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Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure?
FERTILITY AND STERILITY威 VOL. 77, NO. 3, MARCH 2002 Copyright ©2002 American Society for Reproductive Medicine Published by Elsevier Science Inc. Printed on acid-free paper in U.S.A.
TECHNIQUES AND INSTRUMENTATION
Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure? Ludovico Muzii, M.D.,a Antonella Bianchi, M.D.,b Clara Croce`, M.D.,a Natalina Manci, M.D.,a and Pierluigi Benedetti Panici, M.D.a Libera Universita` Campus Bio-Medico, Rome, Italy
Objective: To determine whether the stripping technique by laparoscopy is a tissue-sparing procedure. Design: Prospective study. Setting: University hospital. Patient(s): Forty-two women, 21 to 35 years of age, who had a unilateral ovarian cyst (26 endometriomas, 7 serous, 6 dermoid, and 3 mucinous cysts). Intervention(s): Laparoscopic excision of ovarian cysts by using the stripping technique. Main Outcome Measure(s): Histologic analysis of the excised specimens was done to evaluate the presence and nature of ovarian tissue adjacent to the cyst wall. Result(s): Recognizable ovarian tissue adjacent to the cyst wall was present in 15 of 42 excised specimens (36%). A significant difference was present for endometriomas versus nonendometriosis cysts (ovarian tissue was present in 14 of 26 specimens [54%] vs. 1 of 16 specimens [6%]; P⬍.005). No specimen showed the normal follicular pattern observed in healthy ovaries. Conclusion(s): The stripping technique appears to be a tissue-sparing procedure. In 36% of the cysts, ovarian tissue is excised together with the cyst wall, but this tissue does not show the morphologic characteristics observed in normal ovarian tissue. (Fertil Steril威 2002;77:609 –14. ©2002 by American Society for Reproductive Medicine.) Key Words: Endometriosis, laparoscopy, ovarian cysts, surgical technique
Laparoscopy is considered the gold standard for treatment of benign ovarian cysts. Compared with traditional surgery by laparotomy, operative laparoscopy is associated with a shorter hospital stay, faster patient recovery, decreased costs (1), and a lower incidence of de novo adhesion formation (2– 4). Received April 19, 2001; revised and accepted September 10, 2001. Reprint requests: Ludovico Muzii, M.D., Area di Ginecologia, Libera Universita` Campus BioMedico, Via E. Longoni 83, Rome 00155, Italy (FAX: 39-06-2252294; E-mail: [email protected]) a Department of Gynecology. b Department of Pathology. 0015-0282/02/$20.00 PII S0015-0282(01)03203-4
The surgical technique of ovarian cyst excision by laparoscopy differs from traditional surgery performed at laparotomy. At laparoscopy (5– 8), most surgeons perform the socalled stripping technique, in which two atraumatic grasping forceps are used to pull the cyst wall and the normal ovarian parenchyma in opposite directions, thus developing the cleavage plane. After excision of the cyst wall, hemostasis is achieved by using bipolar forceps or CO2 laser. The residual ovarian tissue is not sutured, and the ovarian edges are left to heal by secondary intention. In contrast, at laparot-
omy, the cleavage plane is developed by using microsurgical techniques and instruments. After excision of the cyst wall, meticulous reconstruction of the ovarian cortex is performed with sutures. Recently, Brosens et al. (9) and Donnez et al. (10) have questioned the stripping technique because it is associated with removal of ovarian tissue along with the wall of ovarian cysts, especially endometriomas, causing loss of follicles. To our knowledge, however, no study has reported on the histologic features of specimens obtained by using the stripping technique at laparoscopy. Anecdotal reports have suggested that a rim of normal appearing ovary can surround the endometriotic tissue and the fibrotic pseudocapsule in specimens removed by using the stripping technique (6, 11). We performed histologic analysis of specimens obtained by using the stripping technique 609
FIGURE 1 Full-thickness specimen from the cyst wall of a mucinous cyst, obtained by using the stripping technique at laparoscopy. At the right edge, mucinous epithelium is visible, whereas in the left edge, no ovarian tissue is present. Hematoxylin and eosin; magnification, ⫻40.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
for ovarian cyst excision at operative laparoscopy to verify whether ovarian tissue is inadvertently excised together with the cyst wall and to investigate the morphologic characteristics of this tissue.
MATERIALS AND METHODS Between January 1, 1998, and December 31, 1999, 42 patients 21 to 35 years of age underwent laparoscopic excision of ovarian cysts. All patients were experiencing regular menstrual cycles at the time of surgery. No patient had had previous medical or surgical treatment of the ovarian cyst or previous pelvic surgery. At least three spontaneous menstrual cycles were allowed between the first ultrasonographic diagnosis of ovarian cyst and subsequent hospital admission for surgery. At hospital admission, all patients underwent transvaginal ultrasonography to confirm the presence of ovarian cysts. Mean cyst size was 4.5 cm (range, 3.5 to 9.0 cm). Operative laparoscopy was performed as reported elsewhere (8). In brief, after induction of general anesthesia, a 10-mm laparoscope was introduced through the umbilicus, and three accessory 5-mm trocars were placed suprapubically for introduction of accessory instruments. After initial diagnostic evaluation of the pelvis and abdomen and washing, and if no sign of malignancy was present, the ovarian cyst was punc610
Muzii et al.
Laparoscopic excision of ovarian cysts
tured, the contents were aspirated and visually inspected, and the inner wall of the cyst was checked for possible vegetations. In case of ultrasonographic diagnosis of dermoid cyst, the cyst was not intentionally punctured; every effort was made to excise the entire cyst without spilling its content. After identification of the cleavage plane, the cyst wall was stripped off the remaining ovarian parenchyma through traction exerted in opposite directions by using two atraumatic grasping forceps. When necessary, hemostasis was achieved with bipolar forceps applied on the ovarian parenchyma. No sutures were used for reapproximation of the ovarian edges. 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 ovarian fossa, and the final part, usually near the ovarian hilus). The selected specimen was sent for inclusion in our study and was evaluated 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. Portions of the specimen obtained from the initial and final parts of the stripping procedure were excluded from our Vol. 77, No. 3, March 2002
FIGURE 2 Full-thickness specimen from an endometrioma cyst wall. At the lower edge, endometrial epithelium and stroma are visible, whereas at the upper edge, fibroreactive tissue with no evidence of follicles is present. Hematoxylin and eosin; magnification, ⫻40.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
study because the surgical technique of cyst excision in the area of ovarian adhesion to the ovarian fossa and in the area of the hilus, where the cyst wall may be densely adherent, may vary from patient to patient and among different surgeons (6, 12), thus possibly yielding noncomparable specimens. For our study, the blinded pathologist evaluated the presence or absence of ovarian tissue adjacent to the cyst wall and graded the morphologic characteristics of this tissue on a semiquantitative scale of 0 to 4 (0, complete absence of follicles; 1, primordial follicles only; 2, primordial and primary follicles; 3, some secondary follicles; 4, pattern of primary and secondary follicles as seen in normal ovary) (13). Statistical analysis was performed by using the 2 test or the Fisher exact test, where appropriate, for categorical variables. P⬍.05 was considered statistically significant. We did not request institutional review board approval for the study because it did not change the management of patients with endometriosis usually followed at our institution.
postoperative complications occurred. All patients were discharged in the first 24 hours after surgery. Histologic classification of the specimens was as follows: endometriotic cyst in 26 cases (62%), serous cyst in 7 cases (17%), dermoid cyst in 6 (14%) and mucinous cyst in 3 cases (7%). Routine histologic examination of the entire specimen confirmed the blinded histologic examination in all cases. Adjacent ovarian tissue was present in 15 of 42 specimens (36%). This ovarian tissue was approximately 1 to 2 mm in thickness. No ovarian tissue was found in 27 specimens (64%) (Figs. 1 and 2). Ovarian tissue was present in 14 of 26 endometrioma cyst walls (54%), 1 of 6 dermoids (17%), and none of the 7 serous and 3 mucinous cysts (P⫽.0016 for endometriotic versus nonendometriotic cysts). With regard to morphologic characteristics, the ovarian tissue excised with the cyst wall was graded as 0 in 11 of 15 specimens (73%), 1 in 3 specimens (20%) (Figs. 3 and 4), and 2 in 1 specimen (7%). In no specimen, class 3 or 4 ovarian tissue was present.
DISCUSSION RESULTS In the 42 patients, excision of the ovarian cysts was completed successfully by laparoscopy. No intraoperative or FERTILITY & STERILITY威
Some investigators (9, 10) have questioned use of the laparoscopic technique for ovarian cyst excision, particularly in the case of ovarian endometriomas, because stripping of 611
FIGURE 3 Full-thickness specimen from an endometrioma cyst wall. At the lower edge, endometrial epithelium and stroma are visible, whereas at the upper edge, ovarian tissue with scanty primordial follicles is present (grade 1 morphology). Hematoxylin and eosin; magnification, ⫻40.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
the cyst wall may remove excessive ovarian tissue, with possible loss of follicles. Some indirect evidence from the literature shows that ovaries from which ovarian cysts have been excised perform worse than nonoperated ovaries when patients undergo ovarian stimulation for assisted reproduction techniques (14, 15) and in monitored natural cycles (15). In this study, histologic analysis of specimens excised at operative laparoscopy for ovarian cysts showed that some ovarian tissue was inadvertently removed with the cyst wall in 36% of cases. In ovarian endometriomas, in which a real cyst capsule is not present, some ovarian tissue is removed with the cyst pseudocapsule in 54% of cases. In nonendometriotic cysts (dermoids and serous or mucinous cysts), in which a real anatomic cyst capsule is present, some ovarian tissue is removed along with the cyst wall in only 6% of cases. The stripping technique thus appears to be a tissuesparing technique in the treatment of nonendometriotic cysts. Even in endometriomas, however, the stripping procedure can be considered safe. From our series and from other indirect evidence obtained at laparotomy (13), it appears that the ovarian tissue adjacent to the endometrioma wall differs morphologically from the normal ovarian tissue; it never shows the follicular pattern that is observed in normal ovaries. In our study, ovarian tissue was excised together with the cyst wall in 14 cases of endometriosis, but the ovarian tissue adjacent to the cyst wall had some primary follicles 612
Muzii et al.
Laparoscopic excision of ovarian cysts
(grade 2 morphology) in only 1 case. In most cases, no follicles (grade 0 [10 cases]) or scanty primordial follicles (grade 1 [3 cases]) were present. No specimen showed the normal pattern of primordial, primary, and secondary follicles seen in normal ovaries. In 48 patients who underwent laparotomy for benign ovarian cysts, Maneschi et al. (13) found that the ovarian cortex surrounding endometriomas showed morphologic patterns similar to those of the normal ovarian cortex in only 19% of cases, whereas the ovarian cortex surrounding mature teratomas and benign cystoadenomas appears morphologically normal in 92% and 77% of the cases, respectively. The specimens in that report were obtained from the ovarian cortex overlying the cyst, that is, in tissue that would remain on the ovarian parenchyma after cyst excision. It appears, therefore, that the functional potential of the ovarian tissue adjacent to the endometrioma wall may be disrupted. Stretching of the ovarian cortex per se seems to not be associated with morphologic alterations (13). Electrosurgical coagulation of the remaining parenchyma after excision of the cyst wall may cause further damage to the ovarian tissue. However, when appropriate techniques are used, small vessels may be identified and coagulated with bipolar forceps that, under these circumstances, may limit thermal damage to less than 0.2 mm (16). Taking this view, removal of a thin layer of ovarian tissue Vol. 77, No. 3, March 2002
FIGURE 4 Higher-power field (⫻400) from the upper portion of the specimen in Figure 3. Two primordial follicles are visible.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
(if any) at the time of laparoscopic stripping of the cyst wall may not represent overtreatment, because the tissue being removed may be morphologically altered (and possibly nonfunctional). The worse reproductive performance of ovaries that had undergone cyst excision (14, 15) may therefore represent some disruption of the ovarian function due to the presence of the endometrioma rather than the effect of excessive removal of healthy ovarian tissue at laparoscopic excision. Recent reports have compared laparoscopic stripping of the endometrioma wall with simple fenestration and coagulation of the cyst wall (17–19). In a randomized study of 64 patients with endometriomas associated with advanced endometriosis, Beretta et al. (17) found that cystectomy with the stripping procedure proved to be significantly better than fenestration and bipolar coagulation of the cyst wall, both in terms of symptom recurrence (24-month cumulative recurrence rate for dysmenorrhea, 16% for cystectomy vs. 56% for fenestration and coagulation) and subsequent fertility rates (24-month cumulative pregnancy rates, 67% and 24%, respectively). Retrospective series have yielded conflicting results. In a retrospective study of 156 patients (18), the 80 patients who underwent laparoscopic fenestration and bipolar coagulation of the cyst wall achieved pregnancy in a shorter time (1.4 years) than did the 23 patients who underwent laparoscopic cystectomy (2.2 years) and the 53 patients who had ovarian FERTILITY & STERILITY威
cystectomy by laparotomy and microsurgical techniques (2.4 years). Cumulative pregnancy rates at 36 months and recurrence rates at follow-up did not differ significantly among the three groups. In a retrospective study of 231 patients (19), laparoscopic fenestration and ablation of the cyst wall in 70 patients yielded poorer results compared with laparoscopic cyst excision in 161 patients (reoperation rates at 18 and 42 months, 22% and 58% for fenestration versus 6% and 24% for excision, respectively). Therefore, follow-up studies on reproductive outcome and recurrence rates after cyst excision have yielded conflicting results. None of these studies included histologic analysis of the specimens excised by using the stripping technique. The only randomized study (17), however, provides some indirect evidence in support of the tissue-sparing nature of the stripping procedure for ovarian cyst excision. In conclusion, the stripping procedure used at laparoscopy for ovarian cyst excision appears to be an organpreserving procedure. In nonendometriotic cysts, some ovarian tissue was inadvertently excised with the cyst wall in only 6% of the cases. In endometriotic cysts, 54% of the specimens included some ovarian tissue, approximately 1–2 mm in thickness, excised along with the cyst pseudocapsule; this tissue, however, did not show the morphologic characteristics seen in normal ovarian tissue. 613
References 1. Luciano AA, Lowney J, Jacobs SL. Endoscopic treatment of endometriosis-associated infertility. Therapeutic, economic and social benefits. J Reprod Med 1992;37:573– 6. 2. Luciano AA, Maier DB, Koch EI, Nulsen JC, Whitman GF. A comparative study of postoperative adhesions following laser surgery by laparoscopy versus laparotomy in the rabbit model. Obstet Gynecol 1989;74:220 – 4. 3. Postoperative adhesion development after operative laparoscopy: evaluation at early second-look laparoscopy. Operative Laparoscopy Study Group. Fertil Steril 1991;55:700 –1. 4. Lundorff P, Hahlin M, Kallfelt B, Thorburn J, Lindblom B. Adhesion formation after laparoscopic surgery in tubal pregnancy: a randomized trial versus laparotomy. Fertil Steril 1991;55:911–5. 5. Nezhat C, Crowgey SR, Nezhat F. Videolaparoscopy for the treatment of endometriosis associated with infertility. Fertil Steril 1989;51:237– 40. 6. Martin DC. Laparoscopic treatment of ovarian endometriomas. Clin Obstet Gynecol 1991;34:452–9. 7. Canis M, Mage G, Wattiez A, Chapron C, Pouly JL, Bassil S. Second look laparoscopy after laparoscopic cystectomy of large ovarian endometriomas. Fertil Steril 1992;58:611–9. 8. Muzii L, Marana R, Caruana P, Mancuso S. The impact of preoperative gonadotropin-releasing hormone agonist treatment on laparoscopic excision of ovarian endometriotic cysts. Fertil Steril 1996;65:1235–7. 9. 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.
614
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Laparoscopic excision of ovarian cysts
10. Donnez J, Nisolle M, Gillet N, Smets M, Bassil S, Casanas-Roux F. Large ovarian endometriomas. Hum Reprod 1996;11:641– 6. 11. Martin DC, Berry JD. Histology of chocolate cysts. J Gynecol Surg 1990;6:43– 6. 12. Jones KD, Sutton CJG. Laparoscopic management of ovarian endometriomas: a critical review of current practice. Curr Opin Obstet Gynecol 2000;12:309 –15. 13. 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. 14. Nargund G, Cheng WC, Parsons J. The impact of ovarian cystectomy on ovarian response to stimulation during in-vitro fertilization cycles. Hum Reprod 1995;11:81–3. 15. Loh FH, Tan AT, Kumar J, Ng SC. Ovarian response after laparoscopic ovarian cystectomy for endometriotic cysts in 132 monitored cycles. Fertil Steril 1999;72:316 –21. 16. Baggish MS, Tucker RD. Tissue actions of bipolar scissors compared with monopolar devices. Fertil Steril 1995;63:422– 6. 17. Beretta P, Franchi M, Ghezzi F, Busacca M, Zupi E, Bolis P. Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation. Fertil Steril 1998;70: 1176 – 80. 18. Hemmings R, Bissonnette F, Bouzayen R. Results of laparoscopic treatments of ovarian endometriomas: laparoscopic ovarian fenestration and coagulation. Fertil Steril 1998;70:527–9. 19. Saleh A, Tulandi T. Reoperation after laparoscopic treatment of ovarian endometriomas after excision and by fenestration. Fertil Steril 1999;72:322– 4.
Vol. 77, No. 3, March 2002
TECHNIQUES AND INSTRUMENTATION
Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure? Ludovico Muzii, M.D.,a Antonella Bianchi, M.D.,b Clara Croce`, M.D.,a Natalina Manci, M.D.,a and Pierluigi Benedetti Panici, M.D.a Libera Universita` Campus Bio-Medico, Rome, Italy
Objective: To determine whether the stripping technique by laparoscopy is a tissue-sparing procedure. Design: Prospective study. Setting: University hospital. Patient(s): Forty-two women, 21 to 35 years of age, who had a unilateral ovarian cyst (26 endometriomas, 7 serous, 6 dermoid, and 3 mucinous cysts). Intervention(s): Laparoscopic excision of ovarian cysts by using the stripping technique. Main Outcome Measure(s): Histologic analysis of the excised specimens was done to evaluate the presence and nature of ovarian tissue adjacent to the cyst wall. Result(s): Recognizable ovarian tissue adjacent to the cyst wall was present in 15 of 42 excised specimens (36%). A significant difference was present for endometriomas versus nonendometriosis cysts (ovarian tissue was present in 14 of 26 specimens [54%] vs. 1 of 16 specimens [6%]; P⬍.005). No specimen showed the normal follicular pattern observed in healthy ovaries. Conclusion(s): The stripping technique appears to be a tissue-sparing procedure. In 36% of the cysts, ovarian tissue is excised together with the cyst wall, but this tissue does not show the morphologic characteristics observed in normal ovarian tissue. (Fertil Steril威 2002;77:609 –14. ©2002 by American Society for Reproductive Medicine.) Key Words: Endometriosis, laparoscopy, ovarian cysts, surgical technique
Laparoscopy is considered the gold standard for treatment of benign ovarian cysts. Compared with traditional surgery by laparotomy, operative laparoscopy is associated with a shorter hospital stay, faster patient recovery, decreased costs (1), and a lower incidence of de novo adhesion formation (2– 4). Received April 19, 2001; revised and accepted September 10, 2001. Reprint requests: Ludovico Muzii, M.D., Area di Ginecologia, Libera Universita` Campus BioMedico, Via E. Longoni 83, Rome 00155, Italy (FAX: 39-06-2252294; E-mail: [email protected]) a Department of Gynecology. b Department of Pathology. 0015-0282/02/$20.00 PII S0015-0282(01)03203-4
The surgical technique of ovarian cyst excision by laparoscopy differs from traditional surgery performed at laparotomy. At laparoscopy (5– 8), most surgeons perform the socalled stripping technique, in which two atraumatic grasping forceps are used to pull the cyst wall and the normal ovarian parenchyma in opposite directions, thus developing the cleavage plane. After excision of the cyst wall, hemostasis is achieved by using bipolar forceps or CO2 laser. The residual ovarian tissue is not sutured, and the ovarian edges are left to heal by secondary intention. In contrast, at laparot-
omy, the cleavage plane is developed by using microsurgical techniques and instruments. After excision of the cyst wall, meticulous reconstruction of the ovarian cortex is performed with sutures. Recently, Brosens et al. (9) and Donnez et al. (10) have questioned the stripping technique because it is associated with removal of ovarian tissue along with the wall of ovarian cysts, especially endometriomas, causing loss of follicles. To our knowledge, however, no study has reported on the histologic features of specimens obtained by using the stripping technique at laparoscopy. Anecdotal reports have suggested that a rim of normal appearing ovary can surround the endometriotic tissue and the fibrotic pseudocapsule in specimens removed by using the stripping technique (6, 11). We performed histologic analysis of specimens obtained by using the stripping technique 609
FIGURE 1 Full-thickness specimen from the cyst wall of a mucinous cyst, obtained by using the stripping technique at laparoscopy. At the right edge, mucinous epithelium is visible, whereas in the left edge, no ovarian tissue is present. Hematoxylin and eosin; magnification, ⫻40.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
for ovarian cyst excision at operative laparoscopy to verify whether ovarian tissue is inadvertently excised together with the cyst wall and to investigate the morphologic characteristics of this tissue.
MATERIALS AND METHODS Between January 1, 1998, and December 31, 1999, 42 patients 21 to 35 years of age underwent laparoscopic excision of ovarian cysts. All patients were experiencing regular menstrual cycles at the time of surgery. No patient had had previous medical or surgical treatment of the ovarian cyst or previous pelvic surgery. At least three spontaneous menstrual cycles were allowed between the first ultrasonographic diagnosis of ovarian cyst and subsequent hospital admission for surgery. At hospital admission, all patients underwent transvaginal ultrasonography to confirm the presence of ovarian cysts. Mean cyst size was 4.5 cm (range, 3.5 to 9.0 cm). Operative laparoscopy was performed as reported elsewhere (8). In brief, after induction of general anesthesia, a 10-mm laparoscope was introduced through the umbilicus, and three accessory 5-mm trocars were placed suprapubically for introduction of accessory instruments. After initial diagnostic evaluation of the pelvis and abdomen and washing, and if no sign of malignancy was present, the ovarian cyst was punc610
Muzii et al.
Laparoscopic excision of ovarian cysts
tured, the contents were aspirated and visually inspected, and the inner wall of the cyst was checked for possible vegetations. In case of ultrasonographic diagnosis of dermoid cyst, the cyst was not intentionally punctured; every effort was made to excise the entire cyst without spilling its content. After identification of the cleavage plane, the cyst wall was stripped off the remaining ovarian parenchyma through traction exerted in opposite directions by using two atraumatic grasping forceps. When necessary, hemostasis was achieved with bipolar forceps applied on the ovarian parenchyma. No sutures were used for reapproximation of the ovarian edges. 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 ovarian fossa, and the final part, usually near the ovarian hilus). The selected specimen was sent for inclusion in our study and was evaluated 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. Portions of the specimen obtained from the initial and final parts of the stripping procedure were excluded from our Vol. 77, No. 3, March 2002
FIGURE 2 Full-thickness specimen from an endometrioma cyst wall. At the lower edge, endometrial epithelium and stroma are visible, whereas at the upper edge, fibroreactive tissue with no evidence of follicles is present. Hematoxylin and eosin; magnification, ⫻40.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
study because the surgical technique of cyst excision in the area of ovarian adhesion to the ovarian fossa and in the area of the hilus, where the cyst wall may be densely adherent, may vary from patient to patient and among different surgeons (6, 12), thus possibly yielding noncomparable specimens. For our study, the blinded pathologist evaluated the presence or absence of ovarian tissue adjacent to the cyst wall and graded the morphologic characteristics of this tissue on a semiquantitative scale of 0 to 4 (0, complete absence of follicles; 1, primordial follicles only; 2, primordial and primary follicles; 3, some secondary follicles; 4, pattern of primary and secondary follicles as seen in normal ovary) (13). Statistical analysis was performed by using the 2 test or the Fisher exact test, where appropriate, for categorical variables. P⬍.05 was considered statistically significant. We did not request institutional review board approval for the study because it did not change the management of patients with endometriosis usually followed at our institution.
postoperative complications occurred. All patients were discharged in the first 24 hours after surgery. Histologic classification of the specimens was as follows: endometriotic cyst in 26 cases (62%), serous cyst in 7 cases (17%), dermoid cyst in 6 (14%) and mucinous cyst in 3 cases (7%). Routine histologic examination of the entire specimen confirmed the blinded histologic examination in all cases. Adjacent ovarian tissue was present in 15 of 42 specimens (36%). This ovarian tissue was approximately 1 to 2 mm in thickness. No ovarian tissue was found in 27 specimens (64%) (Figs. 1 and 2). Ovarian tissue was present in 14 of 26 endometrioma cyst walls (54%), 1 of 6 dermoids (17%), and none of the 7 serous and 3 mucinous cysts (P⫽.0016 for endometriotic versus nonendometriotic cysts). With regard to morphologic characteristics, the ovarian tissue excised with the cyst wall was graded as 0 in 11 of 15 specimens (73%), 1 in 3 specimens (20%) (Figs. 3 and 4), and 2 in 1 specimen (7%). In no specimen, class 3 or 4 ovarian tissue was present.
DISCUSSION RESULTS In the 42 patients, excision of the ovarian cysts was completed successfully by laparoscopy. No intraoperative or FERTILITY & STERILITY威
Some investigators (9, 10) have questioned use of the laparoscopic technique for ovarian cyst excision, particularly in the case of ovarian endometriomas, because stripping of 611
FIGURE 3 Full-thickness specimen from an endometrioma cyst wall. At the lower edge, endometrial epithelium and stroma are visible, whereas at the upper edge, ovarian tissue with scanty primordial follicles is present (grade 1 morphology). Hematoxylin and eosin; magnification, ⫻40.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
the cyst wall may remove excessive ovarian tissue, with possible loss of follicles. Some indirect evidence from the literature shows that ovaries from which ovarian cysts have been excised perform worse than nonoperated ovaries when patients undergo ovarian stimulation for assisted reproduction techniques (14, 15) and in monitored natural cycles (15). In this study, histologic analysis of specimens excised at operative laparoscopy for ovarian cysts showed that some ovarian tissue was inadvertently removed with the cyst wall in 36% of cases. In ovarian endometriomas, in which a real cyst capsule is not present, some ovarian tissue is removed with the cyst pseudocapsule in 54% of cases. In nonendometriotic cysts (dermoids and serous or mucinous cysts), in which a real anatomic cyst capsule is present, some ovarian tissue is removed along with the cyst wall in only 6% of cases. The stripping technique thus appears to be a tissuesparing technique in the treatment of nonendometriotic cysts. Even in endometriomas, however, the stripping procedure can be considered safe. From our series and from other indirect evidence obtained at laparotomy (13), it appears that the ovarian tissue adjacent to the endometrioma wall differs morphologically from the normal ovarian tissue; it never shows the follicular pattern that is observed in normal ovaries. In our study, ovarian tissue was excised together with the cyst wall in 14 cases of endometriosis, but the ovarian tissue adjacent to the cyst wall had some primary follicles 612
Muzii et al.
Laparoscopic excision of ovarian cysts
(grade 2 morphology) in only 1 case. In most cases, no follicles (grade 0 [10 cases]) or scanty primordial follicles (grade 1 [3 cases]) were present. No specimen showed the normal pattern of primordial, primary, and secondary follicles seen in normal ovaries. In 48 patients who underwent laparotomy for benign ovarian cysts, Maneschi et al. (13) found that the ovarian cortex surrounding endometriomas showed morphologic patterns similar to those of the normal ovarian cortex in only 19% of cases, whereas the ovarian cortex surrounding mature teratomas and benign cystoadenomas appears morphologically normal in 92% and 77% of the cases, respectively. The specimens in that report were obtained from the ovarian cortex overlying the cyst, that is, in tissue that would remain on the ovarian parenchyma after cyst excision. It appears, therefore, that the functional potential of the ovarian tissue adjacent to the endometrioma wall may be disrupted. Stretching of the ovarian cortex per se seems to not be associated with morphologic alterations (13). Electrosurgical coagulation of the remaining parenchyma after excision of the cyst wall may cause further damage to the ovarian tissue. However, when appropriate techniques are used, small vessels may be identified and coagulated with bipolar forceps that, under these circumstances, may limit thermal damage to less than 0.2 mm (16). Taking this view, removal of a thin layer of ovarian tissue Vol. 77, No. 3, March 2002
FIGURE 4 Higher-power field (⫻400) from the upper portion of the specimen in Figure 3. Two primordial follicles are visible.
Muzii. Laparoscopic excision of ovarian cysts. Fertil Steril 2002.
(if any) at the time of laparoscopic stripping of the cyst wall may not represent overtreatment, because the tissue being removed may be morphologically altered (and possibly nonfunctional). The worse reproductive performance of ovaries that had undergone cyst excision (14, 15) may therefore represent some disruption of the ovarian function due to the presence of the endometrioma rather than the effect of excessive removal of healthy ovarian tissue at laparoscopic excision. Recent reports have compared laparoscopic stripping of the endometrioma wall with simple fenestration and coagulation of the cyst wall (17–19). In a randomized study of 64 patients with endometriomas associated with advanced endometriosis, Beretta et al. (17) found that cystectomy with the stripping procedure proved to be significantly better than fenestration and bipolar coagulation of the cyst wall, both in terms of symptom recurrence (24-month cumulative recurrence rate for dysmenorrhea, 16% for cystectomy vs. 56% for fenestration and coagulation) and subsequent fertility rates (24-month cumulative pregnancy rates, 67% and 24%, respectively). Retrospective series have yielded conflicting results. In a retrospective study of 156 patients (18), the 80 patients who underwent laparoscopic fenestration and bipolar coagulation of the cyst wall achieved pregnancy in a shorter time (1.4 years) than did the 23 patients who underwent laparoscopic cystectomy (2.2 years) and the 53 patients who had ovarian FERTILITY & STERILITY威
cystectomy by laparotomy and microsurgical techniques (2.4 years). Cumulative pregnancy rates at 36 months and recurrence rates at follow-up did not differ significantly among the three groups. In a retrospective study of 231 patients (19), laparoscopic fenestration and ablation of the cyst wall in 70 patients yielded poorer results compared with laparoscopic cyst excision in 161 patients (reoperation rates at 18 and 42 months, 22% and 58% for fenestration versus 6% and 24% for excision, respectively). Therefore, follow-up studies on reproductive outcome and recurrence rates after cyst excision have yielded conflicting results. None of these studies included histologic analysis of the specimens excised by using the stripping technique. The only randomized study (17), however, provides some indirect evidence in support of the tissue-sparing nature of the stripping procedure for ovarian cyst excision. In conclusion, the stripping procedure used at laparoscopy for ovarian cyst excision appears to be an organpreserving procedure. In nonendometriotic cysts, some ovarian tissue was inadvertently excised with the cyst wall in only 6% of the cases. In endometriotic cysts, 54% of the specimens included some ovarian tissue, approximately 1–2 mm in thickness, excised along with the cyst pseudocapsule; this tissue, however, did not show the morphologic characteristics seen in normal ovarian tissue. 613
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Vol. 77, No. 3, March 2002