Professional Documents
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severe endometriosis
Fabio Ghezzi, M.D.,a Luigi Raio, M.D.,b Antonella Cromi, M.D.,a Daniela Günter Duwe, M.D.,b
Paolo Beretta, M.D.,a Marco Buttarelli, M.D.,a and Michael D. Mueller, M.D.b
a
Department of Obstetrics and Gynecology, University of Insubria, Del Ponte Hospital, Varese, Italy; and b Endometriosis
Center, Department of Obstetrics and Gynecology, University of Berne, Berne, Switzerland
Objective: To evaluate whether the presence of kissing ovaries at ultrasound is a marker for endometriosis and
whether it correlates with the severity of the disease.
Design: Prospective observational study.
Setting: Gynecologic departments of two university hospitals.
Patient(s): A total of 722 consecutive premenopausal women who had laparoscopic surgery for an adnexal mass
or suspected pelvic endometriosis.
Intervention(s): Preoperative ultrasound evaluation and laparoscopic surgery.
Main Outcome Measure(s): Diagnostic and predictive value of ultrasound identification of kissing ovaries in the
detection of endometriosis.
Result(s): Kissing ovaries were diagnosed at ultrasound and confirmed laparoscopically in 32 patients. Of these,
27 had moderate to severe endometriosis and five others had benign adnexal masses. Bowel (18.5% vs. 2.5%) and
fallopian tube (92.6% vs. 33%) endometriosis were significantly more frequent in patients with kissing ovaries
than in patients without kissing ovaries. In infertile patients (n ⫽ 145), kissing ovaries were associated with a
higher proportion of women with fallopian tube obstruction (80% vs. 8.6%). Considering patients with moderate
to severe endometriosis (n ⫽ 189), the median (range) revised American Fertility Society score (74 [32–148] vs.
35 [16 –146]) and the operative time (115 minutes [65–245 minutes] vs. 50 [15–180 minutes]) were significantly
higher in patients with than in those without kissing ovaries.
Conclusion(s): The detection of kissing ovaries at ultrasound is strongly associated with the presence of
endometriosis and is a marker of the most severe form of this disease. (Fertil Steril威 2005;83:143–7. ©2005 by
American Society for Reproductive Medicine.)
Key Words: Endometriosis, kissing ovaries, ultrasound, laparoscopy, bowel endometriosis
A number of scores have been proposed to interpret the pelvic side (9, 10). Recently, Dessole et al. described a new
gray-scale ultrasound appearance of pelvic masses to differ- procedure, which is based on transvaginal ultrasound com-
entiate benign from malignant tumors (1, 2). The accuracy of bined with the introduction of saline solution in the vagina to
transvaginal ultrasound in evaluating pelvic cysts suspected enhance the identification of rectovaginal endometriosis
to be endometriomas has been widely evaluated (4, 5). (11).
Moreover, the possibility of implementing the conventional
ultrasound assessment of the female pelvis with the use of An improved preoperative assessment of endometriosis,
color Doppler and power Doppler imaging techniques has particularly the identification of severe forms of the disease,
further refined the ability to correctly diagnose endometrio- would allow for better planning of surgery. In these cases, it
mas (6 – 8). is common to observe that the ovaries, although sonographi-
cally normal, are entirely or partly joined together and sta-
However, even when endometriosis is suspected preoper- bilized behind the uterus in the pouch of Douglas (so-called
atively, the difficulty in evaluating its extension remains a kissing ovaries) at the time of laparoscopy. Therefore, we
major limitation. Previously published studies propose some sought to assess the accuracy of preoperative transvaginal
tools for preoperative counseling on the basis of the ultra- ultrasound in correctly identifying the presence of kissing
sound appearance of the ovarian cysts and their relation to ovaries and to establish whether this finding correlates with
the anatomical location of the lesions (9 –11). It has been the severity of endometriosis.
reported that the involvement of the left side of the pelvis is
associated with a higher recurrence risk and with a worse
pregnancy outcome than endometriosis limited to the right MATERIALS AND METHODS
Consecutive premenopausal women with an adnexal mass or
with clinical signs suggestive of pelvic endometriosis and
Received January 26, 2004; revised and accepted May 14, 2004.
scheduled for laparoscopic surgery between January 1, 2000,
Reprint requests: Fabio Ghezzi, M.D., Department of Obstetrics and
Gynecology, University of Insubria, Piazza Biroldi 1, 21100 Varese, Italy and November 30, 2003, were enrolled at the participating
(FAX: 39-0332-299-307; E-mail: fabio.ghezzi@uninsubria.it). institutions. Exclusion criteria were [1] previous surgical
0015-0282/05/$30.00 Fertility and Sterility姞 Vol. 83, No. 1, January 2005 143
doi:10.1016/j.fertnstert.2004.05.094 Copyright ©2005 American Society for Reproductive Medicine, Published by Elsevier Inc.
FIGURE 1 FIGURE 2
Transvaginal ultrasound image of “kissing ovaries” Transvaginal ultrasound image of “kissing ovaries”
in the presence of a unilateral endometrioma. in the absence of definite endometriomas.
144 Ghezzi et al. Kissing ovaries at ultrasound and endometriosis Vol. 83, No. 1, January 2005
TABLE 1
Histological characteristics according to the ultrasound findings.
used to compare continuous variables and proportions, respec- endometriosis (n ⫽ 189), the median rAFS score was sig-
tively. P⬍.05 was considered statistically significant. nificantly higher in those with the ultrasound presence of
kissing ovaries than among patients without kissing ovaries
(median, 74; range, 32–148; vs. median, 35; range 16 –146;
RESULTS
P⬍.001). The median (range) operative time was signifi-
A total of 722 women were enrolled in the study. Twelve cantly longer in the former than in the latter group of patients
cases were excluded for the following reasons: in six cases a (115 minutes [65–245 minutes] vs. 50 minutes [15–180
uterine myoma was misdiagnosed as an adnexal mass, in minutes]; P⬍.001). Considering only patients with bilateral
four cases a malignant ovarian tumor was revealed at frozen ovarian endometriomas (n ⫽ 45), the median (range) rAFS
section examination, in one case an appendicular mucocele score (74 [50 –148] vs. 49 [21–146]; P⬍.005) and the me-
was erroneously diagnosed as a sactosalpinx, and in one case
dian operative time (135 minutes [90 –245 minutes] vs. 65
a large lymphocyst was misdiagnosed as an ovarian cyst. A
minutes [40 –135 minutes]; P⬍.001) were significantly
total of 309 women underwent ultrasound and laparoscopy
higher in patients with (n ⫽ 13) than in those without (n ⫽
because of clinical or ultrasound signs suggestive of endo-
32) kissing ovaries. Among patients with unilateral endo-
metriosis. In the remaining cases, surgery was performed for
metriomas (n ⫽ 126), those with kissing ovaries at ultra-
an adnexal mass nonsuggestive of endometriosis.
sound (n ⫽ 9) had a higher median (range) rAFS score (80
Among the patients who underwent laparoscopy for sus- [32–128] vs. 33 [19 –120]; P⬍.005) and a longer median
pected endometriosis (chronic pelvic pain, dyspareunia, dys- operative time (110 minutes [65–185 minutes] vs. 65 min-
menorrhea), a normal pelvis was found at laparoscopy in 21 utes [20 –180 minutes]; P⬍.005) than women without kiss-
cases. In nine cases, a benign adnexal mass was misdiag- ing ovaries (n ⫽ 117). Among patients without definite
nosed as an endometrioma. In 20 cases, mono-/bilateral endometriomas (n ⫽ 138), those with ultrasound kissing
endometriomas were misdiagnosed as nonendometriotic be- ovaries (n ⫽ 5) had a higher median (range) rAFS score (75
nign adnexal tumors. [32–106] vs. 8 [1–30]; P⬍.005) and a longer median oper-
ative time (80 minutes [65–100 minutes] vs. 35 minutes
Kissing ovaries were diagnosed in 32 (4.4%) patients at
[15–70 minutes]; P⬍.005) than women without kissing ova-
preoperative ultrasound. Laparoscopy confirmed the pres-
ries (n ⫽ 133).
ence of joined ovaries in the pouch of Douglas, adherent to
surrounding tissue in all cases. Table 1 displays the histo-
The most severe form of pelvic endometriosis (rAFS
logical findings of the study population according to the
ⱖ70) was more frequent among patients than among those
ultrasound appearance of the ovaries.
without kissing ovaries (16/32 [50.0%] vs. 27/678 [4.0%];
Pelvic endometriosis was present in 309 (43.5%) cases. P⬍.0001). The presence of dense adhesions requiring sur-
The rAFS classification and location of the disease are pre- gical lysis between the adnexae and the sigmoid was signif-
sented in Table 2. Among patients with moderate to severe icantly higher in patients with endometriosis than in those
without kissing ovaries on ultrasound (25/27 [92.6%] vs. Although the etiology of endometriosis still remains an
99/282 [35.1%]; P⬍.0001). enigma, most investigators agree that the persistence and
progression of ectopic endometrial tissue is intimately con-
The laparoscopic tubal patency test was performed in 145
nected with a local pelvic inflammatory process (13, 14).
infertile patients. Of these, five cases had kissing ovaries,
Thus, it has been demonstrated that women with endometri-
107 patients had pelvic endometriosis; and the remaining 33
osis have higher concentrations of proinflammatory cyto-
patients had nonendometriotic adnexal masses. A higher
proportion of cases with complete obstruction of both fallo- kines in their peritoneal fluid than women without endome-
pian tubes was found among patients with kissing ovaries triosis (15–17). The peritoneal fluid accumulates in the
than among those without kissing ovaries (4/5 [80%] vs. dependent portions of the pelvis (18), especially in the pouch
12/140 [8.6%]; P⬍.001). This figure did not change when of Douglas, and the inflammation triggered by the endome-
the analysis was restricted only to patients with endometri- triosis induces adhesion formation between the adjacent
osis (4/5 [80%] vs. 11/107 [10.3%]; P ⫽ .001). peritoneal surfaces and organs (19), displacing the ovaries
medially and caudally into the Douglas.
In all five cases diagnosed to have kissing ovaries and not
affected by endometriosis, dense adhesions were present Previous studies (1–3) that explored the predictive abil-
between the ovaries, requiring lysis at the time of operation. ity of ultrasound in identifying women with endometriosis
showed an optimal agreement between ultrasound and
intraoperative diagnosis only for ovarian endometriomas.
DISCUSSION
The lack of a noninvasive tool to predict anatomic loca-
The present study shows that the detection of kissing ovaries tions and extension of the disease in the absence of
at ultrasound is strongly associated with the presence of definite endometriomas has deeply limited the preopera-
endometriosis and in particular is a marker of the most tive assessment. Our findings are in keeping with those of
severe form of the disease. Indeed, in all cases an important
Exacoustos et al. (20), who found a high correlation
adhesion formation between the ovaries and the surrounding
between ultrasound and surgical findings. In particular,
pelvic organs and structures (e.g., with the sacrouterine
these investigators reported an 82% agreement between
ligaments, rectum, posterior uterine wall) was present.
ultrasound and intraoperative evaluation in cases of se-
The development of kissing ovaries is probably mimick- vere endometriosis. According to our results, when ultra-
ing the processes induced in pelvic inflammatory disease. sound reveals the presence of kissing ovaries, the surgeon
146 Ghezzi et al. Kissing ovaries at ultrasound and endometriosis Vol. 83, No. 1, January 2005
should expect to find a tangled pelvis with subverted P. Validation study of nonsurgical diagnosis of endometriosis. Fertil
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Sonovaginography is a new technique for assessing rectovaginal endo-
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