Acta Obstetricia et Gynecologica.

2006; 85: 1375
1380

ORIGINAL ARTICLE

Relation between severity of dysmenorrhea and endometrioma

NICOLAS CHOPIN, MARCOS BALLESTER, BRUNO BORGHESE, ARNAUD

FOULOT, CE
CILE MALARTIC & CHARLES CHAPRON
FAUCONNIER, HERVE
Universite Rene Descartes (Paris V); Assistance Publique
Hopitaux de Paris (AP-HP); Groupe Hospitalier Universitaire
Ouest; Service de Gynecologie Obstetrique et Medecine de la Reproduction (Pr Chapron), Unite de Chirurgie Gynecologique,
CHU Cochin, Paris, France

Abstract
Background . To evaluate the relationship between the severity of dysmenorrhea and endometrioma. Methods. Descriptive
study with prospective design. Two hundred and thirty-nine women with histologically proved endometriomas. The severity
of dysmenorrhea was assessed prospectively with a 10-cm visual analog scale. Various indicators concerning the
endometrioma and the extent of deep infiltrating endometriosis were recorded during surgery in 239 patients. Correlations
were sought with a multiple regression logistic model. Results. According to univariate analysis, the following variables were
related to more severe dysmenorrhea: subperitoneal infiltration (uterosacral ligament and rectal infiltration) and R-AFS
score of implants. None of the specific characteristics of endometriomas were associated with severe dysmenorrhea. After
multiple regression analysis, rectal infiltration and R-AFS score of implants were the only factors that remained related to
dysmenorrhea severity. Conclusions. When there is an endometrioma, severe dysmenorrhea is not directly related with the
characteristics specific to these ovarian cysts. The associated deep infiltrating endometriotic lesions and in particular rectal
infiltration could explain these symptoms.

Key words: Endometrioma, deep infiltrating endometriosis, pelvic pain, dysmenorrhea

Deeply infiltrating endometriosis (DIE) is a specific

affliction responsible for painful functional symptoms, sometimes associated with infertility (1,2).
The types of pelvic pain (dysmenorrhea (DM), deep
dyspareunia, non-cyclic chronic pelvic pain, lower
urinary and gastrointestinal symptoms) are related to
the anatomic location of DIE (3). DM is very
common in the general population (4) and is
especially frequent in women with endometriosis
(5). Endometriosis is frequently located on the ovary
and tends to be associated with other sites affected
by the disease (6). In the case of DIE, the intensity of
the pain is recognized as being proportional to the
depth to which the lesions penetrate (1,7,8). The
factors described as being responsible for pelvic pain
in case of endometriomas are not clearly defined
(1,7
12). Most studies address all types of endometriotic lesions without drawing any distinction be-

tween DIE and other types of endometriosis. Their

inclusion criteria are generally the existence of
painful symptoms or infertility, resulting in a heterogeneous population of patients who do not necessarily present any endometriotic cyst.
Our aim is to clarify which factors and which
characteristics of endometriotic cysts are responsible
for severe DM, working on a prospective basis with a
homogeneous population of patients with endometriomas.

Materials and methods

Population study
This descriptive study with a prospective design
includes all the women presenting an endometrioma
who underwent surgery for pelvic pain symptoms
between January 2000 and December 2003. This

Correspondence: Charles Chapron, Service de Gynecologie Obstetrique II, Clinique Universitaire Baudelocque, 123 Bld Port-Royal, 75014 Paris, France.
E-mail: charles.chapron@cch.ap-hop-paris.fr

(Received 21 February 2006; accepted 22 July 2006)

ISSN 0001-6349 print/ISSN 1600-0412 online # 2006 Taylor & Francis
DOI: 10.1080/00016340600935490

1376

N. Chopin et al.

selection was made during the diagnostic phase and

was based on preoperative ultrasound examination
revealing an endometrioma of over 2 cm. Only
histologically proved endometriomas were included.
Endometriotic lesions were considered histologically
confirmed when endometrial glands and stroma
were present at microscopic examination.
Variables
DM intensity was assessed prospectively with a 10cm visual analog scale reading recorded during the
month before surgery by means of a self-assessment
questionnaire. Severe DM was defined as a pain
score of 7 or above on the linear scale (13). The
patients characteristics (age, height, weight, body
mass index (BMI) (kg/m2), parity, history of medical
or laparoscopic treatment for endometriosis) were
recorded. Concerning the endometriomas, the following characteristics were recorded: number of
endometriomas, mean size of each in case of multiple locations, laterality, and CA-125 level.
Associated endometriotic lesions were superficial
peritoneal endometriosis, DIE, adnexal adhesions,
and Douglas pouch adhesions (absent, partial obliteration, complete obliteration). The disease stage
was scored according to the revised American
Fertility Society classification (14) and subscores
for implants and adhesions were also recorded.
Anatomic locations of DIE-associated nodules were
coded according to a previously published classification (15). According to this classification, patients
were classed in four groups according to the location
of the DIE lesions: uterosacral ligament (USL),
when lesions infiltrated the USL(s) only; vagina,
when lesions infiltrated the anterior rectovaginal
pouch, posterior vaginal fornix, and retroperitoneal
area between the anterior rectovaginal pouch and the
posterior vaginal fornix; bladder, when lesions
infiltrated the bladder muscularis propria; and intestine, when lesions involved the muscularis propria of the bowel. When there were several locations
in the same patient, she was classed in the group for
the lesion that was considered to be the most severe.
By definition, the increasing order of severity was the
following: USL, vagina, bladder, intestine.

We used the Kruskal
Wallis test to compare multiple quantitative variables. Subsequently, the variables associated with severe DM at the threshold of
p
/0.20 in univariate analysis were tested in a
multiple logistic regression model. A final model
was constructed including only those variables
independently associated with severe DM at the
threshold of B/0.05. The parameter values of the
final model were estimated by the maximum likelihood method, and adjusted odds ratios and their
confidence intervals calculated from the models
coefficients and their standard deviations.
Results
During the study period, 310 patients presenting a
histologically proven endometrioma measuring
over 20 mm and pelvic pain were operated. Seventy-one (22.9%) were excluded for the following
reasons: amenorrhea and menopausal status
11
cases (3.6%); failure to respond to the questionnaire

60 cases (19.4%). The final study population
included 239 women (77.1%).
Out of the 239 patients eligible, the mean value of
the visual analog DM scale reading was 5.19/3.2.
The symptoms were distributed as follows: 154
patients had DM B/7/10 and 85 women had DM ]/
7/10. Their mean values were 3.39/2.6 and 8.39/1.1
respectively (Table I). Among these 239 women, 211
(88.3%) presented endometrioma(s) only versus 28
(11.7%) associated DIE lesions. Their DM scales
were 5.19/3.2 versus 5.59/3.3; p /0.37.
Disease stage was scored according to the R-AFS
classification and details of the scores are reported in
Table II.
After univariate analysis the following variables
were related to more severe DM: subperitoneal
infiltration (USL and rectal infiltration) and R-AFS
score of implants (Table III). None of the specific
characteristics of endometriomas were associated
with severe DM.
After multiple regression analysis, rectal infiltration and R-AFS score of implants above 26 were the
only factors that remained related to DM severity
(Table III).
Discussion

Statistical analysis
Women with severe DM were compared with the
other patients. For univariate statistical analysis we
used the following tests: Pearsons chi-square test for
qualitative variables or Fishers exact test as appropriate; paired Students t-test for quantitative
variables or Wilcoxon signed-rank as appropriate.

While it is accepted that there is an association

between DM and endometriosis (16), the data in the
literature concerning the painful physiopathology of
endometriotic cysts are heterogeneous, few in number and contradictory (1,7
12).
Our aim is to clarify which factors and which
characteristics of endometriotic cysts are responsible

Relation between severity of dysmenorrhea and endometrioma

1377

Table I. Patients characteristics according to the severity of their dysmenorrhea.

DMB/7/10 (n /154 patients)
Variables
Intensity of dysmenorrhea
Patients characteristics
Age (year)
Weight (kg)
Height (cm)

Mean9/SD (extremes)

n (%)

3.39/2.6 (0/6.9)

DM]/7/10 (n/85 patients)

Mean9/SD (extremes)

n (%)

8.39/1.1 (7/10)

35.19/7.8 (20.5/49.8)
59.59/10.7 (42/103)
165.59/7.2 (148/186)

0.72a
0.32a
0.64a

34.89/7.4 (17.4/49.0)
58.89/9.3 (42/89)
164.59/6.3 (151/182)

No. pregnancies
0
1
]/2

126 (81.8)
14 (9.1)
14 (9.1)

66 (77.7)
11 (12.9)
8 (9.4)

0.48b

History of treatment for endometriosis

Laparoscopic treatment
0
1
2
]/3

101 (66.0)
48 (31.3)
4 (2.61)

48 (56.5)
32 (37.7)
5 (5.9)

0.14b

55 (36.4)
28 (18.5)
2 (1.3)

24 (29.6)
26 (32.1)
1 (1.2)

0.13c

Anatomic location and number of deeply infiltrating endometriosis

Bladder
No
Yes

153 (99.4)
1 (0.7)

84 (98.8)
1 (1.2)

USL
No
Yes

135 (87.7)
19 (12.3)

72 (84.7)
13 (15.3)

0.03b

Vagina
No
Yes

51 (98.1)
3 (2.0)

79 (92.9)
6 (7.1)

0.07b

Rectum
No
Yes

153 (99.4)
1 (0.7)

78 (91.8)
7 (8.2)

0.003b

143
5
5
1

68
7
4
1
1
1
2
1

0.003c

Hormonal treatment
Progestational hormones
LH-RH analogs
Other

Total number of lesions

0
1
2
3
4
5
6
7
Endometrioma characteristics
No. of endometriomas
Size of endometrioma no. 1 (mm)
Size of endometrioma no. 2 (mm)*

1.49/0.6 (1.0/4.0)
43.89/26.6 (20.0/250.0)
27.49/13.5 (5.0/80.0)

Laterality
Right
Left
Bilateral
CA-125 assay (UI/ml)
a

(92.9)
(3.3)
(3.3)
(0.7)

0.36d
0.68d
0.65d

1.69/0.8 (1.0/5.0)
40.29/17.8 (4.0/100.0)
29.59/14.9 (15.0/80.0)
36 (23.38)
80 (51.95)
38 (24.68)

61.79/78.6 (5.0/563.0)

(80.0)
(8.2)
(4.7)
(1.2)
(1.2)
(1.2)
(2.4)
(1.2)

22 (25.88)
34 (40.00)
29 (34.12)
629/54.8 (8.0/238.0)

1b

0.17e
0.39d

Students t -test.
Kruskal
Wallis test.
c
Fishers exact test.
d
Wilcoxon test.
e 2
j test.
*Size of endometrioma no. 2 is size of second endometrioma when there are bilateral cysts (the smaller of the two cysts being taken by
convention as endometrioma no. 2).
b

1378

N. Chopin et al.

Table II. Severity of dysmenorrhea according to the revised American Fertility Society Classification (14).
DMB/7/10 (n /154 patients)
Variable

Mean9/SD (extremes)

n (%)

n (%)

93
3
16
35
5

(61.2)
(2.0)
(10.5)
(23.0)
(3.3)

51
0
9
20
5

(60.0)
(0.0)
(10.6)
(23.5)
(5.9)

112
6
21
12
1

(73.7)
(4.0)
(13.8)
(7.9)
(0.7)

57
1
14
13
0

(67.1)
(1.2)
(16.5)
(15.3)
(0.0)

0.19a

AFS deep peritoneum

0
2
4
6
16
25.29/8.0 (16/46)

0.01b
0.73a

28.09/9.4 (10.0/46.0)
54
19
8
14
39
19

(35.3)
(12.4)
(5.2)
(9.2)
(25.5)
(12.4)

28
5
6
17
18
11

(32.9)
(5.9)
(7.1)
(20.0)
(21.2)
(12.9)
0.22a

Left ovary adhesions

0
1
2
4
8
16

39
13
10
25
44
22

AFS Douglas
0
4
40

90 (58.8)
27 (17.7)
36 (23.5)

AFS total adhesions

AFS total (implants/adhesions)

Mean9/SD (extremes)

0.68a

AFS superficial peritoneum

0
1
2
4
6

AFS total implants

Right ovary adhesions
0
1
2
4
8
16

DM]/7/10 (n /85 patients)

(25.5)
(8.5)
(6.5)
(16.3)
(28.8)
(14.4)

17
8
2
17
24
17

(20.0)
(9.4)
(2.4)
(20.0)
(28.2)
(20.0)
0.99a

23.89/27.7 (0.0/104.0)
49.09/31.5 (16.0/150.0)

48 (57.1)
19 (22.6)
17 (20.2)
25.99/28.9 (0.0/104.0)
53.99/33.7 (14.0/150.0)

0.23b
0.13b

Kruskal
Wallis test.

Wilcoxon test.

for severe DM working on a homogeneous painful

population of patients with endometriomas. To our
knowledge no study has addressed a homogeneous
population of patients with endometriomas on a
prospective basis.
Our study found two independent factors associated with severe DM: rAFS score for implants
exceeding 26 and the presence of associated deeply
infiltrating rectal endometriosis.
The specific characteristics of the endometriomas
do not appear to be correlated with the severity of
the DM. The innervation characteristics of endometriomas could explain this finding. Nerve infiltration
by deeply infiltrating endometriotic lesions has been
shown to correlate with the severity of DM. This
association has been clearly demonstrated in case of
vaginal or GI tract lesions, and implants that

penetrate the wall of adjacent organs have closer

relationships with nerve fibers than those that do not
(13,17). Unlike the case for these lesions, there are
Table III. Determinants for severity of DM results from multiple
logistic regression analysis.
Independent variable Adj OR for severity of DM

95% CI

Rectal infiltration
Yes
No

1
0.082

0.010
0.687

Score rAFS implants*

]/24
B/24

1
0.521

0.300
0.905

CI, confidence interval.

*Score according to the revised American Fertility Society
Classification (14).

Relation between severity of dysmenorrhea and endometrioma

no nerve fibers to be found in endometriomas (18),
which may be the reason why these cysts are not very
painful. Two studies only found a correlation between DM and the presence of endometriomas
(12,19). Fedele et al. found an association between
unilateral or bilateral endometriomas and the severity of DM. Muzii et al. described a correlation
between the presence of an endometriotic cyst and
the severity of DM. On the contrary, for Vercellini
et al. (10) DM was less frequent in patients with
ovarian endometriosis only, than in those with
associated lesions at other sites. Porpora et al. (8)
found an association between DM and endometriomas by univariate analysis. This relationship would
seem to disappear after adjustment, and analysis
suggests that this pain is related to periovarian
adhesions rather than to the cyst itself. The physiopathological mechanism by which these periadnexal
adhesions might be associated with DM remains
unclear. Similar results have been reported by other
authors (10,20).
Our results, concerning rectal involvement as an
independent factor correlated with the severity of
DM in the case of endometrioma, appear to confirm
the results of earlier works (7). Although the initial
population in this study concerned patients with
DIE with or without specific ovarian endometriotic
lesions, the authors had already revealed an association between the severity of DM and the depth of
posterior subperitoneal disease involvement. One of
the hypotheses evoked was the correlation between
compression or infiltration of the nerves by these
endometriotic lesions in the subperitoneal pelvic
space, in particular in the posterior area (20).
For Redwine (6), deep involvement of the bowel is
significantly greater in patients presenting an endometrioma. Moreover, whether in the presence of
an endometrioma or not, many studies have found a
link between the intensity of DM and the extent of
the disease measured by the rAFS score (12,19,21),
the number of endometriotic implants, or the presence of associated deeply infiltrating lesions (11).
So, in agreement with those of other authors, our
results show that in cases of severe DM, the
existence of an endometrioma suggests more diffuse
and in particular subperitoneal presence of endometriotic disease involvement. But it is important to
underline that with respect to the rAFS score for
implants these results remain difficult to interpret.
This is because the weighting associated with an
endometriotic cyst in this classification system is
particularly high, with a score of at least 16 in case of
a cyst measuring over 2 cm and at least 20 in case of
a cyst measuring over 3 cm. To this score for the
cystic implants is then added the score for any

1379

associated deeply infiltrating lesions. All our patients

had at least one endometrioma over 2 cm in size. So
in our study the implant score tends necessarily to
reach a high figure without it being possible,
unfortunately, to know whether this is due to the
presence of the cyst or the associated lesions. As
already mentioned, these results underline the limits
of the rAFS classification with respect to DIE
(10,22). The score was initially proposed for patients
presenting with infertility in a context of endometriosis without taking the problem of pelvic pain into
account when scoring deep endometriotic lesions.
Such lesions appear to be underestimated. In the
case of endometrioma the score is overestimated.
Our results show that endometriomas as such are
not much involved in the genesis of DM. The pain is
most probably secondary to the presence of associated subperitoneal lesions, and rectal lesions in
particular. The existence of an endometriotic cyst
when there is severe DM would appear to form part
of a more diffuse endometriotic disease context. It
justifies a preoperative search for the exact location
of possible associated deeply infiltrating lesions by
precise questioning, perimenstrual clinical examination, and possibly an in-depth imaging work-up.
Acknowledgements
The authors thank Aventis-Synthelabo Laboratories
(France) for providing technical assistance in statistical analysis.

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