Dr Pinar Caglar Aytac, Baskent Universiti, Kisla Saglik Yerleskesi, Uremeye Yardimci Tedavi Merkezi, Kazim Karabekir Mah. Gülhatmi Cad. No: 37/A, Yüregir, Adana 01120, Turkey. Email: [email protected]
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© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
Follicle loss in endometrioma surgery
In this study, we investigated surgically removed endometrioma specimens for morphological detection of ovarian follicles (which were unintentionally removed during cystectomy), in addition to the role of surgical experience and endometrioma size regarding the amount of removed ovarian tissue in the endometrioma cyst wall.
Methods Patients who were operated on at Baskent University, Adana Teaching and Research Hospital, Obstetrics and Gynecology Clinics for endometrioma between the years 2006 and 2013 were determined retrospectively. Only unilateral or bilateral endometriomas were included in the study. Patients who had endometriosis surgery by laparotomy and who had previous ovarian surgery and who were medically treated for endometriosis before surgery were excluded from our study. Informed consent had been provided by all of the patients. Clinical data were obtained from patients’ records, and paraffin blocks of pathological specimens were then restudied. Surgeons were categorized in terms of their laparoscopic surgical experience in endometriosis surgery. Those who had been performing laparoscopic surgery for endometriosis over 5 years and who had completed the learning curve for laparoscopic gynecological surgery were defined as gynecological endoscopists, and the rest were defined as beginners. Baskent University ethics committee approval was obtained for the study. Laparoscopic stripping of the endometrioma was performed under general anesthesia in all of the patients. A Veress needle was used to perform a pneumoperitoneum of 15 mmHg following a 10-mm trocar inserted through a 10-mm umbilical incision. After laparoscopic exploration excluded obvious intraperitoneal coexisting pathologies, two additional 5- and 10-mm pararectal trocars were placed under direct laparoscopic vision. Adhesiolysis was performed if necessary; endometrioma foci were freed, and excised or coagulated by bipolar cautery. Dissection was begun from the anti-parametrial end, where it was closest to the cyst, and continued with a 1-cm incision over the cortex with scissors to clarify the cleavage. In most cases, however, the cyst was perforated during dissection and its content was aspirated; the field was immediately irrigated with saline. Dissection was then continued with stripping, applying bimanual counter traction with atraumatic graspers. Sharp dissection with scissors was done in case of dense adhesions were
found between the endometrioma capsule and hilum of ovary. In most cases, open edges of the ovaries were sutured with 3-0 absorbable polyglactin intracorporeal sutures (Vicryl; Ethicon, Somerville, NJ, USA) for hemostasis. The surgical specimen was taken out of the abdomen through the 10-mm pararectal trocar primarily in a tissue bag. The cyst cavity was examined for gross malignancy macroscopically and sent for pathological examination. One pathologist performed all the pathological examinations of the cases (F. A. B.). There were one to 19 paraffin blocks stored for each case. The number of the paraffin blocks prepared increased as cyst size enlarged. Two sections were taken from the densest part of each block and examined after staining with hematoxylin–eosin. Presence of ovary cortex adjacent to the cyst wall was assessed. We examined the follicular tissue on the specimen to identify the morphological structure of the ovarian tissue; it was then evaluated by semiquantitative scoring, and differed between 0 and 4, as defined by Maneschi et al. in 1993 (0, no follicular tissue; 1, only primordial follicles; 2, primordial and primary follicles; 3, secondary follicles; 4, a pattern of both primary and secondary follicles in the normal ovary).9 These scores were compared according to cyst size and the surgeon’s experience. χ2-Test cross-tables and Mann–Whitney U-tests were used for statistical analyses. Intergroup relations were accepted as significant when P < 0.05. SPSS for Windows version 18.0 (SPSS, Chicago, IL, USA) was used for statistical calculation.
Results Pathological paraffin blocks for patients who were operated on for endometrioma were reexamined. The mean age was 29.5 years (range, 21–39). Dysmenorrhea was present in 82.4%, dyspareunia in 50% and infertility in 69.2% of the patients. The mean diameter of endometriomas as measured by preoperative transvaginal ultrasonography was 42.6 mm (range, 5–100), with 26% (n = 28) of patients with bilateral endometriomas. Intracorporeal hemostatic sutures were used in 78.1% of patients. In 72.6% (n = 98) of endometriomas, a full thickness of ovarian cortical tissue adjacent to the cyst was observed. In 8.1% (n = 11) of them, there were only primordial follicles observed near the cyst wall (Fig. 1). In 19.3% (n = 26), pericystic tissue was free of ovarian tissue.
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
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When pathological findings were evaluated according to laparoscopic surgical experience, no significant difference was seen in terms of cyst wall thickness excised or in terms of primordial, primary and secondary follicle rates and presence of cortical tissue adjacent to the cyst capsule (all P > 0.05, Table 1). The mean diameter of endometriomas operated on by more experienced surgeons was shown to be shorter (P = 0.04). In addition, no difference was seen between surgeon groups in terms of follicular morphology score of the specimens (all P ≥ 0.05, Table 2). When endometriomas were subgrouped by diameter in 2-cm intervals (0–20 mm, 21–40 mm, 41–60 mm, 61–80 mm, 81–100 mm), no difference was observed for the ratio of ovarian tissue excised near the cyst wall (Table 3). Likewise, no significant difference was observed among groups for ovarian tissue loss or follicular scores when endometriomas were separated into two groups of less than 4 cm or 4 cm or more in diameter (P = 0.23 and P = 0.87, respectively).
Figure 1 Endometriotic cyst epithelium and endometrial stroma (short, thick arrows), cyst wall in the primordial follicles (long, thin arrows) and tertiary follicle (asterisk) (hematoxylin–eosin, original magnification ×40).
Among patients who were operated on for infertility, consequent pregnancy was observed in 40.5% (n = 30). The mean duration from surgery to pregnancy was 14 months (range, 2–60). Of all infertile patients, 13.5% had a spontaneous pregnancy, 6.8% became pregnant after intrauterine insemination and 20.3% became pregnant after intracytoplasmic sperm injection (following laparoscopic surgery for endometrioma).
Discussion Ovarian reserve is generally affected adversely after endometrioma surgery. This situation was shown to be the case by studies demonstrating a decrease in the number of follicles via in vitro fertilization treatment, as well as a decrease in serum anti-Müllerian hormone levels in the postoperative period.10–13 These studies draw attention to the results of decreased ovarian reserve due to endometrioma surgery. However, with this study, we assessed the rate of healthy ovary tissue loss after endometrioma surgery by histological analysis. When all the excised endometriomas were examined, 72.6% of them manifested with ovarian cortex, whereas only 8.1% of them had follicular structures near the cyst capsule. In other words, in approximately 80% of cases, some healthy ovarian tissue inevitably had to be removed. In a study performed by Muzii et al., healthy ovarian tissue was demonstrated beneath 54% of the endometriomas excised, but only in 6% of benign ovarian cysts.14 In another study by Dogan et al., normal ovarian tissue was shown to be removed in 92% of endometrioma cases, but in 82% for non-endometriotic cysts.6 Although the ratio of ovary damage differs for nonendometriotic cysts, it unfortunately remains high for endometriomas. Thus, endometrioma surgery is controversial; this is why laparoscopic surgery, a minimally invasive technique for it, is the current gold standard. On the other hand, a laparoscopic approach
Table 1 Comparison of pathological parameters and surgeon’s experience Gynecological endoscopist Ovary diameter (mm) Primordial (n)† Primary (n)† Secondary (n)† Cyst wall thickness (mm)† Positive for ovarian cortex (n)
40.8 ± 19 (5–100) 17.4 ± 24 (0–105) 3.4 ± 4.2 (0–26) 0.5 ± 0.9 (0–4) 3.19 ± 1.2 (1–6) 82 (71.9%)
Beginner endoscopist 52.7 ± 24 (5–100) 9.7 ± 19.2 (0–90) 2.2 ± 3.5 (0–15) 0.48 ± 1 (0–4) 2.95 ± 1 (1–4) 16 (76.2%)
P 0.035 0.22 0.12 0.51 0.53 0.45
†Mean ± standard deviation (range).
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© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
Follicle loss in endometrioma surgery
provides earlier recovery and return to normal activity. However, it also requires a long learning curve with special expertise. Biacchiardi et al. pointed out that laparoscopic stripping of endometriosis can harm ovarian reserve even in experienced surgeons.15 In our study, surgeons were grouped as beginners and gynecological endoscopists who had completed their learning curve in laparoscopic endometriosis surgery. We examined the effect of a surgeon’s experience level on healthy ovarian tissue being excised unintentionally and did not see any significant difference (when assessed for ovarian cortical presence on specimens and with morphological scoring). While surgeons performing laparoscopy for more than 5 years were considered as more experienced in our study, proficiency in laparoscopic endometrioma surgery also may require experience with larger numbers of cases. Retto et al. demonstrated no grade 3 or 4 (resembling healthy ovary tissue) for morphological scores; they found only primordial and a few primary follicles in endometrioma cases treated with laparoscopic stripping.16 In contrast, some grade 4 and numerous grade 3 morphological scores were seen in our study, which points to secondary follicular damage occurring due to the surgery (Fig. 1). In the study mentioned above, Muzii et al. concluded there was an inverse correlation between surgical experience and thickness of the cyst wall excised.8 In our study, there was no difference in terms of cyst wall thickness between surgeon groups. We projected a similar argument based on surgical
Table 2 Semiquantitative scores of endometrioma cysts between surgeon groups Score
Gynecological endoscopist
Beginner endoscopist
P
0 1 2 3 4 Total
23 (20.2%) 14 (12.3%) 39 (34.2%) 32 (28.1%) 6 (5.3%) 114 (100%)
3 (14.3%) 6 (28.6%) 7 (33.3%) 3 (14.3%) 2 (9.5%) 21 (100%)
0.53 0.05 0.94 0.19 0.45
skills to determine dissection quality; however, we did not find any effect in terms of experience. Referral of more difficult cases to the experienced surgeons may help to explain this result. Unlike some other studies3,6 in which cyst wall thickness was found to be approximately 1–2 mm, it was shown to be approximately 3 mm in our study. As for histological examination, cyst wall thickness was measured as the thickest plane of the cyst. This measurement method may explain the difference in cyst wall thickness between the cases mentioned in the above published work and ours. In one study, Roman et al. showed that ovarian diameter is directly proportional to the volume of the ovary tissue excised.4 In another study by Tang and contributors, ovarian damage was shown to increase when endometrioma diameter exceeded 4 cm.17 On the contrary, we did not find any difference in the ratio of ovarian tissue or in morphological scores for endometriomas excised of less than 4 cm or 4 cm or more in diameter. When we examined an endometrioma’s clinical effect with detailed size parsing in 2-cm cases, no significant difference was observed either. The smaller the endometrioma was when dissected, the greater the amount of ovarian tissue that had to be sacrificed: this was due to difficulty in clarifying cleavage. On the other hand, larger endometriomas being dissected may cause much of the adherent ovarian tissue to be excised unintentionally. However, in our study, like Ramacahandran et al., we found no difference in the ratio of ovarian tissue being excised in different endometrioma sizes (Table 3).18 After surgery, in the follow-up period, spontaneous pregnancy ratio was lower than previously reported in other studies.6 We did not know the details of infertility reports of patients regarding whether had other infertility risk factors or not. The major limitation of our study is that the data, except pathology results, were collected retrospectively. There were fewer cases operated by the beginners, reducing the study’s power. We concluded that even when an endometrioma was operated on with a minimally invasive approach, it is
Table 3 Relation between presence of ovarian cortex in specimen and diameter of ovary Presence of ovarian cortex (n) No Yes
Observed (n) Predicted (n) Observed (n) Predicted (n)
P
0–20 (mm)
Diameter of ovary (mm) 21–40 (mm) 41–60 (mm) 61–80 (mm)
81–100 (mm)
7 5.5 13 14.5
14 16.7 47 44.3
2 1.6 4 4.4
10 9.3 24 24.7
4 3.8 10 10.2
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
0.84
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almost inevitable that it will harm ovarian reserve. In our study, we did not find an effect of surgeon’s experience on reducing damage to ovarian reserve during endometrioma surgery. Also, we did not find any difference in ovary damage in varying size of endometriomas excised. Excision of an endometrioma is still a difficult method, as it requires intensive dissection with a potential of loss of ovary reserve. Hence, more efforts will be required to find less invasive techniques.
7. 8.
9.
10.
Disclosure None of the authors have any conflict of interest associated with this study.
11.
References
12.
1. Moen MH, Muus KM. Endometriosis in pregnant and nonpregnant women at tubal sterilization. Hum Reprod 1991; 6: 699–702. 2. Muzii L, Bellati F, Bianchi A et al. Laparoscopic stripping of endometriomas: A randomized trial on different surgical techniques. Part II: Pathological results. Hum Reprod 2005; 20: 1987–1992. 3. Hachisuga T, Kawarabayashi T. Histopathological analysis of laparoscopically treated ovarian endometriotic cysts with special reference to loss of follicles. Hum Reprod 2002; 17: 432–435. 4. Roman H, Tarta O, Pura I et al. Direct proportional relationship between endometrioma size and ovarian parenchyma inadvertently removed during cystectomy, and its implication on themanagement of enlarged endometriomas. Hum Reprod 2010; 25: 1428–1432. 5. Kuroda M, Kuroda K, Arakawa A et al. Histological assessment of impact of ovarian endometrioma and laparoscopic cystectomy on ovarian reserve. J Obstet Gynaecol Res 2012; 38: 1187–1193. 6. Dogan E, Ulukus EC, Okyay E, Ertugrul C, Saygili U, Koyuncuoglu M. Retrospective analysis of follicle loss after laparoscopic excision of endometrioma compared with
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benign nonendometriotic ovarian cysts. Int J Gynaecol Obstet 2011; 114: 124–127. Muzii L, Miller CE. The singer, not the song. J Minim Invasive Gynecol 2011; 18: 666–667. Muzii L, Marana R, Angioli R et al. Histologic analysis of specimens from laparoscopic endometrioma excision performed by different surgeons: Does the surgeon matter? Fertil Steril 2011; 95: 2116–2119. Maneschi F, Marasá L, Incandela S, Mazzarese M, Zupi E. Ovarian cortex surrounding benign neoplasms: A histologic study. Am J Obstet Gynecol 1993; 169 (2 Pt 1): 388–393. Somigliana E, Ragni G, Benedetti F, Borroni R, Vegetti W, Crosignani PG. Does laparoscopic excision of endometriotic ovarian cysts significantly affect ovarian reserve? Insights from IVF cycles. Hum Reprod 2003; 18: 2450–2453. Raffi F, Metwally M, Amer S. The impact of excision of ovarian endometrioma on ovarian reserve: A systematic review and meta-analysis. J Clin Endocrinol Metab 2012; 97: 3146–3154. Alborzi S, Keramati P, Younesi M, Samsami A, Dadras N. The impact of laparoscopic cystectomy on ovarian reserve in patients with unilateral and bilateral endometriomas. Fertil Steril 2014; 101: 427–434. Duru NK, Dede M, Acikel CH, Keskin U, Fidan U, Baser I. Outcome of in vitro fertilization and ovarian response after endometrioma stripping at laparoscopy and laparotomy. J Reprod Med 2007; 52: 805–809. Muzii L, Bianchi A, Crocè C, Manci N, Panici PB. Laparoscopic excision of ovarian cysts: Is the stripping technique a tissue-sparing procedure? Fertil Steril 2002; 77: 609–614. Biacchiardi CP, Piane LD, Camanni M et al. Laparoscopic stripping of endometriomas negatively affects ovarian follicular reserve even if performed by experienced surgeons. Reprod Biomed Online 2011; 23: 740–746. Retto G, Santoro G, Sturlese E et al. Efficacy of laparoscopic stripping for ovarian cysts: Histological and clinical findings. J Obstet Gynaecol Res 2011; 37: 547–552. Tang Y, Chen SL, Chen X et al. Ovarian damage after laparoscopic endometrioma excision might be related to the size of cyst. Fertil Steril 2013; 100: 464–469. Ramachandran A, Dhulkhed S, Bhakta R et al. Influence of endomeriotic cyst diameter and the severity of endometriosis on the ovarian parenchyma excised during laparoscopic cystectomy. J Clin Diagn Res 2013; 7: 2241–2243.
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
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doi:10.1111/jog.12529
J. Obstet. Gynaecol. Res. Vol. 41, No. 2: 264–268, February 2015
Pathological assessment of follicular loss in laparoscopic endometrioma excision: Effects of cyst size and surgeon’s experience Pinar Caglar Aytac1, Huriye Ayse Parlakgumus1, Filiz Aka Bolat2, Tayfun Cok1, Bulent Haydardedeoglu1 and Esra Bulgan Kilicdag1 Departments of 1Obstetrics and Gynecology and 2Pathology, Baskent University Faculty of Medicine, Adana, Turkey
Abstract Aim: We planned to histologically demonstrate unintentional ovarian harm caused by excision of endometriomas. Methods: One hundred and seven patients with 135 endometriomas had laparoscopic excision of endometriomas at a tertiary health-care clinic over a 6-year period. Records were obtained retrospectively and pathological specimens were reevaluated to demonstrate follicular loss. Tissue damage was scored morphologically and compared according to surgeons’ experience and endometrioma size. Results: Ovarian follicles were detected in 80% of endometrioma specimens near the cyst wall. Morphological scores of ovarian follicles were not affected by the surgeon’s experience or endometrioma size. Conclusion: Surgical excision of endometriomas causes inevitable ovarian follicular loss. As observed in our study, this loss rate could not be traced to surgical experience or ovarian size. Key words: endometrioma, excision, follicular loss, stripping, surgeon’s experience.
Introduction Endometriosis is defined as the presence of endometrial glandular structures outside of the uterine cavity; its prevalence is approximately 10–15% at reproductive age.1 As it can settle in extrapelvic locations, it usually manifests itself in the ovary as a cystic mass, which is clinically known as an endometrioma. Because medical treatment is an option that requires constant practice, it is not suitable for patients who cannot use regular medication. Laparoscopic cyst excision is currently considered as the best surgical option for endometriomas. Due to the complexity in distinguishing the cleavage plane of an endometrioma from the surrounding ovarian tissue, dissection and excision of the cyst capsule may result in uninten-
tional removal of some healthy ovarian tissue. Studies concerning endometrioma excision suggest that ovarian follicular tissue was detected in pathological specimens of 50% of the cases.2,3 Even in some patients, this ratio can reach 90% with the increased size of the endometrioma.4,5 When endometriomas and other ovarian cysts were compared in terms of excised ovarian tissue ratios, they were seen to be similar; however, morphological observations demonstrated that excised ovarian tissues were denser in endometriomas.6 Acquiring the skills necessary to perform laparoscopic surgery requires a long learning curve, along with years of experience. Muzii et al. suggested that the surgeon’s experience is an important factor in endometrioma surgery, so as to preclude damage to the ovarian reserve.7,8
Received: April 7 2014. Accepted: June 27 2014. Reprint request to: Dr Pinar Caglar Aytac, Baskent Universiti, Kisla Saglik Yerleskesi, Uremeye Yardimci Tedavi Merkezi, Kazim Karabekir Mah. Gülhatmi Cad. No: 37/A, Yüregir, Adana 01120, Turkey. Email: [email protected]
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© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
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In this study, we investigated surgically removed endometrioma specimens for morphological detection of ovarian follicles (which were unintentionally removed during cystectomy), in addition to the role of surgical experience and endometrioma size regarding the amount of removed ovarian tissue in the endometrioma cyst wall.
Methods Patients who were operated on at Baskent University, Adana Teaching and Research Hospital, Obstetrics and Gynecology Clinics for endometrioma between the years 2006 and 2013 were determined retrospectively. Only unilateral or bilateral endometriomas were included in the study. Patients who had endometriosis surgery by laparotomy and who had previous ovarian surgery and who were medically treated for endometriosis before surgery were excluded from our study. Informed consent had been provided by all of the patients. Clinical data were obtained from patients’ records, and paraffin blocks of pathological specimens were then restudied. Surgeons were categorized in terms of their laparoscopic surgical experience in endometriosis surgery. Those who had been performing laparoscopic surgery for endometriosis over 5 years and who had completed the learning curve for laparoscopic gynecological surgery were defined as gynecological endoscopists, and the rest were defined as beginners. Baskent University ethics committee approval was obtained for the study. Laparoscopic stripping of the endometrioma was performed under general anesthesia in all of the patients. A Veress needle was used to perform a pneumoperitoneum of 15 mmHg following a 10-mm trocar inserted through a 10-mm umbilical incision. After laparoscopic exploration excluded obvious intraperitoneal coexisting pathologies, two additional 5- and 10-mm pararectal trocars were placed under direct laparoscopic vision. Adhesiolysis was performed if necessary; endometrioma foci were freed, and excised or coagulated by bipolar cautery. Dissection was begun from the anti-parametrial end, where it was closest to the cyst, and continued with a 1-cm incision over the cortex with scissors to clarify the cleavage. In most cases, however, the cyst was perforated during dissection and its content was aspirated; the field was immediately irrigated with saline. Dissection was then continued with stripping, applying bimanual counter traction with atraumatic graspers. Sharp dissection with scissors was done in case of dense adhesions were
found between the endometrioma capsule and hilum of ovary. In most cases, open edges of the ovaries were sutured with 3-0 absorbable polyglactin intracorporeal sutures (Vicryl; Ethicon, Somerville, NJ, USA) for hemostasis. The surgical specimen was taken out of the abdomen through the 10-mm pararectal trocar primarily in a tissue bag. The cyst cavity was examined for gross malignancy macroscopically and sent for pathological examination. One pathologist performed all the pathological examinations of the cases (F. A. B.). There were one to 19 paraffin blocks stored for each case. The number of the paraffin blocks prepared increased as cyst size enlarged. Two sections were taken from the densest part of each block and examined after staining with hematoxylin–eosin. Presence of ovary cortex adjacent to the cyst wall was assessed. We examined the follicular tissue on the specimen to identify the morphological structure of the ovarian tissue; it was then evaluated by semiquantitative scoring, and differed between 0 and 4, as defined by Maneschi et al. in 1993 (0, no follicular tissue; 1, only primordial follicles; 2, primordial and primary follicles; 3, secondary follicles; 4, a pattern of both primary and secondary follicles in the normal ovary).9 These scores were compared according to cyst size and the surgeon’s experience. χ2-Test cross-tables and Mann–Whitney U-tests were used for statistical analyses. Intergroup relations were accepted as significant when P < 0.05. SPSS for Windows version 18.0 (SPSS, Chicago, IL, USA) was used for statistical calculation.
Results Pathological paraffin blocks for patients who were operated on for endometrioma were reexamined. The mean age was 29.5 years (range, 21–39). Dysmenorrhea was present in 82.4%, dyspareunia in 50% and infertility in 69.2% of the patients. The mean diameter of endometriomas as measured by preoperative transvaginal ultrasonography was 42.6 mm (range, 5–100), with 26% (n = 28) of patients with bilateral endometriomas. Intracorporeal hemostatic sutures were used in 78.1% of patients. In 72.6% (n = 98) of endometriomas, a full thickness of ovarian cortical tissue adjacent to the cyst was observed. In 8.1% (n = 11) of them, there were only primordial follicles observed near the cyst wall (Fig. 1). In 19.3% (n = 26), pericystic tissue was free of ovarian tissue.
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When pathological findings were evaluated according to laparoscopic surgical experience, no significant difference was seen in terms of cyst wall thickness excised or in terms of primordial, primary and secondary follicle rates and presence of cortical tissue adjacent to the cyst capsule (all P > 0.05, Table 1). The mean diameter of endometriomas operated on by more experienced surgeons was shown to be shorter (P = 0.04). In addition, no difference was seen between surgeon groups in terms of follicular morphology score of the specimens (all P ≥ 0.05, Table 2). When endometriomas were subgrouped by diameter in 2-cm intervals (0–20 mm, 21–40 mm, 41–60 mm, 61–80 mm, 81–100 mm), no difference was observed for the ratio of ovarian tissue excised near the cyst wall (Table 3). Likewise, no significant difference was observed among groups for ovarian tissue loss or follicular scores when endometriomas were separated into two groups of less than 4 cm or 4 cm or more in diameter (P = 0.23 and P = 0.87, respectively).
Figure 1 Endometriotic cyst epithelium and endometrial stroma (short, thick arrows), cyst wall in the primordial follicles (long, thin arrows) and tertiary follicle (asterisk) (hematoxylin–eosin, original magnification ×40).
Among patients who were operated on for infertility, consequent pregnancy was observed in 40.5% (n = 30). The mean duration from surgery to pregnancy was 14 months (range, 2–60). Of all infertile patients, 13.5% had a spontaneous pregnancy, 6.8% became pregnant after intrauterine insemination and 20.3% became pregnant after intracytoplasmic sperm injection (following laparoscopic surgery for endometrioma).
Discussion Ovarian reserve is generally affected adversely after endometrioma surgery. This situation was shown to be the case by studies demonstrating a decrease in the number of follicles via in vitro fertilization treatment, as well as a decrease in serum anti-Müllerian hormone levels in the postoperative period.10–13 These studies draw attention to the results of decreased ovarian reserve due to endometrioma surgery. However, with this study, we assessed the rate of healthy ovary tissue loss after endometrioma surgery by histological analysis. When all the excised endometriomas were examined, 72.6% of them manifested with ovarian cortex, whereas only 8.1% of them had follicular structures near the cyst capsule. In other words, in approximately 80% of cases, some healthy ovarian tissue inevitably had to be removed. In a study performed by Muzii et al., healthy ovarian tissue was demonstrated beneath 54% of the endometriomas excised, but only in 6% of benign ovarian cysts.14 In another study by Dogan et al., normal ovarian tissue was shown to be removed in 92% of endometrioma cases, but in 82% for non-endometriotic cysts.6 Although the ratio of ovary damage differs for nonendometriotic cysts, it unfortunately remains high for endometriomas. Thus, endometrioma surgery is controversial; this is why laparoscopic surgery, a minimally invasive technique for it, is the current gold standard. On the other hand, a laparoscopic approach
Table 1 Comparison of pathological parameters and surgeon’s experience Gynecological endoscopist Ovary diameter (mm) Primordial (n)† Primary (n)† Secondary (n)† Cyst wall thickness (mm)† Positive for ovarian cortex (n)
40.8 ± 19 (5–100) 17.4 ± 24 (0–105) 3.4 ± 4.2 (0–26) 0.5 ± 0.9 (0–4) 3.19 ± 1.2 (1–6) 82 (71.9%)
Beginner endoscopist 52.7 ± 24 (5–100) 9.7 ± 19.2 (0–90) 2.2 ± 3.5 (0–15) 0.48 ± 1 (0–4) 2.95 ± 1 (1–4) 16 (76.2%)
P 0.035 0.22 0.12 0.51 0.53 0.45
†Mean ± standard deviation (range).
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provides earlier recovery and return to normal activity. However, it also requires a long learning curve with special expertise. Biacchiardi et al. pointed out that laparoscopic stripping of endometriosis can harm ovarian reserve even in experienced surgeons.15 In our study, surgeons were grouped as beginners and gynecological endoscopists who had completed their learning curve in laparoscopic endometriosis surgery. We examined the effect of a surgeon’s experience level on healthy ovarian tissue being excised unintentionally and did not see any significant difference (when assessed for ovarian cortical presence on specimens and with morphological scoring). While surgeons performing laparoscopy for more than 5 years were considered as more experienced in our study, proficiency in laparoscopic endometrioma surgery also may require experience with larger numbers of cases. Retto et al. demonstrated no grade 3 or 4 (resembling healthy ovary tissue) for morphological scores; they found only primordial and a few primary follicles in endometrioma cases treated with laparoscopic stripping.16 In contrast, some grade 4 and numerous grade 3 morphological scores were seen in our study, which points to secondary follicular damage occurring due to the surgery (Fig. 1). In the study mentioned above, Muzii et al. concluded there was an inverse correlation between surgical experience and thickness of the cyst wall excised.8 In our study, there was no difference in terms of cyst wall thickness between surgeon groups. We projected a similar argument based on surgical
Table 2 Semiquantitative scores of endometrioma cysts between surgeon groups Score
Gynecological endoscopist
Beginner endoscopist
P
0 1 2 3 4 Total
23 (20.2%) 14 (12.3%) 39 (34.2%) 32 (28.1%) 6 (5.3%) 114 (100%)
3 (14.3%) 6 (28.6%) 7 (33.3%) 3 (14.3%) 2 (9.5%) 21 (100%)
0.53 0.05 0.94 0.19 0.45
skills to determine dissection quality; however, we did not find any effect in terms of experience. Referral of more difficult cases to the experienced surgeons may help to explain this result. Unlike some other studies3,6 in which cyst wall thickness was found to be approximately 1–2 mm, it was shown to be approximately 3 mm in our study. As for histological examination, cyst wall thickness was measured as the thickest plane of the cyst. This measurement method may explain the difference in cyst wall thickness between the cases mentioned in the above published work and ours. In one study, Roman et al. showed that ovarian diameter is directly proportional to the volume of the ovary tissue excised.4 In another study by Tang and contributors, ovarian damage was shown to increase when endometrioma diameter exceeded 4 cm.17 On the contrary, we did not find any difference in the ratio of ovarian tissue or in morphological scores for endometriomas excised of less than 4 cm or 4 cm or more in diameter. When we examined an endometrioma’s clinical effect with detailed size parsing in 2-cm cases, no significant difference was observed either. The smaller the endometrioma was when dissected, the greater the amount of ovarian tissue that had to be sacrificed: this was due to difficulty in clarifying cleavage. On the other hand, larger endometriomas being dissected may cause much of the adherent ovarian tissue to be excised unintentionally. However, in our study, like Ramacahandran et al., we found no difference in the ratio of ovarian tissue being excised in different endometrioma sizes (Table 3).18 After surgery, in the follow-up period, spontaneous pregnancy ratio was lower than previously reported in other studies.6 We did not know the details of infertility reports of patients regarding whether had other infertility risk factors or not. The major limitation of our study is that the data, except pathology results, were collected retrospectively. There were fewer cases operated by the beginners, reducing the study’s power. We concluded that even when an endometrioma was operated on with a minimally invasive approach, it is
Table 3 Relation between presence of ovarian cortex in specimen and diameter of ovary Presence of ovarian cortex (n) No Yes
Observed (n) Predicted (n) Observed (n) Predicted (n)
P
0–20 (mm)
Diameter of ovary (mm) 21–40 (mm) 41–60 (mm) 61–80 (mm)
81–100 (mm)
7 5.5 13 14.5
14 16.7 47 44.3
2 1.6 4 4.4
10 9.3 24 24.7
4 3.8 10 10.2
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
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almost inevitable that it will harm ovarian reserve. In our study, we did not find an effect of surgeon’s experience on reducing damage to ovarian reserve during endometrioma surgery. Also, we did not find any difference in ovary damage in varying size of endometriomas excised. Excision of an endometrioma is still a difficult method, as it requires intensive dissection with a potential of loss of ovary reserve. Hence, more efforts will be required to find less invasive techniques.
7. 8.
9.
10.
Disclosure None of the authors have any conflict of interest associated with this study.
11.
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