doi:10.1111/jog.14191 J. Obstet. Gynaecol. Res.

2020

Accuracy and clinical value of an adhesion scoring system:

A preoperative diagnostic method using transvaginal
ultrasonography for endometriotic adhesion

Masao Ichikawa , Shigeo Akira, Hanako Kaseki, Kenichiro Watanabe, Shuichi Ono and
Toshiyuki Takeshita
Department of Obstetrics and Gynecology, Nippon Medical School, Tokyo, Japan

Abstract
Aim: To investigate the accuracy and clinical value of an adhesion scoring system using transvaginal ultraso-
nography for endometriotic adhesion.
Methods: In this prospective observational study, we included 131 patients with endometriosis who under-
went surgery. Before surgery, transvaginal ultrasonography and adhesion mapping were performed to
determine the presence or absence of adhesions at 10 sites of the pelvis. Mapping accuracy was determined
by comparing the mapping findings with the surgical findings. To determine the severity of pelvic adhe-
sions, we developed an adhesion score (0–10). With the adhesion score, we assessed the effect of surgical
adhesiolysis and evaluated the relationship between postoperative adhesions and infertility.
Results: Of the 10 sites assessed for adhesions, the most frequent site of adhesions was the site between the
left ovary and the uterus (70.5%). The overall sensitivity, specificity, positive predictive value, negative pre-
dictive value, positive likelihood ratio, negative likelihood ratio and accuracy of adhesion mapping were
80.4%, 86.1%, 78.8%, 87.2%, 5.79, 0.23 and 83.9%, respectively. The adhesion score in this system was signifi-
cantly correlated with the adhesion-related score in the revised American Society for Reproductive Medicine
classification (R2 = 0.734). Surgical adhesiolysis yielded only about 30% improvement postoperatively. The
adhesion score 1 month after surgery in the non-in vitro fertilization (IVF) pregnancy group was significantly
lower than that in the IVF pregnancy group (3.45 vs 5.21; P = 0.02).
Conclusion: Our adhesion scoring system allowed an accurate prediction of the pelvic adhesion status and
may potentially be an indicator of postoperative adhesions and infertility.
Key words: adhesion mapping, adhesion score, endometriosis, preoperative diagnosis.

Introduction Endometriotic adhesions have been associated with

infertility.5–7 Furthermore, the presence of severe adhe-
Endometriosis is a disease that presents as various sions has been associated with low pregnancy rates.8
pathological conditions1 including endometrioma, deep Open surgery with colorectal resection for endometri-
infiltrating endometriosis (DIE) and endometriotic osis reportedly triggered the formation of massive
adhesions. Therefore, it is not easy to comprehensively adhesions, leading to poorer pregnancy rates com-
evaluate all these pathologies with a single test.2–4 pared with laparoscopy.9,10 Therefore, it is clinically
Therefore, focusing on one pathological condition and relevant to accurately diagnose endometriotic adhesion
completely grasping its spread and severity is impor- status to predict the possibility of future pregnancy.
tant in the treatment of endometriosis. Thus far, the conventional revised American Society

Received: September 18 2019.

Accepted: December 31 2019.
Correspondence: Dr Masao Ichikawa, Department of Obstetrics and Gynecology, Nippon Medical School, 1-1-5 Sendagi, Bunkyo,
Tokyo, Japan. Email: masai@nms.ac.jp

© 2020 Japan Society of Obstetrics and Gynecology 1

M. Ichikawa et al.

for Reproductive Medicine (r-ASRM) classification,

which is based on surgical findings, is the only
method to completely depict the endometriotic
adhesion status,11,12 and no definitive noninvasive
method to describe endometriotic adhesions has
been established.
Several other methods, such as the Enzian score,13–16
ultrasound mapping17,18 and endometriosis fertility
index (EFI) method19,20 have been proposed as diagnos-
tic methods for endometriosis. The former two diagnos-
tic methods focus on DIE. The EFI method is useful for
estimating postoperative pregnancy rates, but it cannot
be calculated without surgical intervention. The least
function score, part of the EFI method, is estimated dur-
ing surgery. In contrast, magnetic resonance imaging is
a noninvasive method proven useful at detecting Figure 1 Adhesion scoring system. A sheet of adhesion
endometrioma2 and DIE, among other variants16,21–24; scoring system consists of two sections: the adhesion
however, this method may not be ideal for detecting mapping phase and adhesion scoring phase. The
adhesion map has 10 blanks in total: five blanks in
adhesions without structural deformation. the transverse plane and five blanks in the sagittal
The sliding sign technique using transvaginal ultra- plane. Each blank space is filled with one of +, −, ? or
sonography is well known as a noninvasive and effec- NA. In the adhesion scoring phase, the total number
tive approach for detecting endometriotic adhesions at of sites with adhesions (+) was considered as the
the Douglas’ pouch.25,26 However, this method is not adhesion score and was written in parentheses below
the sheet.
suitable for estimating the extent and severity of adhe-
sions in the pelvis because of the limited scan area.
To diagnose the extent and severity of adhesions in
the pelvis, we applied the slide sign technique to adhesion scoring phase, which consisted of calculat-
10 sites in the pelvis and created a new adhesion scor- ing the score based on the lesions detected. During
ing system. the adhesion mapping phase, we evaluated the pres-
ence or absence of adhesions in a total of 10 sites: five
in the uterus–ovarian cross-section (transverse) and
Methods five in the sagittal section of the uterus (sagittal). We
used a 3 × 3 grid in the transverse plane composed of
This was a prospective observational study. All the following five sites: the spaces between the right
patients underwent transvaginal ultrasound examina- ovary and the uterus (Rt O-Ut) and between the left
tion and adhesion scoring using our system preopera- ovary and the uterus (Lt O-Ut), the space between the
tively and 1 month postoperatively. Their examination left and right ovary (Inter O-O), the spaces between
was performed by M. I., a physician with vast surgical the right ovary and the right pelvic sidewall (Rt O-
experience. Postoperative follow-up was performed up Side) and between the left ovary and the left pelvic
to 5 years in reachable patients. This study was sidewall (Lt O-Side) (Fig. 1a). We used a 3 × 3 grid in
approved by the ethics committee of Nippon Medical the sagittal plane composed of the following five
School, and informed consent was obtained from each areas, the upper half (Up Ant) and the lower half
patient who agreed to participate in this study. (Mid Ant) of the anterior side of the uterus, ranging
from the top of the uterus to the vesicouterine pouch
Adhesion scoring system and the upper third (Up Post), the middle third (Mid
The adhesion scoring system was designed to mea- Post) and the lower third (Low Post) of the posterior
sure the extent and severity of endometriotic adhe- side of the uterus, ranging from the top of the uterus
sions (Figs 1a,2a,c). This system comprises two parts: to Douglas’ pouch (Fig. 1a).
(i) the adhesion mapping phase, which consisted of The presence or absence of adhesions in each site
mapping all the detected adhesions to estimate the was determined via transvaginal ultrasonography
extent of the endometriotic adhesions and (ii) the examination using the sliding sign technique (Fig. 2b).

2 © 2020 Japan Society of Obstetrics and Gynecology

 Adhesion scoring system for endometriosis

Figure 2 Adhesion diagnosis in adhesion scoring system. An example of actual adhesion diagnosis in a case showing bilat-
eral endometriomas. (a) The recorded sheet of preoperative adhesion status. In this case, adhesions were found at four
locations on the transverse section (①Rt O-Ut, ③Inter O-O, ④Lt O-Ut and ⑤Lt O-Side) and two locations on the sagittal
plane (⑨Mid Post and ⑩Low Post). Therefore, the adhesion score for this case is 6 points, which is the total of 4 points in
the transverse section and 2 points in the sagittal plane. (b) Adhesion diagnosis images by transvaginal ultrasonography
in each area. I: Cross-sectional image, checking the adhesion around the right ovary (three areas). By moving the ovary
with an ultrasound probe, ①Rt O-Ut and ③Inter O-O were not mobile. On the other hand, the mobility was observed in
②Rt O-side. II: Cross-sectional image, checking the adhesion around the left ovary. The mobility of ④Lt O-Ut and ⑤Lt O-
Side region was not observed. III: Sagittal section, checking the adhesion at the front of the uterus. ⑥Mid Ant and ⑦Up
Ant showed mobility. IV: Sagittal section, checking the adhesion at the back of the uterus. ⑧Up Post showed mobility, but
⑨Mid post and ⑩Low Post were not mobile. (c) Recorded sheet of intraoperative adhesion status. Of the six expected sites
of adhesion diagnosed before surgery, five were actually confirmed to have adhesions. Inter O-O was diagnosed to have
adhesion before surgery, but it showed no adhesion during surgery (circled area). (d) Images of adhesion diagnosis in each
area during laparoscopic surgery. (Note) The left and right sides of the laparoscopic photographic image are opposite to
those of the image diagnosed by transvaginal ultrasonography. I: Overall picture of the pelvic cavity at surgery, bilateral
endometriomas were confirmed, but the adhesion at ③ Inter O-O was not observed. II: Confirmation of adhesions around
the ovary, the outside of the left ovary ⑤ Lt O-Side was not mobile. On the other hand, the outside of the right ovary ② Rt
O-Side could be moved. III: There was no adhesion on the front of the uterus. IV: Adhesion around the Douglas fossa.
The inside of the right ovary ① Rt O-Ut was not mobile. The Douglas fossa ⑩ in this deep place was completely closed.

The sliding sign technique consists of determining placed transvaginally. If sliding occurs, there is no
whether or not an object is sliding against its sur- adhesion at the given site (Fig. 2b-I②, III⑥⑦, IV⑧), and
roundings by pushing it with the examiner’s hand a negative sign (−) is assigned to the corresponding
over the abdominal wall and the ultrasound probe site on the sheet (Fig. 2a). Conversely, if sliding did

© 2020 Japan Society of Obstetrics and Gynecology 3

M. Ichikawa et al.

not occur, an adhesion was detected at the given site described as an intraoperative adhesion score ranging
(Fig. 2b-I①③, II④⑤, IV⑨⑩) and a positive sign (+) is from 0 to 10 (Fig. 2c).
assigned to the corresponding site on the sheet The cyst score was the score obtained by scoring
(Fig. 2a). In the scoring phase, the total number of the size of endometriomas (or fallopian tube swelling)
sites showing adhesions in both images is directly with transvaginal ultrasonography.27 One, four, or
described as adhesion score ranging from 0 to five points (1/4 of the r-ASRM ovary score) were
10 (Fig. 2a). given for unilateral endometrioma with a diameter
Several rules apply for adhesion mapping in this <1, 1–3 or >3 cm, respectively. The sum of the points
system. First, when a uterus is enlarged owing to the on both sides was the cyst score (0–10). Thereafter,
presence of uterine fibroids, for instance, the examiner the sum of this score and the aforementioned adhe-
bisects the anterior side of the uterus, divides the pos- sion score was considered as the total score in this
terior side of the uterus into three sections, and checks system.
for the presence or absence of adhesions in each area. Of note, in this adhesion scoring system, we did
Subsequently, the examiner checks the Inter O-O site, not consider the existence of film-like adhesions. The
which is a common site for adhesions between bilateral transvaginal ultrasonography device used in this
endometriomas resulting in the so-called kissing study was Voluson E 8 (GE Healthcare).
ovaries. However, even in a case of unilateral
endometrioma, if an adhesion was detected between Surgery
the center side of an enlarged ovary and adjacent tis- At the beginning of the surgery, we routinely checked
sue, such as the rectum, this should be judged as a site the r-ASRM classification and the adhesion map via
positive for adhesion. When both ovaries have a nor- laparoscopic view of the pelvis. Additionally, the final
mal size, the Inter O-O site should be judged as nega- status of pelvic adhesions was recorded at the end of
tive for adhesion. However, if they are moved toward the surgery.
the center, and there is no fluidity between them, this During the laparoscopic surgery, adhesions in the
area might be considered positive for adhesion. In case abdominal cavity were removed, and the contents of
of a site where the status of adhesions is unclear by the endometriomas were aspirated. After releasing the
any reason, such as the presence of a huge ovarian adhesions around the ovaries, the uterine posterior
cyst, it might be recorded as unknown (?). Addition- flexion was released. The ureter was identified, and
ally, when an assessment cannot be made because of a the rectovaginal space was opened to identify the
lack of adnexa, the site should be judged as NA. uterosacral ligament (USL). Subsequently, any obstruc-
The accuracy of adhesion mapping recorded preop- tion of the Douglas’ pouch was removed. This was
eratively is confirmed at the time of surgery (Fig. 2c, followed by excision of the USL accompanied with
d) by M. I. and other colleagues, that is, the same visually suspected DIE (e.g., tissue thickening or con-
10 sites evaluated by transvaginal ultrasonography tracture), or laparoscopic uterosacral nerve ablation in
are directly evaluated under laparoscopy of the pelvis some cases with mild lesions. Finally, cystectomy of
to determine whether the adhesions exist or not any endometriomas was meticulously performed to
(Fig. 2d). The presence of adhesions was assessed by preserve ovarian function.28,29 Lesions on the surface
checking whether or not there was mobility between of the rectum were removed by shaving if neces-
an object and its surroundings based on the pressure sary.30,31 In some cases, interventions for vaginal endo-
felt by the examiner on the laparoscopic forceps metriosis, uterine adenomyosis, or fibroids were
(Fig. 2dIII, IV). That is, when mobility can be seen performed in consultation with the patient prior to the
between two structures, it should be judged as a site surgery.
negative for adhesion; otherwise, it should be judged
as a site positive for adhesion. For example, if the Statistics
mobility between the front left side of a right Population characteristics are reported as mean
endometrioma and the posterior right side of the + minimum − maximum or as the number of cases in
uterus (Rt O-Ut) were recognized well, adhesion at each category and its frequency. The sensitivity, speci-
this site would be negative (−). Conversely, if the ficity, positive predictive value, negative predictive
mobility cannot be clearly recognized, the site would value, positive likelihood ratio (LR+), negative likeli-
be positive (+) (Fig. 2dIV①). As a final step, the total hood ratio (LR−) and accuracy were calculated at
number of sites showing adhesions was directly http://statpages.info/ctab2x2.html. The correlations

4 © 2020 Japan Society of Obstetrics and Gynecology

 Adhesion scoring system for endometriosis

between the adhesion score and the adhesion-related adhesive agent or postoperative drug use group and
score of r-ASRM, and the adhesion score + cyst score the nonuse group was examined for significant differ-
and total score of r-ASRM were calculated by ence using two-tailed Student’s t-test. A P-value of 0.05
Pearson’s correlation coefficient (two-tailed test) using or less was considered statistically significant. Similarly,
Statcel 3 software (OMS Publishing LTD). changes in the value of the adhesion score before and
In examining the effects of anti-adhesive agents or after surgery were also examined. Comparative studies
drugs for endometriosis on postoperative adhesions, of the relationship between adhesions and infertility
the adhesion score at each measurement point in anti- were examined in the same way.

Table 1 Patient characteristics and surgeries

Patient characteristics and surgeries (n = 131) Mean (Min–Max); n (%) Subgroup, n (%)
Age (years, mean, Min–Max) 35.6 (23–51)
Body mass index (kg/m2, mean, Min–Max) 21.0 (17.1–34.4)
Parity (n, %) 0.31 (0–3)
Previous medical treatment for endometriosis (n, %) 63 (48.1)
Previous surgery for endometriosis (n, %) 12 (9.2)
Mean operation time (min, mean, Min–Max) 181 (40–421)
Mean blood loss (mL, mean, Min–Max) 76 (0–922)
Endometrioma
None (n, %) 2 (1.5)
Unilateral endometrioma (n, %) 61 (46.6)
Unilateral salpingo-oophorectomy (USO) 6 (4.7)
Unilateral cystectomy 49 (37.4)
Ablation 4 (3.1)
others† 2 (1.5)
Bilateral endometrioma (n, %) 68 (51.9)
Bilateral salpingo-oophorectomy 1 (0.8)
USO + unilateral cystectomy 9 (6.9)
Bilateral cystectomy 31 (23.7)
Unilateral cystectomy + ablation 23 (17.6)
Others‡ 4 (3.1)
Douglas’ Pouch
Normal (n, %) 37 (28.2)
Partial obstruction (n, %) 35 (26.7)
Complete resolution of partial obstruction 35 (26.7)
Incomplete resolution of partial obstruction 0 (0.0)
Complete obstruction (n, %) 59 (45.0)
Complete resolution of complete obstruction 50 (38.2)
Incomplete resolution of complete obstruction 9 (6.9)
Other conditions
Adenomyosis (n, %) 12 (9.2)
No resection 7 (5.3)
Resection 5 (3.8)
Myoma (n, %) 40 (30.5)
Resection of small myoma 21 (16.0)
Resection of large/or multiple myomas 7 (5.3)
No resection 12 (9.2)
Other surgeries§ (n, %) 7 (5.3)
Staging at r-ASRM¶
I 2 (1.5)
II 1 (0.8)
III 32 (24.4)
IV 96 (73.3)
†This includes alcohol fixation and aspiration of cystic contents.; ‡This includes bilateral heat ablation, and USO + unilateral heat ablation.;
§This includes salpingoplasty, resection of vaginal septation, bartholinic cystectomy, endometrial polypectomy and resection of vaginal
endometriosis. and ¶revised American Society for Reproductive Medicine.

© 2020 Japan Society of Obstetrics and Gynecology 5

M. Ichikawa et al.

Results

Accuracy

97.7
96.2
80.2
89.3
84.7
83.1
67.7
87.6
81.4
70.5
83.9
(%)
Between June 2012 and July 2018, we enrolled

†Cases with unknown adhesion assessment at the measurement site were excluded. and LR, likelihood ratio; NPV, negative predictive value; PPV, positive predictive value.
155 patients who visited our hospital, were suspected
of having endometriosis, and were scheduled for sur-

LR−

0.67
0.00
0.28
0.07
0.14
0.19
0.64
0.17
0.20
0.43
0.23
gery. However, 24 patients were excluded from this
study because of insufficient data (n = 7), presence of
a tumor of borderline malignancy confirmed by

42.67
26.00
4.01
5.39
4.11
4.53
2.50
8.22
2.96
2.55
5.79
LR+
pathology (n = 1), and the implementation of laparo-
scopic hysterectomy (n = 16). Therefore, a total of

98.4
100.0
94.6
92.2
81.6
83.9
70.0
89.7
67.5
66.7
87.2
NPV
(%)
131 participants were included in this study.
Details of the patient background characteristics as
well as those of the operation are described in Table 1.

PPV

50.0
16.7
44.7
87.5
86.6
82.4
62.5
84.3
87.6
74.6
78.8
(%)
Of the 131 cases analyzed, 63 patients (48.1%) had
received oral treatment for endometriosis and

Specificity (%)
12 (9.2%) had undergone previous surgery for endo-
metriosis. A total of 61 patients (46.6%) had unilateral

99.2
96.2
80.7
82.5
78.4
81.3
80.8
89.7
71.1
73.3
86.1
endometriomas and 68 (51.9%) had bilateral
endometriomas. With respect to the lesions of Doug-
las’ pouch, 37 (28.2%) of the 131 cases were normal,
35 (26.7%) showed partial obstruction, and 59 (45.0%)

Sensitivity

33.3
100.0
77.3
94.6
88.8
84.8
48.1
84.3
85.7
68.1
80.4
showed complete obstruction. Of the 94 cases with

(%)
obstruction of the Douglas’ pouch (complete closure +
partial closure), the obstruction was completely
resolved at the time of surgery in all cases except for
negative
True
nine cases (6.9%). Regarding the severity of endometri-
127
125
88
47
40
52
63
70
27
44
683
osis according to the r-ASRM classification, the num-
ber of patients with disease stages I and II, stage III
and stage IV were 3 (2.3%), 32 (24.4%) and 96 (73.3%),
negative
False

2
0
5
4
9
10
27
8
13
22
100
respectively.
Table 2 shows the adhesion frequency at each of the
10 sites assessed for adhesion mapping and the
positive

corresponding accuracy. Among the 10 measured

False

110
1
5
21
10
11
12
15
8
11
16
points, adhesion was more frequently observed
(70.5%) in Lt O-Ut, followed by Low Post (61.1%) and
Table 2 Accuracy of adhesion mapping (n = 131)

Mid Post (56.5%), respectively. The overall sensitivity,

positive
True

1
1
17
70
71
56
25
43
78
47
409
specificity, PPV, NPV, LR+, LR− and accuracy of the
adhesion mapping were 80.4%, 86.1%, 78.8%, 87.2%,
5.79, 0.23 and 83.9%, respectively. When the diagnostic
Prevalence,

accuracy of adhesions in each site was examined, the

22 (16.8)
74 (56.5)
80 (61.1)
66 (50.8)
52 (40.0)
51 (39.5)
91 (70.5)
69 (53.5)
3 (2.3)
1 (0.8)

diagnostic accuracy of Mid Post, Rt O-Ut and Inter O-

(%)
n

O was considered very high. However, the adhesion

diagnostic accuracy at Rt O-Ut and Lt O-Side, which
are sites away from the uterus, were slightly lower
131
131
131
131
131
130
130
129
129
129
1302

than that of the former.

n†

The average value of the preoperative adhesion

score in the adhesion scoring system was 3.99
Inter O-O
Rt O-Side

Lt O-Side
Low Post

(N = 131). Conversely, the average value of the

Mid Post
Mid Ant

Up Post

Rt O-Ut

Lt O-Ut
Up Ant

adhesion-related score according to the r-ASRM (the

Total
Site

total score minus the implant lesion-related score) was

38.18. The preoperative adhesion score of our adhesion

6 © 2020 Japan Society of Obstetrics and Gynecology

 Adhesion scoring system for endometriosis

Figure 3 Correlation between the adhesion score in the adhesion scoring system and adhesion-related score in the r-
ASRM (N = 131). (a) The adhesion-related score in r-ASRM is (full score of 104 points) obtained by subtracting the score
for the implant lesion (46 points are assigned to this) from the overall score (full score is 150 points), R2 = 0.734. (b) This
figure compares the total score of r-ASRM with the total score of adhesion score + cyst score, R2 = 0.756.

scoring system showed a high correlation (0.734) with Furthermore, we examined whether postoperative
the adhesion-related score of r-ASRM (Fig. 3a). The drug treatment alleviated the state of postoperative
total score of this system (the adhesion score + the cyst adhesions (Fig. 4d,e). The above patients were divided
score) showed a higher correlation with the overall into two groups, those receiving and those not receiv-
r-ASRM score (0.756; Fig. 3b). ing postoperative medication, and the patterns of
To explore the clinical value of our adhesion scoring change in the adhesion score in both groups were com-
system, firstly, we investigated whether or not the pared. The results showed that the pattern of change
adhesion score could track postoperative changes of in the adhesion score of each group was almost identi-
adhesive status. This was conducted on 114 patients cal. However, the baseline preoperative adhesion score
excluding those who had unilateral or bilateral and the adhesion score at 30 months after surgery in
adnexectomy. Changes in the average adhesion score the group that received medications postoperatively
are shown in Figure 4a (solid line), and changes in rela- were significantly higher than those of the group that
tive value based on the preoperative value of the adhe- did not (4.61 vs 3.35; P = 0.01 and 3.75 vs 2.06; P = 0.03
sion score are shown in Figure 4a (thin dotted line). respectively), implying that the medication tended to
According to these results, even when the adhesion be administered postoperatively to patients with more
was completely released during surgery, the adhesion severe endometriotic adhesions (Fig. 4d). Figure 4e
status at 1 month after surgery was almost the same as shows the average values obtained by subtracting the
that before surgery (3.91 [100%] preoperatively, 0.11 preoperative adhesion score from the postoperative
[2.9%] at end of the surgery and 4.05 [104%] 1 month adhesion score in the group that received the drug
postoperatively). However, after that point, the adhe- after surgery and the group that did not. The changes
sion score gradually decreased and was the lowest in the adhesion status of both groups were almost
between 12 and 24 months postoperatively. Neverthe- identical, except for the postoperative adhesion status
less, the effect of surgical adhesiolysis only improved at 1 month after surgery, which showed significantly
the preoperative adhesion status by 30% (Fig. 4a). higher value in the group using the drug (P = 0.01).
Subsequently, we examined the effect of anti- As an additional clinical value of the scoring sys-
adhesive agents during surgery. The postoperative tem, we examined the role of the adhesion score in
adhesion state in 21 cases using the adhesive agents infertility (Table 3). Of the 131 patients, 61 (61.5%)
was almost the same as that of the group without it and were hoping to achieve a pregnancy, but 44 (72.1%)
there was no significant difference in the mean adhe- actually achieved pregnancy. Non-pregnant patients
sion score and mean value obtained by subtracting the were significantly older than pregnant patients (36.7
preoperative adhesion score from postoperative one vs 33.1, P = 0.001) and showed significantly lower
between the two groups at any time (Fig. 4b,c). value of anti-Mullerian hormone (AMH, 1.33 vs 2.88,

© 2020 Japan Society of Obstetrics and Gynecology 7

M. Ichikawa et al.

Figure 4 Changes in adhesion status over time using adhesion scoring system. This study analyzed 114 cases excluding
cases that had adnexectomy at the time of surgery. (a) This figure shows the change in mean adhesion score before sur-
gery and at each specified time point. The solid line shows the average adhesion value for all cases evaluated. The thin
dotted line shows percent change in the relative value of adhesion score. The relative value was calculated as follows:
the average adhesion score in the reachable cases at the time point of evaluation/the average of the preoperative adhe-
sion score × 100 in the same cases. ( ) Total (absolute value); ( ) total (relative value). (b) This shows the change in
the adhesion score before and after surgery in the group (21 cases) using the anti-adhesion agent during surgery and
the group (93 cases) that did not use it. The breakdown of anti-adhesive agents is 16 for INTERCEED Absorbable Adhe-
sion Barrier, 4 for Seprafilm Adhesion Barrier and 1 for AdSpray Adhesion Barrier. ( ) anti-adhesive agent (+); ( )
anti-adhesive agent (−). (c) This shows the average difference when the adhesion score at each post-surgical measure-
ment point was subtracted from the adhesion score before surgery in each case in the groups similar to b. ( ) anti-
adhesive agent (+); ( ) anti-adhesive agent (−). (d) This shows the average of pre- and postoperative adhesion scores
in the group with postoperative drug administration for endometriosis (N = 51) and the group without (N = 63) it. In
this case, drug administration cases are defined as patients who have received drug treatment for ≥3 months within
1 year after surgery. The breakdown of the drugs administered was 25 cases (49%) in the LEP-only group, 14 (27%) in
the Dienogest alone group, 6 (12%) in the LEP and Dienogest group and 6 in the other groups (12%). * and † indicates
the measurement points where significant differences were observed (P = 0.01, P = 0.03). ( ) Medication (+); ( )
Medication (−). (e) This shows the average difference when the adhesion score at each post-surgical measurement point
was subtracted from the adhesion score before surgery in each case in the groups similar to d. ‡ indicates a measure-
ment point where a significant difference was observed (P = 0.01). ( ) Medication (+); ( ) Medication (−). The last
table shows the number of patients at the time of measurement before and after surgery in each group.

8 © 2020 Japan Society of Obstetrics and Gynecology

 Table 3 Role of the adhesion score in infertility
I. Non-pregnancy II. Pregnant P-value
group group (I vs II)
n (61) 17 (27.9%) 44 (72.1%) —
Age (years, mean) 36.7 33.1 0.001
Body mass index (kg/m2, mean) 21.2 20.7 0.86
Anti-Mullerian hormone (AMH) score at 1 month 1.33 2.88 0.01
after surgery (n = 13, 36 for each group)
Mean r-ASRM score 74.2 64.5 0.29
Mean ovary score in r-ASRM 28.6 25.6 0.27
Mean Culdesac score in r-ASRM 21.5 16.8 0.40
Mean adhesion score (ovary + tube) in r-ASRM 17.9 16.7 0.79
Mean adhesion score (Culdesac + ovary + 40.5 33.5 0.39
tube) in r-ASRM
Mean adhesion score in the system
Before surgery 3.53 3.77 0.83
1 month after surgery 4.65 4.41 0.74
Mean observation period (months) 47.8 42.0 0.17
Mode of conception III. IV. P-value V. Non-IVF VI. IVF P-value P-value

© 2020 Japan Society of Obstetrics and Gynecology

Non-pregnancy Non-pregnancy (III vs IV) pregnant pregnant (V vs VI) (I vs V)
group group with IVF group group
without IVF
n 8 (47.1%) 9 (52.9%) — 20 (45.5%) 24 (54.5%) — —
Age (years, mean) 37.8 37.1 0.78 33.3 32.9 0.74 0.008
Body mass index (kg/m2, mean) 21.1 212 0.95 21.0 20.4 0.38 0.89
Passability of fallopian tubes
Both + 6 (75%) 3 (33.3%) — 15 (75%) 18 (75.0%) — —
Uni. + 2 (25%) 5 (55.6%) — 4 (20%) 6 (25.0%) — —
No passage 0 0 — 0 0 — —
Not evaluated 0 1 (11.1%) — 1 (5%) 0 — —
AMH score at 1 month 1.59 (n = 6) 1.11 (n = 7) 0.54 2.96 (n = 17) 2.81 (n = 19) 0.87 0.06
Mean r-ASRM score 63.3 83.9 0.14 50.5 76.3 0.01 0.004
Mean ovary score in r-ASRM 30.0 27.4 0.62 25.9 25.3 0.86 0.38
Mean Culdesac score in r-ASRM 17.0 27.6 0.27 8.0 24.2 0.003 0.01
Mean adhesion score (ovary + 11.3 23.8 0.03 11.5 21.1 0.04 0.06
tube) in r-ASRM
Mean adhesion score (Culdesac 28.3 51.3 0.06 19.45 45.3 0.002 0.01
+ ovary + tube) in r-ASRM
Mean adhesion score in the system
Before surgery 2.75 4.22 0.21 3.35 4.13 0.26 0.80
1month after surgery 4.38 4.89 0.67 3.45 5.21 0.02 0.03
Mean observation period (months) 51 44 0.31 46 40 0.17 0.60
Time to the first pregnancy (months) NA NA — 13.3 17.5 0.27 —
Time to the first pregnancy except NA NA — 6.2 16.8 2.4E−05 —
for the contraception period
(months)
Adhesion scoring system for endometriosis

9
M. Ichikawa et al.

Figure 5 The difference in time of achieving pregnancy between the non-IVF pregnancy group and IVF pregnancy group.
(a) Distribution of the time required to achieve the first pregnancy after surgery in the non-IVF pregnancy group ( )
and in the IVF pregnancy group ( ). The period of contraception was excluded in both groups. (b) Cumulative preg-
nancy rates of the non-IVF pregnancy groups ( ) and IVF pregnancy groups ( ).

P = 0.01). However, no significant difference was Discussion

found between the two groups regarding the adhe-
sion score. Subsequently, pregnancy groups were The present study results show that our adhesion
divided into non-in vitro fertilization (IVF) pregnancy scoring system can easily and noninvasively predict
groups and IVF pregnancy groups for comparisons. the extent and severity of endometriotic adhesions.
In the non-IVF pregnancy group, the adhesion score Thus, we can evaluate the actual status of endo-
at 1 month postoperatively was significantly lower metriotic adhesions with this method not only preop-
than that in the IVF group (3.45 vs 5.21; P = 0.02), eratively, but postoperatively as well. Based on the
although other factors such as age and AMH did not clinical application, our adhesion scoring system
change (Table 3). The r-ASRM score and its subclass could have great potential.
scores (excluding the ovary score) also showed the Regarding the issues of this system, we should first
same trend as the adhesion score in our system consider the possible measurement error between the
(Table 3). Especially, the scores that included scoring examiners. A previous study showed that the intra-
for the Culdesac score such as Mean Culdesac score class correlation coefficient for adhesion scores among
or adhesion score in r-ASRM showed higher signifi- three examiners was 0.80732; thus, the test is sufficiently
cance (P = 0.003 and P = 0.002, respectively; Table 3). reproducible. Further, as this system and the sliding
Additionally, the time to first pregnancy (except for sign technique are easy to apply, any examiner who is
the contraception period) was significantly shorter familiar with transvaginal ultrasonography should be
in the non-IVF group compared with 6.2 and able to produce similar results. Another issue is that the
16.8 months in the IVF group (P = 2.4E−05). adhesion scoring system alone might not be sufficient
Figure 5a,b shows the relationship between the time to comprehensively evaluate other endometriosis pre-
to pregnancy and the number of pregnancies in both sentations, such as endometriomas or DIE. The ideal
groups and the cumulative pregnancy rate. In the diagnostic method should allow for the diagnosis of all
non-IVF pregnancy group, 94% (19/20) of all preg- the endometriosis variants. In fact, our adhesion scoring
nancies were established within 1 year postopera- system is part of a new diagnostic method called
tively. In contrast, it was only 33.3% (8/24) in the IVF numerical multi-scoring system for endometriosis
pregnancy group. (NMS-E).27 The NMS-E is aimed at the comprehensive
When comparing non-IVF pregnant group and diagnosis of endometriosis to show various presenta-
non-pregnancy group, the age, adhesion-related tions. Thus, at this time, we focused only on developing
scores in r-ASRM, and the adhesion score at 1 month a method to assess endometriotic adhesions.
after surgery were significantly lower in the former From here on, we discuss the clinical application of
group (Table 3). our adhesion scoring system. The first application is to

10 © 2020 Japan Society of Obstetrics and Gynecology

 Adhesion scoring system for endometriosis

track the effect of surgical adhesiolysis. It was disap- Regarding the second application of our scoring sys-
pointing that surgical adhesiolysis was less effective tem, we discuss the role of the adhesion score in infertil-
than we had expected; however, the fact that this sys- ity. The average adhesion score in the non-IVF
tem made it possible to noninvasively track postopera- pregnancy group was significantly lower than that in
tive changes of adhesive status is very important. the IVF pregnancy group 1 month after surgery
Conventionally, additional surgical intervention is (Table 3). A possible explanation for this finding is that
required to determine the presence of postoperative adhesions in the abdominal cavity somehow prevented
adhesions.33,34 However, by using this system, postop- natural pregnancy, which was detected by the adhesion
erative adhesion evaluation would become available score. The average adhesion score 1 month after sur-
without the need for additional surgical information. gery in the IVF pregnancy group (5.21) was very high,
We investigated how the use of anti-adhesion mate- meaning that the peripheral space around the ovary is
rials during surgery and drugs for endometriosis after almost surrounded by adhesions, considering that
surgery affects the postoperative adhesion status. The adhesion frequency on the anterior part of the uterus is
results were not effective in both. However, one inter- very low. This situation would, of course, adversely
esting point is that the adhesion score in the first month affect mechanisms, such as ovulation and subsequent
of the group with postoperative drugs for endometri- capture of the egg, by the fallopian tube. Furthermore,
osis was significantly lower than the group without it is reasonable to think that the adhesion score cap-
them (at this point, postoperative medication had not tured this failure. If so, adhesion scores could be an
been started; Fig. 4e). This may be because the preoper- indicator to evaluate one of the causes of infertility.
ative adhesion score of the group with the postopera- What is more, this system does not require surgical
tive drug was originally high, and there were few new findings, which is a huge advantage compared with
adhesions induced by the surgical operation. Another other diagnostic methods such as the EFI methods. If
reason is that the proportion of patients who took med- this score is improved to predict spontaneous preg-
ication preoperatively was higher in the group with the nancy, additional scores should be added to this if a
postoperative drug than in those without it (60.8% vs complete closure of Douglas’s pouch is suspected. This
39.8%), that is, preoperative drug administration may is because the result of the Culdesac score in r-ASRM
improve postoperative adhesion. However, to ensure shows that the open state of Douglas’s pouch greatly
these results, further studies including RCT are neces- affects the establishment of natural pregnancy (Table 3).
sary in the future. Adding +3 to this adhesion score of the cases with
There are some concerns regarding the interpretation suspected complete obstruction of Douglas’s pouch
of the results in this postoperative adhesion study. (adhesion positive at both Mid Post and Low Post)
First, the change in the adhesion score over time might improved the significance to P = 0.0002, 1 month after
be caused by an inconsistent number of subjects tested. surgery in non-IVF pregnancy group in comparison
However, Figure 4a shows the relative values obtained with the IVF pregnancy group. Also, it should be noted
by dividing the postoperative average adhesion score that this score is more powerful in estimating the likeli-
by the average adhesion score preoperatively among hood of natural pregnancy in the absence of
the same patients at each time point. Therefore, the endometriomas (Table 3). This is because the adhesion
suggested trend of this graph would not be largely score 1 month after surgery was effective in predicting
wrong. Another issue is the different conditions that natural pregnancy but not before surgery. In the future,
adhesion mapping measured, such as the presence of this test may be useful for patients other than endome-
endometriomas preoperatively or in the absence of triosis by adjusting the measurement conditions.
them postoperatively, among others. In principle, if the This study has several limitations. First, there was
ovaries are normal in size and position, the adhesion no significant difference in the adhesion score between
evaluation at the area between them should be nega- the non-pregnant and the pregnant groups. The main
tive. In other words, the adhesion score may relatively reason could be that the average age in the non-
decrease postoperatively after the operation in the pregnant group was significantly higher than that in
absence of ovarian cysts. However, the above possibil- the pregnant group (36.7 vs 33.1; P = 0.001). Infertility
ity could be low because of the fact that the adhesion involves various factors. Adhesions and age are one of
score 1 month after surgery, which was checked with- the main causes. Therefore, to examine the effective-
out endometriomas, had risen rather than that before ness of the adhesion score between the non-pregnant
surgery (104%). group and the pregnant group, basic conditions such

© 2020 Japan Society of Obstetrics and Gynecology 11

M. Ichikawa et al.

as age should be matched. Why did the postoperative 7. al-Badawi IA, Fluker MR, Bebbington MW. Diagnostic laparos-
adhesion score (5.21) in the IVF group at 1 month post- copy in infertile women with normal hysterosalpingograms.
J Reprod Med 1999; 44: 953–957.
operatively increase compared with that before the sur-
8. Japan Society of Obstetrics and Gynecology. The general rules
gery (4.13)? It is possible that the adhesion status after for clinical management of endometriosis 2010; pp. 38–52.
surgery might worsen compared with that preopera- 9. Ferrero S, Anserini P, Abbamonte LH, Ragni N, Camerini G,
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which lead to the higher adhesion score. Therefore, it
Ballester M. Fertility after colorectal resection for endometri-
is extremely important to take measures to prevent the osis: Results of a prospective study comparing laparoscopy
formation of postoperative adhesions at the time of with open surgery. Fertil Steril 2011; 95: 1903–1908.
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Our adhesion scoring system allowed the accurate Society classification of endometriosis: 1985. Fertil Steril
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prediction of the pelvic adhesion status and may
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Oppelt P. Efficacy of the revised Enzian classification: A ret-
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The authors are grateful for the assistance of the staff
solve the problem of duplicate classification in rASRM and
and residents of the Department of Obstetrics and Enzian? Arch Gynecol Obstet 2013; 287: 941–945.
Gynecology, Nippon Medical School Hospital. The 15. Haas D, Oppelt P, Shebl O, Shamiyeh A, Schimetta W,
authors would also like to thank Enago (www.enago. Mayer R. Enzian classification: Does it correlate with clinical
jp) for the language review. symptoms and the rASRM score? Acta Obstet Gynecol Scand
2013; 92: 562–566.
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Pozzi Mucelli R. Detection and localization of deep endome-
triosis by means of MRI and correlation with the ENZIAN
Disclosure score. Eur J Radiol 2015; 84: 568–574.
17. Exacoustos C, Malzoni M, Di Giovanni A et al. Ultrasound
The authors have no potential conflicts of interest to mapping system for the surgical management of deep infil-
declare. trating endometriosis. Fertil Steril 2014; 102: 143–150.e2.
18. Holland TK, Cutner A, Saridogan E, Mavrelos D,
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