doi:10.1111/jog.13872 J. Obstet. Gynaecol. Res.

2018

Impact of endometrial thickness during menstruation

and endometrial scratching on the pregnancy
in frozen–thawed embryo transfer

Wen-juan Liu*, Ying-qi Nong*, Jian-xing Ruan, Ye Chen, Lin Fan, Qian-wen Huang
and Feng-hua Liu†
Department of Reproductive Medical Center, Guangdong Women and Children Hospital, Hospital of Guangzhou Medical
University, Guangzhou, China

Abstract
Aim: This study aimed to investigate the impact of endometrial thickness (EMT) during menstruation and
endometrial scratching on the pregnancy in frozen–thawed embryo transfer (FET).
Methods: About 1298 patients receiving FET were retrospectively analyzed and divided according to EMT
on the 4th or 5th day of menstruation. Group A: EMT ≤ 3.0 mm; Group B: EMT 3.1–5.0 mm; Group C: EMT
5.1–7.0 mm and Group D: EMT > 7.0 mm. Patients in Group D were further divided to scratching group
and nonscratching group. Endometrial growth was defined as the change in EMT from 4th or 5th day of
menstruation to the day of embryo transferred.
Results: We found no significant differences in general conditions among four groups (P > 0.05). The aver-
age EMT during menstruation and differences in inter-group endometrial growth of four groups had statisti-
cal significance (P < 0.05). The pregnancy rate and implantation rate of Group D were significantly lower
than other groups (P < 0.001). Pregnancy rate (68.29% vs 53.26%) and implantation rate (52.67% vs 36.34%)
in endometrial scratching group were higher than those in nonscratching group (P < 0.05).
Conclusion: Higher EMT during menstruation adversely affects pregnancy outcomes following FET. Endo-
metrial scratching may improve the receptivity of endometrium and increase the rate of embryo implanta-
tion and pregnancy.
Key words: endometrial growth, endometrial scratching, endometrial thickness, frozen–thawed embryo
transfer, pregnancy outcome.

Introduction affect the chance of implantation after embryo trans-

Frozen–thawed embryo transfer (FET) has been
widely used in clinical practice in recent years
because it can increase cumulative pregnancy rate,
reduce the number of ovulation induction, reduce the
incidence of ovarian hyperstimulation syndrome and
diminish the risk of ectopic implantation in patients.1
How to further improve FET pregnancy rate is still
the focus of reproductive medicine. Mechanical endo-
metrial scratching has been proposed to positively
fer, but the timing of scratch, surgical methods and
the suitability of patients have been controversial.2
In the clinical practice, there are many indications
for endometrial scratching such as women with recur-
rent implantation failure, unexplained infertility and
endometriosis.2 In this study we retrospectively ana-
lyzed 1298 patients who received FET for the first
time in Department of Reproductive Medical Center
of Guangdong Women and Children Hospital
between November 2014 and November 2016. We

Received: February 14 2018.

Accepted: November 2 2018.
Correspondence: Professor Feng-hua Liu, No. 521 Xingnan Road, Panyu District, Guangzhou, 511442, China. Email: liushine2006@163.com
*These authors contributed equally to this work.

© 2018 Japan Society of Obstetrics and Gynecology 1

W.-j. Liu et al.
investigated the association of endometrial thickness
(EMT) during menstrual period with pregnancy out-
comes following FET, and we applied endometrial
scratching to women with EMT > 7.0 mm during
menstruation and performed histology analysis to
confirm our conclusion.
Methods
Subjects
This study enrolled total 1298 infertile patients in the
first cycle of FET in the Department of Reproductive
Medical Center of Guangdong Women and Children
Hospital between November 2014 and November
2016. Patients who underwent endometrial scratching
signed the informed consent form and the protocols
were approved by institutional Ethics Committee.
To be included in this study, women had to be
20–40 years old, and had 25–35 days of menstrual
cycle with 4–7 days in menstruation, had more than
two eligible embryos and at least one high-quality
embryo according to Peter cleavage embryo scoring
system.3 Patients with any uterine anatomy abnormal-
ities such as septate uterus, bicornuate uterus, double
uterus, unicornuate uterus and rudimentary uterus,
uterine or intrauterine lesions such as endometrial
polyps, uterine adhesions, submucosal myoma of
uterus and endometrial tuberculosis, hydrosalpinx,
recurrent miscarriage, chromosome abnormalities, or
more than 1.0 ng/mL of progesterone during men-
struation, or those are in preimplantation genetic
diagnosis/screening (PGD/PGS) were excluded.
Grouping
The patients were divided into four groups according
to EMT on the 4th or 5th day of menstruation, using
the cut-off by the 5th (3 mm), 50th (5 mm) and 95th
(7 mm) percentile of the whole population distribu-
tion: Group A: EMT ≤ 3.0 mm; Group B: EMT
3.1–5.0 mm; Group C: EMT 5.1–7.0 mm and Group
D: EMT > 7.0 mm. Patients whose EMT during men-
strual period was more than 7 mm on the 4th or 5th
day of menstrual cycle voluntarily chose whether to
accept endometrial scratching surgery. Endometrial
growth was defined as the change in EMT from 4th
or 5th day of menstruation to the day of embryo
transferred. Patients in the scratching group under-
went endometrial scratching on the 4th or 5th day of
the menstrual cycle during FET preparation protocol.
2 © 2018 Japan Society of Obstetrics and Gynecology
Patients with combined EMT ≥ 7.0 mm without treat-
ment were grouped as the nonscratching group.
Natural cycle preparation
Patients with regular menstruation and ovulation will
undergo FET in a natural cycle. On the 9th or 11th
day of their cycle, transvaginal ultrasound was used
to monitor ovarian follicles. When the diameter of
dominant follicle was ≥14 mm, urinary luteinizing
hormone (LH) level was tested until LH surge
occurred. If the dominant follicle with diameter more
than 18 mm did not show LH surge, 5000–10 000 IU
of human chorionic gonadotropin (HCG, Livzon
Pharmaceutical Factory, Zhuhai, China) was injected
intramuscularly to induce ovulation. After ovulation,
thawing and transferring were performed. The time
for transplantation depended on the time when
embryo was frozen. Cycles were canceled if no ovula-
tion occurred.
Artificial cycle FET
Patients begin oral estradiol (2 mg Progynova, Bayer,
Leverkusens, Germany) twice a day on cycle day
3. The thickness of endometrium was monitored with
transvaginal ultrasound. The dosage of estradiol val-
erate was adjusted based on the condition of endome-
trium and hormone level, with the maximum being
10 mg/day. When the thickness of endometrium was
equal to or more than 8 mm, 40–60 mg/day of pro-
gesterone was injected intramuscularly to promote
the transformation of endometrium to the secretory
phase. The time for transplantation depended on the
time when embryo was frozen. Progesterone injection
should be continued after transplantation.
HMG stimulated cycles
Human menopausal gonadotropin (HMG, Livzon
Pharmaceutical Factory, Zhuhai, China) was injected
on the 3rd to 5th day of menstruation with its amount
adjusted if necessary. When the EMT was 8 mm or
more and follicle diameter was above 18–20 mm and
urine LH was <25 IU/L, 5000–10 000 IU of HCG
(5000 IU per ampoule, Profasi, Serono) was used to
trigger final oocyte maturation. If urine LH was
≥25 IU/L and EMT did not reach 8 mm, the cycle
was canceled. Cycles with EMT continuously <8 mm
by day 20 were canceled due to poor endometrial
response. The time for transplantation depended on
the time when embryo was frozen.

Ultrasound examination of EMT
All ultrasound tests were performed by one subspe-
cialist clinicians using the same ultrasound system
using the same standardized protocols. Endometrial
thickness was measured using an ultrasound system
TOSHIBA SSA-240 on the 4th or 5th day of menstrua-
tion, the day of urinary LH surge and the day of
embryo transfer, respectively. Endometrial thickness
was measured from the interface between the endo-
metrium and myometrium on one side of the endo-
metrial cavity to the interface between the
endometrium and myometrium on the other side.4
Endometrial scratching
On the 4th or 5th day of the menstrual cycle of FET
preparing cycle, patients with EMT > 7 mm during
menstruation accepted shallow endometrial scratch-
ing. At lithotomy position, the vulva, vagina, cervix
and cervical canal were disinfected. The surgeon
explored the depth and direction of uterine cavity, put
endometrial collector (Jingyou, Saipujiuzhou Sci-Tech
Development, Beijing, China) in the uterine cavity
until it reached the bottom of the cavity, opened the
collector, turned the collector clockwise for 3–5 circles
to fully stimulate the endoscope, removed the collector
and collected endometrial tissues for pathological
examination. After the surgery, patients received
3 days of routine infection prevention treatment.
Outcome measurements
Biochemical pregnancy was confirmed with serum
β-human chorionic gonadotropin (β-HCG) concentra-
tion > 5 IU/L within 13 and 11 days after, day
3 embryo or blastocyst transfer.5 If an intrauterine
gestational sac and a fetal pole were confirmed
2 weeks after the positive pregnancy test with vaginal
ultrasound, clinical pregnancy was diagnosed.
Embryo implantation rate was the proportion of the
number of total gestational sacs to the total number of
embryos transferred. Miscarriage was defined in
patients with fetal heart beating but embryonic devel-
opment stopped before 24 weeks of gestation. Ectopic
pregnancy was diagnosed by transvaginal ultrasound
or by laparoscopic visualization of extrauterine gesta-
tion. A live birth rate was defined as the total number
of pregnancies that progressed to the delivery of a
viable offspring/the total number of transferred
cycles.
© 2018 Japan Society of Obstetrics and Gynecology
Endometrial thickness and pregnancy
Statistical analysis
SPSS software (Statistical Package for the Social Sci-
ences version 17.0, SPSS Inc., Chicago, IL, USA) was
used for all statistical analysis. Student’s t-test was
used to compare quantitative variables. When the var-
iance was equal, two independent samples were used
for t-test. When the variance was unequal, Cochran
approximation t-test was used. The data were ana-
lyzed with chi-square test and Fisher’s exact probabil-
ity method. P-value <0.05 was considered statistical
significance.
Results
Comparison of basic data between different
groups
There were no statistical significances in duration of
infertility, age, body mass index (BMI) and endome-
trial morphology during the day of embryos trans-
ferred among four groups. FET protocols, the number
of embryos transferred, proportion of cleavage
embryos transferred, proportion of single embryo
transfer (SET) and proportion of double embryo trans-
fer (DET) showed no significant differences among
four groups. The demographic information are shown
in Table 1.
Inter-group comparison of endometrium and its
growth
EMT on the 4th or 5th day of menstrual period and
the day of embryo transfer in those groups were sig-
nificantly different (P < 0.05). EMT of Group D
(10.13  1.92 mm) on the day of transfer was signifi-
cantly higher than that of Group A (8.48  1.56 mm).
Endometrial growth among the four groups had sig-
nificant difference (P < 0.05). The average endometrial
growth during menstruation of Groups A, B and C
was significantly higher than that in Group D
(4.68  1.75 mm vs 2.40  2.03 mm, P < 0.05,
Table 2).
Clinical outcomes in the four groups according to
EMT during menstruation
As shown in Table 3, there were significant differ-
ences in clinical pregnancy rate and embryo implanta-
tion rate among four groups (P < 0.05). The clinical
pregnancy rate in Group A was significantly higher
than that in Group D [68.87% (146/212) vs 53.26%
(98/184), P < 0.05]. The implantation rate of embryos
was also significantly higher than that of Group D
3
W.-j. Liu et al.

Table 1 Comparison of demographic characteristic among four groups

Index Group A Group B Group C Group D P value
(≤3.0 mm) (3.1–5.0 mm) (5.1–7.0 mm) (>7.0 mm)
Number of cycles 212 421 481 184
Age (year) 31.59  4.24 31.87  4.53 31.37  4.11 31.15  4.29 >0.05
Infertility duration 4.16  2.71 4.29  3.10 4.08  2.98 4.01  2.91 >0.05
BMI (kg/m2) 21.23  2.35 22.13  2.20 21.56  2.68 22.50  2.18 >0.05
FET protocols (%)
Natural cycle 26 (12.26%) 45 (10.69%) 72 (14.97%) 28 (15.22%) >0.05
Artificial cycle 170 (80.19%) 343 (81.47%) 391 (81.29%) 146 (79.35%) >0.05
HMG stimulated cycle 16 (7.55%) 33 (7.84%) 18 (3.74%) 10 (5.43%) >0.05
Number of embryos transferred 1.91  0.31 1.88  0.35 1.89  0.35 1.87  0.37 >0.05
Proportion of cleavage embryos transferred (%) 108 (50.94%) 203 (48.22%) 270 (56.13%) 103 (55.98%) >0.05
Proportion of SET (%) 14 (6.61%) 47 (11.16%) 35 (7.28%) 15 (8.15%) >0.05
Proportion of DET (%) 90 (42.45%) 171 (40.62%) 176 (36.59%) 66 (35.87%) >0.05
Values are mean  SD unless otherwise noted. BMI, body mass index; DET, double embryo transfer; FET, frozen–thawed embryo trans-
fer; SET, single embryo transfer.

Table 2 Inter-group comparison of menstrual endometrial thickness and growth

Index Group A Group B Group C Group D P value
(≤3.0 mm) (3.1–5.0 mm) (5.1–7.0 mm) (>7.0 mm)
Menstrual endometrial thickness (mm) 2.82  0.37 4.01  0.09* 5.30  0.47*,** 7.73  0.689*,**,*** <0.05
Endometrial thickness on day of 8.48  1.56 8.78  1.57* 9.47  1.78*,** 10.13  1.92*,**,*** <0.05
embryo transfer (mm)
endometrial growth (mm) 5.66  1.59 4.77  1.58* 4.17  1.76*,** 2.40  2.03*,**,*** <0.05
*Compared with Group A, P < 0.05; **Compared with Group B, P < 0.05; ***Compared with Group C, P < 0.05.

Table 3 Comparison of pregnancy outcomes among different groups

Index Group A Group B Group C Group D P value
(≤3.0 mm) (3.1–5.0 mm) (5.1–7.0 mm) (>7.0 mm)
Clinical pregnancy rate (%) 68.87 (146/212) 58.43 (246/421) 61.95 (298/481) 53.26* (98/184) <0.05
Embryo implantation rate (%) 50.74 (205/404) 45.98 (360/783) 47.03 (428/910) 36.34*,**,*** (125/344) <0.05
Twinning rate (%) 38.36 (56/146) 45.12 (111/246) 39.93 (119/298) 42.86 (42/98) >0.05
Miscarriage rate (%) 6.85 (10/146) 4.06 (10/246) 4.36 (13/298) 1.02*,**,*** (1/98) <0.05
Ectopic pregnancy rate (%) 0 (0/146) 1.63 (4/246) 1 (3/298) 2.04 (2/98) >0.05
Live birth rate (%) 60.38 (128/212) 53.68 (226/421) 54.05 (260/481) 44.57*,**,*** (82/184) <0.05
*Compared with Group A, P < 0.05; **Compared with Group B, P < 0.05; ***Compared with Group C, P < 0.05.

[50.74% (205/404) vs 36.34% (125/344), P < 0.05]. The
live birth rate in Group A was significantly higher
than that in Group D [60.38% (128/212) vs 44.57%
(82/184), P < 0.05]. However, there were no signifi-
cant differences in clinical pregnancy rate among
Group A, Group B and Group C (P > 0.05). These
results suggested that the clinical pregnancy rate and
embryo implantation rate of Group D (EMT > 7 mm)
were significantly lower than those in other groups.
There were no significant differences in ectopic preg-
nancy and twinning rate among four groups
(P > 0.05). The miscarriage rate decreased as the
thickness of the menstrual endometrium increased,
and the difference was statistically significant
(P < 0.05). Therefore, we chose group D to perform
endometrial scratching to examine whether it will
lead to thinner endometrium and improved clinical
pregnancy rate and embryo implantation rate.
Comparison of basic data between scratching
group and nonscratching group
There were no significant differences in age, infertility
duration, BMI, number of transplanted embryos, rate
of type B endometrial morphology during the day of

4 © 2018 Japan Society of Obstetrics and Gynecology

 Endometrial thickness and pregnancy

Table 4 Comparison of basic data between scratching group and nonscratching group
Index Scratching group Nonscratching group P value
Number of cycles 82 184
Age (year) 32.22  4.90 31.15  4.29 >0.05
infertility duration 4.36  2.36 4.01  2.91 >0.05
BMI (kg/m2) 21.61  2.92 22.50  2.18 >0.05
FET protocols (%)
Natural cycle 9 (10.98%) 28 (15.22%) >0.05
Artificial cycle 70 (85.37%) 146 (79.35%) >0.05
HMG stimulated cycle 3 (3.66%) 10 (5.43%) >0.05
Endometrial thickness on day of embryo transfer (mm) 11  2.44 10.13  1.92 <0.05
Proportion of cleavage embryos transferred (%) 42 (51.22%) 103 (55.98%) >0.05
Proportion of SET (%) 10 (12.20) 15 (8.15%) >0.05
Proportion of DET (%) 30 (36.58%) 66 (35.87%) >0.05
Number of embryos transferred 1.93  0.44 1.87  0.37 >0.05
DET, double embryo transfer; SET, single embryo transfer.

embryos transferred, FET protocols and proportion of
cleavage embryos transferred, proportion of SET, pro-
portion of DET. Compared to nonscratching group,
EMT on day of embryo transfer was thicker in
scratching group (P < 0.05) (Table 4).
There was no significant difference in ectopic preg-
nancy rate between the two groups (1.79% vs 2.04%,
P > 0.05). The live birth rate was significantly higher
in scratching group than in nonscratching group
(56.10% vs 44.57%, P < 0.05, Fig. 1).

Histologic findings in scratching group

Of the 82 patients who underwent endometrial Discussion
scratching, 77 had pathological diagnosis based on
endometrial diagnostic pathology.6 Of these, 50 cases Menstrual period is a process of disintegrating, shed-
had proliferative endometrium and 2 cases had secre- ding, repairing and growing of the functional layer of
tory endometrium, suggesting that the development endometrium. Generally, EMT is less than 5 mm after
of endometrium is not synchronized to the menstrual menstrual blood volume reaches the maximum.7 If
cycle. Nine cases had irregular hyperplasia, 9 cases EMT is still thicker when menstrual period ends, it
had endometrial polyps or polypoid hyperplasia and indicates that the endometrium may not be shed
7 cases had endometritis (Table 5). completely or has hyperplasia.8,9 Endometrium
develops from the proliferative phase to the secretory
Comparison of clinical pregnancy rates between phase. Proliferative endometrial dysplasia may affect
scratching group and nonscratching group endometrial receptivity, resulting in decreased
The clinical pregnancy rate was significantly higher in embryo implantation rate and clinical pregnancy
scratching group than in nonscratching group (68.29% rate.10 Recent studies showed that on the day of HCG
vs 53.26%, P < 0.05). The embryo implantation rate administration or embryo transfer, the pattern and
was significantly higher in scratching group than in thickness of endometrium were significantly corre-
nonscratching group (52.67% vs 36.34%, P < 0.05). lated with clinical pregnancy rate and embryo
implantation rate.11,12 However, Kasius et al. sug-
Table 5 Histologic finding of endometrial scratching
gested that the pregnancy rate threshold on the day
group of HCG administration should be equal to or more
Histologic finding Cycles n (%) Clinical pregnancy
than 8 mm.13 The above-mentioned assessment of
rate (%) EMT is limited to a fixed stage, while endometrial
Proliferative 50 60.98 38 (76.00%) growth is a dynamic process. The evaluation of endo-
Secretory 2 2.44 2 (100.00%) metrial growth in different stages of in-vitro-fertilization
Hyperplasia 9 10.98 4 (44.44%) (IVF) ovarian stimulation cycle was more significant
Polyps 9 10.98 9 (66.67%) than single stage assessment on the day of HCG admin-
Endometritis 7 8.54 6 (85.71%) istration.14 Zhao et al. retrospectively analyzed
Scant/inactive 5 6.10 0 (0.00%)
3319 cycles and found that compared with pregnancy

© 2018 Japan Society of Obstetrics and Gynecology 5

W.-j. Liu et al.
group, the nonpregnant group had thinner endome-
trium on the 3rd day of ovarian hyperstimulation,
thicker endometrium on HCG administration day
and better growth of endometrium in ovarian stimu-
lation cycle, indicating that adequate endometrial
development is favorable for improved pregnancy
rate.15
In this study we retrospectively analyzed the rela-
tionship between EMT during menstrual period and
the pregnancy outcome of FET, and focused on the
growth of endometrium during the entire menstrual
cycle. We found that endometrial growth of Group A
(EMT ≤ 3 mm) was greater in the process of endome-
trium preparation, accompanied by higher clinical
pregnancy rate and live birth rate, while clinical preg-
nancy rate and live birth rate of the group with more
than 7 mm of EMT were the lowest. These data sug-
gest that EMT > 7.0 mm during menstrual period of
FET cycle might affect clinical outcomes and reduce
pregnancy rate and live birth rate. Endometrial
growth reflects the responsiveness of endometrium
throughout the menstrual cycle. This study showed
that the mean intimal increase of Groups A, B and C
(EMT ≤ 7 mm) was significantly higher than that of
Group D (EMT > 7.0 mm). This indicates that groups
with intimal hyperplasia had better endometrial
growth status, which is conducive to embryo implan-
tation, and our results are consistent with a previous
study.16 Therefore, during FET endometrial prepara-
tion EMT during menstrual period should be paid
attention. Patients with thick endometrium when
menstruation ends may have poor pregnancy out-
comes following FET.
A Cochrane review including 14 randomized con-
trolled trials (RCTs) reported moderate quality evi-
dence of a modest increase in pregnancy rates or live
birth rates in patients who underwent endometrial
6 © 2018 Japan Society of Obstetrics and Gynecology
Figure 1 Comparison
of clinical pregnancy
rates between scratch-
ing group and non-
scratching group. *P <
0.05 indicated signifi-
cant differences between
scratching group and
nonscratching group.
( ) scratching group,
( ) nonscratching
group.
scratching in the cycle prior to IVF cycle.17 However,
a large RCT study showed that endometrial scratch-
ing in the preceding cycle did not improve pregnancy
rate in unselected subfertile women undergoing IVF
and subgroup analyses suggested that endometrial
scratching may have negative effect on those with
recurrent implantation failure.18 A recent study
reported no significant difference in clinical outcomes
between endometrial injury in the proliferative phase
and injury in the luteal phase.19 However, in our study,
patients with endometrial thickening during the period
of FET underwent endometrial scratching on the 4th or
5th day of the menstrual cycle. The timing of endome-
trial scraping was early follicular phase, making the
recovery of endometrium growth longer. Histology
analysis showed that 60.98% were proliferative phase,
21.96% were irregular or polypoid hyperplasia, 8.54%
were endometritis and 2.44% were secretory reaction.
Early follicular endometrial scratching during the men-
struation can remove endometrial local lesions, such as
polyps, dysplasia and abnormal thickening.20 Shallow
endometrial scratching not only removed abnormal
endometrium, but also increased the secretion of cer-
tain cytokines or growth factors such as interleukin
1, heparin-binding epidermal growth factor-like
growth factor and proinflammatory factors which play
important role in embryo implantation.21,22 In this
study, the clinical pregnancy rate of Group D
(EMT > 7 mm) was significantly lower compared to
other groups. After endometrial scratching, clinical
pregnancy rate, implantation rate and live birth rate of
Group D were significantly higher than those of the
nonscratch group, suggesting that endometrial scratch-
ing surgery could improve the efficacy of FET and
pregnancy rate and live birth rate.
An important limitation of this study is that it is ret-
rospective in nature. Selection bias could not be

avoided. Furthermore, the cases of intervention group
in this study are limited. A well designed and ran-
domized clinical trial will be needed to confirm our
conclusion.
In conclusion, this study showed that EMT during
menstruation was associated with clinical pregnancy
outcome following FET. On the 4th or 5th day of the
menstruation cycle during FET endometrial prepara-
tion, endometrial scratching helps improve clinical
pregnancy rate and live birth rate in patients with
EMT > 7 mm.
Acknowledgment
This study was supported by Guangzhou Science Tech-
nology and Innovation Commission (No. 201510010175).
Disclosure
None declared.
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