Download Endometrial thickness as a predictor of

Human Reproduction vol 11 no 7 pp 1538-1541, 1996
Endometrial thickness as a predictor of pregnancy after
in-vitro fertilization but not after intracytoplasmic
sperm injection
Leonardo Rinaldi1'3, Franco Lisi1, AttUia Floccari1,
Rosella Lisi1, Giampiero Pepe1 and Simon Fishel1'2
'Biogenesi, Servizio di Fisopatologia della Riproduzione, Casa di
Cura Villa Europa, 27 Via Eufrate, Roma EUR, 00144, Italy and
2
NURTURE (Nottingham University), Department of Obstetrics and
Gynaecology, University Hospital, Queen's Medical Centre,
Nottingham NG7 2UH, UK
^To whom correspondence should be addressed
An ultrasonographic evaluation of the endometrium was
performed in 158 patients undergoing ovarian stimulation
for an in-vitro assisted reproduction programme. Endometrial thickness was evaluated in 109 patients undergoing
in-vitro fertilization (TVF) for female indications and in
49 patients undergoing intracytoplasmic sperm injection
(ICSI) for male indications. The maximal endometrial
thickness was measured on the day of human chorionic
gonadotrophin (HCG) administration by longitudinal scanning of the uterus on the frozen image using electronic
callipers placed at the junction of the endometriummyometrium interface at the level of the fundus. Cases in
which the endometrial thickness was 2*10 mm were
included in group A; cases in which the endometrial
thickness was <10 mm were assigned to group B. The age
of the patients, serum 17-p* oestradiol concentrations on
the day of HCG administration, the length of follicular
stimulation, the number of follicles, 17-f} oestradiol concentrations per follicle on the day of HCG and the number of
embryos transferred were analysed in each case. When
comparing endometrial thickness and results in IVF and
ICSI patients, an endometrium <10 mm predominated in
FVF patients (27.5%) compared with those undergoing
ICSI (16.7%) {P = 0.05); conversely an endometrium 5=10
mm was more frequent in ICSI than in IVF patients. The
incidence of pregnancy was higher in IVF group A patients
(32/79; 41%) than in IVF group B patients (5/30; 17%)
(P = 0.03), whereas no significant difference was found
between ICSI group A (13/42; 31%) and ICSI group B
(3/7; 43%) patients. Thus, a higher percentage of IVF
patients had thin endometrium when compared with ICSI
patients,* thin endometrium was a prognostic indicator of
pregnancy only in the case of a female indication for
infertility (TVF). A thin endometrium in cases of female
infertility may reflect a previous or present uterine pathology, whereas in indications of male infertility (i.e. cases
using ICSI), in the absence of any associated uterine
pathology, the presence of a thin endometrium is not
predictive.
Key words: endometrial thickness/ICSI/IVF/ultrasonography
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Introduction
The use of intracytoplasmic sperm injection (ICSI) has recently
resulted in a dramatic improvement of the prognosis for couples
affected by severe male factor infertility (Van Steirteghem et al.,
1993). In fact, in these couples the fertilization and pregnancy
rates (per cycle) have almost reached those of standard invitro fertilization (TVF) for other indications, so that the use
of ICSI has even been proposed for each case of FVF (Lisi
et al, 1995).
Endometrial receptivity is required for successful implantation in natural and IVF cycles. In the attempt to identify a
non-invasive uterine predictor of implantation and pregnancy
during IVF procedures, endometrial features have been widely
studied by transabdominal and, more recently, transvaginal
ultrasonography. Despite the large number of papers concerning
this issue, the prognostic value of ultrasonographic endometrial
thickness or the appearance of the endometrium, or a combination of the two, in conception and non-conception IVF cycles
remains controversial (Glissant et al, 1985; Fleischer et al.,
1986; Rabinowitz et al, 1986; Gonen et al, 1989; Welker
et al, 1989; Sher et al, 1991; Check et al, 1991, 1993; Bergh
et al, 1992; Dickey et al, 1992; Khalifa et al, 1992; Eichler
et al, 1993; Oliveira et al, 1993; Coulam et al, 1994; Serafini
et al, 1994; Strohmer et al, 1994; Takahashi et al, 1995).
The routine use of ICSI in male infertility has recently
allowed the role of endometrial ultrasonography to be evaluated
in predicting implantation in healthy women undergoing an
in-vitro assisted reproduction programme for male factor
infertility; moreover, these data can be compared with those
obtained from women undergoing IVF for female indications.
Materials and methods
From January 1995 to April 1995, 158 patients were treated with
buserelm (Suprefact; Hoechst) using the nasal spray at a dose of
three inhalations per nostnl every 8 h from day 21 of the previous
cycle until pituitary desensitization was achieved, followed by follicle
stimulating hormone (FSH; Metrodin HP; Serono) administration at
a dose of two to four ampoules daily. FSH was administered at a
variable dose, depending on individual response to stimulation.
No statistical significance was attributed to the variable dose of
gonadotrophins. Human chononic gonadotrophin (HCG; 10 000 IU;
Profasi HP; Serono) was administered to initiate ovulation 32-36 h
before oocyte retrieval. The latter was performed by the transvaginal
route under ultrasonic control and local anaesthesia. Oocyte fertilization and embryo culture for IVF and ICSI were performed as reported
previously (Fishel and Jackson, 1986; Fishel et al, 1995). About
48 h after oocyte retrieval, a maximum of three embryos were
transferred into the uterine cavity, according to availability. All
© European Society for Human Reproducuon and Embryology
EndometriaJ thickness as a predictor of pregnancy
patients received 50 mg 1 m. progesterone (Gestone; AMSA) daily,
from the day of oocyte retrieval, to support the luteal phase
The cause of infertility was represented by male factors alone
(patients in whom male factor and female factor were associated
were excluded; n = 49) or female factors (absolute tubal factor or
relative tubal factor in association with endometriosis; n = 109)
In female indications, conventional IVF was performed; in male
indications, ICSI was the procedure of choice
The endometnum was imaged on the day of HCG administration
by transvaginal ultrasonography using a 5 MHz vaginal transducer.
Each scan was performed by the same operator blinded to the
hormonal response The maximal endometnal thickness was measured
by longitudinal scanning of the uterus (carefully avoiding tangential
views) on the frozen image using electronic callipers placed at the
junction of the endometnum—myometnum interface at the level of
the fundus. No patient showed sonographic evidence of submucosal
fibroids or endometrial polyps at scanning
Endometnal thickness was assessed on the day of HCG administration in all cases Cases in which the endometnal thickness was 3= 10
mm were included in group A, cases in which the endometnal
thickness was <10 mm were assigned to group B.
The following parameters were analysed: age of the patients, 17P oestradiol concentration, as determined by a radioimmunoassay on
the day of HCG administration; the length of folhcular stimulation
(days); the number of follicles; 17-p oestradiol concentration per
follicle; and the number of embryos transferred.
Serum (J-HCG concentrations were measured on day 14 after
embryo transfer to diagnose all the pregnancies (including the
biochemical pregnancies). Clinical pregnancies (presence of a gestational sac) were diagnosed by ultrasonography at ~6 weeks of
gestation.
The data obtained were compared using Student's r-test for unpaired
results, the Fisher's exact test, the Z-test for a companson of
proportions and linear regression and correlation when necessary.
Significance was defined as P ^ 0.05
Results
Age was not significantly different between patients undergoing
IVF for female indication and patients undergoing ICSI for
male infertility.
The pregnancy rates for IVF and ICSI were 34 (37/109)
and 33% (16/49) respectively. These were not statistically
different (Table I).
In all, 121 patients had an endometrial thickness 5*10 mm
on the day of HCG (group A); 37 patients had an endometrial
thickness <10 mm on the day of HCG (group B).
No statistical differences were noted between group A and
group B patients with regard to oestradiol concentration on
the day of HCG administration (8722 ± 3694 versus 10 377
± 4872 pmol/1), the duration of follicular stimulation (12.20
± 1.78 versus 11.90 ± 1.64 days), the number of follicles
(11.10 ± 4.24 versus 12.70 ± 6.19), oestradiol concentration
per follicle measured on the day of HCG (787.8 ± 206.9
versus 860.2 ± 218.6 pmol/1 per follicle) and the number of
embryos transferred (2.86 ± 0.41 versus 2 73 ± 0.66). The
same was true when patients were subdivided according to the
treatment received.
In group A, 45 pregnancies were achieved (37%); eight
pregnancies were achieved in group B (22%) (not significant).
Table L Distribution of patients and pregnancy rates m relation to
endometrial thickness on the day of human chonoruc gonadotrophin
administration among the whole cohort of patients [m-vitro fertilization
(IVF) plus lntracytoplasmic sperm injection (ICSI)] and for patients
undergoing IVF and ICSI separately
Endometnal thickness
Total no. of patients (IVF + ICSI)
Total pregnancy rate (IVF + ICSI) (%)*
No of patients undergoing IVF11
Pregnancy rale in patients with IVF (%)c
No of patients undergoing ICSIb
Pregnancy rate m patients with ICSI (%)d
*P =
P =
P=
6
P =
b
C
Group A
<10 mm
Group B
»10 mm
37
22 (8/37)
30
17 (5/30)
7
43 (3/7)
121
37 (45/121)
79
41 (32/79)
42
31 (13/42)
not significant (Z test for companson of proportions)
0 05 (Fisher's exact test)
0 03 (Z test for companson of proportions)
not significant (Z test for companson of proportions)
With regard to endometnal thickness, Table I shows that a
higher proportion of IVF compared with ICSI patients had
endometrium <10 mm thick (27.5 and 14.2% respectively)
(P = 0.05). Conversely, a higher proportion of ICSI compared
with IVF patients had endometrium 5*10 mm thick (96 and
72% respectively) (not significant).
Patients undergoing ICSI presented a higher concentration
of oestradiol on the day of HCG (11 746 7 ± 4240.1 pmol/1)
and a higher number of follicles (14.20 ± 4 93) when compared
with patients undergoing IVF (9279.7 ± 4567.8 pmol/1 and
11.30 ± 5.90 respectively) (P =£ 0.005 Student's f-test),
whereas the duration of follicular stimulation (12.10 ± 1.73
days in ICSI versus 11.90 ± 1.64 days in IVF), the concentration of oestradiol per follicle (839 4 ± 198.2 pmol/1 per follicle
in ICSI versus 841.5 ± 227.0 pmol/1 per follicle in IVF) and
the number of embryos transferred (2.79 ± 0.53 in ICSI versus
2.75 ± 0.65 in IVF) were similar between the two groups. No
correlation was found between endometnal thickness and
oestradiol concentrations, or between endometrial thickness
and the number of follicles, in either ICSI or IVF patients,
whereas a positive correlation (P < 0.001) was found between
oestradiol concentration and the number of follicles in both
ICSI (n = 49; r = -0.846) and IVF (n = 109; r =
-0.863) patients
The pregnancy rate was higher in IVF group A patients (32/
79; 41%) than in IVF group B patients (5/30; 17%) (P =
0.03), whereas no significant difference was found in the
pregnancy rate between ICSI group A (13/42; 31%) and ICSI
group B (3/7; 43%) (Table I)
Discussion
Our data show a higher percentage of patients with thin
endometnum in the IVF group when compared with the ICSI
group (P = 0.05) Moreover, a higher pregnancy rate was
observed in IVF patients with thick endometrium when compared with IVF patients with thin endometrium (P = 0.03),
whereas no significance related to endometrial thickness was
found in the pregnancy rate among groups A and B ICSI
patients or when comparing pregnancy rates in groups A and
1539
L.Rinaldi et aL
B in the whole cohort of patients (IVF plus ICSI) undergoing
ovarian stimulation and embryo transfer.
We believe that the differences observed in the thickness of
endometrium among the patients undergoing IVF for female
indications and patients undergoing ICSI for male factor may
be attributed mainly to the different pathogenesis of infertility
in the two groups of patients. Tubal occlusion or stenosis is
usually related to an ascendant infection that may damage the
endometrium before affecting the tubes, and endometriosis,
when present, is often associated with adenomyosis affecting
the uterine structure and lining. On the other hand, women
undergoing ICSI for male factor are usually (and in every case
in our study) healthy women whose endometrium has never
been exposed to any noxious agent and therefore has a
physiological response to ovarian stimulation.
With regard to the higher concentration of oestradiol in ICSI
patients when compared with IVF patients, we believe that
this is related to the higher number of oocytes retrieved in
ICSI patients, and is confirmed by the lack of correlation found
between endometrial thickness and oestradiol concentration or
the number of follicles and by the strong positive correlation
between oestradiol concentration and the number of follicles
in all the groups of patients.
We believe that the statistically significant difference found
in pregnancy rate between group A and B IVF patients and
the non-significant difference in pregnancy rate between group
A and B ICSI patients can both be attributed to the same
above-mentioned causes, i.e. patients undergoing IVF for
female indications usually have a history of noxious agents
affecting the endometrium, whereas women undergoing ICSI
for male factors usually have no past history of endometrial
diseases.
These data may have some relevance to the controversial
issue of endometrial thickness as a prognostic factor for
implantation. Although there are many studies concerning
this issue, there is no agreement in the literature about the
effectiveness of the ultrasonographic evaluation of endometrial
thickness in predicting the pregnancy.
During the past 10 years some investigators have found
(Glissant et aL, 1985; Gonen et al., 1989; Gonen and Casper,
1990), whereas some have not found (Fleischer et aL, 1986;
Rabinowitz et aL, 1986; Welker et aL, 1989), a positive
correlation between endometrial thickness and pregnancy rate.
In the same way, some investigators have found (Sher et aL,
1991; Dickey et aL, 1992), and some have not found (Khalifa
et aL, 1992; Eichler et aL, 1993; Oliveira et aL, 1993; Noyes
et aL, 1995), a positive correlation between both endometrial
ultrasonographic appearance and thickness and pregnancy rate.
Some investigators have studied both endometrial appearance
and thickness, but have only found a positive correlation
between pregnancy rate and endometrial appearance (Ueno
et aL, 1991; Check et aL, 1993; Coulam et aL, 1994; Serafini
et aL, 1994) or between pregnancy rate and endometrial
thickness (Bergh et aL, 1992), but not for the other endometrial
variables taken into account.
These discrepancies may be attributed to various different
factors, e.g. the use of transabdominal ultrasonography (Smith
et aL, 1984; Glissant et aL, 1985; Fleischer et aL, 1986;
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Rabinowitz et aL, 1986) versus trans vaginal ultrasonography
(Gonen et aL, 1989; Welker et aL, 1989; Gonen and Casper,
1990; Sher et aL, 1991; Ueno et aL, 1991; Bergh et aL, 1992;
Dickey et al., 1992; Khalifa et al, 1992; Check et aL, 1993;
Eichler et al., 1993; Oliveira et aL, 1993; Coulam et aL, 1994;
Serafini et al., 1994; Noyes et al., 1995). Similarly, the
observed differences may be in part attributed to the different
stimulation protocols used: clomiphene citrate plus gonadotrophin treatment alone (Smith et al., 1984; Glissant et al.,
1985; Gonen et aL, 1989; Gonen and Casper, 1990; Oliveira
et al., 1993); the exclusive use of gonadotrophin (Fleischer
et al., 1986; Rabinowitz et al., 1986); the combined use
of gonadotrophin-releasing hormone (GnRH) analogues plus
gonadotrophin after pituitary desensitization (Check et al.,
1991; Serafini et al., 1994); the combined use of GnRH
analogues plus gonadotrophin using both short and long
protocols (Khalifa et al., 1992); the combined use of GnRH
analogues plus gonadotrophin after pituitary desensitization
and during the natural cycle (Ueno et al., 1991); clomiphene
citrate plus gonadotrophin and GnRH analogues plus gonadotrophin according to the long or short protocol (Welker et aL,
1989; Bergh et al., 1992; Dickey et aL, 1992; Eichler et al.,
1993); GnRH analogues plus gonadotrophin and gonadotrophin
alone (Sher et al., 1991); or eventually GnRH analogues plus
gonadotrophin, gonadotrophin alone or clomiphene citrate plus
gonadotrophin (Noyes et al., 1995). The different timing of
the assessment of endometrial thickness may be relevant
to the explanation of the discordant findings. In fact, the
endometrium has been assessed on the day of HCG (Sher
et aL, 1991; Dickey et al., 1992; Khalifa et al., 1992; Check
et al., 1993; Eichler et al., 1993; Oliveira et aL, 1993), on the
day of oocyte retrieval (Welker et al., 1989; Khalifa et al.,
1992), on the day before oocyte retrieval (Fleischer et al.,
1986; Gonen et al., 1989; Gonen and Casper, 1990; Bergh
et al., 1992; Noyes et al., 1995) and on the day before HCG
(Ueno et al., 1991; Khalifa et al., 1992).
The study that is closest to the one described here is that
of Check etal. (1991) who, using the same stimulation protocol
at the same threshold value for endometrial thickness measured
by transvaginal ultrasound (<10 versus 3*10 mm), found a
statistically significant difference in the pregnancy rate between
the two groups of patients. In that study, Check et al. (1991)
were also able to evaluate the endometrial echogenicity and
found a positive correlation between endometrial echogenicity
and pregnancy rate. However, they excluded from their study
nine patients who did not achieve fertilization and did not
report on the percentage of patients suffering from male factor
infertility included in the study.
In fact, most of the previous studies have excluded patients
undergoing IVF for male factor infertility (Bergh et al., 1992;
Khalifa et aL, 1992; Serafini et al., 1994; Takahashi et al.,
1995), or have investigated groups of patients in whom the
main indications for IVF were tubal factor, endometriosis or
unexplained infertility (Dickey et aL, 1992; Oliveira et al.,
1993), because FVF results in terms of fertilization and pregnancy rates in cases of male infertility used to be lower than
those for other indications.
Endometrial thickness as a predictor of pregnancy
Only Sher et al. (1991) have considered the role of the
negative impact of uterine pathologies on endometrial development, noting a higher rate of poor endometnal grades (endometrial thickness < 9 mm and a homogeneous endometrial
pattern, or endometrial thickness > 9 mm but a heterogeneous
endometrial pattern) in women with uterine pathologies; however, the impact of this finding in the ultrasonographic assessment of endometrium in the prediction of pregnancy was not
fully evaluated.
Similarly, Takahashi et al. (1995) have shown that in patients
with a history of ectopic pregnancy, a thinner endometrium is
a predictor of poor outcome These authors were unable to
show any difference in endometrial thickness between patients
who conceived and patients who did not conceive in the
general population of patients undergoing F/F.
The use of ICSI, because of its high fertilization and
pregnancy rates, has enabled us to compare at all levels patients
undergoing assisted reproductive treatment for either female
or male indications of infertility.
Our data, showing a higher percentage of thin endometrium
in IVF patients when compared with ICSI patients, are in
agreement with the previously reported finding (Sher et al,
1991) of a higher rate of poor endometrial lining in uterine
pathologies. In addition, our results show that endometnal
thickness may be taken into account as a predictor of pregnancy
only in assisted reproduction treatment for female indications
of infertility (TVF), in which case a thin endometrium may
reflect the previous or present action of a noxious agent on
the uterine lining. However, in assisted reproductive treatment
for male indications of infertility (ICSI), in the absence of
any associated uterine pathology, the presence of a thin
endometrium does not seem to affect pregnancy and cannot
be used to predict the chance of pregnancy.
Further studies are doubtless needed, and we currently have
one underway to evaluate the role of endometrial appearance
in addition to endometrial thickness, both in patients undergoing FVF for female indications and in patients undergoing
ICSI for male indications of infertility.
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