Download as pdf or txt
Download as pdf or txt
You are on page 1of 8

Ultrasound Obstet Gynecol 2013; 41: 328–335

Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.11200

Automated three-dimensional coded contrast imaging


hysterosalpingo-contrast sonography: feasibility in office
tubal patency testing
C. EXACOUSTOS*, A. DI GIOVANNI*, B. SZABOLCS*, V. ROMEO*, M. E. ROMANINI*,
D. LUCIANO†, E. ZUPI* and D. ARDUINI*
*Department of Obstetrics and Gynecology, Università degli Studi di Roma ‘Tor Vergata’, Rome, Italy; †Department of Obstetrics and
Gynecology, Center for Fertility and Women’s Health University of Connecticut School of Medicine, New Britain, CT, USA

K E Y W O R D S: hysterosalpingography; three-dimensional ultrasound; transvaginal hysterosalpingo-contrast sonography;


ultrasound contrast medium; ultrasound imaging

ABSTRACT Conclusions HyCoSy with automated 3D-CCI technol-


ogy retains the advantages of conventional 2D HyCoSy
Objective To evaluate the feasibility of transvaginal
while overcoming the disadvantages. 2D HyCoSy is highly
hysterosalpingo-contrast sonography (HyCoSy) with new
observer-dependent and is only accurate in the hands of
automated three-dimensional coded contrast imaging
experienced investigators; by obtaining a volume of the
(3D-CCI) software in the evaluation of tubal patency
uterus and tubes, automated 3D volume acquisition per-
and visualization of tubal course.
mits visualization of the tubes in the coronal view and
Methods Patients undergoing HyCoSy with automated of the tubal course in 3D space, and should allow less
3D-CCI software were evaluated prospectively. First, to experienced operators to evaluate tubal patency status
evaluate the feasibility of 3D visualization of tubal course, relatively easily. Copyright  2012 ISUOG. Published
we performed consecutive volume acquisitions while by John Wiley & Sons, Ltd.
injecting SonoVue contrast agent. We then performed
conventional two-dimensional (2D) real-time HyCoSy to
INTRODUCTION
confirm tubal patency status by detection of saline and air
bubbles moving through the Fallopian tubes and around Evaluation of Fallopian tubal patency is one of the
the ovaries. We also evaluated visualization with CCI of initial steps in the diagnostic workup of infertile
the contrast agent around the ovaries, side effects and women. Hysterosalpingo-contrast sonography (HyCoSy)
pain during and after the procedure, by visual analog is currently performed as an office procedure to assess
scale (VAS) (ranging from 0 to 10, with 0 corresponding tubal patency by transvaginal sonography (TVS)1,2 .
to no pain and 10 corresponding to maximum pain). Because it can be performed in an outpatient setting,
it is a useful tool in one-stop infertility clinics3 .
Results A total of 126 patients (252 tubes) underwent
HyCoSy is based on the introduction into the uterine
3D-CCI HyCoSy followed by 2D real-time HyCoSy.
cavity and Fallopian tubes of a sonographic-enhancing
According to the final 2D real-time evaluation, bilateral
positive-contrast fluid that can be visualized by TVS. In
tubal patency was observed in 111 patients, bilateral tubal
a previous paper4 we showed that HyCoSy using saline
occlusion in four patients and unilateral tubal patency
solution mixed with air is an effective and inexpensive
in 11 patients. The concordance rate for tubal patency
screening tool with which to assess tubal patency
status between the first 3D volume acquisition and the
status, with high diagnostic accuracy when compared
final 2D real-time evaluation was 84% and that between
to hysterosalpingography (HSG) and laparoscopic dye
the second 3D volume acquisition and the final 2D real-
perturbation, which is the gold standard procedure in
time evaluation was 97%. A pain score >5 on VAS
tubal patency evaluation.
was recorded in 58% of patients during the procedure,
However, HyCoSy has limitations. It is highly observer-
but a pain score ≤ 5 was recorded in 85.7% of patients
dependent and it is only accurate in the hands of
immediately after the procedure.
experienced investigators4 – 7 , because the Fallopian tubal

Correspondence to: Dr C. Exacoustos, Obstetrics and Gynecology Department, Università degli Studi di Roma ‘Tor Vergata’, Ospedale
Generale S. Giovanni Calibita ‘Fatebenefratelli’, Isola Tiberina 1, 00186 Rome, Italy (e-mail: caterinaexacoustos@tiscali.it)
Accepted: 26 April 2012

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER
3D-CCI HyCoSy and tubal patency testing 329

course is not linear and lies on different planes, so rapid with risk factors such as heart disease, especially heart
movements of the probe are needed to visualize the entire shunt hypertension and stroke. Exclusion criteria also
tubal course and the passage of fluid through the tube included presence of pelvic or vaginal infection and tubal
during infusion. Furthermore, HyCoSy is not as accurate pathology that was detectable by TVS (hydrosalpinx,
when tubes are occluded, possibly due to intermittent acute salpingitis). Patients who met our criteria underwent
tubal spasm and to difficulties in distinguishing saline and 3D-CCI HyCoSy followed by 2D real-time HyCoSy
air in the tubes from air moving in the bowels. Moreover, during the proliferative phase of their cycle (Days 5–12).
HyCoSy with air/saline solution does not provide an Our Institutional Review Board approved this study, and
image of the entire tube and its course, as HSG does. written informed consent was obtained from each patient.
The use of ultrasound-enhancing contrast media has HyCoSy was performed, using a Voluson E8 ultrasound
been introduced to improve the evaluation of tubal machine (GE Healthcare, Zipf, Austria) with automated
patency status8,9 . Recently, second-generation contrast 3D-CCI HyCoSy software (GE Healthcare) and SonoVue
agents have been proposed to evaluate various gyneco- (Bracco International BV, Amsterdam, The Netherlands)
logical lesions10 – 15 and for sonographic tubal patency ultrasound contrast medium, according to the technique
evaluation16 – 19 . These agents provide a substantial har- described in our previous studies4,17,20 .
monic response at low acoustic pressure and can be seen After inserting a speculum into the patient’s vagina,
more easily and endure longer than do the earlier con- a 5-Fr salpingographic balloon catheter (PBN Medicals,
trast agents. Their safety for intravenous use has been Stenløse, Denmark) was placed in the uterine cavity and
confirmed by the United States Food and Drug Adminis- filled with 1–2 mL air. This step ensured that the cervical
tration and by the European Commission. canal was closed, thus preventing leakage of fluid and
Special ultrasound technologies have been keeping the catheter in the correct position. The TVS
proposed15,17 – 19 for optimization of the use of probe was positioned to visualize the transverse section
ultrasound contrast media by means of low acoustic of the uterus and, if possible, both ovaries laterally. The
pressure. In coded contrast imaging (CCI)20 , the ultra- CCI mode was then started, causing the view of the pelvis
sound machine emits a beam at a selected frequency and to become completely anechoic. Using CCI technology
receives a narrow band of harmonic signal, avoiding during HyCoSy, the intrauterine injection of ultrasound
overlap between the tissue and the contrast response. contrast medium in a completely anechoic pelvis was
The image displayed is based only on harmonic signals visualized as hyperechoic fluid, seen first in the uterus,
produced by contrast-medium microspheres; broadband then in the tube if it was proximally patent and, finally,
ultrasonic signals from surrounding tissue are filtered out as it spilled into the abdominal cavity if the tube was
completely. completely patent distally. 3D volume acquisition was
In an attempt to overcome the limitations of conven- performed during injection, with the region of interest set
tional two-dimensional (2D) HyCoSy, with its need for as wide as possible so that uterus and both ovaries could
an experienced sonographer to visualize the entire tubal be seen and allowing the whole length of the Fallopian
course, two ultrasound technologies have been combined: tube to be detected.
CCI, to better evaluate the signals coming from the con- The sonographic volume acquisition technique was
trast medium, and three-dimensional (3D) sonography, to standardized according to the following criteria: fre-
acquire a volume of the Fallopian tubes20 . quency, 6–9 MHz; sweep angle, as wide as possible to
Several studies4 – 9,16 – 20 have shown high accuracy include the uterus in transverse section and both ovaries
(85–95%) in determining tubal patency with different laterally (maximum 120◦ ); sweep velocity, medium to
ultrasound techniques and contrast media, including auto- maximum quality; 3D box size, exceeding the uterus and
mated 3D-CCI HyCoSy21 . In this study, we investigated both ovaries by 1 cm on each side. The contrast medium
further the feasibility of HyCoSy with the new automated was highly echogenic and could be visualized for sev-
3D-CCI software in the evaluation of tubal patency and eral minutes, allowing the tubal course and shape to be
visualization of the tubal course. studied and more than one 3D volume acquisition to
be performed. For each patient, 3D volume acquisition
PATIENTS AND METHODS was performed consecutively twice, while injecting up
to 4 mL contrast media: 1.5 mL SonoVue diluted with
Patients with primary and secondary infertility undergo- 2.5 mL saline solution the first time and 2–4 mL saline
ing evaluation of tubal patency were included in this study. (which pushed the residual contrast agent through the
Infertile patients were defined as women who had been catheter into the tubes) the second time.
actively trying to become pregnant for more than 1 year. The multiplanar view of the uterus and tubes, obtained
Before the HyCoSy procedure, all patients gave their during injection of the contrast medium (Figure 1), was
history and underwent clinical examination including 2D- converted automatically, by dedicated software, to the
and 3D-TVS. During 2D TVS we described precisely volume image. This resulted in a view of the uterine
and recorded the presence of: fibroids; any intrauterine cavity in coronal section, with both tubes laterally and
pathology; any adnexal lesion; and retroperitoneal deep the contrast medium spilling around the ovaries if both
infiltrating endometriosis (DIE). We excluded all patients tubes were patent. The possibility to rotate this volume
with ongoing pregnancy, reproductive tract cancer or showed the tubal course in 3D space (Figure 2 and

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2013; 41: 328–335.
330 Exacoustos et al.

Figure 1 Automated three-dimensional coded contrast imaging hysterosalpingo-contrast sonography: multiplanar view showing contrast
medium in uterus and tubes and automated reconstruction of the volume.

Figure 2 Automated three-dimensional (3D) coded contrast imaging hysterosalpingo-contrast sonography. (a) Automated reconstructed
volume of contrast medium in uterus and patent tubes with spillage of contrast around the ovaries. (b,c) The possibility to rotate this volume
shows the tubal course in 3D space.

Videoclip S1). In addition, the software permitted the


sonographer to combine gray-scale imaging of the uterus
in coronal section, with automated reconstruction of the
contrast medium in the uterine cavity and patent tubes
superimposed in red (Figure 3 and Videoclip S2). In cases
of unilateral tubal occlusion, the tubal course was seen
on one side only (Figure 4b) and was not detectable if
both tubes were occluded (Figure 4c). Using 2D gray-
scale ultrasound of the ovary after contrast medium
injection in parallel with CCI permitted visualization of
the contrast agent around the ovaries as a hyperechoic
ring in anechoic tissue (Figure 5), thus confirming
tubal patency and spillage of the contrast fluid in the Figure 3 Automated three-dimensional coded contrast imaging
pelvis. hysterosalpingo-contrast sonography: gray-scale coronal section of
To determine final tubal patency status we then uterus, with automated reconstructed volume of contrast medium
performed real-time 2D HyCoSy, using at least one in uterine cavity and patent tubes superimposed in red.

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2013; 41: 328–335.
3D-CCI HyCoSy and tubal patency testing 331

Figure 4 Automated three-dimensional coded contrast imaging hysterosalpingo-contrast sonography: automated reconstructed volumes of
contrast medium in uterus and tubes in cases of bilateral tubal patency (a) and unilateral (b) and bilateral (c) tubal occlusion.

Figure 5 Visualization of the ovary with conventional two-dimensional gray-scale transvaginal sonography (a,c) and with coded contrast
imaging (CCI) mode (b,d), prior to (a,b) and following (c,d) injection of SonoVue contrast agent. Note the hyperechoic contrast around the
ovary on CCI after injection (d), confirming patency of the ipsilateral tube.

injection of 4–5 mL saline mixed with air and noting Patients were asked to grade the discomfort experi-
the microbubbles’ movement throughout the tubes; if a enced with the aid of a 10-point visual analog scale (VAS),
tube was patent on 3D-CCI HyCoSy and not initially with 0 corresponding to ‘no pain experienced’ and 10
on 2D HyCoSy, which may occur due to tubal spasm, corresponding to ‘maximum pain experienced’. The pain
we administered a further injection or waited a few score was evaluated during the procedure and 5–10 min
seconds and reassessed patency until the patency seen after. The need for analgesic drugs after the procedure
on 3D imaging was confirmed. Determination of tubal or symptoms of a vagal reaction (nausea, bradycardia,
sweating, hypotension) during the procedure were also
patency on 2D HyCoSy required all three of the following
recorded.
criteria4,17,20 : passage of air and saline bubbles through
To determine the feasibility of the method in the eval-
the interstitial part of the tube; detection of air bubbles
uation of tubal patency we therefore considered: visual-
moving around the ovary (observation of flow around the ization of tubal patency during first and second injections
ovaries was possible even without visualization of passage of SonoVue and 3D volume acquisition; visualization of
through the whole tubal course); detection of the solution the contrast agent around the ovaries with CCI; detection
and air bubbles in the pouch of Douglas. on 2D real-time HyCoSy of bubbles moving in the tube,
Immediately after the procedure, all patients received around the ovaries and in the pouch of Douglas; pain dur-
antibiotic prophylaxis as a single 1-g dose of azithromycin, ing and after the procedure (using 0–10 VAS); and other
administered orally. side effects (vagal reactions, need for analgesic drugs).

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2013; 41: 328–335.
332 Exacoustos et al.

126 infertile patients

3D-CCI HyCoSy
First injection

Bilateral tubal patency Bilateral tubal occlusion Unilateral tubal occlusion


(n = 79) (n = 12) (n = 35)

3D-CCI HyCoSy (n = 6) (n = 19) (n = 1)


Second injection

Bilateral tubal patency Bilateral tubal occlusion Unilateral tubal occlusion


(n = 104) (n = 5) (n = 17)

2D HyCoSy
real-time
(n = 7) (n = 1)

Bilateral tubal patency Bilateral tubal occlusion Unilateral tubal occlusion


(n = 111) (n = 4) (n = 11)

Figure 6 Flow chart of tubal patency status observed in 126 patients during hysterosalpingo-contrast sonography (HyCoSy) at first and
second SonoVue injections with three-dimensional coded contrast imaging (3D-CCI) volume acquisition, and after two-dimensional (2D)
real-time HyCoSy final evaluation. Numbers of patients who had incorrect classification of their tubal status at the first 3D evaluation and
needed further injections are given in the small dotted-line boxes.

Statistical analysis chi-square or Fisher’s exact test, as appropriate. P < 0.05


was considered statistically significant.
Final tubal patency status was determined by considering
all results, after completion of the procedure (both 3D
and 2D evaluations and all injections), i.e. if passage RESULTS
of fluid in the tube was observed by either 3D or 2D
From March 2009 to February 2010 we enrolled 131
HyCoSy, we considered the tube patent. This means
patients into the study. Five patients were excluded
that we could have only false-positive occluded tubes
because of cervicovaginal infection (n = 4) or hydro-
with no false-negative occlusions. For the purposes
salpinx (n = 1) detected at the time of preliminary
of analysis, all 126 patients were considered to have
TVS. Thus, 126 patients, 83 with primary and 43
two tubes even if a previous salpingectomy had been
with secondary infertility, underwent 3D-CCI HyCoSy
performed.
followed by 2D real-time HyCoSy.
Statistical analysis was conducted to assess whether Population characteristics are summarized in Table 1.
tubes found to be patent or occluded at 3D-CCI HyCoSy Patients with primary infertility differed significantly from
had the same status on 2D HyCoSy. This was done by those with secondary infertility in only a few studied
determining the concordance rate of tubal patency status features, with a higher prevalence of endometriosis in
at first and at second 3D volume acquisitions with that patients with primary infertility and, as might be expected,
at final 2D real-time HyCoSy, by calculating accuracy the occurrence of miscarriages and ectopic pregnancies
(percentage agreement) and Cohen’s kappa index for only in the secondary infertility group.
each. The percentage of time that the contrast medium At the end of the entire procedure (both 3D and
was visualized around the ovaries was also calculated, as 2D real-time HyCoSy) we observed 111 patients with
was the mean degree of pain reported during and after bilateral tubal patency, 11 patients with unilateral tubal
the procedure and the incidence of other side effects. patency and four patients with bilateral tubal occlusion,
Descriptive analysis was achieved using proportions, giving a total of 232 (92%) patent and 20 (8%)
means and SD and statistical analysis was performed using occluded tubes (252 tubes in 126 patients). We considered
Student’s t-test for mean and SD. Patients with primary final tubal patency status results from primary and
infertility (defined when patients had never been pregnant) secondary infertile patients together because they were not
or secondary infertility (defined when patients had had at statistically significantly different. Tubal patency status
least one previous spontaneous pregnancy) were placed in results at the first and second injections of contrast agent
separate subgroups, and proportions were compared with and 3D volume acquisition and the final result after 2D

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2013; 41: 328–335.
3D-CCI HyCoSy and tubal patency testing 333

Table 1 Population characteristics in 126 infertile patients who underwent hysterosalpingo-contrast sonography, according to level of
infertility

Characteristic Primary infertility (n = 83) Secondary infertility (n = 43) P* Total (n = 126)

Age (years) 34.8 ± 4.4 38.4 ± 4.3 < 0.0001 36.1 ± 4.7
Body mass index (kg/m2 ) 20.9 ± 2.9 22.2 ± 2.8 0.017 21.4 ± 2.8
Presence at initial TVS of:
Endometriosis 15 (18.1) 2 (4.6) 0.05 17 (13.5)
Myomas 10 (12.1) 6 (13.9) 0.78 16 (12.7)
History of:
Ectopic pregnancy 0 (0) 7 (16.3) 0.0004 7 (5.5)
Pelvic inflammatory disease 3 (3.6) 0 (0) 0.55 3 (2.4)
Recurrent miscarriage 0 (0) 9 (20.9) < 0.0001 9 (7.1)
Salpingectomy 1 (1.2) 5 (11.6) 0.017 6 (4.8)
Myomectomy 3 (3.6) 2 (4.6) 1.00 5 (3.9)
Metroplasty 1 (1.2) 1 (2.3) 1.00 2 (1.6)
Surgery for endometriosis 3 (3.6) 1 (2.3) 1.00 4 (3.2)

Data are given as mean ± SD or n (%). *Primary vs secondary infertility patients (Student’s t-test, chi-square test or Fisher’s exact test). TVS,
transvaginal sonography.

real-time HyCoSy are shown in Figure 6 and Table 2. Bilateral tubal occlusion was confirmed by laparoscopy
The first and second 3D volume acquisitions in relation to in all four patients with bilateral occlusion on 2D HyCoSy.
final tubal patency status on 2D evaluation had accuracy Among the 11 patients with unilateral tubal occlusion we
(concordance rate) of 84% and 97%, respectively, and had no laparoscopic confirmation of tubal patency status;
Cohen’s kappa index of 27% and 68%. Bilateral tubal however, five of these patients had a previous unilateral
patency was observed in 79 (62.7%) patients at first salpingectomy for ectopic pregnancy or endometriosis and
injection and 3D volume acquisition, in 104 patients in one patient HSG confirmed unilateral tubal occlusion.
(82.5%) at second injection and 3D volume acquisition, In one case of previous salpingectomy for ectopic
and finally was confirmed in 111 patients (88%) at 2D pregnancy we detected contrast media and fluid passage;
real-time evaluation. In only eight patients were further this was in fact likely through the residual proximal tube.
injections and 2D real time examination necessary to Contrast agent around the ovaries was observed in 121
achieve the correct final tubal patency status (Figure 6); out of 126 patients (96%) (Figure 5). It was detected
the concordance rate to the final TVS tubal patency status bilaterally in all cases of bilateral tubal patency except
for tubal status following the second injection and 3D one (spillage of contrast medium in the peritoneal cavity
volume acquisition was 94% (Table 2). was observed but it did not surround both ovaries clearly,
possibly due to the presence of adhesions). In four of
the 11 patients with unilateral tubal occlusion it was
detected bilaterally, even around the ovary ipsilateral to
Table 2 Tubal patency status results in 126 infertile patients (252 the occluded tube (perhaps because of diffusion of fluid in
Fallopian tubes) after first and second SonoVue contrast medium
injection with three-dimensional coded contrast imaging (3D-CCI) the pelvis). Contrast agent spillage around the ovaries was
evaluation, and after two-dimensional (2D) real-time absent in the four patients with bilateral tubal occlusion.
hysterosalpingo-contrast sonography (HyCoSy) final evaluation A pain score >5 (on 0–10 VAS) was recorded in 57.9%
of patients during the procedure, but a pain score ≤ 5
HyCoSy modality was recorded in 85.7% of patients immediately after the
3D-CCI volume procedure (Table 3), with only 11% of patients (n = 14)
acquisition
2D real-time
requiring analgesic drugs and only 5.6% (n = 7) with
Tubal patency status First Second final evaluation vagal reactions. All seven of the latter patients responded
well to atropine administration. In no case was hospital
Patients (n = 126)
admission required.
Bilaterally patent 79 (62.7) 104 (82.5) 111 (88.1)
Bilaterally occluded 12 (9.5) 5 (4.0) 4 (3.2)
Unilaterally occluded 35 (27.8) 17 (13.5) 11 (8.7)
Concordance rate to 94 (74.6) 119 (94.4) 126 (100)
DISCUSSION
final results*
Tubes (n = 252)
Several studies4 – 9,17 – 21 attest to the high accuracy
Patent tube 193 (76.6) 225 (89.3) 233 (92.5) of transvaginal HyCoSy in the assessment of tubal
Occluded tube 59 (23.4) 27 (10.7) 19 (7.5) patency compared with laparoscopic chromopertuba-
Concordance rate to 212 (84.1) 244 (96.8) 252 (100) tion and HSG. However, 2D HyCoSy, even when per-
final results* formed with ultrasound-enhancing contrast media, is
Data are given as n (%) of patients or tubes. *Concordance rate a highly operator-dependent technique. An experienced
between each 3D volume acquisition and final 2D real-time sonographer is necessary to manipulate the TVS probe
evaluation. efficiently in order to detect the contrast medium echoes

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2013; 41: 328–335.
334 Exacoustos et al.

Table 3 Pain evaluation by visual analog scale (VAS) in 126 studies6,22 , the greater the volume of fluid injected, the
infertile patients during and after hysterosalpingo-contrast
more pain is felt by the patient; however, there is no
sonography (HyCoSy)
association with the incidence of vagal reactions. While
Score ≤ 5 Score >5 VAS score more than 50% of our patients reported pain during
(n (%)) (n (%)) (mean ± SD) the procedure, it disappeared in most cases immediately
afterwards. This was probably because the cramping and
Pain during HyCoSy 53 (42.1) 73 (57.9) 5.31 ± 2.8
Pain after HyCoSy 108 (85.7) 18 (14.3) 2.41 ± 2.7
discomfort was due not only to the injections but also to
Pain during and after 55 (43.6) 13 (10.3) 3.86 ± 2.0 the balloon catheter inside the uterine cavity.
HyCoSy Another major advantage of HyCoSy with automated
Vagal reactions 2 (1.6) 5 (4.0) 3D-CCI is the possibility to obtain images of the uterus
Analgesic drugs 2 (1.6) 12 (9.5) and tubal course that are similar to those obtained by
administered
HSG, with the advantage that the volume can be moved
VAS score ranges from 0 to 10, with 0 corresponding to ‘no pain and rotated in 3D space. They can also be shared easily
experienced’ and 10 corresponding to ‘maximum pain experienced’. with other clinicians, whereas 2D HyCoSy is a dynamic
real-time exam in which the passage of fluid is seen only
and visualize the different parts of the tubes, as only by the ultrasound examiner and images are very difficult
rarely can the entire tube be visualized during fluid injec- to interpret. Moreover, the acquired volumes can be
tion. 3D acquisition starting from a transverse section of stored and analyzed later, reducing the examination time
the uterus is static, does not require probe movement and for patients.
automatically generates the multiplanar image and the A disadvantage of this new technique compared with
reconstruction of the entire uterine cavity and bilateral 2D HyCoSy is the cost, of both a 3D machine and the
tubal course in case of patency. contrast medium. Another limitation is the fact that
Combination of a second-generation contrast medium most ultrasound contrast media are approved in many
with CCI, which discriminates the harmonic response countries only for intravenous injection, and not for
of contrast microbubbles from ultrasound echoes of injection into the uterus and tubes.
surrounding tissues, is very helpful for clearer visualiza- In conclusion, HyCoSy with automated 3D-CCI
tion of the fluid passage throughout the tubes. Recently, technology retains the advantages of conventional 2D
high accuracy (90%) of automated 3D-CCI HyCoSy in HyCoSy while at the same time overcoming the disadvan-
detecting tubal patency has been reported21 , but the pro- tages. This technology permits visualization of the tubal
cedure seems difficult to perform for many sonographers. course, creating images of the tubes in the coronal view
With this feasibility study, therefore, we wanted to and obtaining a volume so that the tubal course in 3D
assess first how simple it is to perform automated 3D-CCI space can be evaluated. It provides imaging of the entire
HyCoSy and second if it is as accurate as the more diffi- tube and its course, similar to HSG, with the advantages
cult 2D HyCoSy. Concordance with final tubal patency of: requiring no exposure to radiation; the possibility of
status of 97% was obtained at the second 3D volume repeating injections if needed; and the possibility of being
acquisition, demonstrating that when tubal patency by performed in an outpatient setting. The clarity with which
3D ultrasound is observed, no further evaluation is spillage is seen and the ease of automated 3D volume
needed. With previous studies we have demonstrated that acquisition without any difficult probe movements makes
HyCoSy has a high concordance rate to laparoscopy4 , this diagnostic method straightforward even for an inex-
which is still considered the gold standard for evaluation perienced sonographer. With this study we have shown
of tubal patency status. that this 3D-CCI HyCoSy method has high diagnostic
If tubal occlusion is detected during 3D ultrasound, feasibility, and can be performed easily in the office. It pro-
further injections are required, especially in cases of vides the possibility of infertile patients having only one
unilateral tubal occlusion. In many of these cases, the scan in the proliferative phase of the cycle, while obtain-
fluid passage is better in one tube whereas the other tube ing information about uterine and adnexal morphology,
seems to be occluded, possibly due to spasm. After waiting as well as tubal patency (One-stop Infertility Clinic). We
some minutes and repeating the injection, often the tube are confident that 3D-CCI HyCoSy will find a place in
is seen to be patent. However, on repeated injections, the early outpatient investigation of infertile women.
3D volume acquisition cannot show accurately the tubal
course, because spillage of fluid in the peritoneal cavity
provides a diffuse image of contrast medium around the REFERENCES
pelvic organs and not just in the tube. 1. Nargund G. Time for an ultrasound revolution in reproductive
Moreover, with 2D real-time HyCoSy, for each tube one medicine. Ultrasound Obstet Gynecol 2002; 20: 107–111.
injection and often more than one is needed to visualize the 2. Lim CP, Hasafa Z, Bhattacharya S, Maheshwari A. Should a
passage of fluid in the tubes bilaterally. Because both tubes hysterosalpingogram be a first-line investigation to diagnose
are visualized simultaneously during 3D HyCoSy volume female tubal subfertility in the modern subfertility workup?
Hum Reprod 2011; 26: 967–971.
acquisition with only one or two injections, less contrast 3. Kelly SM, Sladkevicius P, Campbell S, Nargund G. Investigation
agent and fluid is required in comparison to 2D real-time of the infertile couple: a one-stop ultrasound-based approach.
HyCoSy. In our experience, and in accordance with other Hum Reprod 2001; 16: 2481–2484.

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2013; 41: 328–335.
3D-CCI HyCoSy and tubal patency testing 335

4. Exacoustos C, Zupi E, Carusotti C, Lanzi G, Marconi D, transvaginal sonography of benign versus malignant ovarian
Arduini D. Hysterosalpingo-contrast sonography compared masses: preliminary findings. J Ultrasound Med 2008; 27:
with hysterosalpingography and laparoscopic dye pertubation 1011–1018.
to evaluate tubal patency. J Am Assoc of Gynecol Laparosc 15. Testa AC, Timmerman D, Van Belle V, Fruscella E, Van
2003; 10: 29–32. Holsbeke C, Savelli L, Ferrazzi E, Leone FP, Marret H,
5. Volpi E, Zuccaio G, Patriarca A, Rustichelli S, Sismondi P. Tranquart F, Exacoustos C, Nazzaro G, Bokor D, Magri F,
Transvaginal sonographic tubal patency testing using air and Van Huffel S, Ferrandina G, Valentin L. Intravenous contrast
saline solution as contrast media in routine infertility clinic ultrasound examination using contrast-tuned imaging (CnTI)
setting. Ultrasound Obstet Gynecol 1996; 7: 43–48. and the contrast medium SonoVue for discrimination between
6. Savelli L, Pollastri P, Guerrini M, Villa G, Manuzzi L, benign and malignant adnexal masses with solid components.
Mabrouk M, Rossi S, Seracchioli R. Tolerability, side effects Ultrasound Obstet Gynecol 2009; 34: 699–710.
and complications of hysterosalpingocontrast sonography 16. Connor V. Contrast infusion sonography in the post Essure
(HyCoSy). Fertil Steril 2009; 92: 1481–1486. setting. J Minim Invasive Gynecol 2008; 15: 56–61.
7. Spalding H, Martikainen H, Tekay A, Jouppila P. Transvaginal 17. Exacoustos C, Zupi E, Szabolcs B, Amoroso C, Di Giovanni A,
salpingosonography for assessing tubal patency in women Romanini ME, Arduini D. Contrast tuned imaging and second
previously treated for pelvic inflammatory disease and benign generation contrast agent SonoVue: a new ultrasound approach
ovarian tumors. Ultrasound Obstet Gynecol 1999; 14: to evaluate tubal patency. J Minim Invasive Gynecol 2009; 16:
205–209. 437–444.
8. Prefumo F, Serafini G, Martinoli C, Gandolfo N, Gandolfo 18. Lanzani C, Savasi V, Leone FPG, Ratti M, Ferrazzi E. Two
NG, Derchi LE. The sonographic evaluation of tubal patency dimensional HyCoSy with contrast tuned imaging technology
with stimulated acoustic emission imaging. Ultrasound Obstet and a second generation contrast media for the assessment of
Gynecol 2002; 20: 386–389. tubal patency in an infertility program. Fertil Steril 2009; 92:
9. Dietrich M, Suren A, Hinney B, Osmers R, Kuhn W. Evaluation 1158–1161.
of tubal patency by HysterocontrastSonography (HyCoSy, 19. Luciano DE, Exacoustos C, Johns DA, Luciano AA. Can
Echovist) and its correlation with laparoscopic findings. J Clin hysterosalpingo-contrast sonography replace hysterosalpingog-
Ultrasound 1996; 24: 523–527. raphy in confirming tubal blockage after hysteroscopic ster-
10. Orden MR, Juvenlin JS, Kirkinien PP. Kinetics of a US contrast ilization and in the evaluation of the uterus and tubes
agent in benign and malignant adnexal tumors. Radiology 2003; in infertile patients? Am J Obstet Gynecol 2011; 204:
226: 405–410. 79–84.
11. Marret H, Sauget S, Giraudeau B. Contrast-enhanced sonogra- 20. Exacoustos C, Di Giovanni A, Szabolcs B, Binder-Reisinger H,
phy helps in discrimination of benign from malignant adnexal Gabardi C, Arduini D. Automated sonographic tubal patency
masses. J Ultrasound Med 2004; 23: 1629–1639. evaluation with three-dimensional coded contrast imaging
12. Testa AC, Ferrandina G, Fruscella E, Van Holsbeke C, Ferrazzi (CCI) during hysterosalpingo-contrast sonography (HyCoSy).
E, Leone FP, Arduini D, Exacoustos C, Bokor D, Scambia G, Ultrasound Obstet Gynecol 2009; 34: 609–612.
Timmerman D. The use of contrasted transvaginal sonography 21. Zhou L, Zhang X, Chen X, Liao L, Pan R, Zhou N, Di N. Value
in the diagnosis of gynecologic diseases: a preliminary study. J of three-dimensional hysterosalpingo-contrast sonography with
Ultrasound Med 2005; 24: 1267–1278. SonoVue in the assessment of tubal patency. Ultrasound Obstet
13. Testa AC, Timmerman D, Exacoustos C, Fruscella E, Van Gynecol 2012; 40: 93–98.
Holsbeke C, Bokor D, Arduini D, Scambia G, Ferrandina 22. Socolov D, Boian I, Boiculese L, Tamba B, Anghelache-Lupascu
G. The role of CnTI-SonoVue in the diagnosis of ovarian masses I, Socolov R. Comparison of the pain experienced by infertile
with papillary projections: a preliminary study. Ultrasound women undergoing hysterosalpingo contrast sonography or
Obstet Gynecol 2007; 29: 512–516. radiographic hysterosalpingography. Int J Gynaecol Obstet
14. Fleischer AC, Lyshchik A, Jones HW Jr. Contrast-enhanced 2010; 111: 256–259.

SUPPORTING INFORMATION ON THE INTERNET


The following supporting information may be found in the online version of this article:
Videoclip S1 Video showing rotation of uterine and tubal volume obtained by three-dimensional (3D) coded
contrast imaging hysterosalpingo-contrast sonography and how tubal course in 3D space can be better
evaluated.
Videoclip S2 Video showing automated reconstructed uterine volume in gray scale, with overlapping red
contrast media in Fallopian tubes.

Copyright  2012 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2013; 41: 328–335.

You might also like