To assess the endometrial receptivity in terms of endometrial thickness and vascularity and to assess the potential relationship between perifollicular vascularity following ovulation inducing drugs and outcome in intrauterine insemination (IUI) using the Doppler ultrasonography.

1. Colour Doppler Ultrasound in Controlled Ovarian Stimulation with
Intrauterine Insemination

2. Apollo Medicine 2012 September
Volume 9, Number 3; pp. 252e262
Case Report
Colour Doppler ultrasound in controlled ovarian stimulation with
intrauterine insemination
Kavita Bhadauriaa,*, Reeti Sahnib, Sohani Vermab, Payal Q. Khatric
ABSTRACT
Aim: To assess the endometrial receptivity in terms of endometrial thickness and vascularity and to assess the
potential relationship between perifollicular vascularity following ovulation inducing drugs and outcome in intrauterine
insemination (IUI) using the Doppler ultrasonography.
Materials and methods: Infertile couple in our hospital was subjected to colour Doppler ultrasound examination and
the parameters were tabulated and analysed in terms of pregnant and not pregnant.
Results: There were 23 pregnancies out of 100 cycles. The endometrial receptivity has a significant role in predicting
successful outcome with thicker endometrium, multifocal zone 3/4 vascularity and with distinct five line appearance.
The pregnancy rate was higher with grade 4 perifollicular vascularity.
Copyright © 2012, Indraprastha Medical Corporation Ltd. All rights reserved.
Keywords: Colour Doppler, Controlled ovarian stimulation, Intrauterine insemination, Endometrial receptivity,
Perifollicular vascularity
INTRODUCTION
Infertility in today’s world has reached almost epidemic
proportion with the treatment modalities and options developing almost compulsorily at exponential rates. Both IUI
(intrauterine insemination) and IVF (in vitro fertilization)
are now practiced in reasonably large numbers at most reported infertility centres.
Intrauterine insemination (IUI) with or without
controlled ovarian stimulation (COS) is a popular modality
for treatment of subfertility. Although considerable discussion and debate have appeared in western literature
regarding the utility of COS and IUI, lately the National
Institute of Clinical Excellence (NICE), UK has revised
the evidence for assessment and treatment of infertile
couples and has recommended that IUI should be offered
to couples with infertility because it is as effective as
IVF, less invasive and requires fewer resources.1
The use of gonadotrophins in IUI is now widespread,
and has been shown to improve significantly the odds of
pregnancy. However, significant risks of ovarian hyperstimulation syndromedand in particular multiple pregnanciesdremain.2 Despite this, IUI has significant cost
savings and is less invasive, without necessarily a reduction
in effectiveness, compared with other forms of assisted
reproduction treatment such as IVF or gamete intra-fallopian transfer (GIFT) in particular for non-tubal infertility.3
The rationale put forward in support of COS and IUI is
that ovarian stimulation corrects subtle, unpredictable
ovulatory dysfunction and there is increased probability
of conception if increased density of motile spermatozoa
is placed closer to multiple fertilizable oocytes.1
With the progressive standardization of these techniques
it also becomes imperative to develop parameters to predict
suitability and thus the success of the procedure. As in most
gynaecological condition, sonography and Doppler are
a
Resident, bSenior Consultant, cAssociate Consultant, Department of Radiodiagnosis and AARU, Indraprashta Apollo Hospitals, New Delhi
110076, India.
*
Corresponding author. email: drkbhadauria@gmail.com
Received: 14.5.2012; Accepted: 4.7.2012; Available online: 13.7.2012
Copyright Ó 2012, Indraprastha Medical Corporation Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.apme.2012.07.014

3. Colour Doppler ultrasound in controlled ovarian stimulation
Case Report
253
Fig. 1 Longitudinal scans showing endometrial patterns. (a and b) Hazy five line appearance.
powerful tools. Goswamy and Steptoe4 were the first to
suggest that abnormal uterine artery blood flow might be
associated with infertility and to develop a classification
of uterine artery blood flow waveforms. Subsequently,
other authors have confirmed a relationship of uterine and
ovarian blood flow to unexplained infertility,5,6 and to
successful implantation following IVF.7e10
Power Doppler or colour ultrasonography has been
generating increasing clinical interest since its introduction.11 Despite the fact that the application of power
Doppler in gynaecology remains in its infancy, recent
studies suggest potential applications especially in relation
to the assessment of uterine and perifollicular vascularity12,13 and outcome in IVF treatment cycles.
Statistical models have been reported for predicting
success rates in IUI which suggested that follicle number,
endometrial thickness, duration of subfertility and semen
parameters were the most significant variables in predicting
outcome.14 The application of Doppler ultrasound in IUI
has tended to relate uterine perfusion to outcome and few
data exist on ovarian vascularity in these treatment cycles.15
This study was thus designed to collect statistically
significant data in large numbers for IUI so as to achieve
superior results and outcome.
MATERIALS AND METHODS
The cycles of ovarian-stimulationeintrauterine insemination (COSeIUI) treatment in infertile couples presenting
to Apollo Assisted Reproduction Unit (AARU), from
June 2009 to December 2010 were screened in our study.
These patients were subjected to inclusion and exclusion
criterias and 100 COSeIUI cycles were then analysed
and assessed for the successful outcome of pregnancy.
Inclusion criteria
Women aged <42 years, primary or secondary infertility
lasting for at least 12 months, tubal patency assessed by
hysterosalpingography and/or laparoscopy with chromosalpingography, with at least one patent fallopian tube, normal
semen analysis.
Exclusion criteria
Patients with coexisting disease such as bilateral tubal
block, congenital uterine anomalies which are liable to
affect outcome, associated male subfertility and infertility,
patients who were started on ovulation induction regime
Fig. 2 Longitudinal scans showing endometrial patterns. (a and b) Distinct five line appearance.

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Bhadauria et al.
Fig. 3 Longitudinal scans showing endometrial patterns. (a and b) Thin endometrium with no layering.
but were not subjected to IUI due to inappropriate follicular
growth (follicular size less than 16 mm till 22nd day of the
cycle) were excluded from our study, patients with multiple
dominant follicles (four or more) were excluded from our
study considering the risk for multifetal pregnancies.
Ultrasound examination was carried out in all patients in
each cycle of COSeIUI at day 2 (baseline). Each patient
was informed and written consent was taken for COSeIUI
as well as for colour Doppler US evaluation in addition to
routine follicular monitoring US protocol. Patients were
examined in lithotomy position and transvaginal ultrasound
evaluation was done using transvaginal probe of 8 Hz
(E8C). All studies were performed by a single operator
on LOGIC 5 PRO (GE Healthcare) ultrasound machine.
On day 2 of menstrual cycle, all patients were subjected
to baseline US. The uterus was screened for endometrial
lining (thickness and pattern), echogenicty of myometrium
(fibroids, adenomyosis, past myomectomy). The uterine
imaging was done to rule out congenital anomalies if any.
The ovaries were evaluated to rule out presence of cysts,
number of antral follicles in either ovaries. The Doppler
US was done to evaluate the uterine and intraovarian arterial impedance as described below.
On day 7, the patients were evaluated for follicular and
endometrial growth and were examined thereon every alternate day till the follicle reached the size 14 mm or more and
then everyday till ovulation. Patients were subjected to 5000
units of HCG administration intravenously when one or
more follicles attained the size >16 mm and endometrial
thickness was >7 mm. The IUI was done 48 h (or 24 h if
follicle was ruptured earlier) after the HCG administration.
Doppler US was carried and various parameters were
recorded as described on subsequent patient visits. For
colour and power Doppler study, the pulse repetition
frequency (PRF) and wall filters were set at the lowest
possible frequencies. We used wall filter 40 Hze75 Hz
for evaluating low resistance intraovarian and endometrial
vessels. The wall filters were 60 Hze115 Hz for evaluating
the ascending branches of both uterine arteries. The pulse
repetition frequency (PRF) was 45e60 Hz.
The uterus was screened for
1) Size and configuration to rule out congenital anomalies if any.
2) The endometrium was evaluated for:
Thickness of endometrium
i) Measured from the myometrialeendometrial junction to
the endometrialemyometrial junction in sagittal plane.
ii) Layering of endometrium (endometrial echogenic
pattern), distinct five line appearance, hazy five line
appearance, or no layering (Figs. 1e3).
iii) Endometrial blood flow
The endometrial and periendometrial areas are
divided into the following four zones16,17
(Figs. 4 and 5).
Zone 1 e a 2 mm thick area surrounding the
hyperechoic outer layer of the endometrium
Zone 2 e the hyperechoic outer layer of the
endometrium
Zone 3 e the hypoechoic inner layer of the
endometrium
Zone 4 e the endometrial cavity
3) Uterine arteries. The ascending branches of both
uterine arteries were examined at lower uterine segment
and Doppler parameters were recorded as (Fig. 6):
Fig. 4 Endometrial zones of vascularity.

5. Colour Doppler ultrasound in controlled ovarian stimulation
Case Report
255
Fig. 5 Zone 3/4 endometrial vascularity with (a) sparse and (b) multifocal vascularity.
i)
ii)
iii)
iv)
Peak systolic velocity (PSV)
End diastolic velocity (EDV)
Pulsatility index (PI)
Resistive index (RI)
THE FOLLICLES
The number of dominant follicles (>16 mm) in each
COSeIUI cycle were recorded and each follicle was
assessed for perifollicular vascularity (Fig. 7). When more
Fig. 6 Different waveforms of uterine artery. (a) Normal waveform with characteristic early diastolic notch with high PI value in (a)
and low PI in (b). (c) Absent early diastolic flow and (d) absent diastole flow.

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Bhadauria et al.
Fig. 7 (a) Normal ovary on base day 2, (b) follicular diameter measured in two perpendicular planes, (c) showing dominant follicle
with cumulus oophorus (arrow), (d) rt ovary showing multiple3 follicles.
than one follicle was observed, grading was performed for
all of them, and the highest vascularity grade was recorded.
The vascularity of each follicle was subjectively graded
using Power Doppler imaging (according to the grading
system by Chui et al, 1997)13 (Fig. 8).
Grade 1: 25% of the circumference;
Grade 2: 26e50%;
Grade 3: 51e75%;
Grade 4: >75%.
THE OVARIES
The intraovarian arterial supply was studied in the periovulatory and periluteal phase. The intraovarian arterial
Doppler indices were recorded as (Fig. 9)
i) Peak systolic velocity (PSV)
ii) End diastolic velocity (EDV)
iii) Pulsatility index (PI)
iv) Resistive index (RI).
RESULTS AND ANALYSIS (TABLE 1)
A total of 100 women undergoing consecutive COSeIUI
CYCLES were analysed in our study. There were 23 pregnancies with pregnancy rate being 23%. The youngest patient
was 20 years old, with 2 years duration of infertility. The
eldest female was 41 years old with 10 years of infertility.
Twenty-three pregnant patients, 13 patients had endometrial thickness 8e10 mm, eight patients had endometrial
thickness 10e12 mm, one patient had endometrial of 8 mm.
We found significant relation between endometrial
thickness and pregnancy rates, highest (42%) with endometrial thickness ranging from 10 to 12 mm (p < 0.05).
However not all pts with thicker endometrium had positive
outcome. In case endometrial thickness was 6e8 mm, it
showed a significantly lower rates of pregnancy (p < 0.01).
Correlation: Pearson coefficient between endometrial
thickness and pregnancy is 0.31, it is a positive correlation
which suggest that more the endometrial thickness more the
pregnancy rate.

7. Colour Doppler ultrasound in controlled ovarian stimulation
Case Report
257
Fig. 8 Grades of perifollicular vascularity (a)-grade 1 (<25% of circumference) (b)-grade 2 (25%e50%) (c)-grade 3 (50%e75%) (d)grade 4 (>75% of circumference).
There is significant correlation between pregnancy rate
and endometrial vascularity. Of 16 patients with multifocal
vascularity in zone 3/4, 14 patients (88%) had positive
outcome (highly significant p < 0.001). Whereas only
22% (9 out of 41) patients had conception with sparse
vascularity in zone 3/4. No conception was reported in
women having zone 1/2 endometrial vascularity (highly
significant p < 0.001, significantly lower chances of pregnancy if in zone 2).
Statistically higher pregnancy rate (40%) was reported in
women with distinct five line appearance (p < 0.05).
Patients with no endometrial layering had poor pregnancy
rate (6%) and 19% pregnancy was seen with hazy five
line appearance.
Lesser the uterine artery impedance, more the number of
pregnancies reported. No pregnancy was reported in
women when uterine artery impedance PI was more than
2.99 (statistically significant p < 0.05). There was no
significant difference in pregnancy rates when uterine arterial PI was low, 36% when PI was <2.19, 29% when PI
was 2.2e2.49, 32% when PI was 2.5e2.75 and 13% with
PI 2.75e2.99 (not significant > 0.05).
The median number of pre-ovulatory follicles (>17 mm
in diameter) on the IUI day among the pregnant patents was
2 (Æ1.6) and in non-pregnant cases was 1.79 (Æ1.2). In
cycles with a single pre-ovulatory follicle (>17 mm in
diameter) the pregnancy rate (17%) was significantly lower
than in cycles with more follicles (35% and 36% respectively with two or three dominant follicles).
The perifollicular vascularity was associated with better
pregnancy rate. No pregnancy was achieved with perifollicular vascularity with grade 1 and grade 2 (which is highly
significant p < 0.001). The pregnancy rate was 19% with
grade 3 perifollicular vascularity (not significant) and was
68% with grade 4 perifollicular vascularity (which is highly
significant p < 0.001).
DISCUSSION
Many studies have been conducted to evaluate the role of
various ultrasound parameters in predicting pregnancy
during ART18e20 but little information exists in the literature with regard to their role in predicting subsequent pregnancy outcomes.21 Our study was attempted to assess the
prognostic uterine and ovarian IUI variables with regard
to successful outcome (pregnant/non-pregnant) using
colour Doppler transvaginal ultrasound so that the outcome

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Apollo Medicine 2012 September; Vol. 9, No. 3
Fig. 9 Intraovarian waveform pattern (a) In proliferative phase,
and (b) In secretory phase.
of subsequent COSeIUI cycles could be more accurately
predicted than before.
In our study pregnancy occurred in 23 patients (23%) of
total 100 infertility COSeIUI cycles. In Mehrafza et al
study undertaken on 336 IUI cycles, the overall pregnancy
rate was 18.2%.22 In another study by Delgadillo et al the
pregnancy rate was 21.7%23 which was similar to the
results of our study. Yousefi et al had 27% pregnancy
rate.24 However, the success rate in some studies was lower
than ours, about 12%.25e27
As regards the diagnosis of infertility, the highest pregnancy rate (33%) was achieved in women with ovulatory
disorders. No conception was reported in women suffering
from endometriosis. Patients with unexplained infertility
had second highest pregnancy rate (23%). Farimani and
Amiri reported the highest pregnancy rate (23.1%) in women
with ovulatory disorders and the lowest (7.7%) in women
suffering from endometriosis.24 Most of studies did show
higher pregnancy rates in patients with unexplained infertility
and ovulatory disorders and significantly low pregnancy rates
Bhadauria et al.
in patients suffering from endometriosis.27,28 IUI should not
be opted for patients having severe endometriosis.
Endometrial thickness and pattern, as a predictor of
outcome, have been investigated by numerous studies
with variable results. While some study groups found
a significant correlation between thickness and pattern of
the endometrium and pregnancy rate, others reported no
such relationship. In our study, the endometrial receptivity
has a significant role in predicting outcome of pregnancy.
No pregnancy was reported when endometrial thickness
was less than 8 mm and when endometrial vascularity
was less than zone 3. Pregnancy rate was highest (88%)
with multifocal vascularity in zone 3/4 and 22% with sparse
vascularity in zone 3/4. Number of pregnancies were highest when endometrial thickness was 10e12 mm. Friedler
et al in their study of literature survey (concerning endometrial thickness, which included 25 reports comprising 2665
assisted reproduction treatment cycles) found that in 1203
cycles the difference in the mean endometrial thickness of
conception and non-conception cycles was statistically
significant, while in 331 cycles found no such significant
difference. They found that an endometrial thickness
<6 mm has a strong NPV for the subsequent occurrence
of pregnancy.29 Strohmer et al proposed that endometrial
thickness is mainly related to individual uterine size and
therefore has no predictive value for implantation. Similarly, no correlation was found between implantation and
the mean cross-sectional area of the endometrium.30 In
the study of Katib reported that mean of endometrial thickness in infertile was 0.7 cm, and the mean of endometrial
thickness in fertile women was 1.3 cm hence significant
decrement in endometrial thickness at p < 0.05. In addition,
pregnancy rates were higher when the endometrium was
thicker than 10 mm. A periovulatory endometrial thickness
more than 10 mm defined 91% of conception cycles. No
pregnancy occurred when the endometrium measured less
than 7.31 M. Aghahoseini et al found no significant difference in endometrial thickness between pregnant and nonpregnant groups.32 It seems that the correlation between
endometrial thickness as a single parameter and pregnancy
is controversial. In general, most authors agree that the PPV
of endometrial thickness alone is low. The low predictive
value of endometrial thickness could be explained by its
weak relationship with uterine receptivity.33
In Chien et al study, although pregnancy and implantation rates were significantly higher in patients with zone 3
compared with zone 1 or 2 penetration, there was no significant difference between the groups with zone 1 and 2 penetrations were found.17
In our study the pregnancy rate was 40% with distinct five
line endometrial pattern, 19% with hazy five line Endometrial
pattern, and 6% with no endometrial layering. Pregnancy rate

9. Colour Doppler ultrasound in controlled ovarian stimulation
Case Report
259
Table 1 Comparison between pregnant and non-pregnant patients.
Parameter
Pregnant
Non pregnant
Sample size
23
77
Age in years
31.00 ± 4.25
31.08 ± 4.69
Primary
17
65
Secondary
6
12
4.87 ± 2.07
5.18 ± 2.98
0.639
10.13 ± 1.47
8.94 ± 1.60
<0.001
Zone 1
0
7
Zone 2
1
35
Zone 3/4 (sparse)
7
34
Zone 3/4 (multifocal)
15
01
No layering
1
17
Hazy five line
10
43
Distinct five line
12
17
Type of infertility
Duration of infertility(years)
Endometrial thickness in mm
Endometrial
receptivity on day
of IUI
Endometrial
layering
Endometrial
Vascularity
Type of layering
P value
0.943
0.557
<0.001
<0.05
Right
2.38 ± 0.32
2.64 ± 0.46
<0.01
Left
2.43 ± 0.28
2.70 ± 0.54
<0.01
Mean
2.40 ± 0.28
2.67 ± 0.44
<0.01
Uterine artery
doppler (PI)
No of follices
1
12
57
more than
2
6
11
17 mm
3
5
9
Grade 1
0
3
Perifollicular
Grade 2
0
40
vascularity
Grade 3
6
26
Grade 4
17
8
0.737
Follicles on day
of IUI
was higher in distinct five line endometrial appearance. Friedler et al in their study found that the difference in the
endometrial patterns of conception and non-conception
cycles was statistically significant in 2892 cycles, however
in 844 cycles no such significance was noted.33
<0.001
Uterine artery impedance is inversely related to pregnancy outcome. No pregnancy was reported when uterine
PI was >2.99. Pregnancy Rate was higher in women with
uterine artery PI <2.19. However no significant difference
was noted in patients with uterine arterial PI 2.19e2.99.

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Apollo Medicine 2012 September; Vol. 9, No. 3
The predictive value of the PI, calculated from the published data, using a PI upper limit of 3.0 or 3.3, the Doppler
assessment of uterine blood flow had a high NPV and sensitivity (in the ranges 88e100 and 96e100% respectively)
and a relatively higher range of PPV and specificity
(44e56 and 13e35% respectively) compared with the other
ultrasonic parameters.33 Tsai et al reported no pregnancy
when the pulsatility index of the ascending branch of the
uterine arteries was more than 3. The fecundity rate was
18% when the pulsatility index was less than 2 and was
19.8% when the pulsatility index was between 2 and 3
(not significant). The continuing pregnancy rate was 18%
when the pulsatility index was less than 2, compared with
12.1% when the pulsatility index was between 2 and 3
(P < 0.05).34
In our study we found that PR was low in COSeIUI
cycles with single pre-ovulatory follicles which was significantly lower than in cycles with more follicles. The perifollicular vascularity was associated with better pregnancy
rate. No pregnancy was achieved when perifollicular vascularity was grade 1 or grade 2. The pregnancy rate was 19%
with grade 3 perifollicular vascularity (not significant) and
was 68% with grade 4 perifollicular vascularity (which is
highly significant p < 0.001). Bhal et al in their study reported that the pregnancy rate was low in the low-grade
perifollicular vascularity, and it was higher in cycles with
grade 3 and grade 4 perifollicular vascularity.35 Ragini
et al in their study reported that follicular vascularity did
not appear to predict the chance of pregnancy in women
undergoing mild COS and IUI cycles. Pregnancy rate in
the low-, medium- and high-grade vascularity groups was
14.1, 10.0 and 11.8%, respectively.36 Stefano et al also
confirmed that the perifollicular vascularity is related to
good-quality oocytes.37
CONCLUSIONS
The endometrial receptivity (thickness and vascularity) is
a predeterminant in predicting the outcome of pregnancy
in COSeIUI treatment cycles. The pregnancy rates were
higher in women with thick, multilayered endometrium
and zone 3/4 endometrial vascularity. No conception was
reported when endometrial thickness was less than 8 mm
and zone 1/2 vascularity. The importance of measuring
endometrial receptivity at around the time of intrauterine
insemination is to ensure the presence of a minimal thickness to permit implantation. An evaluation of endometrial
pattern, simplified to multilayered and non-multilayered,
may serve to postpone or cancel those cycles in which
poor endometrial development is demonstrated. The
measurement of the impedance in the uterine artery during
Bhadauria et al.
IUI has provided an indirect assessment of uterine receptivity. Colour Doppler analysis allows an assessment of
the impedance of the vascular flow of the uterine artery
and measurement of uterine perfusion. If a PI upper limit
for the uterine artery of 3 is defined, Doppler blood flow
has a high negative predictive value and sensitivity. The
positive predictive value and the specificity of uterine
vascularization remain low. In our study, no pregnancy
occurred with uterine PI values of more than 2.99. However
not all patients conceived with lower uterine PI. At this
time, however, the usefulness of ultrasonographic parameters in monitoring improvements of uterine receptivity in
COSeIUI still remains to be proved by controlled prospective studies.
Perifollicular vascular perfusion appears to be an important factor in determining the outcome in stimulated IUI
cycles, and may have clinical implications in assisted reproduction techniques. As there were no pregnancies in
women with low-grade vascularity, the identification of
these cycles would be valuable early in cycles (before
HCG/IUI). This could allow cancellation of treatment after
careful counselling and cancellation of the cycles, could be
cost-effective both financially and emotionally. However
more longitudinal data would be needed before this form
of prospective management of treatment cycles could be
applied clinically.
CONFLICTS OF INTEREST
All authors have none to declare.
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