Journal of Minimally Invasive Gynecology (2006) 13, 145–149
Efficacy of laparoscopically-assisted extracorporeal cystectomy in patients with ovarian endometrioma Temel Ceyhan, MD, Vedat Atay, MD, Sadettin Gungor, MD, Ates Karateke, MD, Ozay Oral, MD, and Iskender Baser, MD From the Department of Obstetrics and Gynaecology, Gulhane Military Medical Academy and Medical School (Drs. Ceyhan, Gungor, and Baser), Ankara, the Department of Obstetrics and Gynecology, GATA Haydarpasa Training Hospital (Dr. Atay), and the Department of Obstetrics and Gynecology, Zeynep Kamil Training Hospital (Drs. Karateke and Oral), Istanbul, Turkey. KEYWORDS: Endometrioma; Laparoscopic stripping; Extracorporeal cystectomy
Abstract STUDY OBJECTIVE: To investigate the usefulness and effectiveness of the extracorporeal surgical technique in the treatment of endometriomas. DESIGN: Retrospective evaluation (Canadian Task Force Classification II-2). SETTING: Department of gynecology in a tertiary care faculty hospital and training hospital. PATIENTS: Of 89 patients with endometrioma, 53 had laparoscopic stripping, and 36 had laparoscopically-assisted extracorporeal cystectomy. INTERVENTIONS: Laparoscopic stripping and laparoscopically-assisted extracorporeal cystectomy were performed for the treatment of endometriomas diagnosed laparoscopically. MEASUREMENTS AND MAIN RESULTS: The size of the endometrioma diagnosed by the ultrasonographic examination was not statistically related to the severity of the endometriosis (p ⫽ .42). Conversion to extracorporeal technique was required in 17 of 58 cases with moderate endometriosis and 14 of 31 cases with severe endometriosis (p ⫽ .04). Operation time, visual analogue pain score, and hospitalization periods were similar between the 2 techniques. Among 53 specimens obtained with laparoscopic stripping, 29 (55%) had no ovarian tissue, and 24 (45%) had ovarian tissue with follicles. Of 36 specimens obtained with extracorporeal technique, 19 (52%) had no ovarian tissue, and 17 (48%) had ovarian tissue with follicles. Preservation of the ovarian tissue was not significantly different between both surgical techniques. CONCLUSIONS: Extracorporeal technique with laparoscopically-assisted minilaparotomy is a valuable alternative for laparoscopic stripping in selected cases. © 2006 AAGL. All rights reserved.
The incidence of endometriosis among infertile women is about 20% to 30%,1 and approximately 17% to 44% of women with endometriosis have ovarian endometriomas.2,3 Laparoscopic stripping currently continues to be an effecCorresponding author: Dr. Temel Ceyhan, GATA Kadın Hastalıkları ve Dogˇum Anabilim Dalı, 06018 Etlik/Ankara, Turkey. E-mail:
[email protected] Submitted November 2, 2005. Accepted for publication January 8, 2006.
1553-4650/$ -see front matter © 2006 AAGL. All rights reserved. doi:10.1016/j.jmig.2006.01.004
tive approach in the treatment of endometrioma in infertile patients. This technique has emerged as a safe treatment choice in infertility, particularly in patients younger than 35 years of age.4 Various techniques, including cyst fenestration and aspiration and coagulation/ablation with electrical or laser energy, are also used in laparoscopic treatment of endometrioma. Laparoscopic stripping is reported as a more favorable technique compared with other treatment modalities.5
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During laparoscopic stripping, the pseudocapsule of the endometrioma can be removed without bleeding similar to any other benign ovarian cyst. However, difficulty can be encountered in stripping of the fibrotic pseudocapsule of the endometrioma from the ovarian tissue in certain cases.6 In this study, we investigated the impact of laparoscopic-assisted extracorporeal treatment of ovarian endometrioma in selected patients and compared the preservation of ovarian tissue and postoperative pain in extracorporeal technique and laparoscopic stripping.
Patients and methods Eighty-nine infertile women, who underwent surgery for endometrioma from January 2000 to September 2005 were included in this study. The mean age of patients was 29.2 years (21– 40). None of the patients had bilateral tubal contributing factors. Semen analyses of partners were normal. Patients with a body mass index ⱖ35 were not included in the study. Patients with a history of previous pelvic surgery or pelvic infection were excluded from the study. To form a homogenous patient group, patients who had bilateral endometrioma were not included in the study. After two consecutive transvaginal ultrasonographic examinations at 3-month intervals, unilateral ovarian cysts of ⬎3 cm in diameter with characteristics of endometrioma (the presence of a round-shaped homogeneous cyst with low-level echoes within the ovary) were diagnosed in 89 patients. None of the patients had used medications for the treatment of endometrioma previously, and no medication was planned before or after operation. Severity of endometriosis was determined according to the revised American Fertility Society Classification System (r-AFS) at the initial laparoscopic evaluation in all patients. Laparoscopic stripping was preferred as the initial approach for ovarian endometrioma. The events that led to extracorporeal technique during laparoscopic stripping included the following: (1) If vascular damage that entails electrocoagulation occurs during dissection of endometrioma from the fossa ovarica to preserve ovarian reserve. Before the arteria ovarica enters through the ovarian hilus, it converges with the ascending branch at the lower border of the fallopian tube and enters the ovary as arteria rete ovary. Therefore the use of bipolar electrocoagulation in the ovarian hilus may cause a serious ovarian supply problem and ovarian tissue damage. (2) To prevent residual tissue and related recurrence caused by the difficulty in defining the appropriate cleavage plane in densely fibrotic tissue.
Laparoscopic procedure Of 4 trocars used, a 10-mm trocar was inserted at the umbilical site to place the laparoscope. One 5-mm trocar was inserted at the lateral margin of each rectus muscle
Figure 1 site.
Exteriorization of ovarian tissue through enlarged port
sheath in the lower abdominal quadrant. Finally the last 5-mm trocar was inserted at the lateral margin of the rectus muscle sheath almost paraumbilically at the left side to facilitate the operation. During laparoscopic exploration, blunt dissection was used to separate the ovary with endometrioma, which had adhesions to the ovarian fossa. The cystic cavity was irrigated and aspirated, and cystic access was widened by use of grasping forceps and inspected for signs of malignancy. Grasping forceps were used to hold the fibrotic capsule, and a line of demarcation was identified to perform classical stripping. Fibrotic tissue was dissected by laparoscopic scissors without using any energy modality to identify the appropriate cleavage. When required, pinpoint bipolar electrocoagulation was used to control hemorrhage.
Laparoscopically-assisted cystectomy with the extracorporeal technique The cyst was punctured intraperitoneally, and the 5-mm trocar port incision close to the ovary was widened with the curved Kocher clamp inserted about 1.5 to 2.5 cm into the abdominal wall. All layers were equally widened by opening the curved Kocher clamp. Exteriorization of the ovarian tissue was performed with extreme care to avoid tearing caused by exertion of too much traction. While the ovary was grasped with the other clamp, gas insufflation was stopped, and the abdominal wall was allowed to relax with the exit of the gas from the other port. The telescope lamp aided in visualization, and the ovary was gently pulled out with a curved Kocher clamp (Figure 1). On the completion of ovarian stripping, control of bleeding and ovarian reconstruction were accomplished with appropriate suturing. When the gas insufflation was reinstituted, the ovary was gently pulled in with the grasping clamp, and light pressure was applied manually from outside. The abdominal incision was sutured in layers.
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After the removal of endometrioma by either technique, laparoscopic inspection was performed by use of the telescope with irrigation and aspiration in all cases. Endometriotic implants were either coagulated or removed by peritoneal stripping, and also pelvic adhesiolysis was completed. Periportal infiltration of local anesthesia with 10 mL 0.5% bupivacaine before incision and another 20 mL 0.5% bupivacaine diluted with 20 mL saline solution or equal amount of physiological saline solution injected into the peritoneal cavity at the end of either procedure. Postoperative pain was measured, and each patient recorded the severity of her pain on a visual analogue score at the eighteenth hour. The specimens were evaluated by pathologists blinded to the nature of the ovarian tissue and cystic wall and the type of procedure performed for that specific specimen. The mean, standard deviation, and median of counts for each treatment group were determined. The package program SPSS (Statistical package for Social Sciences for Windows 10.0) was used for statistical analysis. Independent sample t testing and Mann-Whitney U testing were used to compare the continuous variables of groups. Differences in response between groups were compared by 2testing. Probability levels less than .05 were considered significant. Local ethics committee approval for the study was not obtained because it did not change the treatment usually followed at our institution of patients with endometriosis.
Results The diagnosis of endometrioma was confirmed laparoscopically in all 89 patients in the study. Numerous endometriotic implants were also detected on the pelvic peritoneum during laparoscopic examination. However, the size of endometrioma did not correlate well with the severity of endometriosis. Staging of endometriosis was performed by use of r-AFS scoring in all patients. Of 31 cases with a diagnosis of endometrioma of 3 to 4 cm diameter according to ultrasonographic examination, 8 patients had severe endometriosis. Ten of 25 patients with diameters between 4 to 5 cm and 13 of 33 cases with ⬎5 cm diameter of endometrioma had severe involvement. Severe endometriosis was observed in 8 of 31, 10 of 25, and 13 of 33 cases with 3 to 4 cm, 4 to 5 cm, and ⬎5 cm of endo-
3 to 4 cm 4 to 5 cm ⬎5 cm *2 test.
31 25 33
23 (74.2%) 15 (60.0%) 20 (60.6%)
8 (25.8%) 10 (40.0%) 13 (39.4%)
Table 2 Relationship between the size of endometrioma and conversion to extracorporeal technique Size of Laparoscopic Extracorporeal endometrioma Total (n ⫽ 53) (n ⫽ 36) p Value* 3 to 4 cm 4 to 5 cm ⬎ 5 cm
32 25 32
19 (35.9%) 15 (28.3%) 19 (35.9%)
13 (36.1%) 10 (27.8%) 13 (36.1%)
.95
*2 test.
metrioma, respectively. Ultrasonographic measurement of endometrioma was not correlated with the severity of disease (p ⫽ .42) (Table 1). Fifty-three and 36 patients of 89 were treated with laparoscopic stripping and extracorporeal cystectomy with minilaparotomy, respectively. The reasons to proceed with the extracorporeal technique were difficulty in defining the appropriate cleavage plane in densely fibrotic tissue and bleeding as a result of dissection in the fossa ovarica in close proximity to the ovarian hilum in 19 and 17 of 36 patients, respectively. The size of the endometriomas stripped laparoscopically was 3 to 4 cm, 4 to 5 cm, and ⬎5 cm in 19, 15, and 19 cases, respectively. The size of endometriomas treated with extracorporeal cystectomy was 3 to 4 cm, 4 to 5 cm, and ⬎5 cm in 13, 10, and 13 cases, respectively. The size of endometrioma did not predict conversion to extracorporeal technique (Table 2) (p ⫽ .95). According to the r-AFS score, moderate and severe endometriosis were detected in 58 and 31 patients, respectively. Conversion to extracorporeal technique was required in 17 of 58 and 14 of 31 cases with moderate and severe endometriosis, respectively. Rate of conversion to extracorporeal technique increased with severity of endometriosis (Table 3) (p ⫽ .04). The mean operation time for laparoscopy and extracorporeal technique were 56.02 ⫾ 8.29 (36-68) and 60.51 ⫾ 8.44 (51-82) minutes, respectively. Operation time, visual analogue pain scores, and hospitalization period were not significantly different between either technique (Table 4). Histologic evaluation of excised endometriomas revealed endometrial endothelium with stromal tissue and surrounding fibro-reactive tissue with or without any follicles. The specimens were evaluated by pathologist blinded
Table 3 Relationship between the severity of endometriosis and conversion to extracorporeal technique
Table 1 Relationship between the severity of endometriosis and the size of endometrioma Severity of endometriosis Size of endometrioma Total Moderate Severe
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Severity of endometriosis
p value* .42
Technique
Total
Moderate
Severe
p Value*
Laparoscopic Extracorporeal
51 38
37 (63,8%) 21 (36,2%)
14 (45%) 17 (55%)
.04
*2 test.
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Table 4
Comparison of both techniques
Characteristics
Laparoscopic (n ⫽ 53)
Extracorporeal (n ⫽ 36)
p Value
Operation time (min) Visual analogue pain score (VAS) 18th hour Hospitalization time (day)
56.02 ⫾ 8.29(36-68) 3(1-6) 2(1-3)
60.51 ⫾ 8.44(51-82) 3(1-6) 2(1-3)
.5* .86† .37†
All values are mean ⫾ SD (range). *Student’s t test. †Mann Whitney U test.
to the type of procedure performed for that specific specimen. Of 53 specimens with laparoscopic stripping, 29 (55%) had no ovarian tissue, and 24 (45%) had ovarian tissue with follicles. Of 36 specimens with extracorporeal technique, 19 (52%) had no ovarian tissue, and 17 (48%) had ovarian tissue with follicles. Histopathologic evaluation of the specimens excised was similar according to ovarian tissue and the cyst wall among both groups (Table 5) (p ⫽ .51).
Discussion Ovarian surgery continues to be the therapy of choice, especially in infertile patients under the age of 35.4 Techniques such as aspiration and coagulation are recommended in laparoscopic treatment of endometriomas; however, cystectomy is the treatment of choice, considering the high recurrence rate observed in the former procedures.5–7 Laparoscopy has more advocates than laparotomy because of its early postoperative advantages. Indeed, laparoscopy seems to have advantages over laparotomy for identification of other components of endometriosis such as localization, and feasibility of treating the co-existing lesions.8,9 However, because of its long learning curve, the procedure continues to be limited to experienced laparoscopists.10,11 Superiority of surgical treatment in minimal and mild endometriosis over expectant therapy has been demonstrated in a meta-analysis undertaken by Olive et al.9 Redwine,3 in his study, has concluded that limiting the treatment to only the ovary may result in incomplete cure. We therefore preferred to start the procedure with laparoscopy, which enables inspection of endometriotic implants in the pelvis, adhesions, and recto-vaginal space lesions. We considered such findings as valuable input for planning opti-
Table 5 Histopathologic results of the specimens according to the techniques. Histopathology
Laparoscopic Extracorporeal (n ⫽ 53) (n ⫽ 36) p Value*
No ovarian tissue 29 (55%) Ovarian tissue with 24 (45%) primordial follicles *2 test.
19 (52%) 17 (48%)
.51
mum outcome for the selected treatment. At this point, lack of experience may be compensated by minilaparotomy that enables a more effective treatment. The surgical teams in our study group had sufficient experience. Thus the decision to use extracorporeal approach was due not to lack of experience, but to real requirements such as incomplete pseudocapsule cleavage that may result in bleeding, which requires coagulation, risk of postoperative recurrence, or risk of ovarian tissue loss. Electrocoagulation is frequently required during laparoscopic stripping, which limits the effectiveness of the procedure.12 We performed extracorporeal cystectomy because of the difficulty in defining the appropriate cleavage plane in densely fibrotic tissue and because of bleeding as a result of dissection in the fossa ovarica in close proximity to the ovarian hilum in 19 and 17 cases, respectively, in this study. The size of endometrioma did not predict conversion to extracorporeal cystectomy. However, the severity of endometriosis positively correlated with the conversion from laparoscopy to extracorporeal cystectomy. Postoperative pain, operation, and hospitalization periods were similar in both techniques in this study. Muzzi et al13 performed a pathologic examination of specimens excised by using a stripping technique (circular excision and subsequent stripping vs immediate stripping), investigating for the presence and nature of ovarian tissue adjacent to the cyst wall. They demonstrated that at initial adhesion sites more ovarian tissue was removed with the circular excision technique, and no significant difference in quality of ovarian tissue was detected between specimens obtained with different surgical techniques at the initial or final part of the procedure. They also demonstrated that the ovarian tissue removed along with the endometrioma wall at the initial adhesion and at the intermediate part of the cyst wall mainly consisted of tissue with no follicles or only primordial follicles (60% and 48% of the specimens from the initial part with both techniques and from the intermediate part, respectively, had no follicles or only primordial follicles). The ovarian tissue removed along with the endometrioma wall close to the ovarian hilus mostly consisted of tissue containing primary and secondary follicles (69% of the cases, combining the 2 groups). In this study, of 53 specimens with laparoscopic stripping, 29 (55%) had no ovarian tissue, and 24 (45%) had ovarian tissue with follicles. Of 36 specimens with extracorporeal technique, 19 (52%) had no ovarian tissue, and 17 (48%) had ovarian tissue with follicles. Histopathologic evaluation of the specimens excised were similar
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in ovarian tissue and the cyst wall between both groups (p ⫽ .51). Kalegyn and Sadykova14 have defined the technique where the endometrioma was initially drained intraperitoneally and afterward was removed through a 2.5-cm laparotomy incision for marsupialization. Canis12 comments that this technique is too traumatic for the ovary. We demonstrated in our study that normal ovarian tissue was preserved in cases where laparoscopic stripping was performed without any difficulty and in cases where the extracorporeal technique was used. The technique preserves ovarian function and avoids further thermal trauma caused by electrosurgical hemostasis of stromal vessels. Furthermore simple coagulation or vaporization might result in the persistence of ectopic endometrium and an increase in the risk of short-term cyst recurrence.5 We therefore conclude that both techniques can be considered as organ preserving. However, this approach may increase the risk of abdominal wall contamination. There was no difference between both techniques with regard to postoperative pain scores and duration of hospitalization, which were considered to be the early advantages of laparoscopy. In conclusion, the extracorporeal technique with laparoscopically assisted minilaparotomy can be a valuable alternative procedure when non-traumatic endometrioma stripping with laparoscopy is not feasible.
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3. Redwine DB. Ovarian endometriosis: a marker for extensive pelvic and intestinal disease. Fertil Steril. 1999;72:310 –315. 4. 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 –321. 5. 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 –1180. 6. Canis M, Pouly JL, Tamburro S, Mage G, Wattiez A, Bruhat MA. Ovarian response during IVF-embryo transfer cycles after laparoscopic ovarian cystectomy for endometriotic cysts of ⬍3 cm in diameter. Hum Reprod. 2001;16:2583–2586. 7. Saleh A, Tulandi T. Reoperation after laparoscopic treatment of ovarian endometriomas by excision and fenestration. Fertil Steril. 1999; 72:322–324. 8. Redwine DB. A marker for extensive pelvic and intestinal disease. Fertil Steril. 2000;73:419 – 420. 9. Olive DL, Pritts EA. The treatment of endometriosis. Ann N Y. 2002; 955:360 –372. 10. Jones KD, Fan A, Suddon CJG. The ovarian endometrioma: why is it so poorly managed? Indicators from an anonymous survey. Hum Reprod. 2002;17:845– 849. 11. Canis M, Mage G, Wattiez A, Pouly JL, Bruhat MA. The ovarian endometrioma laparoscopic treatment of large ovarian endometrioma: why such a long learning curve? Hum Reprod. 2003; 18:5–7. 12. Canis M, Rabischong B, Houlle C, Botchorishvili R, Jardon K, Safi A, et al. Laparoscopic management of adnexal masses: a gold standard? Curr Opin Obstet Gynecol. 2002;14:423– 428. 13. 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;20:1987–1992. 14. Kalegyn AV, Sadykova MH. Marsupialization of the cyst as a step in laparoscopic management of ovarian cysts. J Am Assoc Gynecol Laparosc. 2001;8:568 –572.