Reproductive outcomes of IVF patients with unicornuate uteri
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Article
Reproductive outcomes of IVF patients with
unicornuate uteri
Kemal Ozgur, Hasan Bulut, Murat Berkkanoglu, Kevin Coetzee *
Antalya IVF, Halide Edip Cd. No:7, Kanal Mh., Antalya 07080, Turkey
Kemal Ozgur completed his training in Obstetrics and Gynecology in 1993 at the Akdeniz University, Turkey, after
which he completed a 3-year fellowship at the ART center of Tygerberg Hospital, South Africa and at the Jones
Institute, Norfolk, USA. In 1999, as Clinical Director he founded Antalya IVF, an ART centre in the south of Turkey.
KEY MESSAGE
IVF pregnancies in patients with unicornuate uteri are high risk. Therefore, future investigations should focus
on pre-conception strategies and post-conception care to reduce clinical pregnancy loss and improve peri-
natal outcomes in these patients.
A B S T R A C T
In this retrospective observational study, the pregnancy, perinatal and obstetric outcomes of patients diagnosed with unicornuate uteri were compared with
those of patients with normal uteri after undergoing intracytoplasmic sperm injection (ICSI) with fresh and cryopreserved embryo transfer. From a select
population of 9676 infertile patients receiving IVF treatment, 75 (0.78%) were diagnosed with unicornuate uteri between January 2009 and December 2015.
Fifty of them underwent ICSI treatment, with 90 fresh and cryopreserved embryo transfers. No significant differences were found between the biochemical,
clinical and implantation rates of the first treatment cycles of the two groups; the ongoing pregnancy rate was significantly lower (P = 0.042; 34.0 versus
53.0%) in the unicornis group, as the result of a clinically higher clinical pregnancy loss rates (22.0 versus 15.9%). Twenty-three clinical pregnancies resulted
from the 50 first treatment cycles in the unicornis group, resulting in 14 live births, one ongoing pregnancy, five miscarriages, one ectopic pregnancy and two
terminations. The 14 live births were delivered at 35.9 gestational weeks, with seven preterm (REPRODUCTIVE BIOMEDICINE ONLINE 34 (2017) 312–318 313
different populations, and found the prevalence to be 5.5% in an patient numbers. In this study, analysing 7 years of patient fertility
unselected population, 8.0% in infertile women, 13.3% in women who examinations at a single assisted reproduction technology centre, it
have experienced recurrent miscarriage and 24.5% in women who was found that a relatively large number of patients were diag-
have experienced recurrent miscarriage and infertility. The preva- nosed with unicornuate uteri and had received IVF treatment. In this
lence of unification defects that only include bicornuate, unicornuate study, we, therefore, analysed the reproductive outcomes (implan-
and didelphic uteruses are, however, considerably lower, with a preva- tation, perinatal and obstetric) of patients with unicornuate uteri who
lence of 0.1% in unselected populations and a prevalence of 0.5% received IVF treatment with the use of ICSI, fresh embryo transfer
prevalence in women with infertility (Chan et al., 2011a). and frozen embryo transfer (FET) of both supernumerary and freeze-
The unilateral development of the Müllerian ducts, with the con- all embryos, describe the unicornuate uteri classes diagnosed and
tralateral part either not developing or developing incompletely, results assess the incidence observed.
in a unicornuate uterus with an often unique ‘banana-shaped’ ap-
pearance. The unicornuate uterus classification consists of two
sub-classes: a unicornuate uterus with a communicating or non-
communicating functional rudimentary horn; and a unicornuate uterus Materials and methods
with a non-functional rudimentary horn, or no horn. Female con-
genital uterine anomalies may often be associated with cervical, Participants
vaginal, organ anomolies, or all, i.e. kidney agenesis (Grimbizis et al.,
In this study, the files of patients who had first infertility consulta-
2013; Reichman et al., 2009).
tions at a single assisted reproduction technique centre between
Controversially, depending on the classification system, a unicornis
January 2009 and December 2015 were screened to identify those pa-
uterus may be defined as having normal cervical and vaginal anatomy
tients who were diagnosed with unicornuate uteri, with the relatively
(American Fertility Society, 1988) or unilateral aplasia (Grimbizis et al.,
low incidence resulting in a 7-year study period. The long study period
2013). In a recent prospective observational study, this inconsis-
spanned two distinct technological periods: incubator class and culture
tency of definition was challenged, with the authors subsequently
media type. Cleavage-stage embryos were used between 2009 and
recommending caution in the use of the ESHRE-ESGE classification
2011 and blastocyst stage embryos were used between 2012 and 2015.
system (Ludwin and Ludwin, 2015). Nonetheless, any co-existing patho-
Although all IVF treatments received by patients with unicornuate uteri
physiologies may increase the risk for poor reproductive outcomes,
were followed up and analysed, only the first IVF treatment cycle out-
i.e., increased rate of ectopic implantation, placental complications,
comes (unicornis group, n = 50) were compared with the first treatment
first- and second-trimester miscarriage, fetal mal-presentation, in-
cycles of a matched control group of patients (control group, n = 100).
trauterine growth retardation, intrauterine fetal demise, preterm birth
The matched control cycles were selected randomly from cycles
and, ultimately, long-standing infertility (Khati et al., 2012; Reichman
carried out during the study period. The matching criteria used were
et al., 2009; Taylor and Gomel, 2008). It has been suggested that the
as follows: embryo transfer strategy, i.e., fresh embryo transfer or
mechanisms underlying the adverse reproductive outcomes associ-
FET after ICSI freeze-all; woman’s age; number of oocytes re-
ated with unicornuate uteri involve abnormal uterine and placental
trieved at oocyte collection; and antral follicle count (AFC). The control
blood flow, decreased uterine muscle mass and decreased cervical
cycles only included cycles of patients with anatomically normal uteri,
competence. All mechanisms that tend to regulate pregnancy main-
with no intrauterine abnormalities. Ethics committee approval was
tenance rather than embryo implantation (Khati et al., 2012; Reichman
not sought for this retrospective study as patients provided in-
et al., 2009).
formed consent before treatment, which included an agreement to
In the asymptomatic patient with infertility, i.e., no dysmenor-
use their anonymized data for research. This was in accordance with
rhoea or chronic pelvic pain, the challenge lies in the accurate and
Section Five of the 1982 Turkish Constitution entitled ‘Privacy and Pro-
effective diagnosis of the cause. Although, both invasive and non-
tection of Private Life’.
invasive modalities have extensively been used, the current evidence-
based recommendation is for the newly innovated non-invasive
modalities to preferably be used in the diagnosis of congenital uterine Diagnosis
anomalies (Practice Committee of the American Society for
Reproductive Medicine, 2016). An accurate diagnosis, however, may At first consultation, a standard set of infertility work-up proce-
require the use of multiple modalities to ensure both the inner and dures and tests were carried out or requested (medical and fertility
outer uterine contours are accurately assessed, i.e., transvaginal ul- history, physical examination, TVS, hormone analysis and semen analy-
trasound examination (transvaginal scan [TVS] and two-and three- sis). All TVS examinations were two-dimensional examinations carried
dimensional scans), magnetic resonance imaging, saline-infused out by three experienced gynaecologists (KO, HB, and MB) using the
sonography, hysteroscopy, or both (Ludwin et al., 2011; Grimbizis et al., same ultrasound system (Voluson 730 Pro, GE Healthcare Ultra-
2016; Practice Committee of the American Society for Reproductive sound, Milwaukee, WI, USA) and volumetric intra-vaginal probe (GE
Medicine, 2016). This combined modality use may be of particular im- RIC 5–9 MHz 3D/4D; GE Healthcare Ultrasound) for the full study
portance in the diagnosis of unicornuate uteri, because of its unique period. Two-dimensional TVS was used to screen patients for fea-
echogenic characteristics, i.e., small cavity, lateral deviation and ru- tures that suggest the presence of uterine or intrauterine anomalies.
dimentary horn (Khati et al., 2012). Unlike some other congenital Patients in whom TVS suggested the presence of an anomaly were
uterine anomalies, these may not require surgery before IVF treat- scheduled for the clinically most appropriate diagnostic procedure,
ment (Ludwin et al., 2011). i.e., hysterosalpingography, saline-infused sonography or hysteros-
Although numerous studies and reviews have reported on copy or laparoscopy. For example, all tubal anomaly and pathology
unicornuate uteri, the earliest of which may be the study of Alexander were confirmed by hysterosalpingography and agenesis by laparos-
(1947), most have only included specific cases or studies with small copy. Unicornuate uteri were classified on the basis of the American314 REPRODUCTIVE BIOMEDICINE ONLINE 34 (2017) 312–318
Fertility Society classification system (American Fertility Society, 1988). Embryo transfer
For example, a unicornuate uterus with (Class IIa,b,c) or without (Class
IId) a rudimentary horn and whether the uterus deviated to the left All transfer procedures were carried out using a glass syringe (50 μL,
or the right. The potential complications of pregnancy and ulti- Hamilton, Giarmata, Romania) attached to an embryo replacement
mately the chance of having a successful live birth were thoroughly catheter (Wallace, Smiths Medical, Kent, UK) and trans-abdominal
discussed with patients diagnosed with unicornuate uteri before start- ultrasound guidance. All fresh transfers were carried out on oocyte
ing IVF treatment. No patients underwent therapeutic surgery before retrieval + 2, 3, or 5 and all subsequent cryopreserved transfers on
starting treatment. progesterone + 2, 3, or 5.
Outcomes and statistics
Ovarian stimulation and oocyte retrieval
Patient factors recorded included age, infertility duration, BMI, AFC
All IVF treatment cycles used ovarian stimulation with GnRH antago- and cause of infertility. The primary outcome measures recorded were
nist (Cetrotide, 0.25 mg, Merck Serono, Istanbul, Turkey) co-treatment related to pregnancy and perinatal outcomes, under the following defi-
and a combination of recombinant FSH (150–375 IU, Gonal-F, Merck nitions. A transfer cycle with a beta-HCG serum concentration of over
Serono, Istanbul, Turkey) and HMG (75–150 IU, Menopur, Ferring Phar- 30 IU/L was defined as a biochemical pregnancy, a cycle with a fetal
maceuticals, Mumbai, India). The drug doses were based on patient heart observed on ultrasound after 5 weeks of gestation was defined
age, body mass index (BMI), AFC and previous ovarian stimulation out- as a clinical pregnancy, and a cycle with a pregnancy developing beyond
comes. Final oocyte maturation was triggered when three or more 14 weeks of gestation was defined as an ongoing pregnancy. The ratio
follicles reached 17 mm or wider in diameter. The triggers used were of the number of fetal hearts to the number of blastocysts trans-
HCG (250 ug/0.05 ml, Ovidrel, Merck Serono, Turkey), a combina- ferred was converted to a percentage for the implantation rate.
tion of HCG and gonadotrophin-releasing hormone agonist (0.2 mg, Gestational age was defined as the number of days between oocyte
Gonapeptyl®, Ferring Pharmaceuticals, India) or GnRHa, depend- retrieval and end of pregnancy plus 14 days, converted to unit weeks.
ing on ovarian response to stimulation. The oocyte retrieval procedures A miscarriage was defined as the spontaneous loss of a clinical preg-
were carried out 36 h after trigger. In period 1, Cook Medical (G20538, nancy before week 22 of gestation. A very preterm delivery was the
Brisbane Australia) and in period 2, Reproline (461230LF, Rheinbach, delivery of an infant before 32 weeks of gestation and a preterm de-
Germany), single lumen oocyte aspiration needles were used. livery was a delivery before 37 weeks of gestation. A live birth was
defined as a pregnancy delivered after 22 weeks of gestation with a
In-vitro culture and embryo assessment live infant discharged from hospital. A low birth weight delivery was
a live infant delivered weighing less than 2500 g and a very low birth
Oocyte manipulation and embryo culture were carried out using the weight delivery was a live infant delivered weighing less than 1500 g.
Cook Medical media (Sydney IVF, Brisbane, Australia) in period 1 and All twin pregnancies in the unicornis group were reduced to single-
SAGE media (Origio, Malov, Denmark) in period 2 of the study. Incu- tons, based on the personal experience of the authors (KO, HB, and
bation conditions were set at 6% CO2 and 37.0oC (Heracell, Thermo MB), and evidence of some benefit (Gupta et al., 2015; Hasson et al.,
Scientific, San Jose, CA, USA) in period 1 and at 6% CO2, 5% O2 and 2011).
37.0oC (K-Systems, Kivex Biotec ltd, Birkerod, Denmark) in period 2. Patients were provided with perinatal care, i.e. serial ultrasound
All inseminations were carried out using ICSI. Embryos and blasto- examinations, for the first 8 weeks of their pregnancies, where pos-
cysts were assessed for selection according to conventional sible, at Antalya IVF. Thereafter, obstetricians independent of Antalya
parameters (Alpha Scientists in Reproductive Medicine and ESHRE IVF and chosen by patients themselves provided the perinatal and ob-
Special Interest Group of Embryology, 2011). stetric care. Antalya IVF only provided the obstetricians with all relevant
clinical information regarding the patients’ fertility history and current
treatment outcomes. Antalya IVF received limited perinatal and ob-
Embryo and blastocyst cryopreservation stetric information from both the patient and the obstetrician, with
a system alert actively requesting pregnancy information to be con-
Freezing and thawing of cleavage stage embryos were carried out using firmed at regular intervals during pregnancy and most importantly
slow-freeze (Kryo 360, Planer PLC, Sunbury-on-Thames, Middle- on the date of expected delivery.
sex, UK) and rapid-thaw technology, with Vitrolife (Freeze kit and Thaw MedCalc version 13.0.6 (MedCalc Software, Ostend, Belgium) was
kit, Göteborg, Sweden) media and CBS straws (CryoBio System, L’Aigle, used for statistical analysis and for obtaining the confidence inter-
Normandy, France). Vitrification and warming of blastocysts were vals and risk ratios. Descriptive statistics were presented as the mean
carried out using ultra-rapid technologies (Cryotop, Kitazato BioPharma and standard deviation for continuous data and as percentages for
Co. Ltd, Fuji-city, Japan), using Cryotop Safety Kits and containers. the categorical data. The independent samples t-test was used to
compare the means, and the chi-squared or Fisher’s exact test was
Cryopreserved embryo transfer cycle used to determine statistical significance between percentages. A sta-
tistical value of P < 0.05 was considered significant.
Cryopreserved embryo transfers were carrired out in artificial cycles,
with endometria prepared using a step-up regimen of oestrogen
supplementation (2 mg, 4 mg, 8 mg, Estrofem, Novo Nordisk, Istan- Results
bul, Turkey) and endometrium–embryo synchronization was carried
out using progesterone supplementation (8% twice per day, Crinone, The incidence of unicornuate uteri in the study centre’s infertile popu-
Merck Serono, Istanbul, Turkey) starting on day 15 of oestrogen. lation was 0.78%, with 75 out of 9676 first infertility consultationREPRODUCTIVE BIOMEDICINE ONLINE 34 (2017) 312–318 315
Table 1 – Patient characteristics and cause of infertility.a
Unicornis Control P-valuea
Cycles n 50 100
Patient characteristics
Age (years) mean (std) 30.9 (4.82) 30.9 (4.84) NS
Body mass index (kg/m2) mean (std) 26.0 (5.20) 24.4 (3.80) 0.034
Infertility duration (years) mean (std) 5.7 (3.98) 4.3 (3.77) 0.037
Antral follicle count mean (std) 20.5 (11.90) 19.8 (13.66) NS
Cause of infertility
Male n (%) 14 (28.0) 48 (48.0) 0.019
Unexplained n (%) 22 (44.0) 34 (34.0) NS
Anovulatory n (%) 1 (2.0) 7 (7.0) NS
Decreased ovarian reserve n (%) 7 (14.0) 8 (8.0) NS
Tubal n (%) 6 (12.0) 3 (3.0) NS
NS, not significant.
a
P < 0.05 (significant).
patients diagnosed with a unicornuate uterus. The variant distribu- (P = 0.037) and incidence of male factor significantly lower (P = 0.019);
tion of the unicornuate uteri was 31 (41.3%) left-unicornuates, 26 all other characteristics and causes were not significantly different
(34.7%) right-unicornuates, 12 (16.0%) left-unicornuates with non- between the two groups.
functional right rudimentary horn and six (8.0%) right-unicornuates The 50 first treatment cycles of the patients with unicornuate uteri
with left non-functional rudimentary horn. Eight patients had addi- included 34 (68.0%) ICSI with fresh embryo transfer and 16 (32.0%)
tional intrauterine anomalies: polyps (n = 6), myoma (n = 1) and ICSI freeze-all with FET (Table 2). The first treatment cycle preg-
adhesions (n = 1); seven patients had associated anomalies: tubal factor nancy outcomes of patients with unicornuate uteri were compared
( n = 6) and ovarian agenesis ( n = 1). None of the patients with with the outcomes of matched control patient cycles, with cycles
unicornuate uteri had any evidence of cervical or vaginal anomalies. matched according to woman’s age and oocyte number at the time
Fifty of the 75 patients diagnosed with a unicornuate uteri under- of oocyte retrieval. The biochemical pregnancy, clinical pregnancy and
went IVF treatment in the study period, January 2009 to December implantation rates were non-significantly different between the two
2015. Patient characteristics and causes of infertility of the two groups groups. The number of embryos transferred was also non-significantly
are presented in Table 1. In the unicornis group, BMI was signifi- different between the two groups, although the number transferred
cantly higher (P = 0.034), mean infertility duration significantly longer was higher and the single embryo transfer proportion was lower (27
Table 2 – Intracytoplasmic sperm injection cycle data and pregnancy outcomes.
Unicornus Control P-valueh RRi (95% CI)
Cycles N 50 100
Oocytes retrieveda Mean (SD) 18.5 (11.27) 17.9 (11.88) NS
Embryo transfer
Fresh n (%) 34 (68.0) 68 (68.0)
Frozenb n (%) 16 (32.0) 32 (32.0)
Embryos transferred Mean (SD) 1.7 (0.71) 1.90 (0.66) NS
1 22 (44.0) 27 (27.0)
2 21 (42.0) 56 (56.0)
3 7 (14.0) 17 (17.0)
Pregnancy
>30 IU beta – HCGc n (%) 27 (54.0) 63 (63.0) NS 0.86 (0.637 to 1.154)
Clinicald n (%) 23 (46.0) 58 (58.0) NS 0.79 (0.563 to 1.118)
Clinical pregnancy loss n (%) 6 (22.0)e 10 (15.9) NS 1.40 (0.566 to 3.465)
Ongoingf n (%) 17 (34.0) 53 (53.0) 0.042 0.64 (0.418 to 0.984)
Implantation Rateg % (n) 34.1 (29/85) 39.5 (75/190) NS 0.89 (0.629 to 1.247)
a
Oocytes retrieved from source cycle.
b
First frozen embryo transfer after an intracytoplasmic sperm injection freeze-all cycle.
c
> 30 IU beta-HCG; blood serum level on day 14 after oocyte retrieval.
d
Fetal heart on ultrasound at over 5 weeks of gestation.
e
Five miscarriages and one ectopic pregnancy.
f
A pregnancy developing beyond 14 weeks of gestation. Includes two ongoing pregnancies in the unicornis group, which were terminated due to aneuploidy
at over14 weeks’ gestation.
g
The ratio of the number of fetal hearts to the number of blastocysts transferred.
h
P < 0.05 was considered significant.
i
Risk ratios and 95% confidence intervals.316 REPRODUCTIVE BIOMEDICINE ONLINE 34 (2017) 312–318
ment cycle of the control group, on the other hand, was potentially
Table 3 – Perinatal outcomes in the first and subsequent fresh
49.3% (75/152). Moreover, of the 50 patients with unicornuate uteri
or cryopreserved embryo transfer cycles in women with a
unicornuate uterus.e treated, 54% (27/50) had a live birth or have an ongoing pregnancy.
In comparison, of the 100 control patients treated, 70% (70/100) had
First cycle Cumulative
a live birth or have an ongoing pregnancy.
Cycles n 50 90 In the unicornis group, 50 of the embryo transfers were first treat-
Clinical pregnanciesa n 23 39
ments, 27 were second treatments, nine were third treatments, three
Singleton n (%) 17 (73.9) 27 (69.2)
Twinb n (%) 6 (26.1) 12 (30.8)
were fourth treatments, and one was a fifth treatment, with per cycle
Perinatal outcomes live birth rates of 29.2% (n = 14), 22.2% (n = 6), 33.3% (n = 3), 66.7%
First-trimester loss n 6 8 (n = 2), and 0% (n = 0), respectively. In total, 41 of the embryo trans-
Second-trimester loss n 0 1 fers were fresh embryo transfer and 49 were FET; 68% (n = 34) of
Clinical terminationsc n 2 2 the first treatments were fresh embryo transfers and 82.5% (n = 33)
Ongoing pregnancyd n 1 3
of the subsequent treatments were FET. The per cycle live birth rate
Live birth n (%) 14 (28.0) 25 (27.8)
for the fresh embryo transfers was 34.0% (n = 14) and 22.4% (n = 11)REPRODUCTIVE BIOMEDICINE ONLINE 34 (2017) 312–318 317
contrary to the right deviated prevalence reported previously (Caserta limited amount of obstetric data were available for analysis. The
et al., 2014; Heinonen, 1997). strengths of the study were the large number of patients diagnosed
Even though the two major reviews that have examined the with unicornuate uteri, the large number of IVF cycles completed,
effect of unicornuate uteri on reproductive outcomes compared the and that no patients with unicornuate uteri were lost to follow-up,
natural conception outcomes of women with and without unicornuate with only two missing data points, i.e., birth weights, in each of the
uterI, the outcomes were remarkably consistent with those ob- unicornis and the control group.
served in this IVF study. In the review by Reichman et al. (2009), the Although it is unclear whether any interventions during preg-
effect of unicornuate uteri was assessed in 290 women. The follow- nancy decidedly improved obstetric outcomes, it is clear that the
ing outcomes were reported: a 2.7% ectopic pregnancy rate; 24.3% abnormal uterine and placental blood flow decreased uterine cavity,
first- trimester miscarriage rate; 9.7% second-trimester miscar- decreased uterine muscle mass, and increased cervical incompe-
riage rate; 20.1% preterm delivery rate; 10.5% rate of intrauterine tence associated with unicornuate uteri, which significantly increases
fetal demise; and a 49.9% per clinical pregnancy live birth rate. In the risks for miscarriage and preterm delivery (Khati et al., 2012).
the review by Chan et al. (2011b), the outcomes of 3805 women Further research is, therefore, essential, to establish the optimal ob-
were examined, and those women with unification anomalies, and stetric management strategy of this unique high-risk patient group.
in particular unicornuate uteri, were found to have reduced clinical Recent improvements in in-vitro technologies related to embryo culture
pregnancy, increased first-and second-trimester miscarriage and and cryopreservation have resulted in improved reproductive out-
increased preterm delivery compared with women with normal comes in assisted reproduction techniques and, with assured future
uteri. All the studies therefore confirm that the risks of first- improvements, may result in an increasing number of pregnant pa-
trimester pregnancy loss and preterm delivery were of greatest tients with unicornuate uterI, all of whom will require intensive
clinical significance, with the significance determined by the patho- obstetric care.
physiology of the uterine anomaly and any associated anomalies.
The use of IVF in the treatment of patients with unicornuate uteri
A R T I C L E I N F O
did not significantly change the unicornuate uterus pregnancy risk
profile other than potentially increasing the live birth rate per Article history:
clinical pregnancy (about 50 versus 70%). Received 18 February 2016
The reduced and adverse reproductive outcomes observed in Received in revised form 7 December 2016
this study and corroborated by most other studies commands that Accepted 9 December 2016
patients with unicornuate uteri are thoroughly informed of their Declaration: The authors report no
chance of live birth, the complications of pregnancy and the pos- financial or commercial conflicts of
sible therapies they may be confronted with during the course of a interest.
pregnancy. In this study, 3.5 embryo transfers were carried out for
every live birth delivered; many patients may, therefore, have to
Keywords:
undergo at least three IVF treatments with embryo transfers before
IVF
re-evaluating their commitment to pregnancy. To prevent any in-
Live birth
creased risks, single embryo ttansfer should be mandatory in the
Obstetric care
treatment of patients with unicornuate uteri, so as to avoid the
Pregnancy
added complications of multiple gestations. If pregnant, these pa-
Unicornuate uterus
tients must be informed that they may have a 50% chance of a
preterm delivery or a threatened preterm delivery. All pregnant
patients with unicornuate uteri must therefore be considered to be
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