Journal of Obstetrics and Gynaecology

ISSN: 0144-3615 (Print) 1364-6893 (Online) Journal homepage: http://www.tandfonline.com/loi/ijog20

Risk of ovarian torsion is reduced in GnRH agonist

triggered freeze-all cycles: a retrospective cohort
study

Murat Berkkanoglu, Kevin Coetzee, Hasan Bulut & Kemal Ozgur

To cite this article: Murat Berkkanoglu, Kevin Coetzee, Hasan Bulut & Kemal Ozgur (2018): Risk
of ovarian torsion is reduced in GnRH agonist triggered freeze-all cycles: a retrospective cohort
study, Journal of Obstetrics and Gynaecology, DOI: 10.1080/01443615.2018.1479381

To link to this article: https://doi.org/10.1080/01443615.2018.1479381

Published online: 19 Sep 2018.

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JOURNAL OF OBSTETRICS AND GYNAECOLOGY
https://doi.org/10.1080/01443615.2018.1479381

ORIGINAL ARTICLE

Risk of ovarian torsion is reduced in GnRH agonist triggered freeze-all cycles:

a retrospective cohort study
Murat Berkkanoglu, Kevin Coetzee, Hasan Bulut, and Kemal Ozgur
Antalya IVF, Antalya, Turkey

ABSTRACT KEYWORDS
Ovarian torsion (OT) in IVF is rare, however, the consequences are significant, which include ovariotomy. Agonist trigger; freeze-all;
In the present study, it was aimed for the first time to compare the incidence of OT between hCG trig- torsion; detorsion; ovarian
gered cycles with ICSI and fresh transfer and GnRH-agonist triggered cycles with the ICSI-freeze-all and hyperstimulation syndrome
frozen embryo transfer (FET). In total, 15,577 ICSI cycles performed between 2001 and 2016 were cate-
gorised into two groups (Group 1, n: 9978): cycles with controlled ovarian stimulation (COS) and hCG-
triggered (Group 2, n: 5599) and COS, with GnRH-agonist only triggered and freeze-all. Thirteen patients
(0.13%) were diagnosed with OT and corrected by laparoscopy (12) and laparotomy (1) in Group 1. One
patient (0.018%) was diagnosed with OT and corrected by laparotomy in Group 2 (Group 1 vs. Group 2,
p ¼ .049). The incidence of severe ovarian hyperstimulation syndrome (OHSS) was 2.4% in Group 1 and
0.05% in Group 2 (p < .001). The use of freeze-all with GnRH agonist trigger in ART significantly reduced
the incidence of OT and concomitantly OHSS, with no effect on the reproductive outcome.

IMPACT STATEMENT
 What is already known on this subject? Adnexal ovarian torsion (OT) is a well-known gynaeco-
logical event that constitutes a surgical emergency. Assisted reproduction technologies (ART) may
result in ovarian conditions that predispose patients to ovarian hyperstimulation syndrome (OHSS)
and torsion.
 What the results of this study add? The combined use of GnRH agonist trigger for final oocyte
maturation after OS with freeze-all and frozen embryo transfer (FET) significantly reduces the inci-
dence of OT, as well as OHSS.
 What the implications are of these findings for clinical practice and/or further research? The
treatment strategy of GnRH agonist trigger with freeze-all significantly reduces the risks of adverse
complications.

Introduction The increased use of gonadotropins in the management

Ovarian torsion (OT) results from the twisting of the ovary
around its own axis, as the result of certain physical condi-
tions or disease, resulting in the occlusion of the ovarian
artery and vein. Ovarian torsion is generally poorly recog-
nised and an infrequently encountered incident in artificial
reproductive technology (ART) treatments.
The majority of the patients present with abdominal pain
(midline or in one or both lower pelvic quadrants), together
with a palpable mass. At times, patients may experience epi-
sodes of pain interspersed with asymptomatic intervals, as is
seen with intermittent torsion. Nausea and vomiting are
common accompanying symptoms, as well as a low-grade
pyrexia and leukocytosis (Pinto et al. 2001). Risks of a pro-
longed torsion to ovaries may include atrophy, necrosis, loss
of function, and ultimately ovariotomy. An early laparoscopy
not only aids in the diagnosis, but also allows for the simple
unwinding of the affected adnexa.
of infertility commonly results in ovarian enlargement sec-
ondary to hyperstimulation and in ovarian hyperstimulation
syndrome (OHSS); all of which predisposes patients to
adnexal torsion (Hibbard 1985; Ben-Rafael et al. 1990). In con-
trolled ovarian stimulation (COS) with gonadotropins, it is
common to trigger final oocyte maturation with hCG in IVF,
which increases the risk of OHSS (Shapiro et al. 2005; Practice
Committee of American Society for Reproductive Medicine
2008). This risk can be significantly reduced by replacing hCG
with GnRH agonist (GnRHa) to induce the required surge of
LH in GnRH antagonist cycles (Engmann et al. 2008). The
short half-life of LH combined with pituitary desensitisation
results in a rapid, complete and irreversible luteolysis, thus
eliminating the risk of significant OHSS (Kol 2004).
In this first-ever study, the incidence of OT complica-
tions in COS cycles that included either hCG trigger and
fresh embryo transfer (ET) or GnRHa trigger, the blasto-
cyst-freeze-all, and frozen embryo transfer (FET) was

CONTACT Murat Berkkanoglu mberkkan@hotmail.com Antalya IVF Halide Edip Cd. No.: 7, Kanal Mh., Antalya 07080, Turkey
Presented at a meeting: Partly presented at the 69th Annual Meeting of the ASRM, Boston, Massachusetts, USA, on 12–17 October 2013.
ß 2018 Informa UK Limited, trading as Taylor & Francis Group
2 M. BERKKANOGLU ET AL.
investigated. In addition, OHSS complications and obstetric
and live birth (LB) outcomes following detorsion were
investigated.
Materials and methods
This retrospective cohort study was conducted on ICSI
cycles performed between January 2001 and June 2016 at
Antalya IVF (Antalya, Turkey); in 2001 approximately 200
treatment cycles were performed, and in 2016 approxi-
mately 1800 treatment cycles were performed. In the
study period, there were two consecutive phases, each
with a particular treatment strategy. For the analysis, the
patient treatment cycles were therefore divided into two
groups to represent these treatment strategies. In Group
1, patients had human chorionic gonadotropin (hCG) final
oocyte maturation triggers, with fresh ET; in Group 2,
patients had gonadotropin releasing hormone (GnRH)
agonist triggers, with freeze-all, and FET.
The database of the ART centre was searched for all of
the patients eligible for allocation into two specific patient
cohorts; patients who had undergone specific treatment
sequences during the study period. The patients eligible
for the study group were 18–44 years of age (female) who
underwent the following treatment sequence; COS with
gonadotropins, triggered with hCG or GnRHa, OPU (oocyte
pick-up), with a fresh ET or FET following the freeze-all.
Only the patients having a cancelled COS because of their
lack of follicle development were excluded.
The institutional ethics committee approval (reference
number: 449/2017) was obtained for this retrospective
study, with patients also providing consent for the use of
their anonymised data in research.
Stimulation protocol
In Group 1, COS were performed using the long (Lucrin
depot 3.75 mg, Abbott, Istanbul, Turkey) and GnRH antag-
onist (Cetrotide, 0.25 mg, Merck Serono, Istanbul, Turkey)
co-treatment protocols (Isıkoglu et al. 2007), with a com-
bination of rFSH (Gonal-F, Merck Serono, Istanbul, Turkey)
and hMG (Menopur, Ferring Pharmaceuticals Ltd., Mumbai,
India), and ovulation induction with hCG (Pregnyl
10,000 IU, Merck Sharp and Dohme, Istanbul, Turkey, or
250 mcg, OvitrelleV, Merck Serono, Istanbul, Turkey). In
R
Group 2, the COS were performed using only the GnRH
antagonist (Cetrotide, 0.25 mg, Merck Serono, Istanbul,
Turkey) co-treatment protocols with a combination of
rFSH (Gonal-F, Merck Serono, Istanbul, Turkey) and hMG
(Menopur, Ferring Pharmaceuticals Ltd., Mumbai, India),
and ovulation induction with GnRHa (0.2 mg, GonapeptylV,
R
Ferring Pharmaceuticals Ltd., Mumbai, India) (Ozgur et al.
2016; Berkkanoglu et al. 2017).
Oocyte retrieval, embryo development and transfer
Oocyte collection was performed 36 ± 2 hours following
the ovulation induction. The embryo culture was per-
formed using Cook Medical (Sydney IVF, Brisbane,
Australia) and SAGE (SAGE, Origio, Malov, Denmark) media.
Incubation conditions were set at 6% CO2, 5% O2 and
37.0  C (K-Systems, Kivex Biotec Ltd., Birkerød, Denmark).
The embryos were assessed according to the blasto-
mere number, blastomere size and regularity, and the per-
centage of fragmentation. Good quality embryos were
those with equal sized, spherical blastomeres with <10%
fragmentation and scored as 1 on a scale of 1–5 (Alpha
Scientists in Reproductive Medicine and ESHRE Special
Interest Group of Embryology 2011). Blastocysts were
scored according to the three-part grading system; blasto-
cyst expansion on a scale of 1–6, the inner cell mass (ICM)
on a scale of A–C according to the number and degree of
compaction of the cells, and the trophectoderm (TE) on a
scale of A to C according to the number, size and the con-
tiguous arrangement of the TE cells (Alpha Scientists in
Reproductive Medicine and ESHRE Special Interest Group
of Embryology 2011).
The vitrification and warming of blastocysts were per-
formed using the Cryotop method, as described by the
manufacturer (Kitazato, BioPharma Co. Ltd., Fuji, Japan).
All of the FET procedures were performed as artificial
cycles (Ozgur et al. 2016), with a step-up regimen of oes-
trogen (Estrofem, Novo Nordisk, Istanbul, Turkey; 2 mg/day
from day 1 to 6, 4 mg/day from day 7 to 10, and 8 mg/day
from day 11 to 14). A progesterone supplementation was
started on day 15 (twice a day, Crinone 8%, Merck Serono,
Istanbul, Turkey) and oestrogen supplementation contin-
ued at 6 mg/day, with the vitrified warmed blastocyst
transfer performed on the sixth day of progesterone.
All of the transfer procedures were performed using a
Hamilton syringe (50 mL, Hamilton Company, Reno, NV)
attached to an embryo replacement catheter (Wallace,
Smiths Medical International, Ashford, UK) and trans-abdom-
inal ultrasound guidance. In Group 1, cleavage stage (day 2
and day 3) embryos and blastocysts were transferred, while
in Group 2 only the blastocysts were transferred.
Luteal phase support consisted of daily oestrogen (6 mg/
day) and progesterone (8% BD) supplementation. In the case
of pregnancy, luteal phase support was continued for
12 weeks of gestation.
Outcomes
The primary outcome measure recorded was the incidence
of OT. The secondary outcome measures were OHSS, LB
and obstetric outcomes following detorsion. The patient
variables recorded were maternal age, infertility duration,
BMI (body mass index) and the AFC (antral follicle count).
The treatment cycle variables were the total dosage of
 JOURNAL OF OBSTETRICS AND GYNAECOLOGY 3

Table 1. Patient and cycle demographics of fresh ET and freeze-all periods.

Group 1: fresh ET Group 2: freeze-all with FET p-value
Number of cycles N 9978 5599 NA
Maternal age Years 32.3 ± 0.6 30.4 ± 0.1 .018
Infertility duration Years 5.69 ± 0.07 5.32 ± 0.12 .004
Body mass index (BMI) kg/m2 26.09 ± 0.09 24.46 ± 0.24 <.001
Antral follicle count (AFC) N 17.80 ± 0.26 24.82 ± 0.55 <.001
Total FSH þ HMG IU 3896.45 ± 23.81 3072.06 ± 35.44 <.001
Controlled ovarian stimulation duration Days 9.09 ± 1.75 8.95 ± 2.07 .480
Oocyte number n 15.82 ± 0.15 24.90 ± 0.40 <.001
Number embryos transferred n 2.77 ± 0.02 1.50 ± 0.01 <.001
Biochemical pregnancy % 57.38 84.32 <.001
OHSS (paracentesis required) % 2.4 (240/9978) 0.05 (3/5599) <.001
OHSS: ovarian hyperstimulation syndrome, biochemical pregnancy; day 14 bhCG serum concentration of >5 IU/L,
with appropriate increase.
p<.05: statistically significant.

used follicle stimulating hormone (FSH), the human meno-
pausal gonadotropin (HMG), COS duration, oocyte number,
number of embryos transferred, biochemical pregnancy
(day 14 bhCG serum concentration of >5 IU/L) and the LB
(delivery at >20 weeks of gestation).
Statistical analysis
SigmaPlot version 12.5 (www.sigmaplot.com) was used for
all statistical analyses. The independent samples t-test was
used for the continuous data analyses and depended on
the data sets passing a normality testing (Shapiro–Wilk’s
test). The Chi-square test was used for the categorical data
analyses and depended on the data set being sufficiently
large. The low incidence rates of OT observed in the two
sample populations of the study provide a power between
60 and 80% at an a ¼ 0.05 (type I error rate) to detect the
significant difference in the sizes reported.
Results
In total, 17,269 COS cycles were started between January
2001 and June 2016 at Antalya IVF. Of the cycles started,
9.8% were cancelled because of a lack of follicle develop-
ment or for personal reasons. Consequently, 15,577 cycles
of ICSI were performed. Two uniquely different treatment
strategies were used in the study period at the IVF centre,
dividing the total accordingly into two cycle groups;
Group 1 (n ¼ 9978; 64.1%, 2001–2013) with an hCG trigger
with a fresh ET and Group 2 (n ¼ 5599; 35.9%, 2013–2016)
with a GnRHa trigger with a blastocyst-freeze-all and FET.
The patient demographics of the two treatment groups
are presented in Table 1.
Clinically, the patients in Group 2 were younger with
higher ovarian reserves (ORs). Even though COS duration
was reduced and correspondingly the total FSH was
administered because of significantly higher AFC signifi-
cantly more oocytes were retrieved in Group 2. Moreover,
significantly fewer embryos were transferred in Group 2
for a significantly higher biochemical pregnancy rate.
Notwithstanding the OHSS conducive conditions in the
Group 2 cycles, the OHSS was significantly reduced com-
pared to Group 1 (0.05 vs. 2.4%, p < .001).
In total, 14 (0.09%) of the 15,577 treatment cycles per-
formed resulted in patients developing OT, with 13 diag-
nosed in Group 1 and one diagnosed in Group 2 (0.13 vs.
0.018%, p < .049) (Table 2). The incidence of OT was sig-
nificantly higher in Group 1. OT occurred in cycles with a
high AFC (12–79; min–max) and relatively high oocyte
numbers (3–46; min–max). Of the 14 diagnosed patients,
five (35.7%) developed OHSS symptoms and of the 13 OT
patients who had an ET, 11 (84.6%) became pregnant with
two patients (18.2%) experiencing pregnancy loss
(Table 3).
Twelve patients diagnosed with OT in Group 1 had
their OT corrected in a laparoscopic procedure (Table 2).
One patient from Group 1 had their OT corrected in lap-
aroscopic procedure that was converted to a laparotomy.
The one patient diagnosed with OT in Group 2 also had
their torsion corrected in a laparoscopic procedure that
converted to a laparotomy. OT was predominantly diag-
nosed to be torsion of the right ovary, eight patients had
right-sided OT and six patients had left-sided OT. The
median time from the oocyte retrieval to the start of the
first symptoms was 10 days (0–56 days; min–max). The
median time between the first symptoms and laparoscopy
was five hours (3–48 hours; min–max).
Discussion
In the present study, the incidence of OT in two different
IVF treatment strategies was investigated, one in which
ICSI and fresh ET were performed after hCG trigger and
another in which the ICSI, the blastocyst-freeze-all and the
FET were performed after GnRHa trigger. The incidence of
OT, as previously reported (Roest et al. 1996; Govaerts
et al. 1998; Gorkemli et al. 2002), was a rare complication,
with 14 (0.09%) of the 15,577 treatment cycles performed
resulting in OT complications. Of the 14 diagnosed OT, 13
were diagnosed in Group 1 and one was diagnosed in
Group 2 (0.13 vs. 0.018%, p < .049). Although the total
oocyte number obtained in the Group 2 was higher than
4 M. BERKKANOGLU ET AL.

Table 2. Patient and cycle demographics of torsion patients in fresh ET and freeze-
all periods.
Group 2:
Group 1: fresh ET freeze-all with FET p-value
Torsion % (n) 0.13 (13/9978) 0.018 (1/5599) .049
Antral follicle count (AFC) n 30.54 ± 18.58 48 (one case) NA
Oocyte number n 23.46 ± 10.14 24 (one case) NA
Detorsion procedure Laparoscopy (12) Laparotomy (1)a NA
Laparotomy (1)a
OHSS in torsion cycles % (n) 30.8 (4) 100.0 (1) NA
p<.05: statistically significant.
a
Detorsion procedure converted from laparoscopy to laparotomy.

Table 3. Pregnancy outcomes of torsion patients in fresh ET and freeze-all periods.

Group 2:
Group 1: fresh ET freeze-all with FET p-value
Biochemical pregnancies % (n) 84.6 (11/13) 0a NA
Pregnancy losses % (n) 18.2 (2/11)b NA
Live births % (n) 69.2 (9/13) NA
OHSS: ovarian hyperstimulation syndrome, biochemical pregnancy; day 14 bhCG serum concentra-
tion of >5 IU/L, with appropriate rise.
a
No frozen embryo transfer performed.
b
Pregnancy losses; one 8-week miscarriage and one 15-week premature delivery of twins.

in Group 1, the incidence of OT was significantly lower in
Group 2. The possible reason for this outcome was that
using the agonist trigger, blastocyst-freeze-all and FET in
Group 2 resulted in a significantly lower incidence of
OHSS complications (0.05 vs. 2.4%, p < .001).
Ovarian torsion in IVF is rare, however, the consequen-
ces are significant, which include ovariotomy. In the pre-
sent study, the incidence and detorsion of OT in cycles
with ICSI and fresh transfer and ICSI-freeze-all and FET
were investigated. In total, 14 (0.09%) of the 15,577 treat-
ment cycles performed resulted in patients developing OT,
with 13 diagnosed in Group 1 and one diagnosed in
Group 2 (0.13 vs. 0.018%, p < .049). Although the total
oocyte obtained in the Group 2 was higher than in the
Group 1, the OT was seen to be fewer in the Group 2. The
possible reason for this event was that agonist triggered and
freeze-all cycles (Group 2) resulted in much fewer OHSS
cases. The OHSS in the Group 2 cycles was significantly
reduced compared to Group 1 (0.05 vs. 2.4%, p <.001).
The prompt management of OT will ensure the preserva-
tion of ovarian function without compromising pregnancy
outcomes. However, if the diagnosis is done late, an ooferec-
tomy may be inevitable. All 14 patients who developed OT
complications successfully underwent detorsion, with good
reproductive outcomes as the result of ET (i.e. pregnancy
loss rate of 18.2% and a LB rate of 69.2%). In addition,
choosing FET will provide a lesser risk of OT which could be
also offered to those patients who have a history of OT.
OT is a well-recognised event and constitutes a surgical
emergency. The patients usually present with abdominal
pain together with a palpable mass, with often accompa-
nying symptoms of nausea and vomiting, as well as a low-
grade pyrexia and leukocytosis (Pinto et al. 2001). The clin-
ical diagnosis of torsion is especially difficult in the cases
of OHSS because of the abdominal distension and
tenderness secondary to cyst formation. Five of the 14
patients diagnosed with OT in the present study devel-
oped OHSS. Ultrasound not only aids in the evaluation of
a pelvic mass, but also helps in the evaluation of ovarian
blood flow with a decrease in diastolic blood flow to the
ovary (Fleischer 1991).
In the past, the untwisting of the pedicle in cases of OT
was not advocated because of the fear of releasing an
embolus from a thrombotic vein. However, with better
diagnostic tools available and the liberal use of laparos-
copy, surgical treatment has become more commonplace.
Moreover, no cases of embolisation after untwisting have
been reported. Long-term follow-up of patients after lap-
aroscopic detorsion of ischaemic and apparently non-
viable ovaries has revealed a normal ovarian appearance
at subsequent surgery, with normal function (Ben-Rafael
et al. 1990). As the risk of thromboembolism has not been
seen to be increased in detorsion procedures (Cohen et al.
2003; Oelsner et al. 2003), the conservative but the
prompt surgical management of OT should be encouraged
to ensure the preservation of ovarian function.
The incidence of OT is increased in patients undergoing
ovulation induction with gonadotropins, specifically in
those with OHSS. Enlarged cystic ovaries because of ovar-
ian stimulation, especially when complicated by OHSS,
may predispose ovaries to torsion (Ben-Rafael et al. 1990;
Kemmann et al. 1990; Mashiach et al. 1990; Gorkemli et al.
2002). Three large studies determined the incidence of OT
after IVF to be 0.08–0.13% (Roest et al. 1996; Govaerts
et al. 1998; Gorkemli et al. 2002) but in the women with
OT, the rate of concomitant OHSS ranged from 1% to 33%
(Oelsner et al. 2003; Varras et al. 2004). Similar rates for
both incidences, OT and OHSS with OT, were obtained in
the present study for cycles with fresh ET, 0.13% and
30.8%, respectively.

Kemmann et al. (1990) reviewed 1303 women who had
a total of 6919 gonadotropin-induced cycles. Four women
developed OT, all of whom were pregnant, representing
an incidence of one in 162 pregnancies and one in 1730
gonadotropin treatment cycles. When patients conceive
after ovarian stimulation and in the setting of OHSS, the
ovarian cysts persist and this prolongs the period of the
increased risk of an adnexal torsion (Gorkemli et al. 2002).
Mashiach et al. (1990), investigating 201 ovarian stimula-
tion cycles complicated by OHSS, found 15 (7.5%) patients
to have the complication of unilateral OT. Moreover, 12
(16%) of the associated 75 pregnancies were complicated
by OT, while only three (2.4%) of the non-pregnant
patients had OT; therefore, concluding that pregnancy in
the setting of OHSS increased the likelihood of OT. The
results of the present study certainly confirm that preg-
nancy increases the risk of OT, as 84.6% of patients that
developed the complication in Group 1 were pregnant.
The use of GnRHa trigger as an alternative to hCG
came as an important breakthrough in IVF (Imoedemhe
et al. 1991). Segal and Casper (1992) demonstrated that
using agonist trigger in IVF prevents OHSS. Subsequently,
many trials in autologous cycles (Humaidan et al. 2011)
and donor oocyte cycles showed the effectiveness of
GnRHa trigger in OHSS prevention, with an incidence of
0% reported with the agonist (Bodri et al. 2009).
However, there have still been cases of OHSS observed,
even in freeze-all cycles (Mahajan et al. 2015). Moreover,
in the present study, the authors have for the first time
not only shown that OHSS was significantly reduced in
agonist triggered ICSI with freeze-all cycles, but that con-
comitantly there was also a significant reduction in OT,
notwithstanding, the potential for a higher risk of OHSS
(i.e. increased oocyte numbers), but also a significantly
higher pregnancy rate.
In addition, surgical detorsion was also observed to
have no impact on the obstetric outcomes of pregnancies.
Several case studies showed that successful pregnancy
and LB could be accomplished following the operative
detorsion of affected adnexa after an in vitro fertilisation
(Rackow and Patrizio 2007; Arena et al. 2009). In the pre-
sent study, 11 pregnancies were observed with OT cases.
Following the detorsion procedure, nine of them reached
the term pregnancy and delivered healthy babies.
In this large retrospective observational study, two dif-
ferent treatment strategies were compared, with the strat-
egy of the agonist trigger, freeze-all and FET resulting in
significantly reduced OT and severe OHSS complications.
While the present study shows significant evidence favour-
ing the use of agonist trigger and freeze-all in IVF, with
the comparison of large sample sizes, the evidence has to
be considered within the context of its limitations; the
retrospective analysis of data, the analysis of data from
sequential periods, and the low incidence of the primary
JOURNAL OF OBSTETRICS AND GYNAECOLOGY 5
(OT) and secondary (OHSS) outcome measures. The inci-
dence levels reported in the study therefore require a
meta-analysis of several studies to provide high quality
evidence of benefit or superiority. Moreover, implementing
the treatment strategy of agonist trigger, freeze-all and
FET reduces the potential of clinical significant iatrogenesis
and may, therefore, be good IVF practice particularly in
patients at risk of these complications.
Disclosure statement
No potential conflict of interest was reported by the author(s).
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