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Ultrasound Obstet Gynecol 2010; 36: 241 –248
Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.7689
Value of transvaginal ultrasound in assessing severity
of pelvic endometriosis
T. K. HOLLAND*, J. YAZBEK*, A. CUTNER†, E. SARIDOGAN†, W. L. HOO† and D. JURKOVIC†
*Early Pregnancy and Gynaecology Assessment Unit, King’s College Hospital and †Department of Obstetrics and Gynaecology, University
College Hospital, London, UK
KEYWORDS: diagnosis; endometriosis; laparoscopy; severity; transvaginal ultrasound
ABSTRACT
Objective The objective of this study was to examine
the ability of preoperative transvaginal ultrasound (TVS)
scanning to assess the severity of pelvic endometriosis.
Methods Consecutive women with clinically suspected
or proven pelvic endometriosis, who were booked for
laparoscopy, were invited to join the study. The severity of
endometriosis was assessed preoperatively using TVS and
the findings were compared with the results obtained by
laparoscopy using the American Society for Reproductive
Medicine (ASRM) classification.
Results In total, 201 women had preoperative TVS and
laparoscopies. Of these, no endometriosis was found at
laparoscopy for 62/201 (30.8%; 95% CI, 24.8–37.5),
whereas 33/201 (16.4%; 95% CI, 11.9–22.2) had mini-
mal endometriosis, 31/201 (15.4%; 95% CI, 11.1–21.1)
had mild endometriosis, 27/201 (13.4%; 95% CI,
9.4–18.8) had moderate endometriosis and 48/201
(23.9%; 95% CI, 18.5–30.2) had severe endometrio-
sis. The sensitivity and specificity of the TVS diag-
nosis of severe pelvic endometriosis were 0.85 (95%
CI, 0.716–0.934) and 0.98 (95% CI, 0.939– 0.994),
respectively, and the positive and negative likeli-
hood ratios were 43.5 (95% CI, 14.1–134) and
0.15 (95% CI, 0.075–0.295), respectively. Overall,
there was a good level of agreement between ultra-
sound and laparoscopy in identifying absent, minimal,
mild, moderate and severe disease (quadratic weighted
kappa =0.786). The mean ASRM score difference
between TVS and laparoscopy in assessing severity
of endometriosis was −2.398 (95% CI, −4.685 to
−0.1112) and the limits of agreement were −34.62
(95% CI, −38.54 to −30.709) to 29.83 (95% CI,
25.91–33.74).
Conclusions TVS is a good test for assessing the severity
of pelvic endometriosis. TVS is particularly accurate
in detecting severe disease, which could facilitate more
effective triaging of women for appropriate surgical care.
Copyright 2010 ISUOG. Published by John Wiley &
Sons, Ltd.
INTRODUCTION
Endometriosis is a common gynecological condition,
defined as the presence of endometrial-like tissue outside
the uterus, which impairs quality of life1. In more severe
cases it forms cysts in the ovaries and deeply infiltrates
pelvic organs.
The revised American Society for Reproductive
Medicine (ASRM) classification is the most widely
accepted staging system for endometriosis; however,
there is no consensus regarding the definition of severe
endometriosis.
In the last few decades, a non-invasive preoperative
diagnosis of endometriosis has been made possible by
advances in imaging methods such as ultrasound and
magnetic resonance imaging (MRI)2,3. The value of
ultrasound for the diagnosis of ovarian endometriomas
has been established4. Rectal endoscopic sonography
(RES), transrectal sonography (TRS) and transvaginal
ultrasound (TVS) have all been shown to be useful in
the diagnosis of non-ovarian features of endometriosis,
such as intestinal, bladder and uterosacral ligament
involvement5–7. A recent study showed the high degree
of accuracy of good-quality TVS when combined with
a bimanual examination for the diagnosis of deep pelvic
endometriosis8. In addition, three other studies showed
that TVS is comparable with, and may be superior to,
MRI3,9,10.
Correspondence to: Mr D. Jurkovic, Department of Obstetrics and Gynaecology, University College Hospital, 235 Euston Road, London
NW1 2BU, UK (e-mail: davor.jurkovic@uclh.nhs.uk)
Accepted: 20 April 2010
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. O R IG INAL PA P E R
242 Holland et al.
The success of surgery for pelvic endometriosis is highly
dependent on the expertise and training of the operating
surgeon11,12.Inanattempttooptimizethetreatmentof
women suffering from severe endometriosis, tertiary refer-
ral endometriosis centers have been established11.These
centers provide comprehensive care for endometriosis
patients, including high-quality surgical care. The capac-
ity of tertiary centers, however, is limited and the critical
issue in routine clinical practice is the ability to assess the
severity of endometriosis in order to facilitate the triaging
of women for treatment.
The aim of the present study was to establish whether
preoperative ultrasound examination is an accurate
method for diagnosing severe pelvic endometriosis.
METHODS
This was a prospective, observational, multicenter
study, which was conducted at King’s College Hospital
and at University College Hospital in London. These
are major teaching hospitals and the latter includes
a specialist tertiary endometriosis center. Consecutive
women with clinically suspected or proven pelvic
endometriosis were invited to join the study. The
inclusion criteria were: premenopausal women with a
clinical suspicion of endometriosis awaiting diagnostic
laparoscopy; women diagnosed with pelvic endometriosis
at diagnostic laparoscopy awaiting operative treatment;
age ≥16 years; and the ability to provide informed
consent. Exclusion criteria were: women who could not
undergo a TVS scan; and women who became pregnant
whilst awaiting surgery.
The study was approved by the local ethics committee,
and an information leaflet was given to all eligible women
before assessment. Informed consent was obtained from
all patients who agreed to take part in the study.
Procedures
All women were assessed by the attending clinicians
who obtained a detailed medical history, which was
recorded on a dedicated clinical database (ViewPoint; GE
Healthcare, Fairfield, CT, USA). Women were specifically
asked about symptoms associated with endometriosis
such as dysmenorrhea, chronic pelvic pain, dyspareunia,
subfertility, dyschezia and cyclic rectal bleeding.
TVS examination was performed by four ultrasound
operators who were all gynecologists with a high
level of expertise in gynecological ultrasonography. The
ultrasound operators were blinded to any previous
surgical findings. All patients were operated on by four
different laparoscopic surgeons with a high level of
expertise in laparoscopic surgery. When moderate, severe
or deeply invasive endometriosis (DIE) was present, a
complete surgical exploration of the pelvis was performed,
involving dissection of the pouch of Douglas when
obliterated and resection of any DIE, especially of the
bowel or the rectovaginal septum (RVS), in order not to
miss any disease. The operating surgeons were blinded to
the detailed TVS findings.
TVS assessment of pelvic endometriosis
All women were examined in the dorsal lithotomy position
using a high-resolution TVS probe. The examinations
were performed in a standardized and systematic way.
First of all, the uterus was assessed in the transverse and
sagittal planes. Then, the ovaries were found and their
size was measured in three orthogonal planes.
Ovarian cysts were diagnosed as endometriomas when
they appeared as well-circumscribed thick-walled cysts
that contained homogeneous low-level internal echoes
(‘ground glass’)13. Measurements were recorded from the
inside of the cyst wall in three orthogonal planes. The
average of the three diameters (D1+D2+D3)/3 was used
for scoring. The adnexa were also systematically examined
for the presence of tubal dilatation. When tubal dilatation
was present, a score of 16 was given, in accordance with
the ASRM system.
Ovarian mobility was assessed by a combination of
gentle pressure with the vaginal probe and abdominal
pressure with the examiner’s free hand, as in a bimanual
examination. The ovary was deemed to be completely
free when it could be seen sliding across the surrounding
structures without any resistance. Minimal adhesions
(classified in the ASRM classification as <1
/
3enclosure
with dense adhesions) were considered to be present
when some of the surrounding structures could not be
separated from the ovary with gentle pressure but the
ovary could be mobilized from the majority (>2
/
3)ofthe
surrounding structures. Moderate adhesions (classified
in the ASRM classification as 1
/
3to 2
/
3enclosure with
dense adhesions) were thought to be present when the
ovarian mobility was reduced as a result of adhesions
with the surrounding structures but the structures on 2
/
3
to 1
/
3of the surface of the ovary slid across it with the
application of gentle pressure. Fixed ovaries (assessed in
the ASRM classification as >2
/
3enclosure with dense
adhesions) could not be mobilized at all with gentle
pressure or separated from the surrounding structures.
If the tubes were dilated, the mobility of the dilated tubes
was documented in a similar manner. Normal Fallopian
tubes are difficult to identify in the absence of background
fluid in the pelvis and therefore it was not possible to
score non-dilated tubes for adhesions. Filmy adhesions
were scored separately from dense adhesions of the tubes
andovariesintheASRMsystem.Itisdifficulttoseefilmy
adhesions on TVS unless there is fluid entrapped within
the adhesions, giving rise to the ‘flapping sail sign’, or
unless the mobility of the affected organs is reduced, and
therefore these features were not scored separately at TVS
examination.
Next, the presence of adhesions in the pouch of Douglas
was assessed. The uterus was gently mobilized by a
combination of pressure on the cervix with the ultrasound
probe alternating with pressure on the fundus from the
examiner’s free hand on the abdominal wall. The aim was
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 36: 241–248.
Assessment of pelvic endometriosis using TVS 243
to watch the interface of the posterior uterine serosa and
the bowel behind to ensure that the two structures were
sliding easily across one another. If these two surfaces
were completely free of one another, this was assessed as
no adhesions present. Complete obliteration was assessed
as the absence of any sliding between the serosa on the
posterior surface of the cervix or uterus and the bowel
behind. Partial obliteration of the pouch of Douglas was
present if there were some adhesions between the bowel
and the uterus, but some free sliding was seen. Partial
obliteration was also present when adnexal structures
were firmly adherent to the posterior aspect of the uterus
but the bowel appeared to be free.
Endometriotic nodules or DIE were typically visualized
as stellate hypoechoic or isoechogenic solid masses with
irregular outer margins14,15, which were tender on palpa-
tion and fixed to the surrounding pelvic structures. They
were usually located in the uterosacral ligaments, adnexa,
rectovaginal septum and urinary bladder. Endometriotic
nodules located in the wall of the rectosigmoid colon tend
to appear as hypoechoic thickenings of bowel muscularis
propria, which sometimes protrude into the lumen of the
bowel16. The presence and largest diameter of any deep
lesions were documented.
The above features were documented and scored using
the ASRM classification17. The score was used to grade
the disease as absent (0), minimal (1–5), mild (6– 15),
moderate (16–40) or severe (>40). DIE is given a
maximum score of six on the ASRM classification and
therefore we recorded the presence of these lesions
separately. All findings were recorded on a database
file using a Microsoft Excel for Windows spreadsheet
to facilitate data entry and retrieval. The severity of
endometriosis, as assessed by TVS, was compared with
laparoscopic findings using the same ASRM classification.
Statistical analysis
As no previous studies have been conducted to assess the
accuracy of ultrasound scanning, carried out by experts,
to determine the severity of endometriosis, there are
no figures on which to base a power calculation. In
clinical practice it would be ideal to identify all cases
of endometriosis. Our hypothesis was that it would be
clinically acceptable if TVS had a sensitivity of 90% in
identifying severe pelvic endometriosis. This study was
designed to have 90% power to detect a 10% difference
between the sensitivity of diagnostic laparoscopy and TVS
in detecting severe pelvic endometriosis with a two-sided
alpha of 0.05. The study needed a minimum of 190
patients, but we recruited 211 patients to allow for loss
of power as a result of cancellations or pregnancy.
All statistical analyses were carried out using MED-
CALC version 9.2.0.2 (Medcalc Software, Mariakerke,
Belgium). The diagnostic accuracy of the tests was
assessed using sensitivity, specificity, positive likelihood
ratio (LR+) and negative likelihood ratio (LR−) measure-
ments. Correlation was calculated using the coefficient
of correlation r. In order to determine any systematic
bias between the two diagnostic methods and to assess
the relationship between any differences and the magni-
tude of the scores, the differences in score were plotted
against the mean of the two scores on a scatter diagram.
Systematic bias between the two observers was deter-
mined by calculating the 95% CI of the mean (mean ±
1.96 SD), as described by Bland and Altman18,19.Over-
all levels of agreement were calculated using Cohen’s
quadratic weighted kappa coefficient. Kappa values of
0.81–1.0 indicated very good agreement, kappa values
of 0.61–0.80 indicated good agreement, kappa values of
0.41–0.60 indicated moderate agreement, kappa values
of 0.21–0.40 indicated fair agreement and kappa values
of <0.20 indicated poor agreement20.
RESULTS
In the 30-month period from July 2006 to December 2008
we recruited 211 women into this study. Ten women were
excluded from the final analysis: five became pregnant
whilst awaiting surgery, one cancelled her operation, one
laparoscopy was unsuccessful and three women were lost
to follow-up.
In total, 201 women were included in the final analysis.
The mean age was 34.9 (95% CI, 33.98–35.86; SD,
6.79) (range, 19– 51) years. The presenting symptoms
were: dysmenorrhea (142/201, 70.6%), chronic pelvic
pain (104/201, 51.7%), dyspareunia (78/201, 38.8%),
infertility (38/201, 18.9%), dyschezia (7/201, 3.5%) and
cyclic rectal bleeding (2/201, 1%) women. A single
presenting symptom was present in 72 (35.6%) women,
two presenting symptoms in 78 (38.8%) women and three
or more symptoms in 51 (25.4%) women.
The ultrasound examinations were performed by
four examiners: Examiner A performed 104 (51.7%),
Examiner B performed 68 (33.8%), Examiner C
performed 18 (9%) and Examiner D performed 11 (5.5%)
examinations. All patients were operated on by one of
four laparoscopic surgeons: Surgeon A operated on 70
(34.8%), Surgeon B operated on 52 (25.9%), Surgeon C
operated on 45 (22.3%) and Surgeon D operated on 34
(16.9%) women. The mean interval between TVS and
surgery was 37.5 (95% CI, 34.3–40.8; SD, 23.2) (range,
0–87) days.
Table 1 shows the findings of ultrasound examination
compared with laparoscopy. There was a good overall
level of agreement between ultrasound examination
and laparoscopy in identifying absent, minimal, mild,
moderate and severe disease (quadratic weighted kappa =
0.786, standard error (Kw=0) =0.068, standard error
(Kw#0) =0.033).
The sensitivity, specificity, LR+and LR−of TVS in
diagnosing pelvic endometriosis are shown in Table 2.
Table 3 shows the accuracy of Examiners A and B
for detecting severe pelvic endometriosis. There was
no significant difference found in overall accuracy
between these two examiners when the area under
the receiver–operating characteristics (ROC) curve was
compared. The numbers of women examined by
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 36: 241–248.
244 Holland et al.
Table 1 Comparison of ultrasound and laparoscopic assessment of severity of pelvic endometriosis using the American Society for
Reproductive Medicine classification
Laparoscopy
Ultrasound Absent Minimal Mild Moderate Severe Total
Absent 59 29 27 3 2 120 (59.7)
Minimal 0 1 0 0 0 1 (0.5)
Mild 1 1 4 2 1 9 (4.5)
Moderate 2 1 0 20 4 27 (13.4)
Severe 0 1 0 2 41 44 (21.9)
Total (%) 62 (30.8) 33 (16.4) 31 (15.4) 27 (13.4) 48 (23.9) 201 (100)
Data are expressed as nor as n(%).
Table 2 Accuracy of ultrasound in diagnosing different stages of pelvic endometriosis using laparoscopy as the gold standard
Sensitivity
(n(%, 95% CI))
Specificity
(n(%, 95% CI))
LR+
(95% CI)
LR−
(95% CI)
Absent vs. present 78/139 (56.1, 47.8– 64.1) 59/62 (95.2, 86.7– 98.3) 11.60 (3.81 –35.32) 0.461 (0.379– 0.561)
Absent to mild vs. moderate to severe 67/75 (89.3, 80.3– 94.5) 122/126 (96.8, 92.1–98.8) 28.14 (10.69– 74.0) 0.11 (0.057 –0.212)
Absent to moderate vs. severe 41/48 (85.4, 72.8– 92.8) 150/153 (98.0, 94.4 –99.3) 43.5 (14.12–134.39) 0.149 (0.075 – 0.295)
LR+, positive likelihood ratio; LR−, negative likelihood ratio.
Table 3 Comparison of performance of Examiners A and B at
diagnosing severe pelvic endometriosis using ultrasound, with
laparoscopy as the gold standard
Examiner A Examiner B
Sensitivity (%) 81.8 (47.7– 96.8) 93.3 (78.7– 98.2)
Specificity (%) 98.9 (93.3 –99.9) 97.4 (86.5–99.5)
LR+76.1 (10.6– 545) 33.4 (4.82–231)
LR−0.184 (0.0524– 0.644) 0.099 (0.0339–0.292)
PPV (%) 89.8 96.6
NPV (%) 97.8 94.9
Accuracy (AUC)*0.904 0.938
Data shown in parenthesis are 95% CI. *Comparison of area under
receiver– operating characteristics curves (AUC), P=0.627.LR+,
positive likelihood ratio; LR−, negative likelihood ratio; NPV,
negative predictive value; PPV, positive predictive value.
Examiners C and D were not sufficient to make individual
comparisons of accuracy meaningful and therefore the
results of these examiners are not presented in Table 3.
The 17 cases of mild disease where DIE was present
included the uterosacral ligaments in 12 (70.6%; 95%
CI, 46.8–86.7), pelvic side wall in four (23.5%; 95%
CI, 9.6–47.3), uterovesical fold/bladder in two (11.8%,
95% CI, 3.3–34.3), pararectal space in one (5.9%;
95% CI, 1.1–27.0), rectovaginal septum in one (5.9%;
95% CI, 1.1–27.0) and rectum in one (5.9%; 95% CI,
1.1–27.0). Thirteen (76.5%; 95% CI, 52.7–90.4) cases
had one site of DIE and the other four (23.5%; 95%
CI, 9.6–47.3) had two sites. Only one case, involving
the bladder, was correctly diagnosed as having DIE on
TVS. Table 4 shows the prevalence of DIE, and TVS
sensitivity for DIE, in relation to severity as classified by
the ASRM classification. It also shows that DIE becomes
more prevalent with increasing severity of disease, and
the sensitivity of TVS at diagnosing DIE increases with
severity of endometriosis.
Table 5 shows the sensitivity, specificity, LR+and
LR−, and areas under the ROC curves, for the diagnosis
of: DIE involving the bladder and uterovesical fold; DIE
of the rectovaginal septum and bowel; and complete
obliteration of the pouch of Douglas. Histological
confirmation of endometriosis was not possible in all cases
because the study design did not state that histology was
necessary. However, where available, the histology results
are shown in Table 6. Table 7 shows the distribution of
the individual features of endometriosis according to the
overall stage of disease.
Figure 1 demonstrates correlation of ultrasound and
laparoscopic assessment of the severity of pelvic
endometriosis as classified by ASRM. The intermethod
correlation coefficient was 0.867 (95% CI, 0.829– 0.898).
The mean difference between TVS and laparoscopy in
assessing severity of endometriosis was −2.398 (95% CI,
−4.685 to −0.1112) and the limits of agreement were
−34.62 (95% CI, −38.54 to −30.709) to 29.83 (95% CI,
25.91–33.74). The difference is normally distributed as
95% of the values lie within 1.96 SD of the mean. Visual
inspection of the scatterplot revealed that the magnitude
of the difference did not change with increasing severity
of endometriosis (Figure 2).
There were seven false-negative cases for severe
endometriosis: two were diagnosed as no endometriosis,
one as mild disease and four as moderate disease. The
two cases of severe endometriosis that were classified as
not having endometriosis both had the pouch of Douglas
correctly classified as partially or completely obliterated
by adhesions but the endometriotic nodules were not seen
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 36: 241–248.
Assessment of pelvic endometriosis using TVS 245
Table 4 Prevalence of deeply invasive endometriosis (DIE) and transvaginal ultrasound sensitivity for detection of DIE, in relation to severity
classified using the American Society for Reproductive Medicine (ASRM) classification
Severity as classified by the ASRM score at laparoscopy
Absent Minimal Mild Moderate Severe
Total cases 62 33 31 27 48
DIE prevalence 0 (0, 0– 5.8) 0 (0, 0 –10.4) 17 (54.8, 35.2– 67.5) 17 (63.0, 44.2– 78.5) 37 (77.1, 63.5 –86.7)
Sensitivity NA NA 1/17 (5.9, 1.1 –27.0) 6/17 (35.3, 17.3–58.7) 18/37 (48.7, 33.5–64.1)
Data are given as nor n(%, 95% CI). NA, not applicable.
0 20 40 60 80 100 120 140
140
120
100
80
60
40
20
0
Laparoscopy score
TVS score
Figure 1 Scatterplot of transvaginal ultrasound (TVS) and
laparoscopic findings in individual women with and without
evidence of pelvic endometriosis. Severity of the disease was
determined using the American Society for Reproductive Medicine
(ASRM) classification. Sample size, n=201; correlation coefficient
r=0.8677; 95% CI for r=0.8289–0.8982;P<0.0001.
0 50 100 150
100
80
60
40
20
0
−20
−40
−60
−80
−100
Average of TVS score and laparoscopy score
TVS score – laparoscopy score
Mean
−2.4
−1.96 SD
−34.6
+1.96 SD
29.8
Figure 2 Scatterplot of the difference in American Society for
Reproductive Medicine (ASRM) score of severity of endometriosis
between transvaginal ultrasound (TVS) and laparoscopy vs. mean
score.
and there were no ovarian endometriomas present. These
cases were correctly classified as having severe adhesions
but not as a consequence of endometriosis. The one
case of severe disease that was classified as having mild
endometriosis had a rectovaginal septum nodule with an
obliterated pouch of Douglas which was not seen on TVS.
Of the four cases of severe disease that were diagnosed
as moderate disease, three had the pouch of Douglas
incorrectly classified as partially obliterated when it was
completely obliterated and the other case had ovaries that
were fixed when they were classified as mobile. Three
cases were false positive for severe endometriosis: one
had minimal disease and the other two had moderate
disease. The minimal case had the pouch of Douglas
misclassified as obliterated. One of the moderate cases
had smaller ovarian endometriomas at laparoscopy than
on TVS and the other had a unilateral endometrioma on
laparoscopy when there were bilateral cysts on TVS. There
were 29 cases of minimal disease and 27 cases of mild
disease which were falsely diagnosed on TVS as having
no disease. The majority of these cases had superficial
peritoneal disease only.
DISCUSSION
Our study confirms that TVS is an accurate diagnostic
method for the assessment of women with suspected
pelvic endometriosis. There was a high level of agreement
between TVS and laparoscopy in assessing the severity
of disease. The accuracy of TVS in diagnosing cases
of moderate and severe pelvic endometriosis was 94%.
However, the sensitivity of diagnosis in minimal and mild
pelvic endometriosis was relatively low, probably because
of the small size of lesions in these cases. The false-negative
results in cases of moderate or severe disease occurred as
a result of difficulty in identifying DIE and in classifying
pouch of Douglas obliteration, a limitation also noted
by Bazot21. He also reported a high specificity, but a
low sensitivity, of diagnosing DIE involving the RVS10.
The findings were similar in our study, confirming the
difficulty in identifying these lesions.
Some authors have advocated transrectal scans in
order to improve the ultrasound diagnosis of DIE. This
technique was particularly helpful for the diagnosis of
uterosacral and intestinal endometriosis6,7,22,23. How-
ever, Bazot et al.5achieved better diagnosis of uterosacral
and rectosigmoid endometriosis using TVS compared with
the transrectal approach. They also showed that TVS is
very accurate in the diagnosis of intestinal and bladder
endometriosis, but less so in detecting uterosacral, vagi-
nal and rectovaginal septum involvement21. Our results
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 36: 241–248.
246 Holland et al.
Table 5 Diagnostic accuracy of transvaginal ultrasound (TVS) in the assessment of features of severe endometriosis not clearly scored using the American Society for Reproductive Medicine
classification
Feature
Sensitivity
(n(%, 95% CI))
Specificity
(n(%, 95% CI))
LR+
(95% CI)
LR−
(95% CI)
AUC (95% CI)
with P
DIE of bladder or uterovesical fold 5/9 (55.56, 21.4– 86.0) 192/192 (100, 98.1–100) N/A 0.44 (0.214 – 0.923) 0.778 (0.714–0.833) (P=0.0027)
DIE of rectovaginal septum or rectum/sigmoid 14/31 (45.16, 27.3–64.0) 170/170 (100, 97.8–100) N/A 0.55 (0.398–0.755) 0.726 (0.659–0.786) (P=0.0001)
Obliterated pouch of Douglas 18/25 (72.00, 50.6 –87.9) 171/176 (97.16, 93.4 –99.0) 25.06 (10.32–62.2) 0.29 (0.154 –0.541) 0.846 (0.788–0.893) (P=0.0001)
Any of these features 23/38 (60.53, 43.4– 75.9) 156/163 (95.71, 91.3– 98.2) 14.09 (6.53– 30.41) 0.412 (0.278–0.612) 0.781 (0.718–0.836) (P=0.0001)
AUC, area under the receiver–operating characteristics curve; DIE, deeply invasive endometriosis; LR+, positive likelihood ratio; LR−, negative likelihood ratio.
are concordant with their findings as we also experienced
difficulties in identifying endometriosis in the rectovaginal
septum. Hudelist8found that combining TVS with biman-
ual examination gave higher levels of accuracy than did
bimanual examination alone. We did not perform digital
examinations in our study and therefore our sensitivities
might be increased using a combined technique. Abrao3
compared TVS with digital vaginal examination and MRI
and found that TVS had better sensitivity, specificity and
accuracy in cases of deep ‘retrocervical’ and rectosig-
moid endometriosis when compared with the other two
techniques.
Okaro24 assessed ovarian mobility, in terms of being
either mobile or fixed, with a good level of accuracy.
We agree with their findings; however, our study could
be criticized for using a subjective distinction between
the levels of ovarian adhesions, which may be a source
of bias. Interobserver reproducibility of these subjective
criteria has yet to be evaluated in further studies.
The ASRM classification of severe endometriosis, used
in our study, has been criticized for not providing an
accurate description of deep infiltrating endometriosis25.
Although other systems have been developed to comple-
ment the ASRM system, these are not widely known and
they are rarely used in routine clinical practice26.We
therefore recommend stating the exact site and extent of
any DIE found on either TVS or at surgery in addition to
using the ASRM scoring system.
The presence of DIE on the bladder, bowel or RVS, or
obliteration of the pouch of Douglas, warrants surgery
by an expert laparoscopic surgeon. The presence of any
of these features could be used as an alternative way
of diagnosing severe endometriosis. The sensitivity of
detecting these features varies in our study, but the
specificity was very high.
Histological diagnosis was not a condition of inclusion
into this study and biopsies were not sent for analysis in
all cases. However, when biopsies were sent for analysis in
moderate or severe cases, endometriosis was confirmed.
Endometriosis was confirmed in 77.8% of mild cases
when histology was available.
Ultrasound examinations in this study were performed
by operators with a high level of expertise in gynecological
ultrasonography. There was no significant difference in
diagnostic accuracy between the two operators who
performed the majority of ultrasound examinations
in this study. This indicates that the ultrasound
features of endometriosis are likely to be reproducible
with good interobserver agreement. However, the
reproducibility of ultrasound in assessing morphological
features of pelvic endometriosis needs to be examined
further in a prospective study. It remains to be
seen whether the accuracy of ultrasound diagnosis of
endometriosis will remain high when the examinations
are performed by less experienced operators in other
centers.
Guerriero et al.27 studied a novel technique for
diagnosing vaginal and RVS deep endometriosis using
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 36: 241–248.
Assessment of pelvic endometriosis using TVS 247
Table 6 Histological confirmation of endometriosis in relation to severity as classified according to the American Society for Reproductive
Medicine (ASRM)
Severity as classified by the ASRM score at laparoscopy
Characteristics Absent Minimal Mild Moderate Severe
Total cases 62 33 31 27 48
Histology available 9 (14.5, 7.8–25.3) 3 (9.1, 3.1– 23.6) 9 (29.0, 16.1–46.6) 25 (92.6, 76.6–97.9)) 44 (91.7, 80.5–96.7)
Endometriosis confirmed 0 (0, 0–29.9) 3 (100, 43.9 – 100) 7 (77.8, 45–93.7) 25 (100, 86.7– 100) 44 (100, 92.0– 100)
Data are expressed as nor n(%, 95% CI).
Table 7 Distribution of features of endometriosis in relation to laparoscopic stage of disease according to the American Society for
Reproductive Medicine (ASRM) classification
Severity as classified by the ASRM score at laparoscopy
Feature found at surgery
Minimal
(n=33)
Mild
(n=31)
Moderate
(n=27)
Severe
(n=48)
Superficial peritoneal 33 22 16 28
Deep peritoneal 0 17 17 37
No endometriotic cysts 33 31 11 11
Largest cyst <1cm 0 0 0 0
Largest cyst 1–3 cm 0 0 11 16
Largest cyst >3cm 0 0 5 21
Partial POD obliteration 0 0 7 12
Complete POD obliteration 0 0 0 24
Minimal ovarian adhesions 0 4 1 0
Moderate ovarian adhesions 0 1 5 4
Fixed ovaries 0 1 14 41
Tubal adhesions 0 0 0 7
Tubal dilatation 0 2 0 2
POD, pouch of Douglas.
extra gel to create a stand-off to visualize the near-
field area. They concluded that this was an accurate
and inexpensive technique for evaluating patients for
deep endometriosis. This technique may have benefits
over the standard TVS routines, but a direct comparison
would be required in order to conclude that this
technique is superior. Our study, however, differs from
previously published research in that we were attempting
to establish the ability of TVS to give an overall assessment
of the severity of pelvic endometriosis, rather than
trying to examine the accuracy in diagnosing individual
morphological features of the disease.
Zanardi et al.28 examined the value of MRI for staging
of pelvic endometriosis. This study used a scoring system
based on the ASRM classification with modifications
to allow for MRI interpretation. They found a high
degree of agreement between the MRI findings and
operative findings. The authors recognized, however,
that MRI is not a good test for diagnosing adhesions
or complete obliteration of the pouch of Douglas. In
some cases endometriotic nodules were not seen on MRI,
and superficial disease was almost impossible to assess,
which is similar to the results of our study, using TVS.
Although it is clear that both MRI and TVS are, to some
extent, limited in the assessment of pelvic endometriosis,
the ability of TVS to establish the presence of adhesions
directly using dynamic manipulation of the pelvic organs
may be an important advantage over MRI.
In conclusion, our study has shown that a targeted
TVS scan is an accurate test for the diagnosis of severe
pelvic endometriosis. This implies that, in women with
evidence of severe disease on ultrasound examination, a
confirmatory diagnostic laparoscopy may not be required
and these women could be referred directly to a surgical
expert in minimally invasive endometriosis, locally, or
at a regional tertiary referral endometriosis center. This
approach could facilitate more effective triaging of women
with severe endometriosis, resulting in shorter, safer, more
rational and cost-effective management.
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