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
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Abstract |
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Key words: endometrioma/endometriosis/laparoscopy/ovarian reserve
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Introduction |
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Recently, the stripping procedure has been reported to be preferable to cyst wall ablation since recurrence rates may be lower (Beretta et al., 1998; Vercellini et al., 2003
). Nevertheless, a major concern that remains is the possible loss of follicles associated with the procedure (Brosens et al., 1996
; Donnez et al., 1996
). In addition, poorer performance in IVF protocols (Garcia-Velasco et al., 2004
) and reduced ovarian volumes (Exacoustos et al., 2004
) 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., 2002). 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., 2002
). 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.
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Materials and methods |
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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., 2005). 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., 2005
).
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).
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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., 2002).
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 2-test was used to evaluate the difference between the presence or absence of ovarian tissue between groups, at different cyst sites. The MannWhitney 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 KruskalWallis 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.
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Results |
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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.
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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.
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Discussion |
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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., 1996; Donnez et al., 1996
) 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., 1996
; Loh et al., 1999
) or in monitored natural cycles (Loh et al., 1999
). 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., 1996
; Loh et al., 1999
; Donnez et al., 2001
; Ho et al., 2002
; Somigliana et al., 2003
). On the contrary, in similar settings, other groups were unable to find clinically significant differences (Canis et al., 2001
; Marconi et al., 2002
).
In a recent study (Muzii et al., 2002) 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., 2002
), and from other indirect evidence obtained at laparotomy (Maneschi et al., 1993
), 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., 2002
), Hachisuga and Kawarabayashi (2002)
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., 2002
), 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., 2002), 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, 1990
).
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 0.10.3 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, 0.10.8 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.
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References |
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Submitted on December 9, 2004; resubmitted on February 10, 2005; accepted on February 17, 2005.
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