Ultrasound Obstet Gynecol 2011; 37: 257263

Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.8858

Diagnostic accuracy of transvaginal ultrasound for

non-invasive diagnosis of bowel endometriosis: systematic
review and meta-analysis
G. HUDELIST*, J. ENGLISH, A. E. THOMAS, A. TINELLI, C. F. SINGER**
and J. KECKSTEIN
*Department of Obstetrics and Gynaecology, Endometriosis and Pelvic Pain Clinic, Wilhelminen Hospital, Vienna, Austria; SEF, Stiftung
Endometrioseforschung; Department of Obstetrics and Gynaecology, University of Brighton Medical School, Brighton, UK; Department
of Methodological Research and Statistics, Institute of Psychology, Alpe Adria University Klagenfurt, Klagenfurt, Austria; Department of
Obstetrics and Gynaecology, Lecce Hospital, Lecce, Italy; **Department of Obstetrics and Gynaecology, University of Vienna, Vienna,
Austria; Department of Obstetrics and Gynaecology, Center for Endometriosis, Villach Hospital, Villach, Austria

K E Y W O R D S: deep infiltrating endometriosis; presurgical diagnosis; transvaginal ultrasound

ABSTRACT

INTRODUCTION

Objective To critically analyze the diagnostic value

of transvaginal sonography (TVS) for non-invasive,
presurgical detection of bowel endometriosis.

Over the past decade, the use of transvaginal sonography (TVS) has improved the quality of non-invasive
assessment of patients with suspected pelvic pathologies.
With respect to endometriosis TVS has been shown
to be a highly sensitive tool for the detection of
ovarian endometriomas1 and is far superior to routine
clinical examination alone2,3 . Moore et al.1 systematically
reviewed 67 papers on the validity of TVS for the detection
of pelvic endometriosis, out of which seven fulfilled
the inclusion criteria and focused on TVS imaging of
ovarian endometriomas. The prevalence of the condition
ranged between 13 and 38%. Sensitivities, specificities and
positive (LR+) and negative likelihood ratios (LR) in six
studies using gray-scale ultrasonography ranged between
64 and 89%, 89 and 100%, 7.6 and 29.8 and 0.1 and 0.4,
respectively. The authors therefore concluded that TVS
should be regarded as a useful test for identifying cystic
ovarian endometriosis presurgically.
Recent studies also suggest that TVS could be an
accurate method for the detection of endometriosis in
extra-ovarian locations, i.e. uterosacral ligament involvement, endometriosis of the rectovaginal space, the pouch
of Douglas, the vagina, the urinary bladder and deep infiltrating endometriosis (DIE) of the rectosigmoid3 8 . Since
TVS is a readily available, cost- and time-effective diagnostic instrument when compared to other radiological
procedures such as computed tomography and magnetic
resonance imaging (MRI)9,10 , several investigators have
further examined the diagnostic value of TVS for the noninvasive detection of DIE infiltrating the bowel. The aim

Methods MEDLINE (19662010) and EMBASE (1980

2010) databases were searched for relevant studies investigating the diagnostic accuracy of TVS for diagnosing deep
infiltrating endometriosis involving the bowel. Diagnosis
was established by laparoscopy and/or histopathological analysis. Likelihood ratios (LRs) were recalculated in
addition to traditional measures of effectiveness.
Results Out of 188 papers, a total of 10 studies fulfilled
predefined inclusion criteria involving 1106 patients
with suspected endometriosis. The prevalence of bowel
endometriosis varied from 24 to 73.3%. LR+ ranged from
4.8 to 48.56 and LR ranged from 0.02 to 0.36, with wide
confidence intervals. Pooled estimates of sensitivities and
specificities were 91 and 98%; LR+ and LR were 30.36
and 0.09; and positive and negative predictive values were
98 and 95%, respectively. Three of the studies used bowel
preparations to enhance the visibility of the rectal wall;
one study directly compared the use of water contrast vs.
no prior bowel enema, for which the LR was 0.04 and
0.47, respectively.
Conclusions TVS with or without the use of prior
bowel preparation is an accurate test for non-invasive,
presurgical detection of deep infiltrating endometriosis of
the rectosigmoid. Copyright 2011 ISUOG. Published
by John Wiley & Sons, Ltd.

Correspondence to: Prof. G. Hudelist, Department of Obstetrics and Gynaecology, Endometriosis and Pelvic Pain Clinic, Wilhelminen
General Hospital, Montlearstrasse 37, A-1160 Vienna, Austria (e-mail: gernot hudelist@yahoo.de)
Accepted: 7 October 2010

Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.

SYSTEMATIC REVIEW

Hudelist et al.

258

of this work was to systematically analyze the published

literature evaluating the role of TVS for the detection of
DIE involving the rectosigmoid.

METHODS
The MEDLINE (19662010) and EMBASE (19802010)
databases were searched using the following search
strategy:
1. (pelvic or ovarian or deep infiltrating) near2 (mass or
cyst* or tumo* r)
2. ENDOMETRIOSIS in MeSH or 1 or BOWEL
ENDOMETRIOSIS
3. 2, not case reports, not review articles
4. with checktags female and human
5. with ULTRASOUND/all subheadings or TRANSVAGINAL/all subheadings or SONOGRAPHY
Abstracts of all studies identified were read and
manuscripts were then fully reviewed. In addition,
reference lists of all reviewed manuscripts were searched
for additional data. Study selection and assessment of
quality were performed independently by two reviewers
(G. H. and J. E).

Selection criteria
All studies included in the present review had to be
prospective and were required to involve both TVS examination and surgical exploration of the pelvis either
by laparoscopy or by laparotomy (as stated by Moore
et al.1 ). Scientific publications including case reports, studies on adenomyosis or extrapelvic endometriotic disease
as well as retrospective case series and review articles
were excluded. Studies reporting on pregnant women,
rectal ultrasound as the only examination and endoscopic
sonography were also excluded from this review. Patients
included in the studies presented with either subfertility
or symptoms suggestive of endometriosis.
According to the criteria of Moore et al.1 , studies were
considered to be of good quality when information on
recruitment of patients, blinding of ultrasound operators
and surgeons and data on the technical equipment were
provided. In order to define the stage and severity of
disease (i.e. the final endpoint of diagnosis), studies had
to describe the anatomical location of deep infiltrating
disease combined with histological confirmation of
endometriosis. Moore et al.1 considered that studies
missing one or two of these criteria were of moderate/poor
quality.

Data extraction and presentation of results

As described by Moore et al.1 , 2 2 tables were created to
validate test results against surgical and histopathological
findings aimed at defining whether DIE involving the
rectosigmoid can be detected by TVS. In addition,
QUADAS (quality assessment of diagnostic accuracy of

Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.

studies) was used to assess the studies11 . As described

previously, study quality is defined as high when 9
items out of 14 are met, moderate when 6 items are
met and low when < 6 criteria are met12 . LR+, LR
and test accuracy were calculated in studies lacking
these data. Confidence intervals (CIs) were calculated
as described previously1 using CATMaker statistical
software (Centre for Evidence-Based Medicine, Oxford,
UK). In two cases raw data (true and false positive
and negative rates) were obtained from the authors.
Since heterogeneity is a common finding in diagnostic
meta-analyses we calculated Cochrans Q and I2 for
all measures to assess the significance and magnitude
of study heterogeneity13 . A forest plot was used to
assess eventual outlier studies (data not shown). Potential
sources of heterogeneity were explored by random-effects
meta-regression. Number of subjects, year of publication,
QUADAS scores and prevalence were used as study-level
covariates that predicted the logarithm of diagnostic odds
ratios (DORs). The studies were weighted by the inverse of
variance of the DOR to consider the precision with which
each study measured it. Relative DORs were calculated to
compare the overall DOR with the adjusted DOR. When
heterogeneity between studies is present, a random-effects
model can be used to obtain pooled estimates14 .
We applied random-effects models with the DerSirmonianLaird estimator in order to determine overall
estimates of sensitivity, specificity, LR+, LR and DOR.
For data with zero counts a continuity correction of 0.5
was added to every value in that study, thereby allowing
the calculation of all LRs15 . For the assessment of publication bias Eggers test and Beggs test were conducted
and funnel plots were investigated (data not shown). The
tests for publication bias and funnel plots were performed
with R statistical software version 2.11.1 metafor package (R Development Core Team, Vienna, Austria)16 . All
other analyses were performed with MetaDiSc statistical
software version 1.417 (Hospital Universitario, Madrid,
Spain).

RESULTS
The initial implementation of the research strategy
revealed 188 studies relating to endometriosis and/or
adenomyosis and/or ovarian endometriosis diagnosed
by laparoscopy or laparotomy and/or ultrasonography.
Out of these only 51 papers specifically used TVS
and surgical exploration to diagnose DIE. Of these 51
papers, seven were excluded because they were case
reports or descriptive in nature. A further 18 papers
did not meet the inclusion criteria due to the fact
that they were review articles, despite the exclusion
of this article type in the primary search process.
Finally, three other publications included comments on
publications and were also excluded from the final
analysis, leaving 23 manuscripts for review3 5,7,8,18 35 .
Out of these 23 papers, 13 publications were excluded
due to methodological problems; three papers were
purely retrospective in nature18,27,28 ; four manuscripts

Ultrasound Obstet Gynecol 2011; 37: 257263.

Transvaginal ultrasound in the diagnosis of bowel endometriosis

were excluded because they involved a group of
patients already described in a previous publication
by the same group of authors5,7,25,29 and another
four papers were not included in the analysis because
insufficient information was provided on the presence
or absence of bowel endometriosis within the group of
women with endometriosis22,30,32,34 . Two papers were
excluded due to the low number of cases with proven
bowel endometriosis24 or insufficient information on the
anatomical localization of DIE affecting the bowel35 . Thus
10 papers fulfilled the inclusion criteria and were included
in the final review. In addition to the quality criteria
described by Moore et al.1 , the QUADAS scores were
calculated for each of the studies. These ranged from 7 to
13, reflecting high methodological quality in eight cases
and moderate quality in two cases.
Out of these, four papers evaluated the diagnostic
value of TVS for the detection of DIE infiltrating the
rectosigmoid excluding other possible locations of DIE in
the analysis8,23,31,33 . All other works also evaluated the
potential of TVS for the visualization of other affected
sites of deep infiltrating disease such as the vagina,
rectovaginal space, uterosacral ligaments, bladder and
pouch of Douglas. Two papers addressed the use of
TVS to diagnose DIE involving the rectum, pouch of
Douglas, vagina, rectovaginal space, uterosacral ligaments
and bladder3,26 using laparoscopic exploration and
histological confirmation of endometriosis as the gold
standard test. One work compared TVS with MRI to
detect DIE preoperatively compared to the gold standard
laparoscopy without histological confirmation21 . One
paper assessed the diagnostic value of TVS vs. rectal
endosonography19 ; two papers compared TVS with MRI,
digital examination4 and rectal endosonography20 to
detect DIE presurgically. Data on the quality of these
studies including number of patients and cases of bowel
endometriosis, recruitment criteria, blinding, information
and presence of diagnostic criteria and technical details,
data on reference standards and assessment of the
grade of study quality are provided in Table 1. Table 2
depicts prevalence rates, sensitivities, specificities, test
accuracies, positive predictive values (PPVs), negative
predictive values (NPVs) and positive and negative LRs
with CIs of all studies included in the final analysis. The
number of patients with proven DIE infiltrating the bowel
undergoing preoperative TVS ranged from 1721 to 8123 .
Sensitivity and specificity varied from 67 to 98% and 92
to 100%, respectively.
As further demonstrated in Table 2, PPVs and NPVs
ranged from 87 to 100% and 75 to 99%, respectively.
LR+ goes up to infinity in cases lacking false-positive
findings and thus are not shown. LR+ of the remaining
studies varied from 4.8 to 48.56 and LR from 0.02 to
0.36.
Three studies used TVS combined with a bowel enema
to provide a better visualization of rectal wall anatomy,
specifically muscularis propria4,23,33 . Valenzano Menada
et al.33 directly compared whether adding water-contrast
in the rectosigmoid (RWC-TVS) during TVS improves

Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.

259

presurgical diagnosis of rectal DIE with TVS. The

sensitivity of RWC-TVS vs. TVS in identifying rectal DIE
was 97 vs. 56%, the specificity 100 vs. 92.5%, the PPV
100 vs. 72% and the NPV 99 vs. 86%. Due to the absence
of false-positive cases in the RWC-TVS cohort, LR+ could
not be calculated, and LR was 0.04 vs. 0.47 for TVS.
Meta-analysis of all studies included in the final review
yielded significant results of Cochrans Q for all measures
except LR+ (sensitivity: P < 0.001, Q = 238.64, df =
9, I2 = 76.7%; specificity: P = 0.037, Q = 17.8, df =
9, I2 = 49.5%; LR+: P = 0.144, Q = 13.4, df = 9,
I2 = 33.0%; LR: P < 0.001, Q = 52.6, df = 9, I2 =
82.9%; DOR: P = 0.001, Q = 27.6, df = 9, I2 = 67.4%),
indicating considerable heterogeneity between studies.
Significant values for study heterogeneity were mainly
caused by two studies21,26 that were aberrant in respect
to sensitivity, LR and DOR. However, meta-regression
including sample size, prevalence, QUADAS and year of
publication did not yield any significant results: number
of subjects (P = 0.197, relative DOR = 1.02 (95% CI,
0.991.04)), prevalence (P = 0.568, relative DOR =
0.97 (95% CI, 0.881.08)), QUADAS score (P = 0.319,
relative DOR = 1.44 (95% CI, 0.653.20)) and year
of publication (P = 0.298, relative DOR = 1.35 (95%
CI, 0.672.71)). This suggests that although there was
relevant heterogeneity between the studies, the influence
of the covariates was not systematic. To account for
heterogeneity we used a random-effects model to perform
pooled estimates and estimate the respective CIs (Table 3).
As all studies were conducted with women who suffered
from pain or infertility, the pooled prevalence of 47%
refers to women with specific symptoms.
Evaluation by both Eggers test (P = 0.221) and Beggs
test (P = 0.293) did not show evidence of publication
bias for logDOR. This result was confirmed by inspection
of the funnel plots, which were all symmetrical for the
investigated diagnostic measures (sensitivity, specificity,
PPV, NPV, LR+, LR and accuracy; data not shown).

DISCUSSION
Endometriosis infiltrating the rectosigmoid can be
suspected in up to 922% of all women with proven
endometriosis36,37 . Symptoms of DIE involving the bowel
vary greatly, ranging from asymptomatic women with
extensive rectal involvement to patients with severe
dysmenorrhea and dyschezia38 . Treatment strategies
include hormonal preparations or surgical excision of
endometriotic nodules37,39 , but presurgical staging of
DIE is crucial for planning surgical treatment options.
The findings of our systematic review clearly suggest
that TVS is a highly valuable tool for the non-invasive
detection of DIE affecting the rectosigmoid. In addition to
sensitivities, specificities, PPVs, NPVs and test accuracies,
we recalculated all positive and negative LRs since these
reflect the diagnostic accuracy and the clinical usefulness
of a test independently of the prevalence of the study
condition in the study population1 . The prevalence of

Ultrasound Obstet Gynecol 2011; 37: 257263.

Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.

Sonographer
blinded

Sonographers
blinded

No information
given

Sonographer
blinded

Radiologists
blinded
Sonographer not
blinded to PV
Sonographer
blinded

Prospective
Prospective

Prospective

Prospective

Prospective

Prospective
Prospective
Prospective

Not described

Yes; nodular, predominantly

solid, hypoechogenic lesion
adhered to the wall of the
intestinal loop
Yes; rectovaginal hypoechoic
mass adherent and/or
penetrated into the
intestinal wall thickening
the muscularis mucosa
Yes; presence of some thin
band-like echoes departing
from the center of the mass
as an Indian head dress.
Yes; irregular hypoechoic
mass, with or without
hypo/hyperechoic foci
involving colon muscularis
Yes; as above

Yes; as above

Yes; long, nodular,

predominantly solid,
hypoechogenic lesion
adhered to the wall of the
intestinal loop

Sonographer
blinded
Not stated

Prospective

Sonographers
blinded

Yes; thickening of the

muscularis propria > 3 mm,
which is hypoechoic and
thin (< 3 mm) under
normal circumstances
Yes; as above

Prospective

Study design Blinding

Consecutive; pain
and infertility
Consecutive; pain
and infertility
Consecutive; pain
and infertility

Consecutive; pain
and infertility

Consecutive; pain
and infertility

Consecutive; pain
and infertility

Consecutive; pain
and infertility
Consecutive; pain
and infertility
Consecutive; pain
and infertility

Consecutive; pain
and infertility

Recruitment;
cause for referral

194

200

92

134

88

90

104

32

142

30

81

48

63

75

39

23

54

17

47

22

Laparoscopic
visualization
Histology

Histology in 29

Histology

Reference
standard

TVS

TVS, MRI,
PV, RES
TVS, PV

TVS

TVS

Histology

Histology

Histology in 54

Histology

Histology

TVS,
Histology
RWC-TVS

TVS, MRI,
PV

TVS, MRI

TVS

TVS, RES

Patients with
Cases of
suspected
rectal/sigmoidal
endometriosis endometriosis Test
( n)
( n)
method

Good (12)

Moderate (13)

Good (12)

Good (12)

Good (11)

Good (12)

Moderate (10)

Poor (7)

Moderate (8)

Moderate (9)

Study quality
according to
Moore criteria
(QUADAS score)

MRI, magnetic resonance imaging; PV, per vaginam clinical examination; QUADAS, quality assessment of diagnostic accuracy of studies; RES, rectal endosonography; RWC, rectal water contrast;
TVS, transvaginal sonography.

Bazot et al.
(2009)20
Hudelist et al.
(2009)8
Goncalves et al.
(2010)23

Piketty et al.
(2009)31

Guerriero et al.
(2008)26

Valenzano
Menada et al.
(2008)33

Bazot et al.
(2004)3
Carbognin et al.
(2006)21
Abrao et al.
(2007)4

Bazot et al.
(2003)19

Study

Diagnostic criteria stated;

ultrasound criteria for
diagnosis

Table 1 Characteristics of the studies included in the analysis

260

Hudelist et al.

Ultrasound Obstet Gynecol 2011; 37: 257263.

261

0.05 (0.010.31)
0.13 (0.060.28)
0.29 (0.140.61)
0.02 (0.000.13)
0.04 (0.010.3)
0.36 (0.230.57)
0.10 (0.050.20)
0.06 (0.020.16)
0.04 (0.010.17)
0.02 (0.010.10)

Table 3 Overall analysis of all studies included in the final analysis

using a random-effects model to perform pooled estimates of
variables
Variable

27.62 (9.0284.58)
4.8 (1.2618.31)

8.17 (3.1121.44)
26.29 (6.72102.83)

48.56 (15.81149.10)

Sensitivity (%)
Specificity (%)
LR+
LR
DOR
Prevalence (%)
PPV (%)
NPV (%)

Estimate (95% CI)

91 (88.193.5)
98 (96.799.0)
30.36 (15.45759.626)
0.09 (0.0460.188)
394.3 (116.31336.0)
47 (36.757.3)
98 (96.799.6)
95 (92.197.7)

DOR, diagnostic odds ratio (values not adjusted); LR+, positive

likelihood ratio (with continuity correction for studies with
null-cells); LR, negative likelihood ratio; NPV, negative predictive
value; PPV, positive predictive value.

LR+, positive likelihood ratio; LR, negative likelihood ratio; NPV, negative predictive value; PPV, positive predictive value.

97
94
84
99
99
81
93
96
98
99
89
94
75
98
99
78
89
88
99
98
100
93
100
100
100
87
97
100
94
100
8/8 (100)
92/95 (97)
15/15 (100)
50/50 (100)
67/67 (100)
45/49 (92)
56/58 (97)
29/29 (100)
149/152 (98)
113/113 (100)
21/22 (95)
41/47 (87)
12/17 (71)
53/54 (98)
22/23 (96)
26/39 (67)
68/75 (91)
59/63 (94)
46/48 (96)
79/81 (98)
22/30 (73)
47/142 (33)
17/32 (53)
54/104 (52)
23/90 (26)
39/88 (44)
75/133 (56)
63/92 (68)
48/200 (24)
81/194 (42)
Bazot et al. (2003)19
Bazot et al. (2004)3
Carbognin et al. (2006)21
Abrao et al. (2007)4
Valenzano Menada et al. (2008)33
Guerriero et al. (2008)26
Piketty et al. (2009)31
Bazot et al. (2009)20
Hudelist et al. (2009)8
Goncalves et al. (2010)23

Study

Prevalence of
rectal/sigmoidal
endometriosis
(n (%))

Table 2 Analysis of data in the included studies

Sensitivity
(n (%))

Specificity
(n (%))

PPV (%)

NPV (%)

Accuracy (%)

LR+ (95% CI)

LR (95% CI)

Transvaginal ultrasound in the diagnosis of bowel endometriosis

Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.

DIE involving the bowel ranged from 24 to 73%, which

may be attributable to different referral patterns and the
availability of tertiary referral centers providing sufficient
expertise in the presurgical diagnosis and treatment of
rectal DIE. LR+ ranged from 4.821 to 27.623 and LR
from 0.0223 to 0.3626 . The combined use of TVS with
vaginal examination may further increase the diagnostic
accuracy, with reported LR+ and LR 48.56 and 0.048 ,
respectively. In addition, it should be noted that LR+
went up to infinity in five studies (Table 2), suggesting
highly accurate presurgical test results.
Performance of a meta-analysis of all included studies
by using a random-effects model to calculate pooled
estimates revealed LR+ and LR of 30.36 and 0.09,
respectively. According to Altman40 , a very helpful test
for establishing or excluding a condition is characterized
by an LR+ > 10 and an LR < 0.1, while a test is
regarded as moderately helpful with an LR+ between 5
and 10 and an LR between 0.1 and 0.2. As depicted in
Table 3, the results of our meta-analysis clearly suggest
that TVS is indeed very useful for sonographic diagnosis
but also presurgical exclusion of bowel endometriosis.
Two studies21,26 were aberrant with respect to sensitivity,
LR and DOR. This may be attributable to low sensitivity
values in association with small patient numbers21 or
the use of tenderness guided transvaginal sonography26 ,
which may be less sensitive in cases of endometriotic
involvement of the upper rectum/lower sigmoid, since
these locations may not appear as painful sites when
using this technique.
The conclusions of this review are weakened by the
fact that blinding of the surgeon was missing in all
studies included in the final analysis, which might have
a potential influence on the results of the gold standard
test, i.e. surgery. On the other hand, information on
the preoperative findings is essential for guiding the
surgical technique and surgical diagnosis of endometriosis
in everyday clinical practice.
An additional variable in the accuracy of the gold
standard test, i.e. laparoscopy, is the fact that several
studies did not provide sufficient information about the

Ultrasound Obstet Gynecol 2011; 37: 257263.

262

surgical exploration of the patients with DIE3,20,21,26

since complete cul-de-sac obliteration secondary to
endometriosis was reported but could not necessarily
be surgically cleared. This may, in cases of DIE
affecting the non-visible, occluded lower rectum, lead
to misinterpretation and observation bias of the gold
standard test and consequently negatively affect the
validation of the index test, i.e. TVS. Hence, full surgical
exploration of patients with an occluded pouch of Douglas
is important for the final and accurate diagnosis of
bowel endometriosis since DIE may be missed at the
time of laparoscopy, thereby questioning the quality
of laparoscopic visualization of the pelvis as the gold
standard test for the diagnosis of endometriosis.
Another limiting factor to the results of this systematic
review is the heterogeneity of populations included in
the studies. Some authors failed to provide sufficient
data on the selection criteria and referral patterns of
centers where studies were conducted. Due to the fact
that most patients were treated in tertiary referral centers,
it is conceivable that the study populations represent an
already preselected patient cohort with a high prevalence
of bowel endometriosis. As a consequence, the conclusions
of this review may therefore only be applicable to a tertiary
referral setting and patients with a high risk for DIE.
In clinical everyday practice, exclusion of DIE is of
critical importance since extensive bowel involvement
warrants an interdisciplinary approach and referral to
a tertiary center. In conclusion, the majority of the
published evidence suggests that TVS is a highly useful
and easy accessible test for the preoperative detection of
DIE infiltrating the rectosigmoid. Whether the widespread
use of TVS and the inclusion of TVS in specialist training
programs lead to a reduction in the diagnostic delay of
patients with endometriosis remains to be seen.

ACKNOWLEDGMENTS
The authors want to thank Dr Simone Ferrero and MMag
Nadja Fritzer for their support and helpful advice. This

work was supported by the OEGEO, Osterreichische

Endokrinologische Onkologie.
Gesellschaft fur

REFERENCES
1. Moore J, Copley S, Morris J, Lindsell D, Golding S, Kennedy S.
A systematic review of the accuracy of ultrasound in the
diagnosis of endometriosis. Ultrasound Obstet Gynecol 2002;
20: 630634.
2. Nezhat C, Santolaya J, Nezhat FR. Comparison of transvaginal
sonography and bimanual pelvic examination in patients with
laparoscopically confirmed endometriosis. J Am Assoc Gynecol
Laparosc 1994; 1: 127130.
3. Bazot M, Thomassin I, Hourani R, Cortez A, Darai E. Diagnostic accuracy of transvaginal sonography for deep pelvic
endometriosis. Ultrasound Obstet Gynecol 2004; 24: 180185.
4. Abrao MS, Goncalves MO, Dias JA Jr, Podgaec S, Chamie LP,
Blasbalg R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the
diagnosis of deep endometriosis. Hum Reprod 2007; 22:
30923097.

Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.

Hudelist et al.
5. Bazot M, Malzy P, Cortez A, Roseau G, Amouyal P, Darai E.
Accuracy of transvaginal sonography and rectal endoscopic
sonography in the diagnosis of deep infiltrating endometriosis.
Ultrasound Obstet Gynecol 2007; 30: 9941001.
6. Hudelist G, Keckstein J. The use of transvaginal sonography
(TVS) for preoperative diagnosis of pelvic endometriosis. Praxis
(Bern 1994) 2009; 98: 603607.
7. Hudelist G, Oberwinkler KH, Singer CF, Tuttlies F, Rauter G,
Ritter O, Keckstein J. Combination of transvaginal sonography
and clinical examination for preoperative diagnosis of pelvic
endometriosis. Hum Reprod 2009; 24: 10181024.
8. Hudelist G, Tuttlies F, Rauter G, Pucher S, Keckstein J. Can
transvaginal sonography predict infiltration depth in patients
with deep infiltrating endometriosis of the rectum? Hum Reprod
2009; 24: 10121017.
9. Kinkel K, Frei KA, Balleyguier C, Chapron C. Diagnosis of
endometriosis with imaging: a review. Eur Radiol 2006; 16:
285298.
10. Brosens I, Puttemans P, Campo R, Gordts S, Kinkel K. Diagnosis of endometriosis: pelvic endoscopy and imaging techniques.
Best Pract Res Clin Obstet Gynaecol 2004; 18: 285303.
11. Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The
development of QUADAS: a tool for the quality assessment of
studies of diagnostic accuracy included in systematic reviews.
BMC Med Res Methodol 2003; 3: 25.
12. Meredith SM, Sanchez-Ramos L, Kaunitz AM. Diagnostic
accuracy of transvaginal sonography for the diagnosis of adenomyosis: systematic review and metaanalysis. Am J Obstet
Gynecol 2009; 201: 107.e16.
13. Sidik K, Jonkman JN. Simple heterogeneity variance estimation
in meta-analysis. J R Stat Soc [Ser C] 2005; 54: 367384.
14. Deville W, Buntix F, Bouter LM, Montori VM, de Vet HC, van
der Windt DA, Bezemer PD. Conductiong systematic reviews of
diagnostic studies: didactic guidelines. BMC Med Res Methodol
2002; 2: 29.
15. Goodacre S, Sampson F, Thomas S, van Beek E, Sutton A.
Systematic review and meta-analysis of the diagnostic accuracy
of ultrasonography for deep vein thrombosis. BMC Med
Imaging 2005; 5: 56.
16. Viechtbauer W. Conducting meta-analysis in R with the
metaphor package. J Stat Softw 2010; 36: 148.
17. Zamora J, Abraira V, Muriel A, Khan K. Coomarasamy MetaDiSc: a software for meta-analysis of test accuracy data. BMC
Med Res Methodol 2006; 6: 612.
18. Balleyguier C, Chapron C, Dubuisson JB, Kinkel K, Fauconnier A, Vieira M, Helenon O, Menu Y. Comparison of magnetic
resonance imaging and transvaginal ultrasonography in diagnosing bladder endometriosis. J Am Assoc Gynecol Laparosc
2002; 9: 1523.
19. Bazot M, Detchev R, Cortez A, Amouyal P, Uzan S, Darai E.
Transvaginal sonography and rectal endoscopic sonography
for the assessment of pelvic endometriosis: a preliminary
comparison. Hum Reprod 2003; 18: 16861692.
20. Bazot M, Lafont C, Rouzier R, Roseau G, Thomassin-Naggara
I, Darai E. Diagnostic accuracy of physical examination,
transvaginal sonography, rectal endoscopic sonography, and
magnetic resonance imaging to diagnose deep infiltrating
endometriosis. Fertil Steril 2009; 92: 18251833.
21. Carbognin G, Girardi V, Pinali L, Raffaelli R, Bergamini V,
Pozzi Mucelli R. Assessment of pelvic endometriosis: correlation
of US and MRI with laparoscopic findings. Radiol Med 2006;
111: 687701.
22. Eskenazi B, Warner M, Bonsignore L, Olive D, Samuels S,
Vercellini P. Validation study of nonsurgical diagnosis of
endometriosis. Fertil Steril 2001; 76: 929935.
23. Goncalves MO, Podgaec S, Dias JA Jr, Gonzalez M, Abrao MS.
Transvaginal ultrasonography with bowel preparation is able to
predict the number of lesions and rectosigmoid layers affected
in cases of deep endometriosis, defining surgical strategy. Hum
Reprod 2010; 25: 665671.

Ultrasound Obstet Gynecol 2011; 37: 257263.

Transvaginal ultrasound in the diagnosis of bowel endometriosis

24. Grasso RF, Di Giacomo V, Sedati P, Sizzi O, Florio G, Faiella E,
Rossetti A, Del Vescovo R, Zobel BB. Diagnosis of deep
infiltrating endometriosis: accuracy of magnetic resonance
imaging and transvaginal 3D ultrasonography. Abdom Imaging
2009; 35: 716725.
25. Guerriero S, Ajossa S, Gerada M, DAquila M, Piras B, Melis
GB. Tenderness-guided transvaginal ultrasonography: a new
method for the detection of deep endometriosis in patients with
chronic pelvic pain. Fertil Steril 2007; 88: 12931297.
26. Guerriero S, Ajossa S, Gerada M, Virgilio B, Angioni
S, Melis GB. Diagnostic value of transvaginal tendernessguided ultrasonography for the prediction of location of deep
endometriosis. Hum Reprod 2008; 23: 24522457.
27. Hensen JH, Puylaert JB. Endometriosis of the posterior culde-sac: clinical presentation and findings at transvaginal
ultrasound. AJR Am J Roentgenol 2009; 192: 16181624.
28. Koga K, Osuga Y, Yano T, Momoeda M, Yoshino O, Hirota Y,
Kugu K, Nishii O, Tsutsumi O, Taketani Y. Characteristic
images of deeply infiltrating rectosigmoid endometriosis on
transvaginal and transrectal ultrasonography. Hum Reprod
2003; 18: 13281333.
29. Menada MV, Remorgida V, Abbamonte LH, Fulcheri E, Ragni
N, Ferrero S. Transvaginal ultrasonography combined with
water-contrast in the rectum in the diagnosis of rectovaginal
endometriosis infiltrating the bowel. Fertil Steril 2008; 89:
699700.
30. Okaro E, Condous G, Khalid A, Timmerman D, Ameye L,
Huffel SV, Bourne T. The use of ultrasound-based soft markers
for the prediction of pelvic pathology in women with chronic
pelvic pain can we reduce the need for laparoscopy? BJOG
2006; 113: 251256.
31. Piketty M, Chopin N, Dousset B, Millischer-Bellaische AE,
Roseau G, Leconte M, Borghese B, Chapron C. Preoperative
work-up for patients with deeply infiltrating endometriosis:
transvaginal ultrasonography must definitely be the first-line
imaging examination. Hum Reprod 2009; 24: 602607.

Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.

263

32. Savelli L, Manuzzi L, Pollastri P, Mabrouk M, Seracchioli R,

Venturoli S. Diagnostic accuracy and potential limitations of
transvaginal sonography for bladder endometriosis. Ultrasound
Obstet Gynecol 2009; 34: 595600.
33. Valenzano Menada M, Remorgida V, Abbamonte LH, Nicoletti A, Ragni N, Ferrero S. Does transvaginal ultrasonography
combined with water-contrast in the rectum aid in the diagnosis of rectovaginal endometriosis infiltrating the bowel? Hum
Reprod 2008; 23: 10691075.
34. Yazbek J, Helmy S, Ben-Nagi J, Holland T, Sawyer E, Jurkovic
D. Value of preoperative ultrasound examination in the selection
of women with adnexal masses for laparoscopic surgery.
Ultrasound Obstet Gynecol 2007; 30: 883888.
35. Holland TK, Yazbek J, Cutner A, Saridogan E, Hoo WL,
Jurkovic D. Value of transvaginal ultrasound in assessing the
severity of pelvic endometriosis. Ultrasound Obstet Gynecol
2010; 36: 241248.
36. Chapron C, Chopin N, Borghese B, Foulot H, Dousset B,
Vacher-Lavenu MC, Vieira M, Hasan W, Bricou A. Deeply
infiltrating endometriosis: pathogenetic implications of the
anatomical distribution. Hum Reprod 2006; 21: 18391845.
37. Chapron C, Fauconnier A, Vieira M, Barakat H, Dousset B,
Pansini V, Vacher-Lavenu MC, Dubuisson JB. Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod 2003;
18: 157161.
38. Ballard K, Lane H, Hudelist G, Banerjee S, Wright J. Can
specific pain symptoms help in the diagnosis of endometriosis?
A cohort study of women with chronic pelvic pain. Fertil Steril
2010; 94: 2027.
39. Keckstein J, Ulrich U, Kandolf O, Wiesinger H, Wustlich M.
Laparoscopic therapy of intestinal endometriosis and the
ranking of drug treatment. Zentralbl Gynakol 2003; 125:
259266.
40. Altman DG. Statistics in medical journals: developments in the
1980s. Stat Med 1991; 10: 18971913.

Ultrasound Obstet Gynecol 2011; 37: 257263.