Laparoscopic stripping of endometriomas: a randomized trial on different surgical techniques. Part II: pathological results

Ludovico Muzii1,4, Filippo Bellati1, Antonella Bianchi2, Innocenza Palaia1, Natalina Manci1, Marzio Angelo Zullo1, Roberto Angioli1 and Pierluigi Benedetti Panici3

1 Department of Obstetrics and Gynaecology and 2 Department of Histopathology, University Campus Bio-Medico of Rome, Via Longoni 83, Rome 00155 and 3 Department of Gynaecology and Obstetrics, Università ‘La Sapienza’, Via Regina Elena 324, Rome 00168, Italy

4 To whom correspondence should be addressed at: Department of Obstetrics and Gynaecology, University Campus Bio-Medico of Rome, Via Longoni 83, Rome 00155, Italy. Email: l.muzii{at}unicampus.it


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
BACKGROUND: The stripping technique for endometriomas excision has been reported to be associated with follicular loss. The objective of this trial was to evaluate the presence and nature of ovarian tissue adjacent to the endometrioma cyst wall obtained by stripping with different techniques. METHODS: Forty-eight patients with ovarian endometrioma were enrolled in two consecutive independent randomized trials. Two different techniques were analysed at the initial adhesion site (circular excision and subsequent stripping versus immediate stripping). Two different techniques were analysed at the ovarian hilus (stripping versus coagulation and cutting). Histology analysis was performed in three portions of the cyst wall (initial adhesion site, intermediate part of the specimen, ovarian hilus). RESULTS: Recognizable ovarian tissue was inadvertently excised together with the endometrioma cyst wall in most cases. At initial adhesion sites more ovarian tissue was removed with the circular excision technique (<0.001). No significant difference in quality of ovarian tissue (number and type of follicles) was found between specimens obtained with different surgical techniques at the initial or at the final part of the procedure. At the initial adhesion site and at the intermediate part of the cyst wall, the ovarian tissue removed along with the endometrioma wall was mainly constituted by 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). Close to the ovarian hilus the ovarian tissue removed along with the endometrioma wall mostly consisted of tissue which contained primary and secondary follicles (69% of the cases, combining the two groups). CONCLUSIONS: Ovarian tissue is inadvertently excised together with the endometrioma wall in most cases. The excised tissue is at normal functional development stages only near the ovarian hilus. The different techniques used do not influence significantly the quality of the resected tissue.

Key words: endometrioma/endometriosis/laparoscopy/ovarian reserve


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Recent randomized trials have demonstrated that laparoscopy should be considered the best approach for the surgical treatment of benign ovarian cysts (Mais et al., 1995Go; Yuen et al., 1997Go). At laparoscopy, in the case of ovarian endometriotic cysts, the cyst wall can be excised with the stripping technique (Reich and McGlynn, 1986Go; Martin, 1991Go; Canis et al., 1992Go, Beretta et al., 1998Go) or ablated with bipolar coagulation or laser after cyst fenestration (Brosens et al., 1996Go; Donnez et al., 1996Go; Sutton et al., 1997Go; Beretta et al., 1998Go).

Recently, the stripping procedure has been reported to be preferable to cyst wall ablation since recurrence rates may be lower (Beretta et al., 1998Go; Vercellini et al., 2003Go). Nevertheless, a major concern that remains is the possible loss of follicles associated with the procedure (Brosens et al., 1996Go; Donnez et al., 1996Go). In addition, poorer performance in IVF protocols (Garcia-Velasco et al., 2004Go) and reduced ovarian volumes (Exacoustos et al., 2004Go) have been reported in patients who had undergone the stripping procedure for endometrioma excision.

In a recent report, we have reported that the stripping procedure may be a tissue-sparing technique (Muzii et al., 2002Go). The pathological analysis of endometriotic cyst wall revealed that ovarian tissue was inadvertently excised together with the cyst wall in more than half of the cases, but in no case did this tissue show a normal follicular pattern as the one present in healthy ovaries (Muzii et al., 2002Go). In the above study, however, only a 2 x 2 cm sample taken from the intermediate part of the cyst wall, midway between the site of ovarian adhesion to the ovarian fossa and the hilus, was evaluated.

The objective of the present trial was to evaluate, in a randomized trial, the quantity and nature of ovarian tissue inadvertently resected along with the endometriotic tissue in the different parts of the cyst wall (i.e. at the cyst adhesion site with the ovarian fossa, in the intermediate part of the cyst wall, and where the cyst is closer to the ovarian hilus), using two different techniques at the initial adhesion site and two different techniques at the final part of the stripping procedure near the hilus.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
The primary objective of this trial was to evaluate the difference in ovarian tissue inadvertently removed together with the endometriotic cysts using different surgical techniques.

In a separate paper the study design and eligibility and exclusion criteria have been described, and a more thorough description of the surgical procedure is also provided (Muzii et al., 2005Go). Briefly, two surgical techniques (direct stripping versus circular excision) were analysed at the initial adhesion site, and two different techniques (stripping versus coagulation followed by cutting) were analysed for the management of the cyst near the ovarian hilus (Muzii et al., 2005Go).

Postoperatively, the surgeon removed three separate specimens from the cyst wall for thorough pathological analysis: specimen 1, removed around the site of the original parietal adhesion, obtained with either surgical procedure (stripping or circular excision) (Figure 1A); specimen 2, removed from the intermediate part of the cyst (midway between specimen 1 and specimen 3) (Figure 1B); and specimen 3 removed from the cyst wall pedicle (close to the ovarian hilus), with either surgical procedure (stripping or coagulation and cutting) (Figure 1C).



View larger version (139K):
[in this window]
[in a new window]
 
Figure 1. Excised endometrioma with the three specimens removed. (A) Specimen 1: removed around the site of the original parietal adhesion. (B) Specimen 2: removed from the intermediate part of the cyst. (C) Specimen 3: removed from the cyst wall pedicle (close to the ovarian hilus). Scale 1:2.

 
The remaining specimen was sent for routine pathological analysis. The pathologist was not informed on which technique was adopted to remove the endometrioma. The same blinded pathologist evaluated each specimen separately. The specimen thickness and the presence of ovarian tissue were recorded. When ovarian tissue was present, the tissue thickness and the morphologic characteristics were recorded. Morphologic characteristics of this tissue were graded 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 the normal ovary) (Maneschi et al., 1993Go).

Statistical analysis
The sample size utilized (24 versus 24 observations) was selected in order to detect, with 80% power at the 0.05 alpha level, a difference of 34% in the rate of presence of ovarian tissue inadvertently excised, given a reference rate for inadvertently removed ovarian tissue of 54%, reported in our previous study (Muzii et al., 2002Go).

Parametric tests were used after having evaluated the normal distribution of the data to be analysed. The Student's t-test was used to evaluate the difference between continuous variables. The {chi}2-test was used to evaluate the difference between the presence or absence of ovarian tissue between groups, at different cyst sites. The Mann–Whitney test was used to evaluate the difference in quality of ovarian tissue removed with the different surgical techniques. Analysis of variance (ANOVA) was used to compare specimens obtained at the three different cyst sites. When significant, Fisher's post-hoc test was used to identify significant comparisons. The Kruskal–Wallis test was used to evaluate the difference in quality of ovarian tissue removed at the three different cyst sites. Statistical significance was set at P<0.05.


    Results
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Between 1 January 2000 and 31 December 2001, 48 patients were enrolled in the trial and evaluated. Patients characteristics and the study flow chart have been previously reported (Muzii et al., 2005Go).

Analysis of specimen 1: at original adhesion site with the ovarian fossa (direct stripping versus circular excision)
Forty-eight patients were evaluated, 24 in each arm. Overall the mean tissue thickness of specimen 1 was 1.2±0.4 mm. The thickness of specimen 1 obtained in patients subjected to circular excision was significantly greater than the one obtained from patients subjected to direct stripping (1.4±0.4 mm versus 1.0±0.4 mm, P<0.05). Ovarian tissue was present in 64% (31/48) of the patients. As expected, there was a tendency of finding ovarian tissue removed with the endometriosis more frequently after circular excision than after direct stripping (79% versus 50%, P=0.07). When ovarian tissue was present, the mean thickness was 0.3±0.2 mm. The circular excision technique removed significantly more ovarian tissue, when present, if compared with the direct stripping technique (0.5±0.1 mm versus 0.1±0.03 mm, respectively, P<0.001). Figure 2 shows a specimen removed with the circular excision technique.



View larger version (124K):
[in this window]
[in a new window]
 
Figure 2. Specimen 1. At the top of the specimen, the thin mesothelium is visible, whereas at the bottom, endometrial glands can be seen. Hematoxylin and eosin; magnification x40.

 
Ovarian tissue inadvertently excised with the endometrioma wall was primarily constituted by tissue with no (grade 0) or only primordial (grade 1) follicles (29/31, 94%). In one case (2%) grade 3 ovarian tissue was present, whereas in another case (2%) grade 4 was present. No difference was present in morphological characteristics of the ovarian tissue between the specimens obtained through the two different surgical techniques (Table I).


View this table:
[in this window]
[in a new window]
 
Table I. Pathological characteristics of specimen

 
Analysis of specimen 2: intermediate part of the cyst wall (midway between specimen 1 and specimen 2)
Forty-eight specimens were analyzed. The surgical technique for the intermediate part was presumably the same stripping technique in all 48 patients. In fact, this part of the procedure was not part of any randomized trial, but was carried out in the usual manner (Muzii et al., 2002Go). Overall, the mean tissue thickness of specimen 2 was 1.4±0.5 mm. Ovarian tissue was present in 54% (26/48) of the patients. When ovarian tissue was present, the mean thickness was 0.3±0.1 mm. Ovarian tissue inadvertently excised with the endometrioma wall primarily consisted of tissue with no or only primordial follicles (23/26, 88%). In three cases (12%), tissue with secondary (grade 2) follicles was found. No difference in quality or quantity of ovarian tissue was identified on the basis of the technique used in trial 1. This specimen represents the tissue that constitutes the greatest part of the cyst wall.

Analysis of specimen 3: close to the ovarian hilus (completion with the stripping technique versus bipolar coagulation followed by cutting with scissors)
Forty-eight patients were evaluated, 24 in each arm. The mean tissue thickness of specimen 3 was 1.6±0.6 mm. No difference in thickness was present between specimens obtained in the two groups (1.6±0.5 mm versus 1.5±0.6 mm for stripping versus bipolar coagulation and cutting, respectively). Ovarian tissue was present in 71% (34/48) of the patients. In particular, ovarian tissue was present in 18/24 (75%) versus 16/24 (67%) of patients who underwent direct stripping versus bipolar coagulation and cutting, respectively. Ovarian tissues mean thickness was 0.8±0.4 mm, with no difference between the two groups. When ovarian tissue was present, this primarily consisted of tissue with primary and secondary follicles, i.e. grade 3 and 4 (29/34, 85%). No significant difference was present between the specimens achieved through the two different surgical techniques (Table II). Figure 3 shows a specimen removed with the direct stripping technique.


View this table:
[in this window]
[in a new window]
 
Table II. Pathological characteristics of specimen

 


View larger version (146K):
[in this window]
[in a new window]
 
Figure 3. Specimen 3. At the top of the slide, endometrial tissue can be seen, whereas at the bottom, a secondary follicle is present. Hematoxylin and eosin; magnification x40.

 
Pathological characteristics of the three specimens obtained by the 48 evaluated patients are reported in Table III. Specimens obtained from the hilus (specimen 3) were significantly thicker than the ones obtained from the initial adhesion site (specimen 1). Specimen 2 tended to be thicker than specimen 1 and thinner than specimen 3, but not in a significant way. No difference was present between specimens in the proportion of specimens with identifiable ovarian tissue. A significant difference was present in the thickness of ovarian tissue inadvertently removed between specimens 1–2 and specimen 3 (P<0.05) (Figure 3), with specimen 3 having more ovarian tissue than the other two specimens. No difference in quality of ovarian tissue was present between specimen 1 and specimen 2. Specimen 3 contained significantly more primary and secondary follicles compared to the other two specimens (P<0.05).


View this table:
[in this window]
[in a new window]
 
Table III. Pathological analysis

 

    Discussion
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Laparoscopy should be considered the gold-standard approach for the treatment of ovarian endometriomas, whereas the choice of which laparoscopic technique to use is still a matter of debate (Jones and Sutton, 2000Go; Vercellini et al., 2003Go). There are strong supporters and detractors for both the technique of cyst wall stripping and the technique of cyst fenestration and subsequent vaporization or coagulation of the inner wall. Recent reports have compared the two techniques, both in prospective (Beretta et al., 1998Go) and retrospective (Hemmings et al., 1998Go; Saleh and Tulandi, 1999Go) studies. In a randomized controlled study by Beretta et al. (1998)Go, 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 and subsequent fertility rates. In uncontrolled series however, higher pregnancy rates were reported with the fenestration and coagulation/ablation technique (Jones and Sutton, 2001Go). Retrospective series yielded conflicting results. In a retrospective series by Hemmings et al. (1998)Go, patients submitted to laparoscopic fenestration and bipolar coagulation of the cyst wall achieved pregnancy in a shorter period of time (1.4 years) than patients undergoing laparoscopic cystectomy (mean time to first pregnancy 2.2 years) or ovarian cystectomy by laparotomy and microsurgical techniques (mean time to pregnancy 2.4 years). Cumulative pregnancy rates at 36 months and recurrence rates at follow-up were not significantly different between the three groups. In a retrospective study by Saleh and Tulandi (1999)Go, laparoscopic fenestration and ablation of the cyst wall yielded poorer results when compared with laparoscopic cyst excision (reoperation rates at 18 and 42 months were 22% and 58%, respectively, for fenestration, versus 6% and 24% for cyst excision).

Therefore, a consensus on which technique should be considered the gold standard as to postoperative reproductive performance and recurrences has not been reached.

Some authors (Brosens et al., 1996Go; Donnez et al., 1996Go) have recently questioned the laparoscopic technique of endometrioma stripping, since stripping of the cyst wall may result in removal of ovarian tissue in excess, with possible loss of follicles. Some indirect evidence from the literature show that ovaries submitted to excision of ovarian cysts perform worse than nonoperated ovaries when the patients undergo ovarian stimulation for assisted reproduction techniques (Nargund et al., 1996Go; Loh et al., 1999Go) or in monitored natural cycles (Loh et al., 1999Go). This hypothesis is supported mostly by studies that have primarily analysed the response of previously operated ovaries to clomiphene or to gonadotropin agonists (Nargund et al., 1996Go; Loh et al., 1999Go; Donnez et al., 2001Go; Ho et al., 2002Go; Somigliana et al., 2003Go). On the contrary, in similar settings, other groups were unable to find clinically significant differences (Canis et al., 2001Go; Marconi et al., 2002Go).

In a recent study (Muzii et al., 2002Go) we demonstrated, by histology analysis of specimens excised at operative laparoscopy for ovarian cysts, that some ovarian tissue is inadvertently removed together with the endometrioma ‘pseudo-capsule’ in 54% of the cases. From the quoted study (Muzii et al., 2002Go), and from other indirect evidence obtained at laparotomy (Maneschi et al., 1993Go), it appears that the ovarian tissue adjacent to the endometrioma wall is morphologically different from the normal ovarian tissue, since it never shows the normal follicular pattern that can be observed in normal ovaries. In this perspective, removal of a thin layer of ovarian tissue, if any, at the time of laparoscopic stripping of the cyst wall may not represent an overtreatment, since it may be morphologically altered (and possibly non functional) tissue that is being removed. At partial variance with our recent experience (Muzii et al., 2002Go), Hachisuga and Kawarabayashi (2002)Go reported that two groups of endometriomas could be identified at the stripping technique. In a group, the endometrioma capsule could be easily stripped from the ovarian parenchyma, and in this setting primordial follicles could be identified in 69% of the cases. In a second group, where the cyst capsule was densely attached to the ovarian parenchyma, primordial follicles were never found in the cyst wall specimens. The thickness of the cyst wall was higher in the first group (2.1 mm) than in the second group (1.8 mm). In our series (Muzii et al., 2002Go), the mean thickness of the cyst wall was only 1.3 mm. These data probably reflect different surgical techniques, with possibly less tissue trauma in our series and in the second group in Hachisuga's series, rather than different natures of the endometriomas.

In the above-mentioned study by our group (Muzii et al., 2002Go), only specimens from the intermediate part of the stripping procedure were evaluated. No information is present in the literature as to histology analysis of specimens from the various sites of the excised cyst wall where surgeons performing the stripping procedure may adopt different surgical techniques, in particular at the beginning of the cyst excision procedure at the initial adhesion site, and at the end of the procedure, near the ovarian hilus (Martin and Berry, 1990Go).

In the present study, we evaluated the different techniques that can be used when stripping the endometrioma wall from the ovary. As a first result of the study, we confirm that a rim of ovarian tissue is inadvertently removed together with the cyst wall in the majority of the cases. This strip of ovarian tissue excised along with the endometrioma wall is ~0.1–0.3 mm thick in the whole specimen, except near the hilus, where it becomes thicker, measuring on average 0.8 mm. In addition, in most of the specimens from the initial and the intermediate parts of the procedure, the ovarian tissue appears to be devoid of follicles, or only scanty primordial follicles can be recognized. On the other hand, when approaching the hilus, in nearly 70% of the specimens, higher functional stages of follicular development can be recognized, resembling the normal pattern of primordial, primary and secondary follicles that can be seen in healthy ovarian tissue.

During any part of the procedure, the surgeon may visually notice small follicles on the side of the cyst wall that is being excised. This finding invariably corresponds histologically to higher stages of follicular development. In a few cases, this has occurred at the initial part of the stripping procedure, possibly reflecting the presence of a cyst wall more adherent to the healthy ovarian parenchyma, or else the development of a wrong cleavage plane. When follicles are observed on the side of the excised cyst wall at the beginning or at the intermediate part of the procedure, the surgeon should consider the possibility of an incorrect surgical plane, and he/she should go back in the developed plane in order to find a cleavage plane deeper toward the cyst wall. When follicles are encountered near the hilus, this represents instead a common occurrence, and the two techniques used do not influence the surgical performance.

In conclusion, in the majority of the cases some ovarian tissue, ~0.1–0.8 mm in thickness, is excised along with the ‘pseudo-capsule’ of the endometrioma, whichever the technique used; this tissue, however, shows the morphologic characteristics seen in normal ovarian tissue only when approaching the hilus. Since the stripping of the greatest part of the pseudo-capsule is not associated with removal of healthy tissue, the stripping procedure, whichever the technique used, appears to be a tissue-preserving procedure.


    References
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Beretta P, Franchi M, Ghezzi F, Busacca M, Zupi E and Bolis P (1998) Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation. Fertil Steril 70, 1176–1180.[CrossRef][ISI][Medline]

Brosens IA, Van Ballaer P, Puttemans P and Deprest J (1996) Reconstruction of the ovary containing large endometriomas by an extraovarian endosurgical technique. Fertil Steril 66, 517–521.[ISI][Medline]

Canis M, Mage G, Wattiez A, Chapron C, Pouly JL and Bassil S (1992) Second look laparoscopy after laparoscopic cystectomy of large ovarian endometriomas. Fertil Steril 58, 611–619.

Canis M, Pouly JL, Tamburro S, Mage G, Wattiez A and Bruhat MA (2001) Ovarian response during IVF-embryo transfer cycles after laparoscopic ovarian cystectomy for endometriotic cysts of >3 cm in diameter. Hum Reprod 16, 2583–2586.[Abstract/Free Full Text]

Donnez J, Nisolle M, Gillet N, Smets M, Bassil S and Casanas-Roux F (1996) Large ovarian endometriomas. Hum Reprod 11, 641–646.[Abstract]

Donnez J, Wyns C and Nisolle M (2001) Does ovarian surgery for endometriomas impair the ovarian responce to gonadotropin? Fertil Steril 76, 662–665.[CrossRef][ISI][Medline]

Exacoustos C, Zupi E, Amadio A, Szabolcs B, De Vivo B, Marconi D, Romanini EM and Arduini D (2004) Laparoscopic removal of endometriomas: sonographic evaluation of residual functioning ovarian tissue. Am J Obstet Gynecol 191, 68–72.[CrossRef][ISI][Medline]

Garcia-Velasco JA, Mahutte NG, Corona J, Zuniga V, Giles J, Arici A and Pellicer A (2004) Removal of endometriomas before in vitro fertilization does not improve fertility outcomes: a matched, case-control study. Fertil Steril 81, 1194–1197.[CrossRef][ISI][Medline]

Hachisuga T and Kawarabayashi T (2002) Histopathological analysis of laparoscopically treated ovarian endometriotic cysts with special reference to loss of follicles. Hum Reprod 17, 432–435.[Abstract/Free Full Text]

Hemmings R, Bissonnette F and Bouzayen R (1998) Results of laparoscopic treatments of ovarian endometriomas: laparoscopic ovarian fenestration and coagulation. Fertil Steril 70, 527–529.[CrossRef][ISI][Medline]

Ho HY, Lee RK, Hwu YM, Lin MH, Su JT and Tsai YC (2002) Poor response of ovaries with endometrioma previously treated with cystectomy to controlled ovarian hyperstimulation. J Assist Reprod Genet 19, 507–511.[CrossRef][ISI][Medline]

Jones KD and Sutton CJG (2000) Laparoscopic management of ovarian endometriomas: a critical review of current practice. Curr Opin Obstet Gynecol 12, 309–315.[CrossRef][ISI][Medline]

Jones KD and Sutton CJG (2001) Endometriotic ovarian cysts: the case for ablative laparoscopic surgery. Gynecol Endosc 10, 281–287.[CrossRef]

Loh FH, Tan AT, Kumar J and Ng SC (1999) Ovarian response after laparoscopic ovarian cystectomy for endometriotic cysts in 132 monitored cycles. Fertil Steril 72, 316–321.[CrossRef][ISI][Medline]

Mais V, Ajossa S, Piras B, Marongiu D, Guerriero S and Melis GB (1995) Treatment of nonendometriotic benign adnexal cysts: a randomized comparison of laparoscopy and laparotomy. Obstet Gynecol 86, 770–774.[Abstract/Free Full Text]

Maneschi F, Marasa L, Incandela S, Mazzarese M, Zupi E and Zupi E (1993) Ovarian cortex surrounding benign neoplasms: a histologic study. Am J Obstet Gynecol 169, 388–393.[ISI][Medline]

Marconi G, Vilela M, Quintana R and Sueldo C (2002) Laparoscopic ovarian cystectomy of endometriomas does not affect the ovarian response to gonadotropin stimulation. Fertil Steril 78, 876–878.[CrossRef][ISI][Medline]

Martin DC and Berry JD (1990) Histology of chocolate cysts. J Gynecol Surg 6, 43–46.[ISI]

Martin DC (1991) Laparoscopic treatment of ovarian endometriomas. Clin Obstet Gynecol 34, 452–459.[ISI][Medline]

Muzii L, Bianchi A, Croce C, Manci N and Benedetti Panici P (2002) Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure? Fertil Steril 77, 609–614.[CrossRef][ISI][Medline]

Muzii L, Bellati F, Palaia I, Plotti F, Manci N, Zullo MA, Angioli R and Benedetti Panici P (2005) Laparoscopic stripping of endometriomas: A randomised trial on different surgical techniques. Part I: Clinical results. Hum Reprod (submitted for publication).

Nargund G, Cheng WC and Parsons J (1996) The impact of ovarian cystectomy on ovarian response to stimulation during in-vitro fertilization cycles. Hum Reprod 11, 81–83.[Abstract]

Reich H and McGlynn F (1986) Treatment of ovarian endometriomas using laparoscopic surgical techniques. J Reprod Med 31, 577–584.[ISI][Medline]

Saleh A and Tulandi T (1999) Reoperation after laparoscopic treatment of ovarian endometriomas after excision and by fenestration. Fertil Steril 72, 322–324.[CrossRef][ISI][Medline]

Somigliana E, Ragni G, Benedetti F, Borroni R, Vegetti W and Crosignani PG (2003) Does laparoscopic excision of endometriotic ovarian cysts significantly affect ovarian reserve? Insights from IVF cycles. Hum Reprod 18, 2450–2453.[Abstract/Free Full Text]

Sutton CJ, Ewen SP, Jacobs SA and Whitelaw NL (1997) Laser laparoscopic surgery in the treatment of ovarian endometriomas. J Am Assoc Gynecol Laparosc 4, 319–323.[ISI][Medline]

Vercellini P, Chapron C, De Giorgi O, Consonni D, Frontino G and Crosignani PG (2003) Coagulation or excision of ovarian endometriomas? Am J Obstet Gynecol 188, 606–610.[CrossRef][ISI][Medline]

Yuen PM, Yu KM, Yip SK, Lau WC, Rogers MS and Chang A (1997) A randomized prospective study of laparoscopy and laparotomy in the management of benign ovarian masses. Am J Obstet Gynecol 177, 109–114.[ISI][Medline]

Submitted on December 9, 2004; resubmitted on February 10, 2005; accepted on February 17, 2005.





This Article
Abstract
Full Text (PDF )
All Versions of this Article:
20/7/1987    most recent
deh851v1
Alert me when this article is cited
Alert me if a correction is posted
Services
Email this article to a friend
Similar articles in this journal
Similar articles in ISI Web of Science
Similar articles in PubMed
Alert me to new issues of the journal
Add to My Personal Archive
Download to citation manager
Search for citing articles in:
ISI Web of Science (1)
Request Permissions
Google Scholar
Articles by Muzii, L.
Articles by Panici, P. B.
PubMed
PubMed Citation
Articles by Muzii, L.
Articles by Panici, P. B.