European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 50–54

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European Journal of Obstetrics & Gynecology and

Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

Full length article

Frozen embryo transfer or fresh embryo transfer: Clinical outcomes

depend on the number of oocytes retrieved
Bing Xu, Ya-qiong He, Yuan Wang, Yao Lu, Yan Hong, Yao Wang* , Yun Sun*
Shanghai Key Laboratory for Assisted Reproduction and Reproductive Genetics, Center for Reproductive Medicine, Renji Hospital, School of Medicine, Shanghai
Jiao Tong University, Shanghai, China

A R T I C L E I N F O A B S T R A C T

Article history: Objective: To establish a safe and effective clinical transplantation strategy for determining when to
Received 30 October 2016 prioritize frozen embryo transfers (FET) or fresh embryo transfers (ET) we conducted a retrospective
Received in revised form 11 April 2017 analysis study, examining several key clinical outcomes.
Accepted 25 May 2017
Study design: In a retrospective cohort study, 1423 patients (age < 40) were categorized into four groups
Available online xxx
according to the number of oocytes retrieved (15–18, 19–21, 22–24 and 25 oocytes). The clinical
outcomes of 1423 in vitro fertilization (IVF) cycles (896 fresh ET and 527 FET) were reviewed for each
Keywords:
group. Data demonstrated that the clinical pregnancy rates (PR) and live birth rate (LBR) of the FET group
Fresh embryo transfer
Frozen embryo transfer
was higher than those of the fresh ET group.
Live birth rate Results: Our study further indicates that the clinical benefits of FET become most meaningful when the
Pregnancy rate number of oocytes retrieved 19. When the number of oocytes retrieved 20,this difference was more
in vitro fertilization significant, with benefits in PR(odds ratio [OR] = 2.46, 95% confidence interval [CI]: 1.74-3.46, P < 0.001)
and LBR (OR = 2.27, 95% CI: 1.60–3.22, P < 0.001).
Conclusion: 20 oocytes retrieved may be the optimal cut-off point number for FET in order to achieve both
a successful pregnancy and a live birth.
© 2017 Elsevier B.V. All rights reserved.

Introduction
The development of assisted reproductive technology has
considerably improved the chances for infertile individuals to
conceive healthy children. Importantly, especially as the use of
assisted reproductive technology becomes more widespread,
many of the concerns associated with whole embryo freezing
have been dispelled. Using embryo cryopreservation technology,
embryo vitrification greatly reduces freezing-induced cell damage,
and the embryo recovery rate can reach as high as 95% [1]. With
these improvements in vitrification, frozen embryo transfer (FET)
may be a viable alternative to fresh embryo transfer (ET) [2,3]. A
series of reports pointed out that the implantation and pregnancy
rates (PR) of FET are higher than those of fresh ET [4–6], while
perinatal outcomes in terms of prematurity, low birth weight, and
being small for gestational age are similar or even better [7–9].
Fresh ET is typically the first choice when the number of oocytes
retrieved is a fat lot. However, in situations where fresh ET is not
appropriate for example, in a scenario where in clinicians want to
avoid ovarian hyperstimulation syndrome (OHSS), more and more
* Corresponding authors.
E-mail addresses: drwangyao@163.com (Y. Wang), syun1972@126.com (Y. Sun).
patients will choose whole embryo freezing [10]. Historically, FET
has been performed for patients because they were at high risk for
OHSS based on the following criteria: ovary diameter >9 cm; fluid
present around the uterus by ultrasound examination; high
hematocrit on the day of implantation; complaints of stomach
swelling and nausea [11]. FET was also used for patients according
to their personal preference or for cases with elevated progester-
one or suboptimal endometrial thickness.
To better determine safe and effective clinical transplantation
guidelines for prioritizing between FET and fresh ET, a total of 1423
women who were undergoing their IVF treatment cycle at the
Reproductive Medical Center from January 2011 to June 2013 were
identified and reviewed. This is a large retrospective cohort study;
patients were categorized into four groups according to the
number of oocytes retrieved (15–18, 19–21, 22–24 and 25
oocytes).Clinical outcomes for fresh ET and FET were assessed by
group. In particular, the goal of this study is to assess the
association between oocyte number and clinical outcome for each
embryo transfer method in order to (i) identify an optimal cut-off
point of number of oocytes retrieved to maximize the clinical PR
and LBR, (ii) to establish a safe and effective clinical transplantation
strategy between FET and fresh ET, and (iii) to guide the IVF
treatment much more effectively.

http://dx.doi.org/10.1016/j.ejogrb.2017.05.023
0301-2115/ © 2017 Elsevier B.V. All rights reserved.
 B. Xu et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 50–54 51

Table 1 levels, and serial transvaginal ultrasound examinations. Gonado-

Patient characteristics by group.
tropin doses were adjusted as needed. The administration of hCG
Index ET group FET group P-value with 4000–10,000 IU was applied to induce follicle maturation,
Number of IVF cycles 896 527 defined by the presence of 2 follicles with a mean diameter
Age (years old) 29.7  3.9 29.2  3.6 0.03 18 mm or 3 follicles with a mean diameter 17 mm. After hCG
Baseline FSH (IU/L) 7.27  1.72 7.19  4.5 0.67 administration of 36 h, oocytes were harvested by transvaginal
Baseline LH(IU/L) 4.78  3.11 5.18  2.85 0.03
ultrasound-guided oocyte aspiration. The IVF/ICSI fertilization
Baseline E2(pg/ml) 126.4  77.5 117.5  86.6 0.06
E2 on the day of HCG(pg/ml) 5283.2  2035.1 6905.9  2545.5 <0.001
method was selected based on semen analysis results, with the
Number of oocytes retrieved(n) 18.2  3.3 22.4  6.1 <0.001 types of insemination including IVF, ICSI.
Ratio of high-quality embryos 0.56  0.29 0.56  0.29 0.93 Embryos that reached the 6–8 cell stage with less than 20%
Number of embryos transferred 2.0  0.27 2.0  0.17 0.84 fragmentation were defined as good quality embryos. Embryo
(n)
transfer was employed under ultrasound guidance, usually on day
Endometrial thickness (mm) 10.0  1.86 9.9  2.04 0.38
3 after insemination. The number of embryos transferred complied
P<0.05, significant difference.
with the national regulations of China, and conformed to
individual patient requests when appropriate. In all cases, no
Materials and methods more than 3 embryos were transferred. Starting the day of oocyte
retrieval, the luteal phase was supported with 90 mg of intra-
Patient data and grouping vaginal progesterone gel (Crinone gel 8%; Serono) daily for a
minimum of five weeks.
In this study, the records of patients who received IVF/
intracytoplasmic sperm injection (ICSI) at the Center for Repro- FET
ductive Medicine, Renji Hospital, School of Medicine, Shanghai Jiao
Tong University, China from January 2011 to June 2013 were Vitrification of embryos was carried out on day 3 after oocyte
retrospectively identified and reviewed. Patients registered in the retrieval.The endometrium was prepared for FET by a natural or
analysis were <40 years of age, had 15 oocytes retrieved, and had hormone replacement cycle. Patients who received FET used oral
an endometrial thickness on the day of embryo transfer 7 mm. E2 (Progynova; Bayer) 4.0 mg daily for 10 days, and were
Patients were further categorized into four groups based on the monitored with serial ultrasonography to determine endometrial
number of oocytes retrieved: 15–18, 19–21, 22–24 and 25 thickness. If the endometrial thickness was <7 mm after 10 days,
oocytes. Meanwhile, clinical outcomes for fresh ET and FET were the dose of E2 was increased up to a maximum dose of 8.0 mg daily
analyzed for each group. to achieve a target endometrial thickness of at least 8 mm, or
Data collected from the medical records included patient age, approaching the endometrial thickness in the follicle aspiration
baseline hormone levels, estradiol (E2) on the day of human cycle. Crinone 8% was then begun once a day (day 0), and ET was
chorionic gonadotrophin (hCG) administration, number of oocytes performed 3 days after the start of progesterone. The same doses of
retrieved, number of high-quality embryos, and endometrial estrogen and progesterone were continued until 14 days after FET
thickness. A series of clinical outcome was also recorded such as when a serum b-hCG test was performed. If the pregnancy test was
PR, LBR, implantation rate and birth weight. This study was subject positive, hormone replacement was continued for another 2
to approval by the Institutional Review Board of Renji hospital, and weeks, and serial ultrasonography was used to determine fetal
the requirement of informed patient consent was waived because viability. Patients with ovulatory menstrual cycles were candidates
of the retrospective nature of the study. All patients provided for a natural FET cycle. Starting on day 10 of the menstrual cycle,
informed consent for all IVF procedures performed. transvaginal ultrasound was performed to confirm ovulation as
well as endometrial development. Examinations were then
IVF and fresh embryo transfer continued every 1–3 days until ovulation occurred. Supplemental
progesterone was provided to all patients (30 mg of oral
A conventional ovarian stimulation protocol (agonist protocol) dydrogesterone daily) at the first day of ovulation, and FET was
was performed. Gonadotropin stimulation was set up with either performed 3 days after the start of progesterone administration.
recombinant follicle stimulating hormone (rFSH) or urine highly The frozen embryo was thawed rapidly in 2 h before use.
purified FSH (Gonal F; Serono SA, Ivrea, Italy), with or without
human menopausal gonadotropin (hMG). The initial dose ranged Pregnancy assessment
from 112.5 to 300 IU per day, based on age, antral follicle count, and
baseline FSH level. During stimulation, the ovarian response was Pregnancy was confirmed by determining serum hCG concen-
monitored by E2, progesterone, and luteinizing hormone (LH) tration 14 days after ET in all patients. When the test results were
positive, ultrasound evaluations were performed 28–35 days after
Table 2 transfer, and clinical pregnancy was defined as a gestational sac
Correlation between the outcome of the ET and basic parameters. with fetal heart beat.
Index OR 95% CI P-value
Statistical analysis
Group(ET,FET) 1.75 1.32–2.37 <0.001
Age (years old) 0.99 0.96–1.02 0.42
Baseline FSH (IU/L) 1.05 0.98–1.12 0.16 Data are presented as mean  standard deviation (SD) for
Baseline LH(IU/L) 0.97 0.93–1.02 0.30 continuous variables, and number and percent for categorical
Baseline E2(pg/ml) 1.00 0.99–1.00 0.99 variables. An independent 2-sample t-test was used to examine
E2 on the day of HCG(pg/ml) 1.00 1.00–1.00 0.81
mean differences in characteristics treated as continuous variables
Number of oocytes retrieved(n) 0.99 0.96–1.03 0.85
Ratio of high-quality embryos 2.58 1.69–3.95 <0.001 between the fresh ET and FET groups, A multiple regression
Number of embryos transferred(n) 2.13 1.13v4.05 0.02 analysis was used to analyze the correlation between outcomes for
Endometrial thickness (mm) 1.09 1.02–1.16 0.01 the1423 patients who received more than 15 oocytes and
P < 0.05, significant difference. parameters, while the Chi-square test was used to examine the
52 B. Xu et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 50–54

Table 3
Compare the outcome of fresh and frozen-thawed embryo transfer.

ET group FET group P-value

Clinical pregnancy rate 41.96% (376/896) 55.60% (293/527) <0.001
Implantation rate 27.22% (490/1800) 38.02% (403/1060) <0.001
Miscarriage rate 10.37% (39/376) 11.26% (33/293) 0.71
Ectopic pregnancy rate 3.46% (13/376) 1.71% (5/293) 0.17
Multiplets pregnancy rate 29.52% (111/376) 36.52% (107/293) 0.06
Live-birth rate 36.27% (325/896) 48.20% (254/527) <0.001
Preterm rate 18.77% (61/325) 23.23% (59/254) 0.19
Birth weight 2955.7  608.30 3008.8  687.84 0.26
Low birth weight rate 21.75% (92/423) 21.49% (72/335) 0.93
OHSS rate(moderate or severe) 1.56% (14/896) 1.15(7/527) 0.72

P < 0.05, significant difference.

Table 4
Clinical outcome of fresh ET or FET in 4 groups according to the number of oocytes retrieved.

Patient groups (oocytes) Pregnancy rate (PR) Live-birth rate (LBR)

ET group FET group P-value ET group FET group P-value

Group 1 44.37% 47.13% 0.54 38.82% 42.04% 0.47
(15–18) (256/577) (74/157) (224/577) (66/157)
Group 2 39.57% 63.16% <0.001 33.69% 57.89% <0.001
(19–21) (74/187) (72/114) (63/187) (66/114)
Group 3 38.96% 64.81% <0.01 32.47% 53.70% <0.01
(22–24) (30/77) (70/108) (25/77) (58/108)
Group 4 29.10% (16/55) 52.03%(77/148) <0.01 23.64% 43.24% <0.05
(25) (13/55) (64/152)

P < 0.05, significant difference.

Fig. 1. Clinical pregnancy rate of patients with 19–21 oocytes. In group 2, patients with 19–21 oocytes, clinical PR with FET were higher than those of ET. * P < 0.05.

association between fresh ET and FET groups and categorical
variables.
To identify an optimal cut-off point for the number of oocytes
retrieved to maximize the clinical PR and LBR, a series of analyses
were carried out. First, all IVF cycles were stratified according to
the number of retrieved oocytes. Second, PR and LBR were assessed
between embryo transfer groups by Chi-square test at each
stratum. Then, the cut-off point was used to determine whether
effects of embryo transfer method (fresh or frozen-thawed) on
both outcomes were significant. All statistical analyses were
performed with SAS software, version 9.2 (SAS Institute Inc., Cary,
NC). A 2-tailed P-value <0.05 was deemed significant.
Results
A total of 1423 IVF cycles were conducted in 1423 patients, and
there were 896 fresh ET cycles and 527 FET cycles. Patients who
were treated with FET were younger (29.2  3.6 vs. 29.7  3.9,
P < 0.05), had higher E2 on the day of hCG testing
(6905.9  2545.5 pg/mL vs. 5283.2  2035.1 pg/mL, P < 0.001),and
 B. Xu et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 50–54
Fig. 2. Live birth rate of patients with 19–21 oocytes. In group 2, patients with 19–21 oocytes, clinical LBR with FET were higher than those of ET. * P < 0.05.
Table 5
Comparison of clinical pregnancy and live birth rates stratified by number of retrieved oocytes.
Number of retrieved oocytes <20
Outcome OR 95% CI
Clinical pregnancy 1.27 0.91–1.76
Live birth 1.26 0.90–1.76
For calculations, the reference was the fresh embryo transfer group.
OR, odds ratio; CI, confidence interval.
had more retrieved oocytes (22.4  6.1 vs. 18.2  3.3, P < 0.001)
(Table 1). Through amultiple regression analysis approaching
on1423 patients who received more than 15 oocytes, there was no
association between the outcome of the first embryo transplanta-
tion cycle with the following parameters: the age of female, E2 on
the day of HCG, and the number of oocytes retrieved. By contrast,
there was a positive association between the pregnancy outcome
and the different transplantation strategy (fresh ET or FET) (odds
ratio [OR] = 1.75, 95% confidence interval [95% CI]: 1.32–2.37,
P < 0.001), the ratio of high-quality embryos (odds ratio [OR] =
2.58, 95% confidence interval [95% CI]: 1.69–3.95, P < 0.05), the
number of embryos transferred (odds ratio [OR] = 2.13, 95%
confidence interval [95% CI]: 1.13–4.05, P < 0.05), and endometrial
thickness(odds ratio [OR] = 1.09, 95% confidence interval [95% CI]:
1.02–1.16, P < 0.05) (Table 2).
The implantation rate was higher in the FET group than in the
fresh ET group (38.02% vs. 27.22%, P < 0.001), and clinical PR and
LBR were higher in the FET group than in the fresh ET group (55.60%
vs. 41.96% for PR, P < 0.001; 48.20% vs. 36.27% for LBR, P < 0.001).
There were no differences noted in the miscarriage rates, ectopic
pregnancy rates, multiplet pregnancy rates, preterm rates, birth
weight, low birth rates of infants and OHSS rate between FET and
fresh ET groups (Table 3).
Depending upon the number of oocytes retrieved, clinical
outcome of patients with fresh ET was similar as FET in Group1(15–
18 oocytes).As the number of retrieved oocytes up to Groups 2–4
(19–21, 22–24 and 25 oocytes), clinical PR and LBR of FET group
were higher than those of fresh ET group (Table 4). Furthermore,
patients with 19–21 oocytes in Group 2, clinical PR with FET were
higher than those of ET (P < 0.05; Fig. 1). For LBR in Group 2,
patients with 19 oocytes, the difference was not significant
53
Number of retrieved oocytes 20
P-value OR 95% CI P-value
0.18 2.46 1.74–3.46 <0.001
0.20 2.27 1.60–3.22 <0.001
(P > 0.05); patients with 20 or 21 oocytes, FET were higher than
those of ET (P < 0.05; Fig. 2).
A comparison of PR and LBR, stratified by number of retrieved
oocytes with the cut-off point of 20 retrieved oocytes, was studied
in subsequent analyses in Table 5. In IVF cycles in which there were
<20 oocytes retrieved, FET technique was not associated with a
benefit in either clinical pregnancy rate (odds ratio [OR] = 1.27, 95%
confidence interval [95% CI]: 0.91–1.76, P = 0.18) or live birth rate
(OR = 1.26, 95% CI: 0.90–1.76, P = 0.20). However, when 20 oocytes
were retrieved, there was a 2-fold greater odds of having a clinical
pregnancy (OR = 2.46, 95% CI: 1.74–3.46, P < 0.001) and live birth
(OR = 2.27, 95% CI: 1.60–3.22, P <.001) with FET as compare to fresh
ET.
Discussion
IVF has become a vital technique in infertility treatment. Both
fresh ET and FET play decisive roles as the transfer method
employed in IVF. Fresh ET is the preferred transfer strategy because
it avoids any impact of freeze-thawing on embryo quality.
However, it also has several limitations, especially with patients
who face a high risk of OHSS [12]. With advancements in freezing
technology, FET has gradually become a viable alternative transfer
method applied in more situations. In particular, embryo
cryopreservation technology has improved dramatically such that
embryo vitrification greatly reduces freezing-induced cell damage,
and increases the embryo recovery rate [1].
Recently, many studies have shown that the pregnancy rates of
FET are consistently higher than those of fresh ET [2,13–16]. For one
reason, FET could use the best embryo owing to whole embryo
freezing right now, instead of using “second best” embryo
54 B. Xu et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 50–54
cryopreserved which morphologically superior siblings were
transferred as fresh embryos in the past typically freeze-thawed
cycles [17]. Another reason may be that embryo-endometrium
asynchrony occurring during a controlled ovarian stimulation
(COS) cycle results in an endometrium that is not receptive to
implantation.There is evidence which suggests that the perinatal
outcome in terms of prematurity, low birth weight and being small
for gestational age for FET are similar or even better than those of
fresh ET [7–9]. A meta-analysis conducted by Roque et al. [16]
demonstrating IVF outcomes are better with FET than fresh ET,
suggested that the results may be due to better embryo-
endometrium synchrony since with endometrial preparation,
the high estrogen state during a COS cycle results in an
endometrium that is not receptive to implantation [3].
A goal of our study is to find a balance between maximum
treatment success and a minimum risk of complications. Excessive
human operation may pose an undefined risk to offspring. Patients
may be affected both psychologically and economically by the
cancellation of fresh embryo transfers. An objective clinical index
was searched to provide valuable information for a safeand
effective embryo transfer strategy.
In this study, clinical outcome of patients with fresh ET was
similar as FET when patients with 15–18 oocytes. When the
number of retrieved oocytes exceeded19, clinical PR of FET groups
was higher than those of fresh ET groups; once the number of
retrieved oocytes exceeded 20, LBR achieved the same trends. Just
as important, other outcomes including the miscarriage rates,
ectopic pregnancy rates, multiplet pregnancy rates, preterm rates,
birth weight and low birth rates of infants were similar between
the groups. These results indicated that a minimum of 20 oocytes
retrieved can maximize outcomes while minimizing complica-
tions. This notion was supported by subsequent analyses: when the
number of retrieved oocytes 20, there was a 2-fold greater odd of
PR and LBR in FET groups as compared to fresh ET groups. These
results are consistent with several previous studies [18,19], in
which LBR increased after an FET benefit was associated with the
number of oocytes retrieved.
There are certain important limitations to our study. The
primary limitation of this study is the retrospective nature of the
analysis. Secondly, our study is limited by the selection of the
patient population. In further studies, samples will be expanded,
far more than 1423 patients.
In conclusion, the results of this study show that at least 20
oocytes retrieved may be the optimal cut-off point number for FET
in order to maximize the likelihood of achieving both successful
pregnancy and live birth with minimal complications.FET is a more
powerful and safe method instead of fresh ET: when 15–19 oocytes,
either method is fine; when beyond 20 oocytes, FET is highly
recommended.
Declaration of interest
There is no conflict of interest that could be perceived as
prejudicing the impartiality of the research reported.
Acknowledgements
This work was supported by the National Basic Research
Program of China (973 Program, Grant No. 2014CB943300),
Research Special Fund of National Health and Family Planning
Commission (Grant No. 201402004); The National Natural
Science Foundation of China (Grant No. 81571499); the Chinese
National Natural Science foundation (81401263); Shanghai
municipal health and Family Planning Commission of tradition-
al Chinese medicine research (2014LP010A); Research project of
Shanghai municipal health and Family Planning Commission
(140826110504864) and The research was also supported from
Shanghai Key Laboratory for Assisted Reproduction and
Reproductive Genetics, Renji Hospital, Shanghai Jiao Tong
University School of Medicine, Shanghai, China (Grant No.
12DZ2260600).
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