Human Reproduction, Vol.29, No.2 pp. 279– 285, 2014
Advanced Access publication on November 25, 2013 doi:10.1093/humrep/det429
ORIGINAL ARTICLE Infertility
Uterine peristalsis exerts control
over fluid migration after mock embryo
transfer
L. Zhu 1, L. Xiao 1, H.S. Che1, Y.P. Li1,*, and J.T. Liao2
1
Department of Reproductive Medicine, Xiangya Hospital, Central South University, 87 Xiangya Road, Changsha City, Hunan Province, P.R.
China 410008 2Department of Ultrasonography, Xiangya Hospital, Central South University, 87 Xiangya Road, Changsha City, Hunan Province,
P.R. China 410008
*Correspondence address. Department of Reproductive Medicine, Xiangya Hospital, 87 Xiangya Road, Changsha City, Hunan Province,
P.R. China. E-mail: [email protected]
Submitted on August 10, 2013; resubmitted on October 30, 2013; accepted on November 4, 2013
study question: What is the effect of uterine peristalsis on fluid migration after mock embryo transfer?
summary answer: Uterine peristaltic wave frequency was positively correlated with the distance that fluid moved after it was deposited in
the uterine cavity.
what is known already: Embryos have been found outside the uterine cavity after embryo transfer. It has been suggested that uterine
contractions expelled these embryos.
study design, size, duration: A prospective cohort study of a total of 112 infertile women was conducted between March 2013 and
May 2013.
participants/materials, setting, methods: Uterine peristaltic activity was assessed before and after a mock embryo transfer, in which 20 ml of ultrasound contrast agent was placed in the uterine lumen 3 days after ovulation in a natural cycle. The movement of this fluid
was measured by ultrasound at 0, 15 and 30 min after placement.
main results and the role of chance: The uterine peristaltic wave frequency was significantly higher after than before mock
transfer (3.06 + 0.99 versus 2.24 + 0.74, P , 0.01). At the conclusion of the 30-min monitoring period, the fluid had remained in place (N ¼ 94),
leaked into the cervix (N ¼ 5), or moved into the Fallopian tubes or the cornua of the uterus (N ¼ 11). The fluid movement was positively correlated with uterine peristaltic wave frequencies before (r ¼ 0.518, P , 0.01) and after embryo transfer (r ¼ 0.371, P , 0.01) and uterine peristaltic wave frequency was significantly higher both before and after embryo transfer in cases where the fluid was extruded.
limitations, reasons for caution: Mock embryo transfer was performed in the luteal phase of a natural cycle instead of a controlled ovarian stimulation cycle. The endometrial environment and uterine peristalsis may be different in a stimulated cycle.
wider implications of the findings: Uterine peristalsis exerts control over embryo migration and could adversely affect the
chances of pregnancy if the wave frequency is too high. It could be used as a predictor of uterine irritability before embryo transfer.
study funding/competing interest(s): The authors declare that they have not received any particular study funding and do
not have competing interests in this study.
Key words: uterine peristalsis / fluid migration / uterine receptivity / assisted reproductive technology
Introduction
In a spontaneous cycle, embryo implantation occurs in the luteal phase
when the uterus is ready for reception with few uterine peristaltic movements (IJland et al., 1997a,b; Bulletti et al., 2000; Fanchin and Ayoubi,
2009). The quiet local milieu is essential to maintain the embryo drifting
in the uterine cavity, facilitating the maternal –fetal dialogue and
recognition (Bulletti and de Ziegler, 2006; Fanchin and Ayoubi, 2009).
In assisted reproduction, embryo transfer is the final, crucial step, but
the invasive insertion of the catheter may disturb the physiological processes of embryo implantation. Although the combination of a soft catheter and ultrasound guidance permit placement with high precision,
intrauterine deposition of embryos does not always mean that they
remain in situ (Poindexter et al., 1986; Knutzen et al., 1992; Mansour
& The Author 2013. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved.
For Permissions, please email: [email protected]
280
et al., 1994; Lesny et al., 1998; Coroleu et al., 2000; Wood et al., 2000;
Allahbadia et al., 2008).
Poindexter et al. (1986) estimated that about 15% of the transferred
embryos were left outside or expelled from the uterine cavity, being
located either at the cervical os on the vaginal speculum or remaining
in the catheter after embryo transfer. In an experimental study of
embryo transfer, radio-opaque dye moved into the Fallopian tubes or
cervix/vagina depending on the patient’s position in 38.2 and 20.6%,
of mock transfers, respectively (Knutzen et al., 1992). Similarly, methylene blue dye was also visualized at the external cervical os after mock
embryo transfer (Mansour et al., 1994). Lesny observed that touching
the uterine fundus with the catheter, to mimic difficult embryo transfer,
generated strong uterine contractions, which expelled the fluid into the
cervix and Fallopian tubes (Lesny et al., 1998). In Woolcott and Stanger’s
study, endometrial wave-like movements appeared to move the
embryo-associated air bubble back and forth around a pivotal point.
Standing up shortly after embryo transfer did not play a significant role
in the final position of the embryo-associated air bubble. In one case
with very active movement, the air bubble migrated to the cervix and
then returned after the patient stood up from a supine position (Woolcott and Stanger, 1997, 1998). Thus previous studies show that transferred embryos may be expelled from the uterine cavity due to active
uterine peristalsis, but how and to what extent uterine peristalsis will
affect embryo migration after embryo transfer has been less investigated.
In the present study, ‘embryo’ drifting was directly monitored after mock
embryo transfer with ultrasound contrast agent in place of embryocontaining medium. Uterine peristalsis was quantitatively compared
with the movement of this fluid.
Materials and Methods
Patients
In this prospective study, patients admitted to the Department of Reproductive Medicine at Xiangya Hospital of Central-south University were recruited
between March and May 2013. A total of 112 consecutive patients, seeking
IVF/ICSI-embryo transfer treatment and with normal ovulation, were analysed. Exclusion criteria were anatomic disorders of the female reproductive
system, leiomyoma, endometriosis, intrauterine adhesion, endometrial
polyp, hydrohystera and any medical illness requiring pharmacologic treatment. This study was approved by the institutional review board of
Xiangya Hospital of Central-south University. All patients participating in
the study gave their informed consent.
Zhu et al.
uterine peristalsis at the mid-sagittal plane of the uterus was recorded for
each patient. All patients were asked to empty their bladder before the
first ultrasound assessment and stay in a supine position till the last measurement was completed. No tranquilizers or medication was given to the
patients throughout the whole procedure.
A mock embryo transfer guided by abdominal ultrasonography was performed using a catheter (CCD131230301, Ultrasoft Frydman Set with
Guide, Laboratoire C.C.D., France) to deliver 20 ml of fluid SonoVue
(Bracco Imaging S.p.A., Italy) into the uterine cavity. No cervix tenaculum
was utilized. Immediately after the mock embryo transfer, transvaginal ultrasonography was performed to locate the position of the fluid in the uterine
cavity. If the tracking medium divided into two or more parts, then the
largest one was tracked. The distance from the fluid to the fundus of the
uterine cavity in the mid-sagittal plane and to the bilateral endometrium in
transverse plane was measured three times as soon as possible. The average
of repeated measurements were expressed as db1 (distance between the
fluid and the fundus of the uterine cavity), dl1 (distance between the fluid
and the patient’s left endometrium) and dr1 (distance between the fluid
and the patient’s right endometrium) (Fig. 1). Within 1 min after the mock
transfer, uterine peristalsis was recorded for a further 5 min using a vaginal
US probe (Mindray DC-6 Expert, 5 – 8 MHz transducer, China). At 15 and
30 min after embryo transfer, the position of the fluid was remeasured and
recorded as db2, dl2, dr2 and db3, dl3, dr3, respectively.
Uterine peristalsis assessment and fluid
movement distance measurement
Images of uterine peristalsis were converted to four times normal speed using
a VLC media player 1.1.11 (VideoLAN team). Uterine peristaltic wave frequency was analysed independently by two observers (L.Z. and L.X.). The
final result of wave frequency was the mean of two numbers from different
observers. The displacement of the fluid between two time points was calculated based on the movement in three planes over the three observation time
points (Fig. 1).
Statistical analysis
The SPSS software version 19.0 was used for statistical analysis. Continuous
data were presented as mean and standard deviation. Inter-observer variation of uterine peristaltic wave frequency was analysed using Wilcoxon
signed-rank test. Changes in uterine peristaltic wave frequency before
and after embryo transfer were assessed using paired Student’s t-test.
Correlations between the uterine peristaltic wave frequency and the distance
of fluid movements were performed using linear correlation analysis.
P , 0.05 was considered statistically significant.
Study design
Results
All subjects underwent mock embryo transfer in the early luteal phase of the
natural menstrual cycle preceding their IVF treatment cycle.
Serial ultrasound examinations for follicular tracking started on Day 10 in
the natural cycle. If the average diameter of the dominant follicle was
,14 mm, the patient was asked to come every other day. Otherwise a
urine LH test was performed and the patient was asked to come next day.
A urine LH test above 45 IU/l and the disappearance of the pre-ovulatory
follicle were used to identify ovulation. Three days after ovulation, uterine
peristalsis assessment and a mock embryo transfer were performed by a
single operator (L.Z.). Just before the mock embryo transfer, a transvaginal
ultrasound scan (Mindray DC-6 Expert, 5 – 8 MHz transducer, China) was
performed to assess the length of the uterine cavity and the cervix, as well
as the position and length of the uterus. As described in our previous study
(Zhu et al., 2012), a 5-min transvaginal ultrasonographic observation of
A total of 112 subjects commenced this study. Two patients were
excluded due to difficulties in visualizing the endometrium. Before the
placement of the fluid, the endometrial contractility was 2.24 +
0.74 waves/min. After the placement, the endometrial contractility
increased to 3.06 + 0.99 waves/min (P , 0.01) (Table I). The uterine
peristaltic wave frequency, both before embryo transfer and after
embryo transfer, was significantly higher in cases where the fluid was
extruded (Table II). Following embryo transfer, fluid moved into the
cervix (5 cases), or into the Fallopian tubes or the cornua of the uterus
(11 cases). In one case, the fluid moved down into the inner os of the
cervix, but after several cervicofundal uterine peristaltic waves, the
fluid moved back into the uterine cavity (Fig. 2 and Supplementary
data, Video S1).
281
Uterine peristalsis and fluid migration after embryo transfer
Figure 1 Calculation of fluid position and the distance of fluid movement. Blue point: the intrauterine fluid just after deposition. Red point: the position of
fluid 15 min after deposition. Purple point: the position of fluid 30 min after deposition. db1: average distance between the fluid and the fundus of the uterine
cavity. dl1: average distance between the fluid and the patient’s left endometrium. dr1: average distance between the fluid and the patient’s right endometrium. d1-2: distance that the fluid moved between the first and the second observation time point. d2-3: distance that the fluid moved between the second and
the third observation time point.
Table I Uterine peristaltic wave frequency (waves/min)
before and after mock embryo transfer.
Observer
N
Before embryo
transfer
After embryo
transfer
P
........................................................................................
A
110
2.22 + 0.75
3.08 + 1.01
B
110
2.25 + 0.73
3.03 + 0.99
Average
110
2.24 + 0.74
3.06 + 0.99
b
b
P
0.094
,0.01a
0.087
a
Changes in uterine peristaltic wave frequency before and after embryo transfer were
assessed using paired Student’s t-test.
b
Inter-observer variation of uterine peristaltic wave frequency was analysed using
Wilcoxon signed-rank test.
The fluid was deposited into the uterine cavity at a distance of 9.56 +
5.20 mm from the fundus. On average, the fluid moved 10.34 +
7.46 mm within 30 min of embryo transfer. In the cases where the
fluid was extruded, it moved much further.
The placement of the fluid within the uterine cavity was not significantly correlated with the distance the fluid moved (P ¼ 0.176). Uterine peristaltic wave frequencies before and after embryo transfer were both
significantly correlated with the distance the fluid moved, with correlation coefficients of 0.518 (P , 0.01) and 0.371 (P , 0.01), respectively
(Fig. 3).
A follow-up survey showed that for 21 patients embryo transfer was
cancelled in the subsequent stimulated cycle. Of the 89 transferred
cases, 40 patients were confirmed to have a clinical pregnancy by ultrasonographic visualization of gestational sacs. However, statistical analysis
shows that there was no difference in uterine peristalsis wave frequency
in the preceding cycle between the pregnant group and non-pregnant
group (before mock transfer: 2.21 versus 2.12, P ¼ 0.903; after mock
transfer: 3.22 versus 3.04, P ¼ 0.402).
Discussion
The current study indicated that uterine peristalsis was quantitatively
correlated with the distance of fluid movement after embryo transfer.
Our approach allowed the transferred embryo analogue to be directly
282
Zhu et al.
Table II Uterine peristaltic wave frequency and distance of fluid movement in patients with different outcome of
transferred fluids.
Fluids
N
Uterine peristaltic wave frequency
(waves/min)
.......................................................
Before embryo
transfer
The rate of increase of
uterine peristalsis
db1
(mm)
Distance of fluid
movement (mm)
After embryo
transfer
.............................................................................................................................................................................................
Inside the uterine
cavity
94
2.15 + 0.71
2.94 + 0.91
36.7%
Extruded outside
16
2.75 + 0.67
3.72 + 1.21
,0.01
,0.01
P
9.58 + 5.14
8.88 + 6.06
35.3%
9.42 + 5.71
18.88 + 9.27
–
0.914
,0.01
db1: distance between the fluid and the fundus of the uterine cavity after fluid deposition.
Figure 2 A sequence showing that fluid could move from the uterine lumen, down into the inner os of the cervix and back to the uterine cavity in response
to cervicofundal uterine peristaltic waves. The red arrow points to the ultrasound contrast agent. SonoVue is made up of sulphur hexafluoride microbubbles. The images show 3 time points: 0, 15 and 30 min after placement.
tracked by ultrasonography and demonstrated that uterine peristalsis did
correlate with fluid migration. It could therefore potentially influence
pregnancy outcomes.
The uterine peristaltic wave frequency after embryo transfer was significantly higher than that before embryo transfer, suggesting that an
embryo transfer procedure may enhance uterine peristalsis. However,
our result was in contrast to Torre’s study (Torre et al., 2010), which
did not find any influence of mock embryo transfer on uterine contractility. Differences in insertion procedures of the catheter may contribute
to the inconsistency of the results. Torre et al. introduced a catheter into
the cervix up to the inner cervical os and immediately withdrew it, while
we completely mimicked a real embryo transfer including the insertion of
the soft inner catheter into the upper half of the uterine cavity and the
ejection of medium. Uterine contractility occurs in vivo with specific patterns mainly related to the ovarian steroid levels. Estrogens promote and
progesterone relaxes uterine contractility (Kunz et al., 1998; Zhu et al.,
2012). Other factors that are strongly involved include prostaglandins
from semen or from the myometrium and endometrium (Dittrich
et al., 2009). Prostaglandins are likely to be released after catheter stimulation of the uterine lumen. This may indicate that catheter insertion and
fluid ejection procedures should be as gentle as possible to avoid triggering an increase in uterine peristalsis.
The placement of the fluids in our study seemed to be a little closer to
the uterine fundus than the recommended distance in previous studies
(9.56 versus 10– 20 mm, respectively) (Coroleu et al., 2002; Pacchiarotti
et al., 2007; Mains and Van Voorhis, 2010; Tiras et al., 2010). However,
these studies all measured the distance between the tip of the catheter
and the uterine fundus. The ejection of transfer medium may push the
embryo a little further forward and closer to the fundus. Lambers et al.
(2007) and Friedman et al. (2011) monitored the location of the air
bubble relative to the fundus after embryo transfer and found that the
pregnancy rate was significantly higher when the air bubbles ended up
closer to the fundus (,10 mm). Thus, the deposition of our fluids
could be considered appropriate. Furthermore, a statistical analysis
showed that fluid placement was not significantly correlated with the distance the fluid moved in our study, suggesting a negligible effect of proper
deposition on fluid migration.
The movement of gametes and zygotes within the uterine lumen is
influenced by ovarian steroid levels, myometrial activity and any myometrial or endometrial pathologies. In 14.5% of our transfers the fluids were
observed to leave the uterine cavity, which was similar to the previous
finding (Poindexter et al., 1986). This cohort of patients had more
active uterine movements than the others, both before embryo transfer
and after embryo transfer. During the 30-min observation period, the
fluid did not move uniformly forward in one direction; instead it was influenced by the uterine peristalsis. The cervicofundal uterine peristaltic
waves tended to spread the fluid, pushing it forward in the direction of
the wave. When the wave reached the fundus, the fluid would then
Uterine peristalsis and fluid migration after embryo transfer
283
Figure 3 Scatter diagram of the uterine peristaltic wave frequency and the distance of fluid movement. The correlation between uterine peristaltic wave
frequency before embryo transfer and distance of fluid movement was r ¼ 0.518 (P , 0.01). The correlation between uterine peristaltic wave frequency
after embryo transfer and distance of fluid movement was r ¼ 0.371 (P , 0.01).
move backwards to varying degrees. Within the cohort that extruded
fluids, the uterine peristaltic wave frequency was significantly increased
and the waves overlapped each other, so that there was no time for
the fluid to move back to counteract the effect of the preceding waves.
The cumulative effect of this to-and-fro motion caused the fluid migration
and may contribute to intrauterine/ectopic pregnancies.
It was worthwhile to note that cervicofundal uterine peristalsis could
return the fluid to the uterine cavity, even once it had reached the inner
os of the cervix (Fig. 2 and Supplementary data, Video S1). This, for the
first time, demonstrates the previous assumption (Kunz et al., 2006)
that the cervicofundal uterine peristalsis in the luteal phase may also
prevent the embryo from implanting in the lower part of the uterus,
avoiding cervical pregnancy or placenta praevia. Interestingly fluid that
moved into the Fallopian tubes (N ¼ 9) did not come back into the
uterine cavity.
Uterine peristalsis wave frequencies in the natural cycle between the
pregnancy group and non-pregnancy group were not significantly different in our study. It may be because controlled ovarian stimulation
changed the uterine peristaltic pattern in the subsequent cycle, as was
observed in our previous study (Zhu et al., 2012). Additionally, there
were many confounding factors such as the patients’ age, peak E2 concentration, number of oocytes retrieved, number of embryos transferred, embryo quality, sample size, etc. Fanchin et al. (1998) evaluated
the uterine contractions just before embryo transfer and divided the
patients into four groups according to uterine contraction frequency:
≤3.0, 3.1–4.0, 4.1–5.0, .5.0. A stepwise decrease in clinical pregnancy
rates occurred from the lowest to the highest uterine contraction frequency groups (53, 46, 23 and 14%, respectively). If we grouped our
patients in the same way, there would have been 80 patients with a
uterine peristalsis wave frequency of no more than 3.0 before mock
transfer, and only 7, 2, 0 patients in the 3.1 –4.0, 4.1 –5.0, .5.0
groups, respectively. A group of 21 patients whose embryo transfer
was cancelled in the stimulated cycle were excluded. The clinical pregnancy rates would have been 45, 42.9, and 50% in the first three
groups, but the wide variation in subgroup sample size and other confounding factors made the correlation analysis invalid. But if inter-subject,
284
observer and cycle differences are put aside, their results resemble our
results in that the uterine peristalsis of those who expelled their
embryos was .3 waves/min. In the present study, there was an approximate 36% increase in uterine peristalsis after embryo transfer.
Therefore, the post-transfer uterine peristaltic wave frequency might
be roughly calculated by measuring the pre-transfer frequency, both of
which might be taken as a noninvasive predictor of the uterine receptivity
and pregnancy outcome. However, it is worthwhile to note that some
other elements may also play a comprehensive role in controlling the
luminal content migration, such as the thickness of the myometrium,
the length of the uterine cavity, the endometrial thickness, the volume
and viscosity of fluid in the endometrium, the amplitude and velocity of
uterine peristaltic waves, the basal tone of the uterine contractility and
others (IJland et al., 1997b, 1998; Eytan et al., 1999, 2001). Thus, the effectiveness of this new index remains to be seen.
One limitation of our study was that the mock embryo transfer was
performed in a natural cycle instead of a stimulated cycle. Thus the endometrial environment and uterine peristalsis may be different from a real
embryo transfer (Eytan et al., 2001; Zhu et al., 2012). Another point that
is worthy of attention is that even though our mock embryo transfer using
ultrasound contrast medium was as close as possible to a real embryo
transfer, it was still different from an actual embryo because the contrast
medium is not the same as the media used in embryo transfers.
In conclusion, uterine peristalsis was shown to play an essential part
in fluid migration and this indicates that it could influence the outcomes
of embryo transfers. We believe that further investigations are necessary to clarify the mechanism behind the regulation of uterine peristalsis
and to apply interventions to reduce the adverse effect of active uterine
peristalsis.
Supplementary data
Supplementary data are available at http://humrep.oxfordjournals.org/.
Authors’ roles
L.Z. participated in the study design, transvaginal ultrasonographic scan,
mock embryo transfer, analysis and interpretation of data. L.X. participated in the acquisition and analysis of data. H.S.C. took part in the transabdominal ultrasound guided embryo transfer, and acquisition of data.
Y.P.L. participated in the study conception and design. J.T.L. provided
the ultrasound contrast agent and critical advice in study design. All
authors contributed to the production of the manuscript.
Conflict of interest
None declared.
References
Allahbadia GN, Gandhi G, Kadam K, Arora S, Awasthi A, Nagwekar A,
Allahbadia S, Wolman I. Antibubble trajectory during embryo transfers
in donor egg IVF does not predict success. Reprod Biomed Online 2008;
16:881 – 885.
Zhu et al.
Bulletti C, de Ziegler D. Uterine contractility and embryo implantation. Curr
Opin Obstet Gynecol 2006;18:473 – 484.
Bulletti C, de Ziegler D, Polli V, Diotallevi L, Del Ferro E, Flamigni C. Uterine
contractility during the menstrual cycle. Hum Reprod 2000;15:81 – 89.
Coroleu B, Carreras O, Veiga A, Martell A, Martinez F, Belil I, Hereter L,
Barri PN. Embryo transfer under ultrasound guidance improves
pregnancy rates after in-vitro fertilization. Hum Reprod 2000;15:616– 620.
Coroleu B, Barri PN, Carreras O, Martı́nez F, Parriego M, Hereter L,
Parera N, Veiga A, Balasch J. The influence of the depth of embryo
replacement into the uterine cavity on implantation rates after IVF: a
controlled, ultrasound-guided study. Hum Reprod 2002;17:341 – 346.
Dittrich R, Mueller A, Oppelt PG, Hoffmann I, Beckmann MW, Maltaris T.
Differences in muscarinic-receptor agonist-, oxytocin-, and prostaglandininduced uterine contractions. Fertil Steril 2009;92:1694– 1700.
Eytan O, Jaffa AJ, Har-Toov J, Dalach E, Elad D. Dynamics of the intrauterine
fluid-wall interface. Ann Biomed Eng 1999;27:372 – 379.
Eytan O, Halevi I, Har-Toov J, Wolman I, Elad D, Jaffa AJ. Characteristics of
uterine peristalsis in spontaneous and induced cycles. Fertil Steril 2001;
76:337 – 341.
Fanchin R, Ayoubi JM. Uterine dynamics: impact on the human reproduction
process. Reprod Biomed Online 2009;18:57– 62.
Fanchin R, Righini C, Olivennes F, Taylor S, de Ziegler D, Frydman R. Uterine
contractions at the time of embryo transfer alter pregnancy rates after
in-vitro fertilization. Hum Reprod 1998;13:1968 – 1974.
Friedman BE, Lathi RB, Henne MB, Fisher SL, Milki AA. The effect of air
bubble position after blastocyst transfer on pregnancy rates in IVF
cycles. Fertil Steril 2011;95:944 –947.
IJland MM, Evers JL, Dunselman GA, Volovics L, Hoogland HJ. Relation
between endometrial wavelike activity and fecundability in spontaneous
cycles. Fertil Steril 1997a;67:492 – 496.
IJland MM, Evers JL, Hoogland HJ. Velocity of endometrial wavelike activity in
spontaneous cycles. Fertil Steril 1997b;68:72 – 75.
IJland MM, Evers JL, Dunselman GA, Hoogland HJ. Endometrial wavelike
activity, endometrial thickness, and ultrasound texture in controlled
ovarian hyperstimulation cycles. Fertil Steril 1998;70:279 – 283.
Knutzen V, Stratton CJ, Sher G, McNamee PI, Huang TT, Soto-Albors C. Mock
embryo transfer in early luteal phase, the cycle before in vitro fertilization and
embryo transfer: a descriptive study. Fertil Steril 1992;57:156–162.
Kunz G, Noe M, Herbertz M, Leyendecker G. Uterine peristalsis during the
follicular phase of the menstrual cycle: effects of oestrogen, antioestrogen
and oxytocin. Hum Reprod Update 1998;4:647 – 654.
Kunz G, Beil D, Huppert P, Leyendecker G. Control and function of uterine
peristalsis during the human luteal phase. Reprod Biomed Online 2006;
13:528 – 540.
Lambers MJ, Dogan E, Lens JW, Schats R, Hompes PG. The position of
transferred air bubbles after embryo transfer is related to pregnancy
rate. Fertil Steril 2007;88:68 – 73.
Lesny P, Killick SR, Tetlow RL, Robinson J, Maguiness SD. Embryo transfer—
can we learn anything new from the observation of junctional zone
contractions? Hum Reprod 1998;13:1540– 1546.
Mains L, Van Voorhis BJ. Optimizing the technique of embryo transfer. Fertil
Steril 2010;94:785 – 790.
Mansour RT, Aboulghar MA, Serour GI, Amin YM. Dummy embryo transfer
using methylene blue dye. Hum Reprod 1994;9:1257 – 1259.
Pacchiarotti A, Mohamed MA, Micara G, Tranquilli D, Linari A, Espinola SM,
Aragona C. The impact of the depth of embryo replacement on IVF
outcome. J Assist Reprod Genet 2007;24:189 – 193.
Poindexter AN 3rd, Thompson DJ, Gibbons WE, Findley WE, Dodson MG,
Young RL. Residual embryos in failed embryo transfer. Fertil Steril 1986;
46:262 – 267.
Uterine peristalsis and fluid migration after embryo transfer
Tiras B, Polat M, Korucuoglu U, Zeyneloglu HB, Yarali H. Impact of embryo
replacement depth on in vitro fertilization and embryo transfer outcomes.
Fertil Steril 2010;94:1341– 1345.
Torre A, Scheffer JB, Schönauer LM, Frydman N, Fanchin R. Mock embryo
transfer does not affect uterine contractility. Fertil Steril 2010;93:1343–1346.
Wood EG, Batzer FR, Go KJ, Gutmann JN, Corson SL. Ultrasound-guided
soft catheter embryo transfers will improve pregnancy rates in in-vitro
fertilization. Hum Reprod 2000;15:107– 112.
285
Woolcott R, Stanger J. Potentially important variables identified by
transvaginal ultrasound-guided embryo transfer. Hum Reprod 1997;
12:963– 966.
Woolcott R, Stanger J. Ultrasound tracking of the movement of
embryo-associated air bubbles on standing after transfer. Hum Reprod
1998;13:2107 – 2109.
Zhu L, Li Y, Xu A. Influence of controlled ovarian hyperstimulation on uterine
peristalsis in infertile women. Hum Reprod 2012;27:2684 – 2689.