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Laparoscopic excision of recurrent endometriomas: long-term outcome and comparison with primary surgery
Laparoscopic excision of recurrent endometriomas: long-term outcome and comparison with primary surgery Luigi Fedele, M.D.,a Stefano Bianchi, M.D.,a Giovanni Zanconato, M.D.,c Nicola Berlanda, M.D.,b Ricciarda Raffaelli, M.D.,c and Eleonora Fontana, M.D.a a
Department of Obstetrics, Gynecology, and Neonatology, Fondazione “Policlinico-Mangiagalli-Regina Elena,” University of Milan, Milan; b Department of Obstetrics and Gynecology, Ospedale San Paolo, University of Milan, Milan; and c Department of Maternal and Child Health, Biology and Genetics, Policlinico Borgo Roma, University of Verona, Verona, Italy
Objective: To compare the laparoscopic excision of primary versus recurrent ovarian endometriomas. Design: Descriptive study. Setting: Tertiary referral center for the treatment of endometriosis. Patient(s): Between 1993 and 2002, 359 consecutive patients: 305 primary surgeries (group A) and 54 reoperations for a recurrent endometrioma in the same ovary of the primary cyst (group B). Intervention(s): Laparoscopic stripping of the cyst wall. Follow-up evaluations every 6 months, including clinical and ultrasonographic evaluations and a questionnaire for pain symptoms (mean follow-up time, ⫾ standard deviation: 35.4 ⫾ 27.6 months). Main Outcome Measure(s): Recurrence of pain symptoms, sonographic recurrence of endometriomas, need for a new medical or surgical treatment, and reproductive outcome. Result(s): In groups A and B, respectively, the 5-year cumulative rates were not statistically significantly different: pain recurrence 20.5% versus 17.4%; ultrasonographic recurrence 18.9% versus 15.1%; retreatment requirement 19.4% versus 17.3%; and pregnancy 40.8% versus 32.4%. Although the difference was not statistically significant, compared with patients of group A, the women of group B underwent assisted reproduction techniques more frequently (50% vs. 32.2%) and had more irregular menstrual cycles associated with follicle-stimulating hormone levels ⱖ 14 IU/mL in the early follicular phase (5.5% vs. 1.3%). Conclusion(s): After laparoscopic excision of recurrent ovarian endometriomas, the recurrence of pain and the reproductive outcome are comparable with those found after primary surgery. (Fertil Steril威 2006;85:694 –9. © 2006 by American Society for Reproductive Medicine.) Key Words: Endometriosis, ovarian cysts, ovarian endometrioma, recurrent endometriosis
There is general agreement that conservative laparoscopic surgery represents the treatment of choice for ovarian endometriomas; either by cystectomy or by fenestration and coagulation, it is effective in removing disease and relieving associated pain symptoms (1–7). Although this is true with regard to primary endometriomas, no studies have documented the effectiveness of a laparoscopic reoperation for recurrent endometriotic cysts. In the latter cases, alternative therapeutic options are represented by medical treatment or, when infertility is the clinical issue, assisted reproduction techniques (ART). The aim of the present study was to compare the recurrence of pain symptoms, the sonographic recurrence of endometriomas, the need for a new medical or surgical treatment, and the reproductive outcome associated with the laparoscopic excision of primary versus recurrent ovarian endometriomas.
Received April 24, 2005; revised and accepted August 11, 2005. Reprint requests: Luigi Fedele, M.D., Clinica Ostetrico-Ginecologica II, Università di Milano, Istituto Luigi Mangiagalli, Via della Commenda 10, 20122 Milano, Italy (FAX: ⫹39 02 503 20252; E-mail: luigi.fedele@ unimi.it).
694
MATERIALS AND METHODS For the present study, all patients were considered eligible who were ⱕ38 years of age and had undergone a conservative laparoscopic treatment for ovarian endometriosis at the Centre for the Study of Endometriosis, a referral center directed by the principal author at the University of Milan from 1993 to 1994, and later from 1995 to 2002 at the University Hospital of Verona. Because of the descriptive nature of this study, institutional review board approval was not requested. Of the total of 458 patients who met the inclusion criteria, 99 were excluded for the following reasons: recurrent endometriotic cyst in the ovary contralateral to that of the primary lesion (11 patients), deep endometriosis of the rectovaginal septum or the urinary tract (28 patients), loss to follow-up evaluation (32 patients), indication for an oophorectomy (no possibility of preserving functioning ovarian tissue due to multiple and/or large cysts and presence of fibrous tissue in 14, difficulty in achieving hemostasis (1 patient) and association with pelvic inflammatory disease (1 patient), presence of a solitary ovary from a previous oophorectomy (8 patients), and obstructive müllerian anomalies (4 patients). Out of the 99 patients excluded, 21 had undergone a reop-
Fertility and Sterility姞 Vol. 85, No. 3, March 2006 Copyright ©2006 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/06/$32.00 doi:10.1016/j.fertnstert.2005.08.028
eration. The remaining 359 women were included in the study and were divided in two groups. Group A was patients who had primary surgery (305 women); Group B was patients who underwent reoperation for a recurrent endometrioma located in the same ovary of the primary cyst (54 women). Main indications for surgery in groups A and B were pelvic pain in 212 and 37 women, infertility in 48 and 8 women, and cyst larger than 5 cm in diameter in 45 and 9 women, respectively. The infertile patients had previously undergone an infertility work-up including the assessment of tubal patency, hormone status, and male factor infertility. No patients underwent preoperative medical treatment. In all cases, the surgical technique was stripping of the cyst wall, achieved by applying simple traction– countertraction with two atraumatic forceps over the edges of the ovary and the cyst wall, as previously described elsewhere (8). All visible peritoneal endometriotic lesions were treated either by excision or bipolar electrocoagulation. Adhesions, when present, were separated and possibly removed. Pelvic denervating procedures such as presacral neurectomy or uterosacral ligaments ablation were never performed. Stage of endometriosis was assessed according to the revised American Fertility Society (AFS) classification (9). The pathology report confirmed the diagnosis of endometriotic cysts in all cases. No patients received postoperative treatment except those receiving oral contraceptive pill for contraceptive purposes. A clinical and transvaginal ultrasonographic evaluation was planned every 6 months thereafter, for a minimum follow-up period of 24 months. Serum CA-125 values were evaluated when a recurrence was suspected. Before laparoscopy and at each follow-up visit, each patient was requested to fill out a
questionnaire (10) that included a 10-point ranked ordinal scale to rate the severity of pain symptoms (dysmenorrhea, pelvic pain, dysmenorrhea with radiation to the rectum, deep dyspareunia, dyschezia): each complaint was graded from absence of pain (score 0) to unbearable pain (score 10). Intensity of pain was classified as mild (score: 1– 4), moderate (score: 5–7) and severe (score: 8 –10) according to the collected data. Recurrent pain was defined as the recurrence or persistence of at least one pain symptom of moderate or severe intensity, as defined by the questionnaire. The suspect sonographic finding of a recurrent mono or bilateral endometrioma was defined as the presence of a homogeneous hypoechogenic cyst, persistent on a repeat scan in the early follicular phase. The onset of a pregnancy as well as the use of ART were noted. In patients with onset of irregular menstrual cycles after surgery, follicle-stimulating hormone (FSH) levels were evaluated in the early follicular phase, and, when necessary, a sonographic exam was performed to assess follicular recruitment. Follow-up evaluation was discontinued in patients who had hypergonadotropic amenorrhea and in those requiring a new treatment. Student’s t-test and chi-square were used where appropriate. Actuarial recurrence rates were assessed using the Kaplan-Meyer survival curves. Recurrence rates of the two groups were compared using the log-rank test. A P value ⱕ.05 was considered significant. RESULTS The characteristics of the 305 patients of group A and the 54 patients of group B are reported in Table 1. Patients who
TABLE 1 Characteristics of patients in the two groups. Primary laparoscopy (group A) (n ⴝ 305)
Reoperation (group B) (n ⴝ 54)
Significance
30.2 ⫾ 5.4 90 (29.5%)
30.8 ⫾ 4.9 24 (44.4%)
NS .01
244 (80%) 61 (20%)
35 (64.8%) 19 (35.2%)
.05
235 (77%) 70 (23%) 228 (74.8%) 118 (38.7%) 97 (31.8%) 98 (32.1%) 6.1 ⫾ 11.8
37 (68.5%) 17 (31.5%) 42 (77.8%) 26 (48.1%) 22 (40.7%) 15 (27.8%) 10.9 ⫾ 14.7
NS
Age (mean ⫾ SD) Infertile Stage III IV Cysts Monolateral Bilateral Dysmenorrhea Pelvic pain Deep dyspareunia Endometrioma diameter ⬎5 cm Adhesions score (mean ⫾ SD)
NS NS NS NS .01
Note: NS ⫽ not statistically significant; SD ⫽ standard deviation. Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
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FIGURE 1 Survival curve of clinical recurrence in the two groups.
Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
underwent reoperation had stage IV disease and a higher AFS adhesion score more frequently, and were more frequently infertile. The mean (⫾ standard deviation) follow-up period was 35.4 ⫾ 27.6 months (range: 12 to 120).
Forty-three patients in group A and eight in group B had recurrence of at least one moderate or severe pain symptom, resulting in a 5-year cumulative pain recurrence rate of 20.5% and 17.4%, respectively (P⫽not statistically signifi-
FIGURE 2 Survival curve of sonographic recurrence in the two groups.
Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
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Vol. 85, No. 3, March 2006
cant [NS]) (Fig. 1). At ultrasound scan, endometrioma recurrence was found in 40 women in group A and in 5 women in group B. Endometrioma recurred in the same ovary of the primary cyst, or in both ovaries, in 36 and five cases respectively, resulting in a cumulative 5-year ultrasonographic recurrence rate of 18.9% and 15.1%, respectively (P⫽NS) (Fig. 2). Moderate or severe pain was associated to cyst recurrence in 31 patients of group A and in all five patients of group B. A further medical and/or surgical treatment for recurrence of homolateral endometrioma was performed in all symptomatic patients of both groups and in four asymp-
tomatic patients of group A who had cysts larger than 5 cm, resulting in a cumulative 5 year retreatment rate for recurrent cyst in the same ovary of 19.4% and 17.3%, respectively (P⫽NS). During the follow-up period, a total of 34 (29.8%) pregnancies were observed among the 114 infertile patients who attempted to become pregnant. Twenty-one (23.3%) women in group A and 8 (33.3%) in group B had a possible cause of infertility in addition to endometriosis. We did not observe statistically significant differences between the two groups
FIGURE 3 Sonographic appearance of recurrent endometriomas: (A) deep intraovarian endometrioma; (B) bilocular endometrioma; and (C) multilocular endometrioma.
Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
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with regard to cumulative pregnancy rates (40.8% and 32.4% in group A and B, respectively), percentage of patients who underwent ART (29 out of 90, 32.2% in group A vs. 12 out of 24, 50% in group B), percentage of pregnancies obtained after ART (12 out of 29, 41.4% in group A; 3 out of 5, 60% in group B), or number of patients with irregular menstrual cycles and FSH ⱖ14 IU/mL in the early follicular phase (4 out of 305, 1.3% in group A; and 3 out of 54, 5.5% in group B). DISCUSSION The results of our study indicate that 60 months after laparoscopic excision of ovarian endometriomas, the cumulative recurrence rate of moderate to severe pain symptoms and the recurrence rate of endometriotic cysts in the same ovary as assessed by transvaginal sonography are about 20%. These rates are very similar for patients undergoing primary surgery and patients operated for a recurrence. We believe that in terms of sample size, length of follow-up and methodology, the present study is adequate to support such conclusions. This is a series of 359 consecutive patients recruited and evaluated over a 10-year period, who were operated upon by the same surgeons using a technique that was not modified substantially during the entire study period. Undoubtedly, the characteristics of the operations were different in the two groups because patients who underwent surgery for a recurrence were more likely to have deep intraovarian or multilocular cysts (Fig. 3), reduced healthy ovarian tissue, and dense adhesions compared with patients who had the operation for the first time; this was reflected by the greater proportion of patients with stage IV disease. Despite such anatomical differences, our patients with recurrent cysts did not experience significantly different pain symptoms than patients with primary ovarian lesions. On the other hand, the presence of extraovarian deeply infiltrating endometriosis was not significantly different in the two groups: this may be explained by the exclusion from the study of patients with deep endometriosis involving the rectosigmoid and urinary tracts. Until now, absence of data on the efficacy of repeat laparoscopic conservative surgery has prevented adequate counseling of patients with recurrent endometriomas. A few previous studies evaluated the surgical management of recurrent endometriosis; in those studies, however, treatment was performed by laparotomy, and the issue of ovarian endometriomas was not specifically addressed (11–13). More recently, several studies reported rates of symptom recurrence, reoperation, and pregnancy after conservative laparoscopic treatment of ovarian endometriomas (1–5, 7). Ours is the first study of the outcome of reoperations for recurrent endometriomas as compared with the outcome of primary surgery. Our results show that a patient with recurrent ovarian endometriosis undergoing repeat conservative laparoscopic surgery, when technically feasible, may expect efficacy with symptoms and disease similar to that of the first 698
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operation, with resolution of pain symptoms in about 80% of cases. No statistically significant differences in pregnancy rate were observed between the two groups. A higher rate of patients who underwent a second operation (rather than a first-line surgery) conceived with ART, although this difference was not statistically significant. Finally, although the retrospective design of our study does not allow us to draw definitive conclusions on the impact of laparoscopic surgery on ovarian function, the finding of comparable postoperative FSH levels between the two groups seems to be in disagreement with previous data showing damage of ovarian reserve after removal of endometriotic cysts (14 –16). On the other hand, it is noteworthy that among patients with bilateral endometriomas who underwent a second procedure, we observed three out of 54 (5.5%) cases of hypergonadotropic oligomenorrhea; among patients undergoing primary surgery, this was observed only in four out of 305 (1.3%) cases. Our study demonstrates that laparoscopic conservative surgery has a role in the treatment of patients with recurrent ovarian endometriotic cysts, because the recurrence of pain symptoms and the reproductive outcome are comparable with those observed after primary surgery. However, the surgical procedure might be technically more challenging and might involve substantial risk of impairment of the ovarian function. REFERENCES 1. Ahmed MS, Barbieri RL. Reoperation rates for recurrent ovarian endometriomas after surgical excision. Gynecol Obstet Invest 1997;43: 53– 4. 2. Bateman BG, Kolp LA, Mills S. Endoscopic versus laparotomy management of endometriomas. Fertil Steril 1994;62:690 –5. 3. 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. 4. Busacca M, Marana R, Caruana P, Candiani M, Muzii L, Calia C, Bianchi S. Recurrence of ovarian endometrioma after laparoscopic excision. Am J Obstet Gynecol 1999;180:519 –23. 5. Hemmings R, Bissonnette F, Bouzayen R. Results of laparoscopic treatments of ovarian endometriomas: laparoscopic ovarian fenestration and coagulation. Fertil Steril 1998;70:527–9. 6. Jones KD, Sutton C. Patient satisfaction and changes in pain scores after ablative laparoscopic surgery for stage III–IV endometriosis and endometriotic cysts. Fertil Steril 2003;5:1086 –90. 7. Marana R, Caruana P, Muzii L, Catalano GF, Mancuso S. Operative laparoscopy for ovarian cysts. Excision vs. aspiration. J Reprod Med 1996;41:435– 8. 8. Fedele L, Bianchi S, Zanconato G, Bergamini V, Berlanda N. Bipolar electrocoagulation versus suture of solitary ovary after laparoscopic excision of ovarian endometriomas. J Am Assoc Gynecol Laparosc 2004;11:344 –7. 9. Revised American Fertility Society classification of endometriosis: 1985. Fertil Steril 1995;43:351–2. 10. Fedele L, Bianchi S, Bocciolone L, Di Nola G, Franchi D. Buserelin acetate in the treatment of pelvic pain associated with minimal and mild endometriosis: a controlled study. Fertil Steril 1993;59:516 –21. 11. Candiani GB, Fedele L, Vercellini P, Bianchi S, Di Nola G. Repetitive conservative surgery for recurrence of endometriosis. Obstet Gynecol 1991;77:421– 4.
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12. Redwine DB. Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease. Fertil Steril 1991;56:628 –34. 13. Wheeler JM, Malinak LR. Recurrent endometriosis: incidence, management, and prognosis. Am J Obstet Gynecol 1983;146:247–53. 14. Loh FH, Tan Tan A, Kumar J, Soon-Chye N. Ovarian response after laparoscopic ovarian cystectomy for endometriotic cyst in 132 monitored cycles. Fertil Steril 1999;72:316 –21.
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15. Geber S, Ferreira DP, Spyer Prates LF, Sales L, Sampaio M. Effects of previous ovarian surgery for endometriosis on the outcome of assisted reproduction treatment. Reprod Biomed Online 2002;5: 162– 6. 16. Ho HY, Lee RK, Hwu YM, Lin MH, Su JT, Tsai YC. Poor response of ovaries with endometrioma previously treated with cystectomy to controlled ovarian hyperstimulation. J Assist Reprod Genet 2002;19: 507–11.
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Department of Obstetrics, Gynecology, and Neonatology, Fondazione “Policlinico-Mangiagalli-Regina Elena,” University of Milan, Milan; b Department of Obstetrics and Gynecology, Ospedale San Paolo, University of Milan, Milan; and c Department of Maternal and Child Health, Biology and Genetics, Policlinico Borgo Roma, University of Verona, Verona, Italy
Objective: To compare the laparoscopic excision of primary versus recurrent ovarian endometriomas. Design: Descriptive study. Setting: Tertiary referral center for the treatment of endometriosis. Patient(s): Between 1993 and 2002, 359 consecutive patients: 305 primary surgeries (group A) and 54 reoperations for a recurrent endometrioma in the same ovary of the primary cyst (group B). Intervention(s): Laparoscopic stripping of the cyst wall. Follow-up evaluations every 6 months, including clinical and ultrasonographic evaluations and a questionnaire for pain symptoms (mean follow-up time, ⫾ standard deviation: 35.4 ⫾ 27.6 months). Main Outcome Measure(s): Recurrence of pain symptoms, sonographic recurrence of endometriomas, need for a new medical or surgical treatment, and reproductive outcome. Result(s): In groups A and B, respectively, the 5-year cumulative rates were not statistically significantly different: pain recurrence 20.5% versus 17.4%; ultrasonographic recurrence 18.9% versus 15.1%; retreatment requirement 19.4% versus 17.3%; and pregnancy 40.8% versus 32.4%. Although the difference was not statistically significant, compared with patients of group A, the women of group B underwent assisted reproduction techniques more frequently (50% vs. 32.2%) and had more irregular menstrual cycles associated with follicle-stimulating hormone levels ⱖ 14 IU/mL in the early follicular phase (5.5% vs. 1.3%). Conclusion(s): After laparoscopic excision of recurrent ovarian endometriomas, the recurrence of pain and the reproductive outcome are comparable with those found after primary surgery. (Fertil Steril威 2006;85:694 –9. © 2006 by American Society for Reproductive Medicine.) Key Words: Endometriosis, ovarian cysts, ovarian endometrioma, recurrent endometriosis
There is general agreement that conservative laparoscopic surgery represents the treatment of choice for ovarian endometriomas; either by cystectomy or by fenestration and coagulation, it is effective in removing disease and relieving associated pain symptoms (1–7). Although this is true with regard to primary endometriomas, no studies have documented the effectiveness of a laparoscopic reoperation for recurrent endometriotic cysts. In the latter cases, alternative therapeutic options are represented by medical treatment or, when infertility is the clinical issue, assisted reproduction techniques (ART). The aim of the present study was to compare the recurrence of pain symptoms, the sonographic recurrence of endometriomas, the need for a new medical or surgical treatment, and the reproductive outcome associated with the laparoscopic excision of primary versus recurrent ovarian endometriomas.
Received April 24, 2005; revised and accepted August 11, 2005. Reprint requests: Luigi Fedele, M.D., Clinica Ostetrico-Ginecologica II, Università di Milano, Istituto Luigi Mangiagalli, Via della Commenda 10, 20122 Milano, Italy (FAX: ⫹39 02 503 20252; E-mail: luigi.fedele@ unimi.it).
694
MATERIALS AND METHODS For the present study, all patients were considered eligible who were ⱕ38 years of age and had undergone a conservative laparoscopic treatment for ovarian endometriosis at the Centre for the Study of Endometriosis, a referral center directed by the principal author at the University of Milan from 1993 to 1994, and later from 1995 to 2002 at the University Hospital of Verona. Because of the descriptive nature of this study, institutional review board approval was not requested. Of the total of 458 patients who met the inclusion criteria, 99 were excluded for the following reasons: recurrent endometriotic cyst in the ovary contralateral to that of the primary lesion (11 patients), deep endometriosis of the rectovaginal septum or the urinary tract (28 patients), loss to follow-up evaluation (32 patients), indication for an oophorectomy (no possibility of preserving functioning ovarian tissue due to multiple and/or large cysts and presence of fibrous tissue in 14, difficulty in achieving hemostasis (1 patient) and association with pelvic inflammatory disease (1 patient), presence of a solitary ovary from a previous oophorectomy (8 patients), and obstructive müllerian anomalies (4 patients). Out of the 99 patients excluded, 21 had undergone a reop-
Fertility and Sterility姞 Vol. 85, No. 3, March 2006 Copyright ©2006 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/06/$32.00 doi:10.1016/j.fertnstert.2005.08.028
eration. The remaining 359 women were included in the study and were divided in two groups. Group A was patients who had primary surgery (305 women); Group B was patients who underwent reoperation for a recurrent endometrioma located in the same ovary of the primary cyst (54 women). Main indications for surgery in groups A and B were pelvic pain in 212 and 37 women, infertility in 48 and 8 women, and cyst larger than 5 cm in diameter in 45 and 9 women, respectively. The infertile patients had previously undergone an infertility work-up including the assessment of tubal patency, hormone status, and male factor infertility. No patients underwent preoperative medical treatment. In all cases, the surgical technique was stripping of the cyst wall, achieved by applying simple traction– countertraction with two atraumatic forceps over the edges of the ovary and the cyst wall, as previously described elsewhere (8). All visible peritoneal endometriotic lesions were treated either by excision or bipolar electrocoagulation. Adhesions, when present, were separated and possibly removed. Pelvic denervating procedures such as presacral neurectomy or uterosacral ligaments ablation were never performed. Stage of endometriosis was assessed according to the revised American Fertility Society (AFS) classification (9). The pathology report confirmed the diagnosis of endometriotic cysts in all cases. No patients received postoperative treatment except those receiving oral contraceptive pill for contraceptive purposes. A clinical and transvaginal ultrasonographic evaluation was planned every 6 months thereafter, for a minimum follow-up period of 24 months. Serum CA-125 values were evaluated when a recurrence was suspected. Before laparoscopy and at each follow-up visit, each patient was requested to fill out a
questionnaire (10) that included a 10-point ranked ordinal scale to rate the severity of pain symptoms (dysmenorrhea, pelvic pain, dysmenorrhea with radiation to the rectum, deep dyspareunia, dyschezia): each complaint was graded from absence of pain (score 0) to unbearable pain (score 10). Intensity of pain was classified as mild (score: 1– 4), moderate (score: 5–7) and severe (score: 8 –10) according to the collected data. Recurrent pain was defined as the recurrence or persistence of at least one pain symptom of moderate or severe intensity, as defined by the questionnaire. The suspect sonographic finding of a recurrent mono or bilateral endometrioma was defined as the presence of a homogeneous hypoechogenic cyst, persistent on a repeat scan in the early follicular phase. The onset of a pregnancy as well as the use of ART were noted. In patients with onset of irregular menstrual cycles after surgery, follicle-stimulating hormone (FSH) levels were evaluated in the early follicular phase, and, when necessary, a sonographic exam was performed to assess follicular recruitment. Follow-up evaluation was discontinued in patients who had hypergonadotropic amenorrhea and in those requiring a new treatment. Student’s t-test and chi-square were used where appropriate. Actuarial recurrence rates were assessed using the Kaplan-Meyer survival curves. Recurrence rates of the two groups were compared using the log-rank test. A P value ⱕ.05 was considered significant. RESULTS The characteristics of the 305 patients of group A and the 54 patients of group B are reported in Table 1. Patients who
TABLE 1 Characteristics of patients in the two groups. Primary laparoscopy (group A) (n ⴝ 305)
Reoperation (group B) (n ⴝ 54)
Significance
30.2 ⫾ 5.4 90 (29.5%)
30.8 ⫾ 4.9 24 (44.4%)
NS .01
244 (80%) 61 (20%)
35 (64.8%) 19 (35.2%)
.05
235 (77%) 70 (23%) 228 (74.8%) 118 (38.7%) 97 (31.8%) 98 (32.1%) 6.1 ⫾ 11.8
37 (68.5%) 17 (31.5%) 42 (77.8%) 26 (48.1%) 22 (40.7%) 15 (27.8%) 10.9 ⫾ 14.7
NS
Age (mean ⫾ SD) Infertile Stage III IV Cysts Monolateral Bilateral Dysmenorrhea Pelvic pain Deep dyspareunia Endometrioma diameter ⬎5 cm Adhesions score (mean ⫾ SD)
NS NS NS NS .01
Note: NS ⫽ not statistically significant; SD ⫽ standard deviation. Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
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FIGURE 1 Survival curve of clinical recurrence in the two groups.
Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
underwent reoperation had stage IV disease and a higher AFS adhesion score more frequently, and were more frequently infertile. The mean (⫾ standard deviation) follow-up period was 35.4 ⫾ 27.6 months (range: 12 to 120).
Forty-three patients in group A and eight in group B had recurrence of at least one moderate or severe pain symptom, resulting in a 5-year cumulative pain recurrence rate of 20.5% and 17.4%, respectively (P⫽not statistically signifi-
FIGURE 2 Survival curve of sonographic recurrence in the two groups.
Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
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Excision of recurrent endometriomas
Vol. 85, No. 3, March 2006
cant [NS]) (Fig. 1). At ultrasound scan, endometrioma recurrence was found in 40 women in group A and in 5 women in group B. Endometrioma recurred in the same ovary of the primary cyst, or in both ovaries, in 36 and five cases respectively, resulting in a cumulative 5-year ultrasonographic recurrence rate of 18.9% and 15.1%, respectively (P⫽NS) (Fig. 2). Moderate or severe pain was associated to cyst recurrence in 31 patients of group A and in all five patients of group B. A further medical and/or surgical treatment for recurrence of homolateral endometrioma was performed in all symptomatic patients of both groups and in four asymp-
tomatic patients of group A who had cysts larger than 5 cm, resulting in a cumulative 5 year retreatment rate for recurrent cyst in the same ovary of 19.4% and 17.3%, respectively (P⫽NS). During the follow-up period, a total of 34 (29.8%) pregnancies were observed among the 114 infertile patients who attempted to become pregnant. Twenty-one (23.3%) women in group A and 8 (33.3%) in group B had a possible cause of infertility in addition to endometriosis. We did not observe statistically significant differences between the two groups
FIGURE 3 Sonographic appearance of recurrent endometriomas: (A) deep intraovarian endometrioma; (B) bilocular endometrioma; and (C) multilocular endometrioma.
Fedele. Excision of recurrent endometriomas. Fertil Steril 2006.
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with regard to cumulative pregnancy rates (40.8% and 32.4% in group A and B, respectively), percentage of patients who underwent ART (29 out of 90, 32.2% in group A vs. 12 out of 24, 50% in group B), percentage of pregnancies obtained after ART (12 out of 29, 41.4% in group A; 3 out of 5, 60% in group B), or number of patients with irregular menstrual cycles and FSH ⱖ14 IU/mL in the early follicular phase (4 out of 305, 1.3% in group A; and 3 out of 54, 5.5% in group B). DISCUSSION The results of our study indicate that 60 months after laparoscopic excision of ovarian endometriomas, the cumulative recurrence rate of moderate to severe pain symptoms and the recurrence rate of endometriotic cysts in the same ovary as assessed by transvaginal sonography are about 20%. These rates are very similar for patients undergoing primary surgery and patients operated for a recurrence. We believe that in terms of sample size, length of follow-up and methodology, the present study is adequate to support such conclusions. This is a series of 359 consecutive patients recruited and evaluated over a 10-year period, who were operated upon by the same surgeons using a technique that was not modified substantially during the entire study period. Undoubtedly, the characteristics of the operations were different in the two groups because patients who underwent surgery for a recurrence were more likely to have deep intraovarian or multilocular cysts (Fig. 3), reduced healthy ovarian tissue, and dense adhesions compared with patients who had the operation for the first time; this was reflected by the greater proportion of patients with stage IV disease. Despite such anatomical differences, our patients with recurrent cysts did not experience significantly different pain symptoms than patients with primary ovarian lesions. On the other hand, the presence of extraovarian deeply infiltrating endometriosis was not significantly different in the two groups: this may be explained by the exclusion from the study of patients with deep endometriosis involving the rectosigmoid and urinary tracts. Until now, absence of data on the efficacy of repeat laparoscopic conservative surgery has prevented adequate counseling of patients with recurrent endometriomas. A few previous studies evaluated the surgical management of recurrent endometriosis; in those studies, however, treatment was performed by laparotomy, and the issue of ovarian endometriomas was not specifically addressed (11–13). More recently, several studies reported rates of symptom recurrence, reoperation, and pregnancy after conservative laparoscopic treatment of ovarian endometriomas (1–5, 7). Ours is the first study of the outcome of reoperations for recurrent endometriomas as compared with the outcome of primary surgery. Our results show that a patient with recurrent ovarian endometriosis undergoing repeat conservative laparoscopic surgery, when technically feasible, may expect efficacy with symptoms and disease similar to that of the first 698
Fedele et al.
Excision of recurrent endometriomas
operation, with resolution of pain symptoms in about 80% of cases. No statistically significant differences in pregnancy rate were observed between the two groups. A higher rate of patients who underwent a second operation (rather than a first-line surgery) conceived with ART, although this difference was not statistically significant. Finally, although the retrospective design of our study does not allow us to draw definitive conclusions on the impact of laparoscopic surgery on ovarian function, the finding of comparable postoperative FSH levels between the two groups seems to be in disagreement with previous data showing damage of ovarian reserve after removal of endometriotic cysts (14 –16). On the other hand, it is noteworthy that among patients with bilateral endometriomas who underwent a second procedure, we observed three out of 54 (5.5%) cases of hypergonadotropic oligomenorrhea; among patients undergoing primary surgery, this was observed only in four out of 305 (1.3%) cases. Our study demonstrates that laparoscopic conservative surgery has a role in the treatment of patients with recurrent ovarian endometriotic cysts, because the recurrence of pain symptoms and the reproductive outcome are comparable with those observed after primary surgery. However, the surgical procedure might be technically more challenging and might involve substantial risk of impairment of the ovarian function. REFERENCES 1. Ahmed MS, Barbieri RL. Reoperation rates for recurrent ovarian endometriomas after surgical excision. Gynecol Obstet Invest 1997;43: 53– 4. 2. Bateman BG, Kolp LA, Mills S. Endoscopic versus laparotomy management of endometriomas. Fertil Steril 1994;62:690 –5. 3. 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. 4. Busacca M, Marana R, Caruana P, Candiani M, Muzii L, Calia C, Bianchi S. Recurrence of ovarian endometrioma after laparoscopic excision. Am J Obstet Gynecol 1999;180:519 –23. 5. Hemmings R, Bissonnette F, Bouzayen R. Results of laparoscopic treatments of ovarian endometriomas: laparoscopic ovarian fenestration and coagulation. Fertil Steril 1998;70:527–9. 6. Jones KD, Sutton C. Patient satisfaction and changes in pain scores after ablative laparoscopic surgery for stage III–IV endometriosis and endometriotic cysts. Fertil Steril 2003;5:1086 –90. 7. Marana R, Caruana P, Muzii L, Catalano GF, Mancuso S. Operative laparoscopy for ovarian cysts. Excision vs. aspiration. J Reprod Med 1996;41:435– 8. 8. Fedele L, Bianchi S, Zanconato G, Bergamini V, Berlanda N. Bipolar electrocoagulation versus suture of solitary ovary after laparoscopic excision of ovarian endometriomas. J Am Assoc Gynecol Laparosc 2004;11:344 –7. 9. Revised American Fertility Society classification of endometriosis: 1985. Fertil Steril 1995;43:351–2. 10. Fedele L, Bianchi S, Bocciolone L, Di Nola G, Franchi D. Buserelin acetate in the treatment of pelvic pain associated with minimal and mild endometriosis: a controlled study. Fertil Steril 1993;59:516 –21. 11. Candiani GB, Fedele L, Vercellini P, Bianchi S, Di Nola G. Repetitive conservative surgery for recurrence of endometriosis. Obstet Gynecol 1991;77:421– 4.
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12. Redwine DB. Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease. Fertil Steril 1991;56:628 –34. 13. Wheeler JM, Malinak LR. Recurrent endometriosis: incidence, management, and prognosis. Am J Obstet Gynecol 1983;146:247–53. 14. Loh FH, Tan Tan A, Kumar J, Soon-Chye N. Ovarian response after laparoscopic ovarian cystectomy for endometriotic cyst in 132 monitored cycles. Fertil Steril 1999;72:316 –21.
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15. Geber S, Ferreira DP, Spyer Prates LF, Sales L, Sampaio M. Effects of previous ovarian surgery for endometriosis on the outcome of assisted reproduction treatment. Reprod Biomed Online 2002;5: 162– 6. 16. Ho HY, Lee RK, Hwu YM, Lin MH, Su JT, Tsai YC. Poor response of ovaries with endometrioma previously treated with cystectomy to controlled ovarian hyperstimulation. J Assist Reprod Genet 2002;19: 507–11.
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