- Email: [email protected]
Histologic analysis of specimens from laparoscopic endometrioma excision performed by different surgeons: does the surgeon matter?
Histologic analysis of specimens from laparoscopic endometrioma excision performed by different surgeons: does the surgeon matter? Ludovico Muzii, M.D.,a Riccardo Marana, M.D.,b Roberto Angioli, M.D.,a Antonella Bianchi, M.D.,c Gaspare Cucinella, M.D.,d Michele Vignali, M.D.,e Pierluigi Benedetti Panici, M.D.,f and Mauro Busacca, M.D.e a
Department of Obstetrics and Gynecology, Universita Campus BioMedico, Rome; b Department of Obstetrics and Gynecology, Istituto Scientifico Internazionale ‘‘Paolo VI’’ Universita Cattolica del Sacro Cuore, Rome; c Department of Pathology, Universita Campus BioMedico, Rome; d Universita degli Studi di Palermo, Palermo; e Department of Obstetrics and Gynecology, Universita degli Studi di Milano, Milan; and f Department of Obstetrics and Gynecology, Universita ‘‘Sapienza’’ Rome, Italy
Objective: To evaluate whether the amount of ovarian tissue inadvertently removed along with the endometrioma cyst wall at laparoscopy differs in relation to the operating surgeon’s level of expertise. Design: Multicenter, prospective trial. Setting: Four tertiary care university hospitals. Patient(s): Fifty patients, aged 25 to 40 years, with monolateral ovarian endometriomas who underwent laparoscopic excision. Intervention(s): Operation with the stripping technique by surgeons with specific expertise in endometriosis surgery in four centers (groups A, B, C, and D) and by residents with average training in laparoscopic surgery (group E). Main Outcome Measure(s): Histologic examination for the evaluation of the mean thickness of the cyst wall from each specimen, and the mean thickness and morphologic characteristics of any ovarian tissue removed. Result(s): No statistically significant differences were present in the rate of presence of ovarian tissue in the endometrioma wall specimens from the different groups (44%, 45%, 55%, 56%, and 60% in groups A, B, C, D, and E, respectively). For groups A þ B þ C þ D versus group E, a statistically significant difference was found in the mean thickness of the tissue specimens (1.51 mm vs. 1.91 mm, respectively) and in the mean thickness of ovarian tissue inadvertently excised (0.49 mm vs. 0.97 mm, respectively). Conclusion(s): Level of expertise in endometriosis surgery is inversely correlated with inadvertent removal of healthy ovarian tissue along with the endometrioma capsule. (Fertil Steril 2011;95:2116–9. 2011 by American Society for Reproductive Medicine.) Key Words: Endometriosis, laparoscopy, ovarian cysts
Laparoscopy is considered today the gold standard for the treatment of ovarian endometriomas (1, 2). At laparoscopy, most surgeons perform the so-called stripping technique, in which two atraumatic grasping forceps pull the cyst wall and the normal ovarian parenchyma in two opposite directions, thus developing the cleavage plane. Some investigators, however, have questioned the stripping technique, because it can be associated with removal of healthy ovarian tissue along with the endometrioma wall, with loss of follicles (3, 4). A few studies have reported on the histologic features of specimens obtained with the stripping technique at laparoscopy (5–11), with results that differed as to the amount of ovarian tissue removed (5, 7–9). Differences in the histologic features of the removed specimens reported in the literature may be due to different surgical techniques or to the differing levels of expertise of the surgeons performing the stripping procedure. Received January 19, 2011; accepted February 15, 2011; published online March 16, 2011. L.M. has nothing to disclose. R.M. has nothing to disclose. R.A. has nothing to disclose. A.B. has nothing to disclose. G.C. has nothing to disclose. M.V. has nothing to disclose. P.B.P. has nothing to disclose. M.B. has nothing to disclose. Reprint requests: Ludovico Muzii, M.D., Department of Obstetrics and Gy Campus BioMedico, Via A Del Portillo 21, 00128 necology, Universita Rome, Italy (E-mail: [email protected]).
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We assessed whether there is a correlation between the surgeon’s level of expertise in endometriosis surgery and the amount of inadvertently removed healthy ovarian tissue. We evaluated by histologic analysis the specimens obtained with the stripping technique at laparoscopy when performed by experienced surgeons from four centers of excellence for endometriosis treatment. We also evaluated specimens obtained after surgery performed by residents with specific training in laparoscopic surgery but with no formal training in endometriosis surgery (i.e., fewer than 10 laparoscopic procedures for endometriomas as first surgeon).
MATERIALS AND METHODS Between January 1, 2008, and December 31, 2009, 50 patients, aged 25 to 40 years, underwent laparoscopic excision of ovarian endometriomas. All patients had regular menstrual cycles at the time of surgery. None of the patients had previously had medical or surgical treatment for endometriosis. None of the patients had undergone previous pelvic surgery. The indication for surgery was chronic pelvic pain in all cases, with associated infertility in 12 cases. The mean cyst size found at preoperative transvaginal ultrasound was 4.5 cm, ranging from 3.5 to 6.5 cm. The mean age of the patients was 30 years (range: 25 to 38 years). Each center contributed 9 to 11 cases; one center, a teaching university hospital,
Fertility and Sterility Vol. 95, No. 6, May 2011 Copyright ª2011 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/$36.00 doi:10.1016/j.fertnstert.2011.02.034
TABLE 1 Tissue thickness of endometrioma cyst wall and of ovarian tissue in millimeters. Tissue Endometrioma cyst walla Ovarian tissueb
Group A (n [ 9)
Group B (n [ 11)
Group C (n [ 11)
Group D (n [ 9)
Groups A D B D C D D (n [ 40)
Group E (n [ 10)
1.60 0.48 0.55 0.44
1.33 0.30 0.42 0.16
1.49 0.31 0.48 0.29
1.62 0.39 0.54 0.36
1.51 0.37 0.49 0.30
1.91 0.44 0.97 0.29
Note: Values are mean standard deviation. a P¼ .005 for groups A þ B þ C þ D (experienced surgeons) versus group E (residents), Student’s t-test. All other comparisons are not statistically significant (Kruskal-Wallis test). b P¼ .002 for groups A þ B þ C þ D (experienced surgeons) versus group E (residents), Student’s t-test. All other comparisons are not statistically significant (Kruskal-Wallis test). Muzii. Techniques and instrumentation. Fertil Steril 2011.
contributed 10 additional cases performed by a resident trained in laparoscopic surgery but with no specific training in endometrioma surgery. Operative laparoscopy was performed as previously reported elsewhere (6, 7). The endometrioma wall, after identification of the cleavage plane, was stripped off the remaining ovarian parenchyma through traction exerted in opposite directions with two atraumatic grasping forceps. When necessary, hemostasis was obtained with bipolar forceps applied on the ovarian parenchyma. No sutures were used for reapproximation of the ovarian edges. All four centers were performing the same surgical technique at the time of the study. Consistency on the technique and on the modalities of specimen selection was obtained by consensus, after video and slide review of surgical cases. The study design aimed at collecting 10 consecutive cases from each center (defined groups A, B, C, and D), with a range tolerance of 9 to 11. Ten additional cases were performed by residents from one of the centers (group E). After excision of the entire cyst wall, the specimen was examined in the operating theater by the surgeon, who selected a 2 2 cm sample taken from the intermediate part of the specimen (i.e., midway between the part where the stripping was initiated, usually at the site of ovarian adhesion to the lateral pelvic wall, and the final part, usually near the ovarian hilus). The selected specimen was sent for inclusion in the present study, and was evaluated centrally at Universita Campus BioMedico by the same pathologist, who was blinded to the clinical and surgical history of the patient. The remaining part of the cyst wall was sent for routine histologic examination at the histology department of each institution. The blinded pathologist evaluated the presence or absence of ovarian tissue adjacent to the cyst wall. The morphologic characteristics of the ovarian tissue, when present, were graded on a semiquantitative scale of 0 to 4 (0 ¼ complete absence of follicles; 1 ¼ primordial follicles only; 2 ¼ primordial and primary follicles; 3 ¼ some secondary follicles; 4 ¼ pattern of primary and secondary follicles as seen in normal ovary) (12). Additionally, the pathologist recorded the mean thickness of the cyst wall from each specimen, measured in millimeters, and the mean thickness of the ovarian tissue removed, when present. Statistical analysis was performed with the chi-square test or the Fisher’s exact test, where appropriate, for categorical variables, with Student’s t-test for continuous variables and with Kruskal-Wallis test for multiple comparisons. P<.05 was considered statistically significant. Specific institutional review board approval was not requested for the present study because this study did not change the management of patients with endometriosis that is usually performed at the four centers. Fertility and Sterility
RESULTS In the 50 patients, excision of the ovarian cysts was completed successfully by laparoscopy. The operating times were not statistically significantly different among in the various groups. No intraoperative or postoperative complications occurred. Endometriosis was confirmed at histology in all cases. No statistically significant differences were present as to the rate of presence of ovarian tissue in the endometrioma wall specimens from the different groups (44%, 45%, 55%, 56%, and 60% in groups A, B, C, D, and E, respectively; P¼.95). The median morphologic grade was 0 (range: 0 to 2) in groups A, B, C, and D, and 1 (range: 0 to 4) in group E. The morphologic grade did not differ statistically significantly among groups (P¼.67). Differences in the mean thickness of the tissue specimens and in the mean thickness of ovarian tissue that was inadvertently excised among groups A, B, C, and D were not statistically significant (Table 1). A statistically significant difference was present in the thickness of the tissue specimens (1.51 0.37 mm vs. 1.91 0.44 mm, P¼.005) and in the thickness of ovarian tissue
FIGURE 1 Full-thickness specimen from the cyst wall of an endometrioma obtained via the stripping technique performed by an experienced surgeon. (Stain: hematoxylin and eosin; magnification: 10.) The tissue specimen thickness is 1.3 mm, and scanty ovarian tissue is present on the right, with no evidence of follicles (grade 0).
Muzii. Techniques and instrumentation. Fertil Steril 2011.
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FIGURE 2 Full-thickness specimen from the cyst wall of an endometrioma obtained via the stripping technique performed by a surgeon in training. (Stain: hematoxylin and eosin; magnification: 10.) The tissue specimen thickness is 1.9 mm, and ovarian tissue is present, with evidence of a primordial follicle (grade 1) on the right upper quadrant of the slide.
Muzii. Techniques and instrumentation. Fertil Steril 2011.
inadvertently excised (0.49 0.30 mm vs. 0.97 0.29 mm, P¼.002) when considering groups A þ B þ C þ D together versus group E (Figs. 1 and 2).
DISCUSSION Recently, the laparoscopic technique of endometrioma excision has been questioned, as stripping of the cyst wall may result in removal of excess ovarian tissue, with possible loss of follicles (3, 4). Some indirect evidence from the literature has shown that ovaries that undergo excision of ovarian cysts perform worse than nonoperated ovaries when the patients receive ovarian stimulation for assisted reproduction techniques (13, 14). In addition, smaller ovarian volumes after surgery have been reported for the operated ovary at sonographic follow-up evaluation (15, 16). Histology studies have consistently demonstrated that some ovarian tissue is inadvertently removed along together with the endometrioma wall. The rate of ovarian tissue removal is between 54% and 100% in the various studies (5–11). Only a few studies, however, have measured the thickness of the removed ovarian tissue (5, 7–9). Also, only rarely have the histologic features of the removed ovarian tissue been described (7–9). In a previous study by our group (7), we demonstrated that, in most of the specimen, the thickness of the cyst wall is 1.4 mm, and the ovarian tissue removed along with it, when present, is only 0.3 mm. Also, for the whole cyst wall specimen, except the part toward the ovarian hilus, the ovarian tissue removed is mainly constituted by tissue with no follicles or with only primordial
follicles. In other words, the ovarian tissue that is being removed is mostly fibrotic, with little or no functional tissue. In another study by our group (8), the mean thickness of the ovarian cyst wall removed was confirmed to be 1.4 mm, reaching a maximal value of 1.8 mm only in few areas of the specimen. Other studies have report data conflicting in part with our previous report. In a study by Hachisuga et al. (5), the mean thickness of the cyst wall is reported as 2.1 mm for endometriomas that are easily stripped, and 1.8 mm for cysts that are hardly stripped from the remaining ovary. Also, in the former group of easily stripped endometriomas, the removed ovarian tissue has more follicles and, sometimes, attached corpus albicans. A possible interpretation of these data is that, particularly in the former group, a wrong plane of cleavage has been developed, yielding loss of follicles. An alternative explanation for the conflicting data could be the difference in study populations, in surgical techniques, or in tissue processing. Vicino et al. (9) recently reported a mean cyst wall thickness of 2.1 mm in a series of 76 patients with ovarian endometriomas. The mean follicular histologic score in this study was 2.3, meaning that most of the patients had both primordial and primary follicles, thus associated with substantial loss of follicles. In our present study, we demonstrated that level of surgical expertise plays a role in the amount of ovarian tissue removed incidentally with the endometrioma wall. In our series, a statistically significant difference was present in the amount of ovarian tissue removed by surgeons who were formally trained in laparoscopic surgery but had no specific expertise in endometriosis surgery. Some ovarian tissue was present in approximately the same rate among the different groups, between 44% and 60%, therefore demonstrating that some ovarian tissue loss is inevitable. In most cases, especially in experienced hands, the ovarian tissue inadvertently excised appeared to be morphologically altered and therefore possibly nonfunctional (6, 12). However, the amount of this loss differed among the groups of patients, with the largest amount in the group operated by residents who were trained in laparoscopic surgery but had no formal training in laparoscopic surgery for endometriomas. The difference in the amount of healthy ovarian tissue removed may be explained only by the difference in surgical expertise, as the patient population was comparable among the groups, the surgical technique was the same, and the specimens were processed centrally and evaluated by the same pathologist. Although some differences were present among the various groups of expert surgeons, they did not reach statistical significance, therefore confirming that the surgical techniques and the levels of expertise were comparable. The level of expertise in endometriosis surgery was inversely correlated with the amount of ovarian tissue inadvertently removed with the endometrioma wall. Surgeons trained in laparoscopic surgery but without specific expertise in endometriosis surgery may be less proficient in surgery for endometriomas. Specimens obtained via surgery performed by residents have statistically significantly more ovarian tissue when compared with those obtained by experienced surgeons with years of practice in the field of reproductive and endometriosis surgery. In experienced hands, laparoscopic stripping of endometriomas appears to be a technique that does not significantly damage the ovarian tissue.
REFERENCES 1. Kennedy S, Bergqvist A, Chapron C, D’Hooghe T, Dunselman G, Greb R, et al. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 2005;20:2698–704.
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Muzii et al.
2. Hart R, Hickey M, Maouris P, Buckett W, Garry R. Excisional surgery versus ablative surgery for ovarian endometriomata: a Cochrane Review. Hum Reprod 2005;20:3000–7.
Techniques and instrumentation
3. Brosens IA, Van Ballaer P, Puttemans P, Deprest J. Reconstruction of the ovary containing large endometriomas by an extraovarian endosurgical technique. Fertil Steril 1996;66:517–21.
Vol. 95, No. 6, May 2011
4. Donnez J, Nisolle M, Gillet N, Smets M, Bassil S, Casanas-Roux F. Large ovarian endometriomas. Hum Reprod 1996;11:641–6. 5. Hachisuga T, Kawarabayashi T. Histopathological analysis of laparoscopically treated ovarian endometriotic cysts with special reference to loss of follicles. Hum Reprod 2002;17:432–5. 6. Muzii L, Bianchi A, Croce’ C, Manci N, Benedetti Panici P. Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure? Fertil Steril 2002;77:609–14. 7. Muzii L, Bellati F, Bianchi A, Palaia I, Manci N, Zullo MA, et al. Laparoscopic stripping of endometriomas: a randomized trial on different surgical techniques. Part II: pathological results. Hum Reprod 2005;20:1987–92. 8. Muzii L, Bianchi A, Bellati F, Cristi E, Pernice M, Zullo MA, et al. Histologic analysis of endometriomas: what the surgeon needs to know. Fertil Steril 2007;87:362–6.
Fertility and Sterility
9. Vicino M, Resta L, Scioscia M, Marzullo A, Ceci O, Bettocchi S. Correlation between serum levels of CA 125 and follicular loss after laparoscopic cystectomy in women with ovarian endometrioma. J Min Invasive Gynecol 2007;14:223–7. 10. Alborzi S, Foroughinia L, Kumar PV, Asadi N, Alborzi S. A comparison of histopathologic findings of ovarian tissue inadvertently excised with endometrioma and other kinds of benign ovarian cyst in patients undergoing laparoscopy versus laparotomy. Fertil Steril 2009;92:2004–7. 11. Matsuzaki S, Houlle C, Darcha C, Pouly JL, Mage G, Canis M. Analysis of risk factors for the removal of normal ovarian tissue during laparoscopic cystectomy for ovarian endometriosis. Hum Reprod 2009;24:1402–6. 12. Maneschi F, Marasa L, Incandela S, Mazzarese M, Zupi E. Ovarian cortex surrounding benign neoplasms: a histologic study. Am J Obstet Gynecol 1993;169:388–93.
13. Garcia-Velasco JA, Mahutte NG, Corona J, Zuniga V, Giles J, Arici A, et al. Removal of endometriomas before in vitro fertilization does not improve fertility outcomes: a matched, case-control study. Fertil Steril 2004;81:1194–7. 14. Somigliana E, Ragni G, Benedetti F, Borroni R, Vegetti W, Crosignani PG. Does laparoscopic excision of endometriotic ovarian cysts significantly affects ovarian reserve? Insights from IVF cycles. Hum Reprod 2003;18:2450–3. 15. Exacoustos C, Zupi E, Amadio A, Szabolcs B, De Vivo B, Marconi D, et al. Laparoscopic removal of endometriomas: sonographic evaluation of residual functioning ovarian tissue. Am J Obstet Gynecol 2004;191:68–72. 16. Candiani M, Barbieri M, Bottani B, Bertulessi C, Vignali M, Agnoli B, et al. Ovarian recovery after laparoscopic enucleation of ovarian cysts: insights from echographic short-term postsurgical follow-up. J Minim Invasive Gynecol 2005;12:409–14.
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Department of Obstetrics and Gynecology, Universita Campus BioMedico, Rome; b Department of Obstetrics and Gynecology, Istituto Scientifico Internazionale ‘‘Paolo VI’’ Universita Cattolica del Sacro Cuore, Rome; c Department of Pathology, Universita Campus BioMedico, Rome; d Universita degli Studi di Palermo, Palermo; e Department of Obstetrics and Gynecology, Universita degli Studi di Milano, Milan; and f Department of Obstetrics and Gynecology, Universita ‘‘Sapienza’’ Rome, Italy
Objective: To evaluate whether the amount of ovarian tissue inadvertently removed along with the endometrioma cyst wall at laparoscopy differs in relation to the operating surgeon’s level of expertise. Design: Multicenter, prospective trial. Setting: Four tertiary care university hospitals. Patient(s): Fifty patients, aged 25 to 40 years, with monolateral ovarian endometriomas who underwent laparoscopic excision. Intervention(s): Operation with the stripping technique by surgeons with specific expertise in endometriosis surgery in four centers (groups A, B, C, and D) and by residents with average training in laparoscopic surgery (group E). Main Outcome Measure(s): Histologic examination for the evaluation of the mean thickness of the cyst wall from each specimen, and the mean thickness and morphologic characteristics of any ovarian tissue removed. Result(s): No statistically significant differences were present in the rate of presence of ovarian tissue in the endometrioma wall specimens from the different groups (44%, 45%, 55%, 56%, and 60% in groups A, B, C, D, and E, respectively). For groups A þ B þ C þ D versus group E, a statistically significant difference was found in the mean thickness of the tissue specimens (1.51 mm vs. 1.91 mm, respectively) and in the mean thickness of ovarian tissue inadvertently excised (0.49 mm vs. 0.97 mm, respectively). Conclusion(s): Level of expertise in endometriosis surgery is inversely correlated with inadvertent removal of healthy ovarian tissue along with the endometrioma capsule. (Fertil Steril 2011;95:2116–9. 2011 by American Society for Reproductive Medicine.) Key Words: Endometriosis, laparoscopy, ovarian cysts
Laparoscopy is considered today the gold standard for the treatment of ovarian endometriomas (1, 2). At laparoscopy, most surgeons perform the so-called stripping technique, in which two atraumatic grasping forceps pull the cyst wall and the normal ovarian parenchyma in two opposite directions, thus developing the cleavage plane. Some investigators, however, have questioned the stripping technique, because it can be associated with removal of healthy ovarian tissue along with the endometrioma wall, with loss of follicles (3, 4). A few studies have reported on the histologic features of specimens obtained with the stripping technique at laparoscopy (5–11), with results that differed as to the amount of ovarian tissue removed (5, 7–9). Differences in the histologic features of the removed specimens reported in the literature may be due to different surgical techniques or to the differing levels of expertise of the surgeons performing the stripping procedure. Received January 19, 2011; accepted February 15, 2011; published online March 16, 2011. L.M. has nothing to disclose. R.M. has nothing to disclose. R.A. has nothing to disclose. A.B. has nothing to disclose. G.C. has nothing to disclose. M.V. has nothing to disclose. P.B.P. has nothing to disclose. M.B. has nothing to disclose. Reprint requests: Ludovico Muzii, M.D., Department of Obstetrics and Gy Campus BioMedico, Via A Del Portillo 21, 00128 necology, Universita Rome, Italy (E-mail: [email protected]).
2116
We assessed whether there is a correlation between the surgeon’s level of expertise in endometriosis surgery and the amount of inadvertently removed healthy ovarian tissue. We evaluated by histologic analysis the specimens obtained with the stripping technique at laparoscopy when performed by experienced surgeons from four centers of excellence for endometriosis treatment. We also evaluated specimens obtained after surgery performed by residents with specific training in laparoscopic surgery but with no formal training in endometriosis surgery (i.e., fewer than 10 laparoscopic procedures for endometriomas as first surgeon).
MATERIALS AND METHODS Between January 1, 2008, and December 31, 2009, 50 patients, aged 25 to 40 years, underwent laparoscopic excision of ovarian endometriomas. All patients had regular menstrual cycles at the time of surgery. None of the patients had previously had medical or surgical treatment for endometriosis. None of the patients had undergone previous pelvic surgery. The indication for surgery was chronic pelvic pain in all cases, with associated infertility in 12 cases. The mean cyst size found at preoperative transvaginal ultrasound was 4.5 cm, ranging from 3.5 to 6.5 cm. The mean age of the patients was 30 years (range: 25 to 38 years). Each center contributed 9 to 11 cases; one center, a teaching university hospital,
Fertility and Sterility Vol. 95, No. 6, May 2011 Copyright ª2011 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/$36.00 doi:10.1016/j.fertnstert.2011.02.034
TABLE 1 Tissue thickness of endometrioma cyst wall and of ovarian tissue in millimeters. Tissue Endometrioma cyst walla Ovarian tissueb
Group A (n [ 9)
Group B (n [ 11)
Group C (n [ 11)
Group D (n [ 9)
Groups A D B D C D D (n [ 40)
Group E (n [ 10)
1.60 0.48 0.55 0.44
1.33 0.30 0.42 0.16
1.49 0.31 0.48 0.29
1.62 0.39 0.54 0.36
1.51 0.37 0.49 0.30
1.91 0.44 0.97 0.29
Note: Values are mean standard deviation. a P¼ .005 for groups A þ B þ C þ D (experienced surgeons) versus group E (residents), Student’s t-test. All other comparisons are not statistically significant (Kruskal-Wallis test). b P¼ .002 for groups A þ B þ C þ D (experienced surgeons) versus group E (residents), Student’s t-test. All other comparisons are not statistically significant (Kruskal-Wallis test). Muzii. Techniques and instrumentation. Fertil Steril 2011.
contributed 10 additional cases performed by a resident trained in laparoscopic surgery but with no specific training in endometrioma surgery. Operative laparoscopy was performed as previously reported elsewhere (6, 7). The endometrioma wall, after identification of the cleavage plane, was stripped off the remaining ovarian parenchyma through traction exerted in opposite directions with two atraumatic grasping forceps. When necessary, hemostasis was obtained with bipolar forceps applied on the ovarian parenchyma. No sutures were used for reapproximation of the ovarian edges. All four centers were performing the same surgical technique at the time of the study. Consistency on the technique and on the modalities of specimen selection was obtained by consensus, after video and slide review of surgical cases. The study design aimed at collecting 10 consecutive cases from each center (defined groups A, B, C, and D), with a range tolerance of 9 to 11. Ten additional cases were performed by residents from one of the centers (group E). After excision of the entire cyst wall, the specimen was examined in the operating theater by the surgeon, who selected a 2 2 cm sample taken from the intermediate part of the specimen (i.e., midway between the part where the stripping was initiated, usually at the site of ovarian adhesion to the lateral pelvic wall, and the final part, usually near the ovarian hilus). The selected specimen was sent for inclusion in the present study, and was evaluated centrally at Universita Campus BioMedico by the same pathologist, who was blinded to the clinical and surgical history of the patient. The remaining part of the cyst wall was sent for routine histologic examination at the histology department of each institution. The blinded pathologist evaluated the presence or absence of ovarian tissue adjacent to the cyst wall. The morphologic characteristics of the ovarian tissue, when present, were graded on a semiquantitative scale of 0 to 4 (0 ¼ complete absence of follicles; 1 ¼ primordial follicles only; 2 ¼ primordial and primary follicles; 3 ¼ some secondary follicles; 4 ¼ pattern of primary and secondary follicles as seen in normal ovary) (12). Additionally, the pathologist recorded the mean thickness of the cyst wall from each specimen, measured in millimeters, and the mean thickness of the ovarian tissue removed, when present. Statistical analysis was performed with the chi-square test or the Fisher’s exact test, where appropriate, for categorical variables, with Student’s t-test for continuous variables and with Kruskal-Wallis test for multiple comparisons. P<.05 was considered statistically significant. Specific institutional review board approval was not requested for the present study because this study did not change the management of patients with endometriosis that is usually performed at the four centers. Fertility and Sterility
RESULTS In the 50 patients, excision of the ovarian cysts was completed successfully by laparoscopy. The operating times were not statistically significantly different among in the various groups. No intraoperative or postoperative complications occurred. Endometriosis was confirmed at histology in all cases. No statistically significant differences were present as to the rate of presence of ovarian tissue in the endometrioma wall specimens from the different groups (44%, 45%, 55%, 56%, and 60% in groups A, B, C, D, and E, respectively; P¼.95). The median morphologic grade was 0 (range: 0 to 2) in groups A, B, C, and D, and 1 (range: 0 to 4) in group E. The morphologic grade did not differ statistically significantly among groups (P¼.67). Differences in the mean thickness of the tissue specimens and in the mean thickness of ovarian tissue that was inadvertently excised among groups A, B, C, and D were not statistically significant (Table 1). A statistically significant difference was present in the thickness of the tissue specimens (1.51 0.37 mm vs. 1.91 0.44 mm, P¼.005) and in the thickness of ovarian tissue
FIGURE 1 Full-thickness specimen from the cyst wall of an endometrioma obtained via the stripping technique performed by an experienced surgeon. (Stain: hematoxylin and eosin; magnification: 10.) The tissue specimen thickness is 1.3 mm, and scanty ovarian tissue is present on the right, with no evidence of follicles (grade 0).
Muzii. Techniques and instrumentation. Fertil Steril 2011.
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FIGURE 2 Full-thickness specimen from the cyst wall of an endometrioma obtained via the stripping technique performed by a surgeon in training. (Stain: hematoxylin and eosin; magnification: 10.) The tissue specimen thickness is 1.9 mm, and ovarian tissue is present, with evidence of a primordial follicle (grade 1) on the right upper quadrant of the slide.
Muzii. Techniques and instrumentation. Fertil Steril 2011.
inadvertently excised (0.49 0.30 mm vs. 0.97 0.29 mm, P¼.002) when considering groups A þ B þ C þ D together versus group E (Figs. 1 and 2).
DISCUSSION Recently, the laparoscopic technique of endometrioma excision has been questioned, as stripping of the cyst wall may result in removal of excess ovarian tissue, with possible loss of follicles (3, 4). Some indirect evidence from the literature has shown that ovaries that undergo excision of ovarian cysts perform worse than nonoperated ovaries when the patients receive ovarian stimulation for assisted reproduction techniques (13, 14). In addition, smaller ovarian volumes after surgery have been reported for the operated ovary at sonographic follow-up evaluation (15, 16). Histology studies have consistently demonstrated that some ovarian tissue is inadvertently removed along together with the endometrioma wall. The rate of ovarian tissue removal is between 54% and 100% in the various studies (5–11). Only a few studies, however, have measured the thickness of the removed ovarian tissue (5, 7–9). Also, only rarely have the histologic features of the removed ovarian tissue been described (7–9). In a previous study by our group (7), we demonstrated that, in most of the specimen, the thickness of the cyst wall is 1.4 mm, and the ovarian tissue removed along with it, when present, is only 0.3 mm. Also, for the whole cyst wall specimen, except the part toward the ovarian hilus, the ovarian tissue removed is mainly constituted by tissue with no follicles or with only primordial
follicles. In other words, the ovarian tissue that is being removed is mostly fibrotic, with little or no functional tissue. In another study by our group (8), the mean thickness of the ovarian cyst wall removed was confirmed to be 1.4 mm, reaching a maximal value of 1.8 mm only in few areas of the specimen. Other studies have report data conflicting in part with our previous report. In a study by Hachisuga et al. (5), the mean thickness of the cyst wall is reported as 2.1 mm for endometriomas that are easily stripped, and 1.8 mm for cysts that are hardly stripped from the remaining ovary. Also, in the former group of easily stripped endometriomas, the removed ovarian tissue has more follicles and, sometimes, attached corpus albicans. A possible interpretation of these data is that, particularly in the former group, a wrong plane of cleavage has been developed, yielding loss of follicles. An alternative explanation for the conflicting data could be the difference in study populations, in surgical techniques, or in tissue processing. Vicino et al. (9) recently reported a mean cyst wall thickness of 2.1 mm in a series of 76 patients with ovarian endometriomas. The mean follicular histologic score in this study was 2.3, meaning that most of the patients had both primordial and primary follicles, thus associated with substantial loss of follicles. In our present study, we demonstrated that level of surgical expertise plays a role in the amount of ovarian tissue removed incidentally with the endometrioma wall. In our series, a statistically significant difference was present in the amount of ovarian tissue removed by surgeons who were formally trained in laparoscopic surgery but had no specific expertise in endometriosis surgery. Some ovarian tissue was present in approximately the same rate among the different groups, between 44% and 60%, therefore demonstrating that some ovarian tissue loss is inevitable. In most cases, especially in experienced hands, the ovarian tissue inadvertently excised appeared to be morphologically altered and therefore possibly nonfunctional (6, 12). However, the amount of this loss differed among the groups of patients, with the largest amount in the group operated by residents who were trained in laparoscopic surgery but had no formal training in laparoscopic surgery for endometriomas. The difference in the amount of healthy ovarian tissue removed may be explained only by the difference in surgical expertise, as the patient population was comparable among the groups, the surgical technique was the same, and the specimens were processed centrally and evaluated by the same pathologist. Although some differences were present among the various groups of expert surgeons, they did not reach statistical significance, therefore confirming that the surgical techniques and the levels of expertise were comparable. The level of expertise in endometriosis surgery was inversely correlated with the amount of ovarian tissue inadvertently removed with the endometrioma wall. Surgeons trained in laparoscopic surgery but without specific expertise in endometriosis surgery may be less proficient in surgery for endometriomas. Specimens obtained via surgery performed by residents have statistically significantly more ovarian tissue when compared with those obtained by experienced surgeons with years of practice in the field of reproductive and endometriosis surgery. In experienced hands, laparoscopic stripping of endometriomas appears to be a technique that does not significantly damage the ovarian tissue.
REFERENCES 1. Kennedy S, Bergqvist A, Chapron C, D’Hooghe T, Dunselman G, Greb R, et al. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 2005;20:2698–704.
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Muzii et al.
2. Hart R, Hickey M, Maouris P, Buckett W, Garry R. Excisional surgery versus ablative surgery for ovarian endometriomata: a Cochrane Review. Hum Reprod 2005;20:3000–7.
Techniques and instrumentation
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