Systematic Review

Gynecol Obstet Invest Received: May 28, 2019

Accepted after revision: January 2, 2020
DOI: 10.1159/000505689 Published online: January 22, 2020

Intraoperative Ultrasound during

Fertility-Sparing Surgery: A Systematic
Review and Practical Applications
Nicolas Galazis a Srdjan Saso a, b Flavia Sorbi a, c Benjamin Jones a, b
       

Chiara Landolfo a, d Maya Al-Memar a Jara Ben-Nagi e J. Richard Smith a, b

       

Joseph Yazbek a, b  

a Department of Gynaecologic Oncology, Queen Charlotte’s and Chelsea Hospital, Imperial College Healthcare
NHS Trust, London, UK; b Division of Surgery and Cancer, Institute of Reproductive and Developmental Biology,
 

Imperial College London, Hammersmith Hospital Campus, London, UK; c Department of Experimental, Clinical and
 

Biomedical Sciences, University of Florence, Obstetrics and Gynecology, Careggi University Hospital, Florence,
Italy; d Department of Development and Regeneration, KU Leuven, Leuven, Belgium; e Centre for Reproductive and
   

Genetic Health, London, UK

Keywords
Intraoperative · Ultrasound · Fertility sparing · Gynaecology
Abstract
Fertility-sparing surgery (FSS) is an established concept
within operative gynaecology. Intraoperative ultrasound
(IOUS) has the potential of assessing lesion margins, allow-
ing complete resection with minimal damage to the sur-
rounding healthy tissue and could potentially play a major
role in FSS for benign or malignant gynaecological patholo-
gies. In this paper, we review the current literature on the use
of IOUS in gynaecological FSS. We also propose technical
guidance on the IOUS during FSS. The findings of this review
demonstrate that IOUS can assist in the safe resection of dis-
ease with high rates of completion, low rates of recurrence
and without damage to the nearby healthy reproductive or-
gans. Improved training in transvaginal ultrasonography
and minimal access surgery are likely to facilitate the applica-
tion of IOUS in FSS. © 2020 S. Karger AG, Basel
Introduction
Fertility-sparing surgery (FSS) is an established con-
cept within operative gynaecology [1]. The concept was
first described in the 1980s with groups comparing clin-
ical outcomes of disease recurrence, survival and preg-
nancy rates in radical versus FSS for malignant ovarian
lesions [2]. It differs from standard surgery because of
its 2-fold aim: removing the diagnosed pathology and
preserving the patient’s fertility. Advancement in diag-
nostic and assisted reproductive technologies has made
fertility preservation a realistic outcome in cases of be-
nign and malignant gynaecological conditions [3]. In-
deed, expert ultrasound (US) and magnetic resonance
imaging assessments have the potential to enable clini-
cians in the appropriate selection of patients for FSS [4,
5].
The rise in maternal age observed in Western societies
renders fertility preservation an integral component in
the clinical management of women diagnosed with a
gynaecological malignancy [6]. This applies to appropri-
193.51.85.197 - 1/25/2020 11:56:12 AM

© 2020 S. Karger AG, Basel Dr. Nicolas Galazis

Department of Gynaecologic Oncology, Queen Charlotte’s and Chelsea Hospital
Imperial College Healthcare NHS Trust
E-Mail karger@karger.com
Du Cane Road, London W12 0NN (UK)
Université de Paris

www.karger.com/goi
Downloaded by:

E-Mail ngalazis @ gmail.com

 Conisation
ge IA1
FIGO sta

Cervical
cancer Radical trachelectomy OR neoadjuvant
FIGO stage IA
2-IB1, and tu chemotherapy ± conisation or simple
mour <2 cm
trachelectomy

Endometrial High dose medroxyprogesterone

cancer Complex atypical endometrial hyperplasia acetate
or FIGO stage IA
(<50% myometrial invasion)

Ovarian
USO, omentectomy, peritoneal biopsies
cancer FIGO stages IA or IC with unilateral
ovarian involvement

Borderline ovarian Ovarian cystectomy or USO omentectomy, peritoneal

tumours Either mucinous or serous biopsies

Improve menorrhagia: tranexamic acid,

mefenamic acid, progestogens including LIUS
ment
manage
Medical Reduce size: ulipristalacetate (MHRA safety
Uterine fibroids Interven alert 10), GnRH agonists
tional ra
diology
Surg UAE, radiofrequency ablation or HIFU
ical
man
age
men
t
Hysteroscopic, laparoscopic or open myomectomy

Improve menorrhagia: tranexamic acid,

t progestogens including LIUS
Medica l managemen
Endometriosis and Improve dysmenorrohoea: COCP, GnRH
adenomyosis Inter v agonists
ention
al rad
aden iology
omyo for
Sur sis
gic
al m UAE, radiofrequency ablation or HIFU
ana
gem
ent

Open or laparoscopic excision of disease

Fig. 1. FSS for gynaecological pathologies. USO, unilateral salpin- Products Regulatory Agency; HIFU, High-Intensity Focused Ul-
go-oophorectomy; UAE, uterine artery embolization; FIGO, In- trasound; COCP, Combined Oral Contraceptive Pill; GnRH, Go-
ternational Federation of Obstetrics and Gynecology; LIUS, Levo- nadotropin-releasing Hormone.
norgestrel Intrauterine System; MHRA, Medicines and Healthcare

ately-selected oncologic cases, including conisation or
trachelectomy for cervical cancer [7], endocrinological
management for endometrial cancer [8] and cystectomy
or unilateral salpingo-oophorectomy for invasive or bor-
derline ovarian tumours (BOT) [9, 10]. FSS also applies
to surgical management of benign disease such as uterine
fibroids, endometriosis and adenomyosis [11–13],
whereby novel techniques achieve excision of the benign
disease with minimal damage to healthy ­reproductive
tissue. The above are summarised in Figure 1.
US is a readily available and portable imaging modal-
ity [5]. In the United Kingdom, obstetrics and gynaecol-
193.51.85.197 - 1/25/2020 11:56:12 AM

2 Gynecol Obstet Invest Galazis/Saso/Sorbi/Jones/Landolfo/

DOI: 10.1159/000505689 Al-Memar/Ben-Nagi/Smith/Yazbek
Université de Paris
Downloaded by:
ogy (O&G) trainees are now required to complete various
competency modules before they complete their specialty
training, as per the recommendations of international US
societies [14–16]. The development of high-resolution
endovaginal probes and 3-dimensional imaging allows
detailed examination of the pelvic anatomy yielding high-
ly accurate results when used by experienced operators
[17]. An important advantage of gynaecological ultraso-
nography is that, as opposed to other specialties, it is per-
formed by gynaecologists who subsequently decide fur-
ther management plans, instead of radiologists.
Intraoperative US (IOUS) was first described in the
1960s in hepatobiliary surgery for the detection of gall
bladder and common bile duct stones during cholecys-
tectomy [18]. It is now well described in breast, vascular
and thyroid surgery [19, 20]. IOUS possesses a number of
advantages, including safety, high accuracy and ability to
guide procedures [21]. In gynaecology, some minor pro-
cedures have been carried out under US guidance include
egg collection in assisted reproduction technology, aspi-
ration of ovarian cysts or pelvic abscesses and suction
evacuation. However, IOUS is not widely applied when it
comes to more complex gynaecological procedures.
The aim of this study was to review the current litera-
ture on the use of IOUS in gynaecological FSS.
Methods
Search Strategy for the Identification of Eligible Studies
Institutional review board approval was not necessary as this
review did not require any patient identifying information. The
systematic search followed PRISMA guidelines [22]. A biblio-
graphic search of English language publications in 3 computerised
databases (PubMed, ScienceDirect and SciFinder) was conducted.
The search was augmented by a snowball strategy, examining the
references cited in primary sources and review manuscripts.
Study Selection
We reviewed studies where IOUS was used to perform FSS, de-
fined as surgery that aimed to treat a gynaecological pathology
whilst conserving either or both ovaries and the uterus. Minor sur-
gical procedures like US-guided surgical management of miscar-
riage or aspiration of ovarian cysts were excluded. Moreover, stud-
ies that described surgical procedures not strictly considered as FSS
but such that could achieve a favourable impact on the patient’s
fertility were included in this review. This applied to cases where
IOUS was used during hysteroscopic resection of polyps and fi-
broids. Finally, studies that utilised IOUS for radioablative proce-
dures such as high-frequency focused US or radiofrequency abla-
tion for fibroids or adenomyosis were not considered for this review
as they do not fall within the remits of standard gynaecologic surgi-
cal practice and are usually performed by interventional radiolo-
gists.
IOUS in FSS
Review articles were also excluded. Only studies published in
English, and in peer-reviewed journals, were considered. Because
of the scarcity of studies on this topic, any study design was deemed
suitable for consideration including nonrandomised and observa-
tional studies as well as case reports. Table 1 lists the search terms
used and the selection criteria for the literature search.
Study Screening and Data Extraction
After the initial search, a total of 3,182 records were screened
by the first author (N.G.) based on the inclusion and exclusion cri-
teria. This process was repeated independently by a second author
(S.S.). An overview of the search results and screening process is
summarized in the study flow diagram (Fig. 2). The screening pro-
cess was cross-checked by a senior author (J.Y.). The selected stud-
ies were examined, and relevant data were extracted for each paper
by the first author (N.G.), then cross-checked by the second author
(S.S.). The information selected included author details, year of
publication and country of the study, study aim, sample size, meth-
odology, outcome measures and conclusions. Tables 2–6 list the
main characteristics of the selected studies.
Outcomes of Interest and Methodological Quality Assessment
Outcomes of interest included operative times, length of stay,
intra- or post-operative complications, future pregnancy out-
comes and follow-up. When available, we identified methods used
in the studies to aid IOUS; for example, distending the urinary
bladder during hysteroscopic surgery for better sonographic eval-
uation of the uterine wall. The above is summarised in Tables 2–6.
Because of the scarcity of relevant studies, non-randomised studies
and case reports were also included for the review. For this reason,
formal methodological quality assessment of the selected studies
was not performed.
Results
Search Strategy and Study Selection
A total of 3,182 records were screened dating from 1990
to 2017. Following an initial screen, 2,814 studies were ex-
cluded from the title alone, and 368 abstracts were exam-
ined further. From those, 311 abstracts were excluded as
they were deemed irrelevant to the research question. Of
the 59 full text publications examined, 45 met the inclu-
sion criteria. Of the 14 studies that were excluded, 4 were
review or opinion articles, 6 were duplicate studies and 4
were unavailable in English. An overview of the search re-
sults and screening process is summarised in Figure 2.
Study Characteristics
The 45 studies involved a total of 2,473 women, 1,783
of that had IOUS-guided FSS while the remaining 667
women served as controls and either had laparoscopic
guidance (during hysteroscopic procedures) or no guid-
ance [23–67]. IOUS was applied in 5 different ways: (1)
transabdominal US (TAUS; n = 17; Table 2); (2) trans-
193.51.85.197 - 1/25/2020 11:56:12 AM
Gynecol Obstet Invest 3
DOI: 10.1159/000505689
Université de Paris
Downloaded by:
Table 1. Search and selection strategy for the systematic review of IOUS in benign and FSS

Databases searched PubMed, ScienceDirect, SciFinder

Search keywords [Ultrasound-guided OR intraoperative ultrasound] AND [fertility-sparing surgery]

[Ultrasound-guided OR intraoperative ultrasound] AND [surgery]
[Ultrasound-guided OR intraoperative ultrasound] AND [gynaecology]
[Ultrasound-guided OR intraoperative ultrasound] AND [laparoscopy]
[Ultrasound-guided OR intraoperative ultrasound] AND [hysteroscopy]
[Ultrasound-guided OR intraoperative ultrasound] AND [ovarian cyst/cancer]
[Ultrasound-guided OR intraoperative ultrasound] AND [endometrial hyperplasia/cancer]
[Ultrasound-guided OR intraoperative ultrasound] AND [endometriosis]
[Ultrasound-guided OR intraoperative ultrasound] AND [adenomyosis]
[Ultrasound-guided OR intraoperative ultrasound] AND [leiomyoma/fibroids]
[Ultrasound-guided OR intraoperative ultrasound] AND [Ashermans/synechiae]
[Ultrasound-guided OR intraoperative ultrasound] AND [metroplasty]
[Ultrasound-guided OR intraoperative ultrasound] AND [hydatiform mole/gestational trophoblastic disease]
[Ultrasound-guided OR intraoperative ultrasound] AND [scar/cervical/cornual ectopic pregnancy]
Other sources Additional studies were identified through references of included studies and reviews
Inclusion criteria IOUS in ablative or excisional gynaecological surgery achieving fertility preservation
IOUS in ablative or excisional gynaecological surgery that improves patient outcomes, for example,
fertility potential, hospital stay, complications
Articles written in English and published in peer-reviewed journals
Any study including randomised, non-randomised and case-control studies and case reports/series
Exclusion criteria Papers not in English
Full articles not available
IOUS in non-gynaecological surgery
IOUS in minor gynaecological procedures not involving ablative or excisional surgery for example,
aspiration of adnexal masses, oocyte collection, retrieval of intra-uterine objects
Other minor procedures where IOUS is well established, for example, for termination of pregnancy or
surgical management of miscarriage

IOUS, intraoperative ultrasound; FSS, fertility-sparing gynaecological surgery.

vaginal US (TVUS; n = 12; Table 3); (3) laparoscopic US Findings

(LUS; n = 9; Table 4); (4) transrectal US (TRUS; n = 5;
Table 5) and (5) contact US (CUS) during open surgery
(n = 3; Table 6).
A wide range of gynaecological pathologies were treat-
ed using IOUS: (1) Müllerian duct anomalies (n = 13); (2)
benign or BOT managed laparoscopically (n = 10); (3)
benign ovarian cysts excised during vaginal surgery (n =
5); (4) submucous fibroids (n = 6); (5) ectopic pregnan-
cies (n = 6); (6) uterine synechiae (n = 4); (7) adenomyo-
sis (n = 2); (8) endometrial polyps (n = 1); (9) endome-
trial osseous metaplasia (n = 1); (10) pelvic adhesions (n =
1); (11) placental site trophoblastic tumour (n = 1). FSS
was performed through 5 different routes: (1) hystero-
scopically (n = 18); (2) laparoscopically (n = 15); (3) tran-
scervically without hysteroscopy (n = 5); (4) vaginally
(n = 5) and (5) open surgery (n = 3).
More details on the above are shown in Tables 2–6.
Of the 18 articles of IOUS during hysteroscopic sur-
gery, 13 used TAUS, 4 TRUS, one TVUS and one LUS for
a total of 567 patients. IOUS demonstrated 100% resec-
tion rate with regular endometrial cavity at follow-up for
hysteroscopic metroplasty of uterine septum in 3 studies
[23–25]. One study comparing hysteroscopic metroplas-
ty for uterine septum with and without US guidance
showed complete resection in 85 and 73% of cases, re-
spectively, but the difference was not statistically signifi-
cant [26]. In the same study, there were 2 cases of uterine
perforations when US was not used against none in the
US group [26]. IOUS during hysteroscopic resection of
fibroids revealed 100% successful completion of the pro-
cedure in one study involving 64 patients [27]. Another
study investigating hysteroscopic resection of fibroids of
120 patients demonstrated a significant difference in the
one-step completion rate between IOUS and no US guid-
193.51.85.197 - 1/25/2020 11:56:12 AM

4 Gynecol Obstet Invest Galazis/Saso/Sorbi/Jones/Landolfo/

DOI: 10.1159/000505689 Al-Memar/Ben-Nagi/Smith/Yazbek
Université de Paris
Downloaded by:
 Search results on PubMed = 2,123
Search results on ScienceDirect = 446
Search results on SciFinder = 614
Total number (n = 3,183) potentially relevant records

79 abstracts were unavailable

Title (n = 3,183)
217 were not in English
Number excluded based on title alone
186 were duplicate studies
(n = 2,814)
2,332 were irrelevant studies

Abstract (n = 369) 54 were not in English

Number excluded after reading abstract 89 were duplicate studies
(n = 316) 173 were irrelevant studied

Number included after including

references found from relevant papers
(n = 6)

Full text articles excluded with

Full texts (n = 59) reasons (n = 14)
number of full texts reviewed 4 texts were not available in English
6 were duplicate studies
4 were reviews or opinion articles

Studies included in systematic review

(n = 45)
Fig. 2. Flow chart of the study selection.
*  One study used both TAUS and TRUS.
TAUS, trans-abdominal ultrasound; TVUS,
TAUS TVUS LUS TRUS CUS
trans-vaginal ultrasound; LUS, laparoscop- (n = 17)* (n = 12) (n = 9) (n = 5)* (n = 3)
ic ultrasound; TRUS, trans-rectal ultra-
sound; CUS, contact ultrasound.

ance (91 vs. 72%, p = 0.02) [28]. In this prospective cohort
study, TRUS was used to guide hysteroscopic resection of
single symptomatic fibroids. Completion rate was as-
sessed 4–8 weeks later by TVUS or diagnostic hysteros-
copy [28].
Three studies directly compared IOUS to laparoscopic
guidance during hysteroscopic surgery [29–31]. TAUS
was used to guide hysteroscopic resection aiming to mi-
nimise potential complications including uterine perfo-
ration and achieve complete restoration of the endome-
trial anatomy [29–31]. All 3 studies demonstrated no dif-
ference in the complication rates between the 2 groups
but reported significantly lower costs associated with
IOUS when compared to laparoscopic guidance [29–31].
One study found a significant difference in the incidence
of post-operative septum at follow-up favouring the
IOUS group [31].
In terms of fertility outcomes, a study investigating 4
patients with subfertility secondary to uterine synechiae
reported subsequent successful pregnancies in all patients
(3 after IVF and one after spontaneous conception) [32].
Another study investigating 34 patients with primary
subfertility due to uterine septum reported 14 spontane-
ous conceptions resulting in 13 term deliveries after hys-
teroscopic resection with IOUS [33]. The same study in-
vestigated 59 patients with history of recurrent miscar-
riages secondary to uterine septum and reported a reduced
miscarriage rate (24.5%) after hysteroscopic resection
with IOUS [33]. Finally, Querleu et al. [34] showed that 8
out of 12 patients with a history of recurrent miscarriage
secondary to uterine septum achieved live deliveries after
US-guided hysteroscopic resection.
Of the 15 articles of IOUS during laparoscopic surgery,
9 used LUS and 6 TVUS for a total of 229 patients. IOUS
was performed trans-vaginally in 5 studies guiding ovar-
ian-preserving surgery; in 2 studies for the management
of recurrent BOT [35, 36]. In these cases, the pelvis was
instilled with saline solution which acted as a sonograph-
193.51.85.197 - 1/25/2020 11:56:12 AM

IOUS in FSS Gynecol Obstet Invest 5

DOI: 10.1159/000505689
Université de Paris
Downloaded by:
 6
Table 2. Main characteristics of studies using intra-operative TAUS
Author/year of
publication, institution
and country of origin
Wang et al.
[25], 2009,
Zhejiang University,
China
Gynecol Obstet Invest
DOI: 10.1159/000505689
Mullesserill et al.
[24], 2003,
Department of Obstetrics
and Gynecology,
Mayo Clinic, USA
Querleu et al. [34], 1990,
University Clinic of
Obstetrics and Gynecology,
Pavillon Paul Gellé, France
Ohl and Bettahar-Lebugle.
[33], 1996,
Obstetrics and Gynaecology
Service, Strasbourg, France
Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
Aim of Study Pathology Surgical Outcome measures and results Conclusions
study design treated, N intervention, N
To determine the Prospective Patients with complete Hysteroscopic resection of Operative time: 25–45’ (mean 38.2’), Procedure has
safety and efficacy observational uterine septum and septum under TAUS- All septa successfully resected, improved anatomical
of complete septum study cervical duplication guidance (25) follow-up TVUS showed regular and functional
resection under presenting with Continuous irrigating flow endometrial cavity outcomes, no
US-guidance sub-fertility and of 5% glucose during Of the 13 patients with recurrent complications could
recurrent hysteroscopy for uterine miscarriages, 10 wished to get pregnant reduce the need for
miscarriage (25) distension at inflow pressure post procedure. All achieved concurrent laparoscopy
of 70–100 mm Hg spontaneous conception and only
Bladder was half-full for better 1 had a miscarriage
sonographic visualisation Of the 9 patients with primary
infertility, 6 wished to get pregnant
post procedure, 2 achieved pregnancy
(1 spontaneously, 1 after IVF) with
3 total pregnancies. One ended with a
miscarriage, 1 achieved a term
delivery and 1 was ongoing.
Of the 3 patients with secondary
infertility, 2 wished to get pregnant
post procedure, 1 had spontaneous
conception which was ongoing
Hysteroscopic Case report A patient with Septal resection under US few months after procedure US-guided resection
resection of uterine complete uterine TAUS guidance (1) revealed an arcuate endometrial aids the surgeon to
septum septum experiencing Urinary bladder distended to cavity enter the contralateral
recurrent aid sonographic visualisation uterine cavity and
miscarriages (1) resect the septum
To evaluate the Retrospective Patients with Septal resection under 15/24 had 3rd trimester deliveries, The procedure is short,
use of hysteroscopic case series uterine septum (24) TAUS guidance (24) Of the 12 patients with recurrent safe, requires no special
resection of uterine Urinary bladder distended to miscarriage, 10 had pregnancies equipment, and does
septum under TAUS aid sonographic. beyond 2nd trimester and 8 had not necessitate
guidance visualisation live deliveries concomitant
laparoscopy
To evaluate the Retrospective 93 patients with Septal resection under Post-operative US: 52.8% normal TAUS-guided
use of hysteroscopic case series uterine septum TAUS guidance (93) uterine cavity, 47.2% arcuate uterus. approach allows easy
resection of uterine suffering from Urinary bladder distended to 8% needed repeat resection, estimation of fundal
septum under TAUS recurrent miscarriage aid sonographic. In patients with previous recurrent thickness and
guidance (59) or subfertility (34). visualisation miscarriages who fell pregnant, avoidance of costly
Total septum (10) 24.5% miscarriage rate versus equipement including
Septum extending 78% before resection. concomitant
2/3 of cavity (34), 62.3% pregnancies reached term laparoscopy
Septum extending versus 5.7% before resection.
1/2 of cavity (33), In 34 patients with primary subfertility,
Septum extending 14 fell pregnant and 13 had a term
1/3 of cavity (16) delivery
 Table 2. (continued)

Author/year of Aim of Study Pathology Surgical Outcome measures and results Conclusions
publication, institution study design treated, N intervention, N

IOUS in FSS
and country of origin

Kresowik et al. To compare costs Retrospective Uterine septum (100), Hysteroscopic resection Uterine perforation rate: 8.7% in TAUS-guided
[30], 2012, and complications cohort study Synechiae (53), of uterine septum and laparoscopic guidance versus hysteroscopic surgery
University of Iowa between US-guided Other (6) synechiae with 1.9% with TAUS guidance (p = 0.12) for synechiae and
Carver College of hysteroscopy, laparoscopic guidance and 5.3% without guidance (p = 0.41) uterine septum is
Medicine, USA hysteroscopy alone (69) versus TAUS Cost comparison: laparoscopic superior to
and laparoscopy- guidance (52) versus no guidance was significantly more laparoscopic guidance
guided hysteroscopy guidance (38) compared to TAUS guidance or no guidance
for uterine septa and TAUS performed by a (p < 0.001), no significant difference
synechiae gynaecologic sonographer in costs between TAUS guidance
and bladder was filled and no guidance
where necessary for
better visualisation
Coccia et al. Hysteroscopic Case report A patient with Hysteroscopic resection TVUS a month later showed normal US-guided
[23], 1996, resection of endometrial of osseous metaplasia with endometrium, no complications hysteroscopic resection
Department of endometrial osseous metaplasia (1) TAUS and TRUS reported offers a less invasive
Obstetrics osseous metaplasia guidance (1) and costly alternative,
and Gynecology, could prevent
University of subsequent
Florence, Italy hysterectomy
Coccia et al. To evaluate the Prospective Patients with uterine TAUS-guided No re-intervention in TAUS group TAUS guidance for
[29], 2000, efficacy and safety comparative septum or submucous hysteroscopic resection versus 4 required further intervention hysteroscopic surgery
Department of Obstetrics of TAUS guidance study fibroids (81) compared of septum or fibroids (81) in laparoscopy group for the is effective and safe
and Gynecology, University compared to to historical control versus above under treatment of uterine septa
of Florence, Italy laparoscopic group with same laparoscopic guidance (45)
monitoring during operation under Urinary bladder distended No complications in either groups.
hysteroscopic laparoscopic with three-way catheter No need to convert to laparoscopy
resection of septum or guidance (45) to aid sonographic in TAUS group
submucous fibroids visualisation

Gynecol Obstet Invest

Song et al. To evaluate the use Retrospecive Patients with uterine TAUS-guided Successful entry and adhesiolysis US-guided

DOI: 10.1159/000505689
[65], 2016, of TAUS guidance case series synechiae with hysteroscopic in all 5 cases hysteroscopic
Fuxing Hospital, in hysteroscopic previous false adhesiolysis (5) Of the 3 patients who wished to adhesiolysis is safe and
Capital Medical management of passage (5) conceive, 2 fell pregnant (1 IVF and recommended in cases
University, China uterine synechiae delivered by Caesarean and 1 with extensive uterine
with a previous false spontaneous conception who synechiae
passage delivered vaginally)
Tsui et al. To evaluate the use Retrospective Patients with TAUS-guided hysteroscopic All 4 conceived post treatment (3 via TAUS guided
[32], 2014, of TAUS guidance case series subfertility adhesiolysis (4) IVF and 1 spontaneously), 2 went to hysteroscopic
Kaohsiung General in hysteroscopic due to severe uterine Urinary bladder distended to full term and had caesarean delivery adhesiolysis was part of
Hospital, Taiwan management of synechiae (4) aid sonographic. a comprehensive
uterine synechiae visualisation management regime
that proved successful

7
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
 8
Table 2. (continued)
Author/year of
publication, institution
and country of origin
Vigoureux et al.
[26], 2016,
Bicetre University
Hospital, France
Zhang et al.
[30], 2015,
Gynecol Obstet Invest
The Third Affiliated
DOI: 10.1159/000505689
Hospital of SunYat-Sen
University, China
Pakrashi et al.
[63], 2013,
Department of Obstetrics
and gynecology, Eastern
Virginia Medical
School, USA
Korkmazer et al.
[26], 2016,
Bursa Sevket Yilmaz
research and Training
Hospital, Turkey
Faschingbauer et al.
[47], 2011,
Department of Gynecology
and Obstetrics, Erlangen
University Hospital, Germany
Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
Aim of Study Pathology Surgical Outcome measures and results Conclusions
study design treated, N intervention, N
To compare rates of Retrospective Patients with complete TAUS-guided Persistent septum (>10 mm) after TAUS guided
re-intervention and observational or partial septum, with hysteroscopic metroplasty metroplasty noted in 17 patients in hysteroscopic
immediate and later cohort study history of recurrent (46) versus the above unguided group versus 7 patients adhesiolysis seems to
complications between miscarriage, subfertility without US guidance (62) in US-guided group (39 vs. 18.4% reduce rates of
TAUS-guided versus or dysmenorrhoea (108) TAUS performed by respectively, p = 0.4) re-intervention and
unguided qualified gynaecologist. 2 uterine perforations in unguided complications
hysteroscopic Urinary bladder distended to group, nil in guided group
metroplasty aid sonographic. visualisation
To compare the Prospective Patients with complete TAUS-guided hysteroscopic US group, Significantly less: operating Both techniques are
effects of TAUS comparative or partial septum (126) metroplasty (70) versus the time, first time to get out of bed, safe and effective.
guidance versus study laparoscopic-guided hospital stay, incidence of TAUS-guided
laparoscopic hysteroscopic metroplasty postoperative septum residue technique is more
guidance for (62) compared to laparoscopy group simple, economical and
hysteroscopic Urinary bladder distended No differences in complications or accurate and less
metroplasty to aid sonographic subsequent pregnancy rates invasive
visualisation between each group
TAUS-guided Case report A patient with 2 Hysteroscopic morcellation Uncomplicated procedure and TAUS-guidance can
hysteroscopic type II submucous of fibroids under TAUS ensured completion of surgery provide reassurance of
morcellation of fibroids (1) guidance (1) completion of surgery
submucous fibroids
To evaluate the Multicentre Patients with Hysteroscopic myomectomy Mean operation time: 42±7’, fluid TAUS-guided
usefulness of TAUS prospective symptomatic under TAUS-guidance (64) deficit 300–1,000 mL (mean 500 mL), hysteroscopic
guidance in pilot study submucous type I estimated blood loss 50–200 mL myomectomy seems to
hysteroscopic and II fibroids (64) (mean 80 mL), be a safe and effective
myomectomy of No uterine perforation or other method for resection of
Type I and II complications occurred type I and II fibroids
submucous fibroids Procedure completed successfully
in all cases
61/64 (95.5%) discharged within
12 h of admission
3 cases stayed overnight to monitor
blood loss
Office hysteroscopy in 3 months
revealed mild intra-uterine synechiae
in 10/67 (15.6%) of cases. No remnant
fibroids detected
TAUS guidance for Case report A patient with TAUS-guided suction Successful treatment with no intra- TAUS guidance
the management of cervical heterotopic curettage of cervical ectopic or post-operative complications. allowed selective
cervical heterotopic pregnancy (1) pregnancy (1) Intrauterine pregnancy progressed termination of the
pregnancy Urinary bladder distended to uneventfully ectopic with
aid sonographic visualisation conservation of the
viable intrauterine
pregnancy
 Table 2. (continued)

Author/year of Aim of Study Pathology Surgical Outcome measures and results Conclusions
publication, institution study design treated, N intervention, N

IOUS in FSS
and country of origin

Morgan et al. TAUS-guided Case report A patient diagnosed TAUS-guided curettage of No postoperative complications. Corneal ectopic
[45], 2008, curettage of cornual of cornual ectopic cornual ectopic pregnancy Complete excision of cornual ectopic pregnancies can be
Queen Elizabeth II ectopic pregnancy pregnancy (1) (1) pregnancy was achieved managed
Hospital, UK transcervically under
TAUS guidance
Ma et al. To evaluate the Retrospective Patients undergoing TAUS- guided insertion of TAUS group: No complication TAUS-guided vaginal
[48], 2011, feasibility and value of comparison THL suffering from trocar needle in posterior arising from trocar insertion or access increases the
Centre for Reproductive TAUS guided access study subfertility with fornix (29) versus insertion operative procedure safety of THL
Medicine, Peking University for THL either inconclusive without TAUS guidance Non-TAUS group: 3 bowel
Third Hospital, China hysterosalpingogram or (162) perforations,1 uterine injury and
for ovarian drilling for Urinary bladder distended 2 cases of retroperitoneal fluid
clomiphene resistant to aid sonographic. collection
PCOS (191) visualisation
Qiu et al. To compare patient Retrospective Patients with caesarean TAUS- guided curettage of TAUS versus hysteroscopy group: Both methods have
[66], 2019, outcomes after D&C comparison scar ectopic being scar ectopic (39) versus D&C Success of procedure: 84.5 vs. 95.7%, good clinical
Department of Gynecologic with TAUS guidance study treated with UAE and and hysteroscopy (23) p = 0.243 outcomes
Oncology, Zhejiang versus hysteroscopic subsequently having Mean intraoperative blood loss: Hysteroscopy had less
University, China guidance after UAE of D&C, either with 59 vs. 29 mL, p = 0.042 complications and had
caesarean scar ectropic US guidance or Diagnosis of diverticulum: the advantage of
pregnancy hysteroscopicalluy 5.1 vs. 60.9%, p < 0.001 discovering potential
Duration of hospitalisation: diverticulum
10 vs. 8.6 h, p = 0.042
Overall complications: 48.7 vs.
21.7%, p = 0.035

TAUS, trans-abdominal ultrasound; N, number of participants; TVUS, transvaginal ultrasound; TRUS, transrectal ultrasound; THL, transvaginal hydrolaparoscopy; IVF, in-vitro fertilisation; D&C,
dilatation and curettage; UAE, uterine artery embilisation.

Gynecol Obstet Invest

DOI: 10.1159/000505689
9
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
 10
Table 3. Main characteristics of studies using intra-operative TVUS

Author/year of Aim of study Study design Pathology treated, N Surgical Outcome measures Conclusions
publication, intervention, N and results
institution and
country of origin

Casadio et al. To evaluate the Prospective Patients with type II Hysteroscopic Operating time 23–43’ (median Complete hysteroscopic
[60], 2011, feasibility of observational submucous fibroids (13) myomectomy with 25’), fluid deficit 550–950 mL myomectomy of type II submucous
Orsola Malpighi hysteroscopic resection study TVUS evaluation of (median 750 mL), all discharged fibroids can be performed
University Hospital, of type II submucous myometrial free margin within 12 h of admission successfully and safely with TVUS
Italy fibroids before and during Procedure completed surveillance
procedure (13) successfully in all cases
Distension of uterine No intra- or post-operative
cavity with saline complications reported
solution for optimal
sonographic evaluation

Gynecol Obstet Invest

DOI: 10.1159/000505689
Lee et al. To investigate the Prospective Patients with Polypectomy with Operating time: 3–34’ Technique is feasible and may
[58], 2006, feasibility of endometrial observational endometrial polyps (37) TVUS guidance, (mean 8’), procedure was reduce costs associated with
King’s College polypectomy under study without hysteroscopy (37) successful in 32 cases hysteroscopic polypectomy
Hospital, United TVUS-guidance without Safe T ChoiceTM (86.5%), failure in 3 cases (8.1%)
Kingdom hysteroscopy which allows TVUS because of inability
probe to be attached to obtain satisfactory images of
to a cervical tenaculum the uterine cavity,
10 mL of saline solution in remaining 2 cases,
instilled thorough failure to grasp the polyp
the cervix for optimal (5.4%)
sonographic evaluation Hysteroscopy was
performed in all 5 cases
to remove polyps
No other complications
Jones et al. TVUS-guided Case report A patient with 8 mm Intraoperative TVUS Procedure performed TVUS-guided laparoscopic wedge
[57], 2017, laparoscopic ovarian dermoid cyst presenting during laparoscopic successfully, no cyst resection is recommended in cases
Imperial College wedge resection in a with acute psychotic wedge resection of spillage, histology where ovarian cyst is too small to
London, United case of anti-NMDA episode and positive affected ovary (1) confirmed mature cystic be detected macroscopically during
Kingdom receptor encephalitis NMDAr antibodies (1) 500 mL of saline solution teratoma with an intact laparoscopy
instilled in the pelvis capsule. No intraoperative
for optimal sonographic complications
evaluation
Jones et al. TVUS-guided Case report A patient with previous Intraoperative TVUS Successful fertility TVUS-guided laparoscopic wedge
[35], 2017, laparoscopic ovarian sBOT treated with during laparoscopic preservation surgery, resection is recommended in cases
Imperial College wedge resection in a cystectomy followed by wedge resection of Normal anti-Mullerian where ovarian cyst is too small to
London, United case of recurrent sBOT oophorectomy, presenting affected ovary (1) hormone concentration be detected laparoscopically, at the
Kingdom with recurrence on 500 mL of saline solution post operatively same time, preserving fertility
contralateral side (1) instilled in the pelvis potential
for optimal sonographic
evaluation

Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
 Table 3. (continued)

Author/year of Aim of study Study design Pathology treated, N Surgical Outcome measures Conclusions
publication, intervention, N and results

IOUS in FSS
institution and
country of origin

Jones et al. To demonstrate the Prospective Patients with recurrent Intraoperative TVUS Ovarian wedge resections Continuous intraoperative TVUS
[36], 2017, use of TVUS-guided cohort study sBOT (7) during laparoscopic performed successfully can be used to facilitate complete
Imperial College ovarian wedge resection wedge resection of with no complications. tumour excision in recurrent sBOT
London, UK in the treatment of affected ovary (7) 1/7 had a third recurrence, with fertility preservation
sBOT that are too small 500 mL of saline solution underwent cryopreservation
to be visualised instilled in the pelvis for after operation and stored 6
laparoscopically optimal sonographic embryos, prior to completion
evaluation surgery. She fell pregnan
but miscarried
3 out of 7 wished to conceive
but not successfully at the
time of article submission
Lipitz et al. To assess the use of Case series Patients with ovarian TVUS guidance during TVUS allowed localisation In selected cases, laparoscopic
[37], 1996, TVUS guidance in cysts and extensive laparoscopic ovarian of ovarian cysts and expedite surgeons should be aware of the
Chaim Sheba operative laparoscopy intrapelvic adhesions (5) cystectomy (5) procedure, avoiding damage feasibility and possible benefits of
Medical Center, 500 mL of saline solution to adjacent pelvic structures. the use of simultaneous IOUS
Tel Hashomer, instilled in the pelvis for In one case, identification of
Israel optimal sonographic ovarian cyst facilitated
evaluation decision to resort to laparotomy
Badiglian-Filho et al. TVUS guidance in Case report A patient with small TVUS guidance during TVUS allowed localisation of A simple, safe and efficient
[59], 2012, laparoscopic treatment dermoid cyst undergoing laparoscopic ovarian small dermoid cyst and technique
Hospital AC of dermoid cyst laparoscopic ovarian cystectomy (1) allowed fertility sparing surgery
Camargo, Brazil cystectomy (1) 500 mL of saline solution
instilled in the pelvis for
optimal sonographic
evaluation
Nabeshima et al. TVUS guided Case report A patient with cystic TVUS-guided laparoscopic Total excision of disease TVUS guidance allowed successful

Gynecol Obstet Invest

[43], 2003, laparoscopic resection adenomyosis suffering resection of lesion (1) achieved. No complications. minimal access fertility sparing

DOI: 10.1159/000505689
Tohoku University of cystic adenomyoma from dysmenorrhoea (1) 500 mL of saline solution Patient’s symptoms resolved surgery
Graduate School of instilled in the pelvis for
Medicine, Japan optimal sonographic
evaluation
Tanaka et al. To evaluate the Retrospective Patients with benign TVUS-guided incision of Operating time: 74–129’ A safe minimally invasive option of
[53], 2012, feasibility of comparison ovarian cysts (75); posterior fornix during (mean 95’) in vaginal group benign ovarian cystectomy
Kanazawa transvaginal ovarian study Vaginal approach (35) vaginal ovarian cystectomy versus 96–140’ (mean 120)
University, Japan cystectomy versus laparoscopic (35) versus standard in standard laparoscopy
approach (40) laparoscopy (40) group (p = 0.15)
TVUS probe with a needle One case of vaginal ovarian
guide attached to it cystectomy had to be converted
to laparoscopy because of
excessive bleeding
No major complications in
either groups including bowel
injury or conversion to
laparotomy

11
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
 12
Table 3. (continued)

Author/year of Aim of study Study design Pathology treated, N Surgical Outcome measures Conclusions
publication, intervention, N and results
institution and
country of origin

Tanaka et al. To evaluate the Retrospective Patients with benign TVUS-guided culdotomy, TVUS guided procedure was TVUS guidance of culdotomy is
[51], 2008, feasibility of TVUS- cohort study ovarian cysts, at least puncture of ovarian cyst successful in 15 out 16 cases safe, reliable and effective method
Kanazawa guided culdotomy using one of them found to be and insertion of guide (94%) for removal of benign ovarian cysts
University, Japan a renal balloon dilator in Pouch of Douglas wire in ovarian cysts (16) Operating time of culdotomy: via a vaginal approach
catheter for transvaginal during pre-operative TVUS probe with a needle mean 22’ (SD 11’) with blood
ovarian cystectomy TVUS (16) guide attached to it loss <10 mL
No bowel or other
complications recorded
Tanaka et al. A novel culdotomy Case series Patients with benign TVUS guidance for Successful culdotomy The method is safe and effective for

Gynecol Obstet Invest

[52], 2009, technique using TVUS ovarian cysts (4) peritoneal access through achieved in all cases vaginal entry in the peritoneal

DOI: 10.1159/000505689
Kanazawa guidance the cul-de-sac (5) Operating time for cavity
University, Japan 300 mL of saline infused in culdotomy was <10’
pelvic cavity though the Blood loss was <10 mL
cervix, uterus and fallopian No bowel injury or any
tubes pelvis for optimal other complications reported
sonographic evaluation
TVUS probe attached to a
needle guide was used
Tanaka et al. To evaluate the Prospective Patients with unilateral TVUS guidance for Culdotomy was successfully This method of entry in the
[50], 2011, feasibility of an US-guided cohort study benign ovarian cysts culdotomy and cyst performed in all cases peritoneal cavity is safe, simple and
Kanazawa cludotomy using a newly (35) and a patient with puncture (36) Operating time for reliable
University, Japan developed umbrella needle bilateral cysts (1) TVUS probe with a needle culdotomy was <10’
guide attached to it Blood loss was <10 mL
No bowel injury or any other
complications reported

N, number of participants; sBOT, serous borderline ovarian tumour; NMDAr, N-methyl D-aspartate receptor; MSP, modified strassman procedure; PSTT, placental site trophoblastic tumour;
TVUS, trans-vaginal ultrasound.

Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
 Table 4. Main characteristics of studies using intra-operative LUS

Author/year of Aim of study Study design Pathology treated, N Surgical Outcome measures Conclusions
publication, institution intervention, N and results

IOUS in FSS
and country of origin

Letterie and Marshall To evaluate Prospective Patients undergoing LUS during Operative time was LUS is useful in monitoring
[38], 2000, the use of LUS in observational ovarian cystectomies (14), hysteroscopic comparable to that of complex intra-uterine
Virginia Mason adnexal and study Patients undergoing and laparoscopic conventional techniques operative procedures
Medical Center, USA hysteroscopic hysteroscopic surgery for surgery (24) LUS is useful in localisation of
surgery synechiae, submucous No complications and incision placement of
fibroids or resection of reported ovarian cysts not obvious on
uterine septum (10) gross inspection
No pelvic or intra-uterine
abnormalities were
detected other than those
noted pre-operatively by
TVUS
Yang et al. To compare Prospective Patients with adnexal Pre-op assessment with Accuracy of LUS in the LUS is superior to TVUS in
[39], 1998, LUS versus case-control masses (58) TVUS versus characterisation of lesions was evaluation of residual
Prince of Wales TVS in the study intraoperative 83.8 vs. 73.5% in the pre-op ovarian tissue in the
Hospital, Hong Kong evaluation of assessment of adnexal TVUS group (p < 0.05), affected ovary which may help
adnexal masses lesions with LUS (58) LUS greater morphologic in surgical planning between
Performed by a radiologist, detail than TVUS, cystectomy and oophorectomy
500 mL of saline was instilled LUS demonstrated the LUS allows more precise
in the peritoneal cavity to presence of residual ovarian morphologic characterisation
optimise sonographic tissue in the affected side in of internal architecture and
visualisation 76.5% of cases versus 59.4% in histologic diagnosis of adnexal
the TVUS group (p < 0.005) lesions
Helin and Kirkinen To evaluate Prospective Patients with benign LUS guidance for LUS allowed 34/40 Diagnostic accuracy in LUS is
[40], 2000, University the usefulness cohort study ovarian masses (40) identifying and treating correct diagnosis versus 27/40 better than in TVUS. LUS
of Kuopio, Finland of LUS in the benign ovarian in pre-operative TVUS facilitates exact tumour
management masses (40) localisation and can be useful
of benign ovarian Saline was instilled in the in confirming the
tumours abdomen for optimal radicality of operation

Gynecol Obstet Invest

sonographic visualisation

DOI: 10.1159/000505689
Nabeshima et al. LUS for Case report A patient with cystic LUS-guided excision of adeno- Complete excision Total laparoscopic
[42], 2008, excision of adenomyosis and severe myosis (1) performed resection of cystic
Iwate Prefectural cystic dysmenorrhoea (1) Saline was instilled in and resolution of signs adenomyoma was achieved
Iwai Hospital, Japan adenomyosis the abdomen for optimal and symptoms achieved which eliminated the patient’s
sonographic visualisation severe signs and symptoms
Gong et al. To explore the Retrospective 40 patients: LUS guidance during LUS facilitates ability to LUS guidance provides a safer
[41], 2015, clinical value of group analysis Fibroids (25), gynaecological surgery (40) find residual lesions and and more valuable assistance
First Affiliated LUS in Uterine septa (4), Gynaecologist operated allows their accurate for clinical application in
Hospital of gynaecologic Endometriomas (4), LUS with the coordination diagnosis, provides guidance laparoscopic gynaecological
Shenzhen laparoscopic Ruptured Ectopic of a sonographer Saline was for their removal and surgery that are superior to
University, China surgery pregnancy (3), instilled in the abdomen for eliminates their recurrence TAUS and TVUS
Pelvic adhesions (2) optimal sonographic
Small nodules visualisation
for biopsy (2)

13
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
 14
Table 4. (continued)

Author/year of Aim of study Study design Pathology treated, N Surgical Outcome measures Conclusions
publication, institution intervention, N and results
and country of origin

Li et al. To explore the Retrospective Patients undergoing LUS guidance for Leiomyoma recurrence LUS guidance in
[44], 2016, value of LUS randomised myomectomy (156): myomectomy (57) rate of LUS group was myomectomy could reduce the
Capital Medical guidance in group analysis LUS guided (57), Saline was instilled in significantly less compared to residual and recurrence rate of
University, China myomectomy laparoscopy (54), the abdomen for optimal laparoscopy and open uterine fibroids
open resection (45) sonographic visualisation resection groups (p < 0.01)
Residual rate of LUS group
was lower than that of
laparoscopic group (p < 0.05),
but no significant difference
when compared to the open
resection group

Gynecol Obstet Invest

DOI: 10.1159/000505689
Lin et al. To evaluate Case report A patient with secondary LUS to identify fibroid LUS allowed accurate LUS guidance can be
[45], 2004, LUS for the infertility found to have a for laparoscopic hysterotomy incision helpful in the excision of
University of isolation of a fibroid 3 cm in diameter excision (1) and successful moderate size fibroids within a
Washington fibroid for with intramural and reconstruction of the uterus of normal contour
School of Medicine, surgical submucous uterus during laparoscopy
USA excision components (1)
Kumakiri et al. LUS guidance Case report A patient 5 weeks LUS for the excision of No postoperative LUS allowed precise
[62], 2005, for laparoscopic pregnant with an interstitial ectopic complications. Complete detection of interstitial ectopic
Juntendo University management of interstitial ectopic pregnancy (1) excision of ectopic and allowed
School of Medicine, interstitial ectopic pregnancy and a large pregnancy was achieved minimally invasive fertility
Japan Juntendo pregnancy adenomyotic uterus (1) sparing surgery
University School of
Medicine
Mascilini et al. LUS for the Case report A patient with recurrent LUS for the excision LUS allowed identification LUS allows identification of
[66], 2019, management of serous BOT not visible of a small serous BOT and excision of the small small lesions and confirms
Gemelli University recurrent serous laparoscopically serous BOT which was complete excision of the
Hospital, Rome, BOT otherwise not visible during disease
Italy laparoscopy
IOUS also allowed
confirmation of absence of
residual disease after excision

LUS, laparoscopic ultrasound; TVUS, trans-vaginal US; BOT, borderline ovarian tumours; IOUS, intra-operative ultrasound.

Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Downloaded by:
Université de Paris
193.51.85.197 - 1/25/2020 11:56:12 AM
Table 5. Main characteristics of studies using intra-operative TRUS

Author/year of Aim of study Study design Patholog Surgical Outcome measures Conclusions
publication, treated, N intervention, N and results
institution and
country of origin

Ludwin et al. Treatment of Case report A patient suffering TRUS during No more dysmenorrhoea The use of TRUS
[63], 2016, Robert’s uterus from Robert’s hysteroscopic after procedure avoided the need for
Jagiellonian uterus- a Müllerian surgery, repeated laparotomy or
University, Poland duct anomaly (1) twice (1) laparoscopy
Ghirardi et al. To evaluate the Prospective Patients with Septal resection More suboptimal or TRUS is safe and may
[61], 2015, use of TRUS in case-control uterine septum (45) without TRUS incomplete resections increase the likelihood
University of hysteroscopic study guidance (18) versus noted in the non-TRUS of complete resection of
Genoa, Italy surgery resection under group compared to the the uterine septum
TRUS guidance (27) TRUS group (p < 0.5)
when assessed 6 weeks
post procedure
Intra-operative time: No
difference,
Volume of fluid infused or
absorbed: No difference,
No complications reported
in either groups
Coccia et al. Hysteroscopic Case report A patient with Hysteroscopic TVUS a month later US-guided
[23], 1996, resection of endometrial resection of osseous showed normal hysteroscopic resection
Department of endometrial osseous metaplasia with endometrium, No offers a less invasive and
Obstetrics and osseous metaplasia (1) TAUS and TRUS complications reported costly alternative, could
Gynecology, metaplasia guidance (1) prevent subsequent
University of hysterectomy
Florence, Italy
Ludwin et al. To predict the Prospective Patients with Hysteroscopic TRUS group had 91% TRUS guidance during
[28], 2013, one-step resection Cohort Study symptomatic myomectomy with one-step completion rate hysteroscopic
Jagiellonian rate after TRUS- single submucous (48) and without (72) versus 73% in patients myomectomy increases
University, guided fibroids (120) TRUS guidance without TRUS the chance of complete
Poland hysteroscopic (p = 0.02) assessed on 1-step removal of
myomectomy TVUS or repeat submucous fibroids that
hysteroscopy 4–8 weeks deeply penetrate the
post procedure myometrium
Thakur et al. To evaluate the Case series Patients with TRUS and No post-operative This approach allows
[47], 2004, use of TRUS and cornual ectopic laparoscopic guidance complications reported minimal access fertility
Basildon laparoscopy pregnancies (4) for dilatation and Complete excision of sparing surgery
University guidance for suction evacuation cornual ectopic
Hospital, United management of of cornual ectopic pregnancies was achieved
Kingdom cornual ectopic pregnancies (4)
pregnancy

TRUS, trans-rectal ultrasound; N, number of participants; TAUS, transabdominal ultrasound.

ic medium. Because the lesions were too small to be seen
with plain laparoscopy, TVUS was used to guide wedge
resection and ensure all abnormal tissue was resected [35,
36]. The authors reported no recurrence at follow-up
demonstrating safe and complete resection of non-be-
nign intra-ovarian lesions using IOUS and minimal ac-
cess surgery [35, 36]. Furthermore, Lipitz et al. [37] em-
phasised the importance of IOUS in avoiding tissue dam-
age of adjacent structures as well as allowing the
identification of ovarian cysts which facilitated the deci-
sion to convert to laparotomy in one case.
Ovarian-preserving laparoscopic surgery was also
achieved using LUS in 5 studies [38–41, 66]. Yang et al.
[39], a cohort of 58 cases, demonstrated a significant im-
provement in the accuracy of characterisation of adnexal
masses by IOUS when compared to pre-operative TVUS
(83.5 vs. 73.5%, p < 0.05). Helin and Kirkinen [40] also
reported improved diagnostic accuracy in LUS when
compared to pre-operative TVUS. Furthermore, LUS was
utilised in a case of recurrent serous BOT where the lesion
was not able to be identified during laparoscopy [66]. Two
case reports described a successful laparoscopic excision
193.51.85.197 - 1/25/2020 11:56:12 AM

IOUS in FSS Gynecol Obstet Invest 15

DOI: 10.1159/000505689
Université de Paris
Downloaded by:
Table 6. Main characteristics of studies using intra-operative contact US (CUS)

Author/year of Aim of study Study design Pathology Surgical Outcome measures Conclusions
publication, treated, N intervention, N and results
institution and
country of origin

Angioli et al. To evaluate the benefit Prospective Patients with Intraoperative CUS Residual fibroids: 6 Intraoperative US
[54], 2010, of intraoperative US cohort study symptomatic on uterine serosa to during intraoperative US is more efficient
Campus applied directly to the fibroids (64) identify fibroids not versus 46 with intraoperative than palpation in
Biomedico, uterine serosa during palpable palpation (p < 0.0001) detecting residual
University of open myomectomy intraoperatively (64) fibroids at the end
Rome, Italy of open
myomectomy
Letterie and To evaluate the use of Case series Patients with Finger-grip CUS US was particularly useful in The finger-grip
Catherino finger-grip US probe multiple fibroids during open fibroids ranging from 3 to 5 US demonstrated
[55], 2002, during open (3) and women surgery (6) cm, those >5 cm imaged poorly intrauterine
Virginia Maso myomectomy and with complex Saline solution was due to poor penetration US anatomy and
Medical Center, uterine reconstruction obstructive instilled in the allowed better definition of allowed directed
USA of uterine horn Mullerian abdomen for relationship of fibroids to the surgical approach,
abnormalities improved endometrial cavity both before both in the
(3) sonographic and after resection placement of
evaluation In 2 cases, the lowermost uterine incision
portion of the obstructed for reconstruction
uterine horn was found to be and excision of the
deep in the paravaginal space obstructed uterine
at a distance approximately horns and in the
2 cm below the cervix. identification and
US provided precise definition dissection of
of the exact location of the fibroids
tissues and lowermost portion
of the obstructed horn in
relationship to the normal
hemiuterus medially, bladder
anteriorly and rectum posteriorly
Saso et al. MSP for the excision Case report A patient with CUS to guide No intraoperative or Fertility-sparing
[56], 2012, of a placental site persistent hysterotomy incision immediate complications surgery was
Imperial College trophoblastic tumour PSTT (1) during open surgery Patient conceived 3 times post achieved with a
London, United for the excision of MSP; a well grown baby was MSP for the
Kingdom PSTT and delivered by excision of PSTT.
reconstruction of caesarean section in the TVUS allowed
uterus (1) last pregnancy, placenta accurate
was not adherent to the MSP hysterotomy
scar and conception was hence minimising
natural radicality

US, ultrasound; CUS, contact US; N, number of participants; PSTT, placental site trophoblastic tumour; TVUS, trans-vaginal US.

of cystic adenomyosis using TVUS and LUS guidance [42,
43]. IOUS in these cases facilitated resection of the lesion,
with complete resolution of the patients’ severe dysmen-
orrhoea while preserving their reproductive potential.
LUS was used in laparoscopic myomectomy in 2 cases
[44, 45]. Li et al. [44] was a randomised trial of laparoscop-
ic myomectomy with or without LUS guidance. The au-
thors reported that fibroid recurrence and residual disease
were significantly less in the LUS group (p < 0.05) [44]. In
addition, both Li et al. [44] and Lin et al. [45] highlighted
the importance of IOUS in guiding a more accurate hyster-
otomy incision, thereby minimising healthy tissue damage.
IOUS was used during transcervical surgery (without
hysteroscopy) in 5 studies; 3 with TAUS, one with TVUS
and one with TRUS, in a total of 82 patients. Two studies
described successful surgical management of cornual ec-
topic pregnancies using TAUS and TRUS guidance [46,
47]. Faschingbauer et al. [48] report a case of cervical het-
erotopic pregnancy where intra-operative TAUS was
used to achieve complete resection of the cervical ectopic
while preserving the intrauterine pregnancy which sub-
sequently resulted in a live term delivery.
Qiu et al. [67] is a retrospective cohort study compar-
ing outcomes in patients undergoing dilatation and cu-
193.51.85.197 - 1/25/2020 11:56:12 AM

16 Gynecol Obstet Invest Galazis/Saso/Sorbi/Jones/Landolfo/

DOI: 10.1159/000505689 Al-Memar/Ben-Nagi/Smith/Yazbek
Université de Paris
Downloaded by:
rettage after uterine artery embolization for Caesarean
scar ectopic pregnancy. Dilatation and curettage was ei-
ther performed transcervically with TAUS guidance or
hysteroscopically (with no IOUS). There was no signifi-
cant difference in the rates of therapeutic success between
the 2 groups. However, the intraoperative blood loss, du-
ration of hospitalisation and overall complications were
significantly lower in the hysteroscopy group (p < 0.05 for
all). Moreover, hysteroscopy had the advantage of discov-
ering potential diverticulum in the lower segment of the
anterior uterine wall [67]. This study defers from others
in that it compares outcomes between US and hystero-
scopic guidance as opposed to hysteroscopic surgery with
or without US guidance [67]. For this reason, the results
of this study should be interpreted with caution.
IOUS was used during vaginal pelvic surgery in 5 stud-
ies; one with TAUS and 4 with TVUS, in a total of 121
patients. This was mainly to guide posterior culdotomy
and access the Pouch of Douglas. Compared to unguided
posterior culdotomy, US guidance was safer and prevent-
ed rectal injury. Ma et al. [49], performed unguided pos-
terior culdotomy in 162 patients while used TAUS-guid-
ance in 29 patients. There were no complications in the
TAUS group, whereas 6 complications were reported in
the unguided group including 3 rectal injuries, one uter-
ine injury and 2 retroperitoneal fluid collections [49].
When compared to conventional laparoscopic ovarian
cystectomy, vaginal ovarian cystectomy under US guid-
ance had overall similar operating times and blood loss.
It, therefore, provided an alternative, minimally invasive
option [50–53].
IOUS was used during open surgery in 3 studies; all
with CUS, in a total of 68 patients. Angioli et al. [54] in-
vestigated the use of CUS during open myomectomy
demonstrating a reduction in the number of residual fi-
broids detected post-operatively when CUS was used
compared to intra-operative palpation only (p < 0.001).
Furthermore, CUS identified intrauterine anatomy en-
abling the surgeon to perform a hysterotomy without
breaching the endometrial cavity [55]. Similarly, Saso et
al. [56] used CUS during open surgery for the manage-
ment of placental site trophoblastic tumour in a patient
wishing to preserve her fertility. CUS allowed accurate
hysterotomy and minimised excision of healthy tissue.
The patient subsequently conceived naturally and deliv-
ered at term by caesarean section [56].
Healthcare Costs
No additional costs were associated with the use of
IOUS, compared to no US, and most studies reported
IOUS in FSS
an improvement in completion and recurrence rates.
These led the authors to conclude that the use of IOUS
is overall cost effective compared to no IOUS [23, 25,
29–31, 33, 34]. This was a secondary outcome in the
studies and formal cost-effectiveness analysis was not
carried out. Similarly, when IOUS was directly com-
pared to laparoscopic guidance during hysteroscopic
surgery, there was a significant reduction in hospital
stay and operating time with no difference in the com-
plication rates [29–31]. It followed that the use of con-
comitant laparoscopy was associated with higher costs,
albeit not been formally assessed. Tables 2–6 provide
further details.
Discussion
Overall, IOUS in patients undergoing FSS has been
used in the management of benign gynaecological condi-
tions with the exception of some oncologic cases (BOT
and choriocarcinoma) [35, 36, 56, 57, 66]. During hys-
teroscopic surgery or transcervical surgery without hys-
teroscopy, IOUS was mostly used trans-abdominally. In
laparoscopic surgery, IOUS was performed either trans-
vaginally or laparoscopically. The limitations such as the
small number of participants used and the scientific qual-
ity of the study designs are discussed later. However,
overall, the findings are promising and suggest that IOUS
during FSS is associated with positive outcomes including
improved complete resection, pregnancy, miscarriage
and complication rates and overall favourable healthcare
costs.
IOUS in FSS
Female cancer survivors regard loss of fertility as one
of the most distressing effects of their cancer treatment
[68, 69]. Moreover, the management of various benign
gynaecological conditions such as fibroids, adenomyosis
and endometrial lesions can also pose adverse effects on
the fertility potential of young women. The American So-
ciety of Reproductive Medicine recommends that fertili-
ty-sparing options are discussed with each patient [70].
The existing evidence suggests that women do not feel
well supported in making decisions regarding fertility-
sparing options, with many patients missing out on the
fertility care at this crucial time [71]. A range of internal
and external factors impact the decision-making process,
including the women’s fears concerning the perceived
risks associated with pursuing fertility-sparing treatment,
which are often overestimated, and non-evidence based
193.51.85.197 - 1/25/2020 11:56:12 AM
Gynecol Obstet Invest 17
DOI: 10.1159/000505689
Université de Paris
Downloaded by:
[5]. Key to that is the delivery of timely and accurate in-
formation on the various fertility-sparing options in
terms of their effectiveness and safety by the clinicians.
The findings of this review are promising in that, subject
to validation in large-scale studies, IOUS could be an im-
portant surgical adjunct for the provision of safe and ef-
fective FSS.
TVUS can detect recurrent BOT at an early stage when
the tumour is small and potentially not visible during lap-
aroscopic surgery [35, 36, 66]. The traditional therapeutic
approach in such scenarios would be oophorectomy to
guarantee complete resection of disease avoiding “blind”
conservative measures which can risk cyst rupture, in-
complete cyst removal and the possibility of excess healthy
ovarian tissue being removed [71]. Alternatively, US
monitoring of the cyst and proceeding to cystectomy
once the cyst is large enough to be visualised laparoscop-
ically may run the risk of upstaging a disease with malig-
nant potential. It has been demonstrated that recurrent
serous BOT can grow as slowly as 0.06 mm per month
[72], meaning that the time taken to reach a level ame-
nable to traditional surgery may not be acceptable to
women wishing to conceive immediately. IOUS during
laparoscopic ovarian wedge resection of recurrent serous
BOT offers a novel surgical option to remove those small
ovarian lesions, allowing tissue preservation, while opti-
mising the chance of complete resection and minimizing
cyst rupture [35, 36]. Instillation of saline in the perito-
neal cavity acts as a sonographic medium, which enhanc-
es the imaging quality of IOUS and improves the charac-
terisation of lesion [35, 36, 39–41].
LUS may also be used for the same procedure as de-
scribed by Mascilini et al. [66]. However, it requires spe-
cific expertise, which is not a core part of specialty train-
ing in O&G, nor is it readily available. Intra-operative
TVUS for the management of small ovarian lesions can
be easily implemented internationally at no additional
costs using standard TVUS equipment which is univer-
sally accessible in a modern gynaecological setting. It re-
quires expertise in minimal access surgery and transvagi-
nal ultrasonography which are both integral components
of gynaecological training, making this approach achiev-
able. The abundance of TVUS probes and machines obvi-
ate the need to purchase new LUS probes.
The latest Guideline on the Management of Uterine
Septum published by the American Soceity of Reproduc-
tive Medicine in 2016 states that the association between
uterine septum and infertility is inconclusive but that sev-
eral observational studies indicate that hysteroscopic sep-
tum incision is associated with improved clinical preg-
18 Gynecol Obstet Invest
DOI: 10.1159/000505689
nancy rates in women with infertility [73]. On the other
hand, there is a recognised association between uterine
septum and recurrent miscarriage. Hysteroscopic septo-
plasty has been found to reduce subsequent miscarriage
rates with improvement in live-birth rates [73]. Although
large trials are needed before reliable conclusions can be
drawn, this review highlights the potential of IOUS in
hysteroscopic septoplasty as a feasible, safer and more
cost-effective option compared to surgery without guid-
ance or with concomitant laparoscopy.
The quality of US examination is highly operator-de-
pendent, and adequate practice and training are required
to minimise errors and subsequent unnecessary interven-
tions [14, 71]. The importance of optimising US training
has recently been highlighted by the National Health Ser-
vice report on maternity claims, identifying US as one of
the major areas of improving patient safety [74]. For these
reasons, the Royal College of Obstetricians and Gynaeco-
logists has revised its approach to US training, making it
mandatory for all O&G trainees to achieve competency
in various US modules by means of objective structured
assessment of technical skills [75]. We, therefore, believe
that the next generation of UK’s gynaecologists will be
more confident in using US, not only for diagnostic pro-
cedures but also intra-operatively.
The findings of this review are promising but require
further validation studies before reliable conclusions can
be drawn. They should therefore be interpreted with cau-
tion. These preliminary findings demonstrate that IOUS
can assist in the safe resection of disease with high rates
of completion, low rates of recurrence whilst potentially
reducing the risk of damage to healthy reproductive or-
gans. From a fertility perspective, the findings are prom-
ising as high rates of conception and low rates of miscar-
riage were observed after US-guided surgery. Finally, this
review suggests a favourable impact on healthcare costs,
by reducing repeat operations and hospital stay. An ad-
vantage of gynaecological, compared to non-gynaecolog-
ical surgery, is that IOUS can be carried out by the gyn-
aecology team. This team is well trained in pelvic US re-
ducing the dependence on other healthcare professionals
like radiologists or radiographers, which will further im-
pact favourably on healthcare costs. We, therefore, envis-
age that the above clinical and financial parameters will
help to establish IOUS as routine practice in FSS.
IOUS in non-gynaecological surgery is helpful in iden-
tifying anatomical structures including blood vessels to
aid tissue dissection [76, 77]. This should be utilised in
FSS, especially in complex cases where endometriosis or
adhesions make the relationship between the ovaries and
193.51.85.197 - 1/25/2020 11:56:12 AM
Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Université de Paris
Downloaded by:
 Fig. 3. Laparoscopic and sonographic views during US-guided laparoscopic ovarian wedgresection for the treat-
ment of BOT. Under US guidance, the surface of the ovary overlying the lesion is demarcated allowing resection
of the lesion with minimal resection of healthy ovarian tissue.
the pelvic side wall containing the iliac vessels and ureter
difficult to be determined laparoscopically. Therefore, the
use IOUS in FSS could avoid excessive tissue dissection
and may reduce intra-operative complications including
ureteric or vascular injury. IOUS for hepatic surgery
shares some common characteristics with LUS or CUS
during myomectomy [78]. As with hepatic surgery, pre-
liminary evidence on LUS and CUS in FSS for uterine
fibroids, demonstrated increased identification of lesions
otherwise not seen or palpated and subsequent resection
with reduced recurrence and re-operation rates [38, 41,
44].
Practical Applications
In this section, we propose 2 techniques of IOUS dur-
ing FSS which we believe, based on the discussion points
above, are the most reproducible and feasible techniques:
(a) TAUS for hysteroscopic or transcervical (without hys-
teroscopic guidance) surgery and (b) TVUS for laparo-
scopic surgery.
a. Indications. TAUS guidance may be used for any in-
trauterine pathology requiring hysteroscopic manage-
ment which may put the patient at risk of uterine perfora-
tion or incomplete resection of the lesion. Such patholo-
gies may include complete or partial uterine septum,
submucous or intramural fibroids, uterine synechiae/
Asherman’s syndrome, thickened endometrium requir-
ing resection, surgical management of miscarriage, ste-
nosed cervical canal following conisation or trachylecto-
my, cervical or cornual ectopic pregnancies and rarer in-
trauterine conditions including atypical placental site
nodules or osseous metaplasia of endometrium.
Procedure. Although TRUS provides good visualisa-
tion of the cervix and uterus, it can be challenging as the
sonographer is required to work in a confined space
IOUS in FSS
alongside the surgeon with the patient in dorsal lithotomy
position. We therefore, advocate the use of TAUS in hys-
teroscopic or transcervical (without hysteroscopic guid-
ance) procedures, where the sonographer is standing at
the side, with the surgeon sitting between the legs of the
patient. For better transabdominal sonographic views,
the urinary bladder can be filled with up to 300 mL of sa-
line solution which causes the uterus to be displaced su-
periorly. During transcervical surgery, when hysterosco-
py is not performed, the uterus can be instilled through
the external os with 30 mL of saline to distend the uterine
cavity and optimise its delineation. Close communication
is required between the surgeon and sonographer to en-
sure that instruments are tracked and their relationship
to the uterine wall is evaluated appropriately. The urinary
bladder is emptied at the end of the procedure and the
patient should be able to pass urine before discharge.
b. Indications. Pelvic lesions that cannot be seen lapa-
roscopically including small BOT and small ovarian cysts
with positive NMDA receptor antibodies or when exten-
sive pelvic adhesions obscures visualisation of the ovaries
during laparoscopy.
Procedure. The patient is placed in lithotomy position.
Following routine laparoscopic entry, the pelvis is filled
with 500 mL of saline. This acts as a conduction agent to
aid sonographic visualisation of the pelvic lesion, as the
CO2 insuflation will have an overall hyperechoic effect on
US resulting in suboptimal views. TVUS probe is inserted
and the lesion is identified. In the case of a small ovarian
cyst, the ovary is suspended above the level of the saline
and diathermy can be used to demarcate the surface of the
ovary as illustrated in Figure 3. Laparoscopic ovarian cys-
tectomy or wedge resection is performed, and the sur-
geon is utilising both sonographic and laparoscopic views
throughout the procedure. In the case of extensive pelvic
193.51.85.197 - 1/25/2020 11:56:12 AM
Gynecol Obstet Invest 19
DOI: 10.1159/000505689
Université de Paris
Downloaded by:
adhesions, the lesion is identified sonographically guid-
ing the surgeon to access the lesion laparoscopically by
minimising tissue dissection and risk to the ureter and
pelvic vasculature. Continuous communication is there-
fore essential between the surgeon and the sonographer
(an appropriately trained gynaecologist). TVUS deter-
mines the completion of the operation and the saline is
aspirated out of the peritoneal cavity.
Limitations
This was an extensive systematic review that examined
the findings of 43 peer-reviewed publications, 9 of which
being comparative studies, while the remaining being
case series or case reports. We evaluated a broad range of
FSS procedures, pathologies and types of IOUS. Signifi-
cant heterogeneity was observed among the studies be-
cause of heterogeneous populations, different study de-
signs, pathologies and types of FSS. Nevertheless, the
findings are promising and provide justification for larg-
er, appropriately-powered and scientifically-sound stud-
ies (ideally randomised-controlled trials) in order to draw
definitive conclusions.
This review presents some novel procedures such as
TVUS-guided laparoscopic ovarian wedge resection,
LUS-guided laparoscopic management of adnexal lesions
or intramural fibroids and TVUS-guided transvaginal
ovarian surgery. The novelty of these procedures is also
indicated from the paucity of experimental studies avail-
able in the literature. The data presented in this review
were often from the first ever cases performed which may
imply that the surgeons performing these procedures
might be at an early phase in their learning curve for that
procedure.
In addition, US technology and operators’ scanning
skills have significantly evolved over the past decade.
Both these statements suggest that the role of IOUS may
not be fully appreciated with the current technology and
skillset. By and large, the studies assessed in this review
described procedures performed by experienced hystero-
scopic and laparoscopic surgeons. It would be interesting
to evaluate surgical outcomes with and without IOUS ac-
cording to surgeons’ experience and capability, to deter-
mine which surgeons would benefit the most from IOUS.
Conclusions
The findings of this review are promising and suggest
that IOUS is associated with favourable clinical out-
comes and healthcare costs. IOUS can be particularly
20 Gynecol Obstet Invest
DOI: 10.1159/000505689
useful in both benign and non-benign conditions to al-
low maximum preservation of healthy tissue and pre-
serve fertility. Established training curricula are likely to
improve the confidence of gynaecology trainees in the
use of transvaginal ultrasonography and minimal access
surgery. This, combined with technological advances
leading to improved resolution and deeper penetration
of ultrasonic waves, is likely to facilitate the application
IOUS in FSS. Finally, the findings of this review should
enable healthcare professionals to provide timely and
accurate information to patients seeking fertility-spar-
ing options for the management of gynaecological dis-
ease.
Acknowledgements
All the individuals who contributed to this study are included
in the list of authors.
Disclosure Statement
The authors report no conflict of interest.
Funding Sources
No funding was required for this study. C.L. was supported by
the Linbury Trust Grant LIN 2600.
Author Contribution
N.G. was responsible for writing the first draft, revised the
manuscript and performed the literature search. S.S. and J.Y. con-
ceived the idea, edited text and contributed to the literature search.
B.J., F.S., C.L., M.A.-M., J.B.-N., and J.R.S. contributed to critical
discussion and revision of the manuscript according to their ex-
pertise.
 1 Rockall AG, Qureshi M, Papadopoulou I,
References
Saso S, Butterfield N, Thomassin-Naggara I,
et al. Role of Imaging in Fertility-sparing
Treatment of Gynecologic Malignancies.
Radiographics. 2016 Nov-Dec; 36(7): 2214–
33.
 2 Miyazaki T, Tomoda Y, Ohta M, Kano T,
Mizuno K, Sakakibara K. Preservation of
ovarian function and reproductive ability in
patients with malignant ovarian tumors. Gy-
necol Oncol. 1988 Jul;30(3):329–41.
  3 Plante M. Fertility preservation in the man-
agement of gynecologic cancers. Curr Opin
Oncol. 2000 Sep;12(5):497–507.
193.51.85.197 - 1/25/2020 11:56:12 AM
Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Université de Paris
Downloaded by:
 4 McEvoy SH, Nougaret S, Abu-Rustum NR,
Vargas HA, Sadowski EA, Menias CO, et al.
Fertility-sparing for young patients with gy-
necologic cancer: how MRI can guide patient
selection prior to conservative management.
Abdom Radiol (NY). 2017 Oct; 42(10): 2488–
512.
  5 Fischerova D. Ultrasound scanning of the pel-
vis and abdomen for staging of gynecological
tumors: a review. Ultrasound Obstet Gynecol.
2011 Sep;38(3):246–66.
  6 Jones G, Hughes J, Mahmoodi N, Smith E,
Skull J, Ledger W. What factors hinder the
decision-making process for women with
cancer and contemplating fertility preserva-
tion treatment? Hum Reprod Update. 2017
Jul;23(4):433–57.
  7 National Institute for Health and Care Excel-
lence on Cervical Cancer. [Accessed Nov
2018]. Available from: https://cks.nice.org.
uk/cervical-cancer-and-hpv.
 8 British Gynaecological Cancer Society on
­Endometrial Cancer. [Accessed Nov 2018].
Available from: https://bgcs.org.uk/BGCS
%20Endometrial%20Guidelines%202017.
pdf.
 9 British Gynaecological Cancer Society on
Ovarian Cancer. [Accessed Nov 2018]. Avail-
able from: https://bgcs.org.uk/BGCS%20
Guidelines%20Ovarian%20Guidelines%20
2017.pdf.
10 Daraï E, Fauvet R, Uzan C, Gouy S, Duvillard
P, Morice P. Fertility and borderline ovarian
tumor: a systematic review of conservative
management, risk of recurrence and alterna-
tive options. Hum Reprod Update. 2013 Mar-
Apr;19(2):151–66.
11 National Institute for Health and Care Excel-
lence on Uterine Fibroids. [Accessed Nov
2018]. Available from: https://cks.nice.org.
uk/fibroids#!scenario.
12 National Institute for Health and Care Excel-
lence on Endometriosis. [Accessed Nov
2018]. Available from: https://www.nice.org.
uk/guidance/ng73.
13 National Institute for Health and Care Excel-
lence on Adenomyosis. [Accessed Nov 2018].
Available from: https://www.nice.org.uk/
guidance/ipg473.
14 EFSUMB: European Federation of Societies
for Ultrasound in Medicine and Biology. [Ac-
cessed Nov 2018]. Available from: http://
www.efsumb.org/guidelines/guidelines01.
asp.
15 AIUM: American Institute of Ultrasound in
Medicine. [Accessed Nov 2018]. Available
from: http://www.aium.org/resources/state-
ments.aspx.
16 ISUOG: International Society of Ultrasound
in Obstetrics and Gynecology training guide-
lines. [Accessed Nov 2018]. Available from:
http://www.isuog.org/StandardsAnd
Guidelines/Statements+and+Guidelines/
Training+Guidelines/Default.htm.
17 Fischerova D, Cibula D. Ultrasound in gyne-
cological cancer: is it time for re-evaluation of
its uses? Curr Oncol Rep. 2015 Jun;17(6):28.
IOUS in FSS
18 Knight PR, Newell JA. Operative use of ultra-
sonics in cholelithiasis. Lancet. 1963 May;
1(7289):1023–5.
19 Silas AM, Kruskal JB, Kane RA. Intraopera-
tive ultrasound. Radiol Clin North Am. 2001
May;39(3):429–48.
20 Matin SF, Gill IS. Laparoscopic ultrasonogra-
phy. J Endourol. 2001 Feb;15(1):87–92.
21 Kane RA. Intraoperative ultrasonography:
history, current state of the art, and future di-
rections. J Ultrasound Med. 2004 Nov;23(11):
1407–20.
22 Moher D, Liberati A, Tetzlaff J, Altman DG;
PRISMA Group. Reprint—preferred report-
ing items for systematic reviews and meta-
analyses: the PRISMA statement. Phys Ther.
2009 Sep;89(9):873–80.
23 Coccia ME, Becattini C, Bracco GL, Scarselli G.
Ultrasound-guided hysteroscopic manage-
ment of endometrial osseous metaplasia. Ultra-
sound Obstet Gynecol. 1996 Aug;8(2):134–6.
24 Mullesserill BT, Dumesic DA, Damario MA,
Session DR. Ultrasound-guided unification of
noncommunicating uterine cavities. JSLS.
2003 Apr-Jun;7(2):155–7.
25 Wang JH, Xu KH, Lin J, Chen XZ. Hystero-
scopic septum resection of complete septate
uterus with cervical duplication, sparing the
double cervix in patients with recurrent spon-
taneous abortions or infertility. Fertil Steril.
2009 Jun;91(6):2643–9.
26 Vigoureux S, Fernandez H, Capmas P, Levail-
lant JM, Legendre G. Assessment of Abdomi-
nal Ultrasound Guidance in  Hysteroscop-
ic  Metroplasty. J Minim Invasive Gynecol.
2016 Jan;23(1):78–83.
27 Korkmazer E, Tekin B, Solak N. Ultrasound
guidance during hysteroscopic myomectomy
in G1 and G2 Submucous Myomas: for a safer
one step surgery. Eur J Obstet Gynecol Re-
prod Biol. 2016 Aug;203:108–11.
28 Ludwin A, Ludwin I, Pityński K, Basta P, Bas-
ta A, Banas T, et al. Transrectal ultrasound-
guided hysteroscopic myomectomy of sub-
mucosal myomas with a varying degree of
myometrial penetration. J Minim Invasive
Gynecol. 2013 Sep-Oct;20(5):672–85.
29 Coccia ME, Becattini C, Bracco GL, Bargelli G,
Scarselli G. Intraoperative ultrasound guid-
ance for operative hysteroscopy. A prospec-
tive study. J Reprod Med. 2000 May; 45(5):
413–8.
30 Kresowik JD, Syrop CH, Van Voorhis BJ,
Ryan GL. Ultrasound is the optimal choice for
guidance in difficult hysteroscopy. Ultra-
sound Obstet Gynecol. 2012 Jun;39(6):715–8.
31 Zhang Y, Yang L, Yang SL, Zhao Q, Xie Y.
Ultrasonography versus laparoscopy in tran-
scervical resection of septa: a randomized
clinical trial. Clin Exp Obstet Gynecol. 2015;
42(4):515–7.
32 Tsui KH, Lin LT, Cheng JT, Teng SW, Wang
PH. Comprehensive treatment for infertile
women with severe Asherman syndrome. Tai-
wan J Obstet Gynecol. 2014 Sep;53(3):372–5.
33 Ohl J, Bettahar-Lebugle K. Ultrasound-guid-
ed transcervical resection of uterine septa: 7
Gynecol Obstet Invest
DOI: 10.1159/000505689
years’ experience. Ultrasound Obstet Gyne-
col. 1996 May;7(5):328–34.
34 Querleu D, Brasme TL, Parmentier D. Ultra-
sound-guided transcervical metroplasty. Fer-
til Steril. 1990 Dec;54(6):995–8.
35 Jones BP, Saso S, Farren J, El-Bahrawy M,
Smith JR, Yazbek J. Intraoperative ultrasound-
guided laparoscopic ovarian-tissue-preserv-
ing surgery for recurrent borderline ovarian
tumor. Ultrasound Obstet Gynecol. 2017 Sep;
50(3):405–6.
36 Jones BP, Saso S, Farren J, El-Bahrawy M,
Ghaem-Maghami S, Smith JR, et al. Ultra-
sound-Guided Laparoscopic Ovarian Wedge
Resection in Recurrent Serous Borderline
Ovarian Tumours. Int J Gynecol Cancer. 2017
Nov;27(9):1813–8.
37 Lipitz S, Seidman DS, Achiron R, Goldenberg
M, Bider D, Mashiach S. Laparoscopic surgi-
cal management of ovarian cysts assisted by
simultaneous transvaginal ultrasonography. J
Reprod Med. 1996 May;41(5):304–6.
38 Letterie GS, Marshall L. Evaluation of real-time
imaging using a laparoscopic ultrasound probe
during operative endoscopic procedures. Ul-
trasound Obstet Gynecol. 2000 Jul;16(1):63–7.
39 Yang WT, Yuen PM, Ho SS, Leung TN, Me-
treweli C. Intraoperative laparoscopic sonog-
raphy for improved preoperative sonographic
pathologic characterization of adnexal mass-
es. J Ultrasound Med. 1998 Jan;17(1):53–61.
40 Helin HL, Kirkinen P. Laparoscopic ultraso-
nography during conservative ovarian sur-
gery. Surg Endosc. 2000 Feb;14(2):161–3.
41 Gong XH, Lu J, Liu J, Deng YY, Liu WZ,
Huang X, et al. A novel ultrasound based ap-
proach for lesion segmentation and its appli-
cations in gynecological laparoscopic surgery.
Australas Phys Eng Sci Med. 2015 Dec;38(4):
709–20.
42 Nabeshima H, Murakami T, Nishimoto M,
Sugawara N, Sato N. Successful total laparo-
scopic cystic adenomyomectomy after unsuc-
cessful open surgery using transtrocar ultra-
sonographic guiding. J Minim Invasive Gyne-
col. 2008 Mar-Apr;15(2):227–30.
43 Nabeshima H, Murakami T, Terada Y, Noda
T, Yaegashi N, Okamura K. Total laparoscop-
ic surgery of cystic adenomyoma under hy-
droultrasonographic monitoring. J Am Assoc
Gynecol Laparosc. 2003 May;10(2):195–9.
44 Li SJ, Li XF, Zhang J, Yang LM, Wu QQ. [Clin-
ical value of assisted laparoscopic ultrasonog-
raphy in laparoscopic myomectomy]. Zhong-
hua Yi Xue Za Zhi. 2016 Sep;96(33):2652–4.
45 Lin PC, Thyer A, Soules MR. Intraoperative
ultrasound during a laparoscopic myomec-
tomy. Fertil Steril. 2004 Jun;81(6):1671–4.
46 Morgan M, Aziz M, Mikhail M, Henein M,
Atalla R. Ultrasound guided treatment of cor-
nual ectopic pregnancy. Eur J Obstet Gynecol
Reprod Biol. 2009 Apr;143(2):126.
47 Thakur Y, Coker A, Morris J, Oliver R. Lapa-
roscopic and ultrasound-guided transcervical
evacuation of cornual ectopic pregnancy: an
alternative approach. J Obstet Gynaecol. 2004
Oct;24(7):809–10.
193.51.85.197 - 1/25/2020 11:56:12 AM
21
Université de Paris
Downloaded by:
48 Faschingbauer F, Mueller A, Voigt F, Beck-
mann MW, Goecke TW. Treatment of het-
erotopic cervical pregnancies. Fertil Steril.
2011 Apr;95(5):1787.e9–13.
49 Ma C, Wang Y, Li TC, Qiao J, Yang Y, Song
X, et al. Trans-abdominal ultrasound guided
transvaginal hydrolaparoscopy is associated
with reduced complication rate. Eur J Obstet
Gynecol Reprod Biol. 2012 Feb;160(2):166–9.
50 Tanaka M, Sagawa T, Hashimoto M, Mizumo-
to Y, Yamazaki R, Myojo S, et al. The culdoto-
my two U procedure for vaginal ovarian cys-
tectomy. Surg Innov. 2011 Jun;18(2):114–8.
51 Tanaka M, Sagawa T, Hashimoto M, Mizu-
moto Y, Yoshimoto H, Yamazaki R, et al. Ul-
trasound-guided culdotomy for vaginal ovar-
ian cystectomy using a renal balloon dilator
catheter. Ultrasound Obstet Gynecol. 2008
Mar;31(3):342–5.
52 Tanaka M, Sagawa T, Hashimoto M, Mizu-
moto Y, Yoshimoto H, Yamazaki R, et al. The
Culdotomy FourS Two U procedure for
transvaginal access to the peritoneal cavity.
Endoscopy. 2009 May;41(5):472–4.
53 Tanaka M, Sagawa T, Yamazaki R, Myojo S,
Dohi S, Inoue M. An alternative system for
transvaginal removal of dermoid cyst and a
comparative study with laparoscopy. Surg In-
nov. 2012 Mar;19(1):37–44.
54 Angioli R, Battista C, Terranova C, Zullo MA,
Sereni MI, Cafà EV, et al. Intraoperative con-
tact ultrasonography during open myomec-
tomy for uterine fibroids. Fertil Steril. 2010
Sep;94(4):1487–90.
55 Letterie GS, Catherino WH. A 7.5-MHz fin-
ger-grip ultrasound probe for real-time intra-
operative guidance during complex repro-
ductive surgical procedures. Am J Obstet Gy-
necol. 2002 Dec;187(6):1588–90.
56 Saso S, Chatterjee J, Yazbek J, Thum Y, Keefe
KW, Abdallah Y, et al. A case of pregnancy
following a modified Strassman procedure
applied to treat a placental site trophoblastic
tumour. BJOG. 2012 Dec;119(13):1665–7.
57 Jones BP, Rees R, Saso S, Stalder C, Smith JR,
Yazbek J. Ultrasound-guided laparoscopic
ovarian preserving surgery to treat anti-
NMDA receptor encephalitis. BJOG. 2017
Jan;124(2):337–41.
58 Lee C, Ben-Nagi J, Ofili-Yebovi D, Yazbek J,
Davies A, Jurkovic D. A new method of trans-
vaginal ultrasound-guided polypectomy: a
feasibility study. Ultrasound Obstet Gynecol.
2006 Feb;27(2):198–201.
22 Gynecol Obstet Invest
DOI: 10.1159/000505689
59 Badiglian-Filho L, Baiocchi G, Faloppa CC,
Fukazawa EM, Kumagai LY, de Oliveira RA.
Intraoperative ultrasound for benign cystic
teratoma. Report of two cases. Arch Gynecol
Obstet. 2012 Mar;285(3):705–7.
60 Casadio P, Youssef AM, Spagnolo E, Rizzo
MA, Talamo MR, De Angelis D, et al. Should
the myometrial free margin still be considered
a limiting factor for hysteroscopic resection of
submucous fibroids? A possible answer to an
old question. Fertil Steril. 2011 Apr; 95(5):
1764–8.e1.
61 Ghirardi V, Bizzarri N, Remorgida V, Ven-
turini PL, Ferrero S. Intraoperative Transrec-
tal Ultrasonography for Hysteroscopic Me-
troplasty: feasibility and Safety. J Minim Inva-
sive Gynecol. 2015 Jul-Aug;22(5):884–8.
62 Kumakiri J, Takeuchi H, Kitade M, Kikuchi I,
Shimanuki H, Kubo M, et al. Interstitial preg-
nancy with huge adenomyosis uteri managed
laparoscopically by using pre-operative and
intra-operative imaging: case report. BJOG.
2005 Nov;112(11):1578–80.
63 Ludwin A, Ludwin I, Martins WP. Robert’s
uterus: modern imaging techniques and ul-
trasound-guided hysteroscopic treatment
without laparoscopy or laparotomy. Ultra-
sound Obstet Gynecol. 2016 Oct;48(4):526–9.
64 Pakrashi T, Ressler IB, Sroga JM, DiPaola KB,
Thomas MA, Lindheim SR. Hysteroscopic
enucleation of type II submucosal uterine
leiomyomas using a TRUCLEAR hystero-
scopic morcellator: case report and review of
the literature. J Laparoendosc Adv Surg Tech
A. 2013 Apr;23(4):378–82.
65 Song D, Xia E, Xiao Y, Li TC, Huang X, Liu Y.
Management of false passage created during
hysteroscopic adhesiolysis for Asherman’s
syndrome. J Obstet Gynaecol. 2016;36(1):87–
92.
66 Mascilini F, Quagliozzi L, Bolomini G, Scam-
bia G, Testa AC, Fagotti A. Intraoperative ul-
trasound through laparoscopic probe in fer-
tility-sparing surgery for borderline ovarian
tumor recurrence. Ultrasound Obstet Gyne-
col. 2019 Aug;54(2):280–2.
67 Qiu J, Fu Y, Xu J, Huang X, Yao G, Lu W.
Analysis on clinical effects of dilation and cu-
rettage guided by ultrasonography versus hys-
teroscopy after uterine artery embolization in
the treatment of cesarean scar pregnancy.
Ther Clin Risk Manag. 2019 Jan;15:83–9.
68 Mancini J, Rey D, Préau M, Malavolti L,
Moatti JP. Infertility induced by cancer treat-
ment: inappropriate or no information pro-
vided to majority of French survivors of can-
cer. Fertil Steril. 2008 Nov;90(5):1616–25.
69 Peate M, Meiser B, Hickey M, Friedlander M.
The fertility-related concerns, needs and pref-
erences of younger women with breast cancer:
a systematic review. Breast Cancer Res Treat.
2009 Jul;116(2):215–23.
70 Ethics Committee of the American Society for
Reproductive Medicine. Disparities in access
to effective treatment for infertility in the
United States: an Ethics Committee opinion.
Fertil Steril. 2015 Nov;104(5):1104–10.
71 Kirkman M, Winship I, Stern C, Neil S, Mann
GB, Fisher JR. Women’s reflections on fertil-
ity and motherhood after breast cancer and its
treatment. Eur J Cancer Care (Engl). 2014 Jul;
23(4):502–13.
72 Franchi D, Boveri S, Fruscio R, Fischerova D,
Guerriero S, Moruzzi MC, et al. Imaging in
gynecological disease (8): ultrasound charac-
teristics of recurrent borderline ovarian tu-
mors. Ultrasound Obstet Gynecol. 2013 Apr;
41(4):452–8.
73 Pfeifer S, Butts S, Dumesic D, Gracia C, Vernon
M, Fossum G, et al.; Practice Committee of the
American Society for Reproductive Medicine.
Electronic address: ASRM@asrm.org; Practice
Committee of the American Society for Repro-
ductive Medicine. Uterine septum: a guideline.
Fertil Steril. 2016 Sep;106(3):530–40.
74 NHS. Ten Years of Maternity Claims. [Ac-
cessed Nov 2018]. Available from: http://
www.nhsla.com/Safety/Documents/Ten%20
Years%20of%20Maternity%20Claims%20
-%20News%20Release%20%20Octobe-r%20
2012.pdf.
75 RCOG Ultrasound Training Programme.
[Accessed Nov 2018]. Available from: https://
www.rcog.org.uk/globalassets/documents/
careers-and-training/resources-and-sup-
port-for-trainers/-08_ultrasound_imple-
mentation_strategy_final.pdf.
76 Castaing D, Emond J, Kunstlinger F, Bismuth
H. Utility of operative ultrasound in the surgi-
cal management of liver tumors. Ann Surg.
1986 Nov;204(5):600–5.
77 Gozzetti G, Mazziotti A, Bolondi L, Cavallari
A, Grigioni W, Casanova P, et al. Intraopera-
tive ultrasonography in surgery for liver tu-
mors. Surgery. 1986 May;99(5):523–30.
78 Bismuth H, Castaing D, Garden OJ. The use of
operative ultrasound in surgery of primary liver
tumors. World J Surg. 1987 Oct;11(5):610–4.
193.51.85.197 - 1/25/2020 11:56:12 AM
Galazis/Saso/Sorbi/Jones/Landolfo/
Al-Memar/Ben-Nagi/Smith/Yazbek
Université de Paris
Downloaded by: