Article Type: Clinical Article

Accepted Article
Three-dimensional 3D ultrasound combined with power Doppler for the

differential diagnosis of endometrial lesions among infertile women

Ni Jia *, Han Bingbing, Liang Jiabin, Wang Fang

Reproductive Medicine Center, Luoyang Center Hospital of Zhengzhou University,

Luoyang, China

* Corresponding author: Ni Jia

Reproductive Medicine Center, Luoyang Center Hospital of Zhengzhou University, No

228, Middle Zhongzhou Road, Luoyang, Henan 471000, China. Telephone:

0086-379-63892147.

Email: nijia666666@126.com

Keywords: 3D ultrasound; Endometrial lesions; Endometrial thickness; Endometrial

volume; Infertility; Power Doppler;

Synopsis: Three-dimensional power Doppler was found to have value for the

diagnosis of endometrial lesions among infertile women.

This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may
lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1002/ijgo.12787
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 Abstract

Objective: To assess three-dimensional (3D) ultrasound combined with power

Accepted Article
Doppler (PD) for the differential diagnosis of endometrial lesions among infertile

women.

Methods: A prospective study carried out at a reproductive medicine center in

Luoyang, China, between January and December 2015. The inclusion criteria were

asymptomatic infertility with normal endometrium or specific endometrial lesions.

Participants were subdivided by whether they had normal endometrium (group 1,

n=357), or endometrial lesions including polyps, hyperplasia, intrauterine adhesions,

or endometritis (group 2, n=99). 3D PD and hysteroscopy were performed in the

follicular phase. Endometrial thickness, volume, vascularization index (VI), flow index

(FI), and vascularization flow index (VFI), and subendometrial VI, FI, and VFI were

calculated. Endometrial lesions were confirmed by pathologic analysis.

Results: The overall prevalence of endometrial lesions was 99/456 (21.3%).

Endometrial thickness and volume were significantly larger in group 2 than in group 1

(9.96 ± 3.24 vs 8.15 ± 2.50 mm and 3.70 ±2.54 vs 2.42 ± 1.64 cm3, respectively; both

P<0.001). Endometrial thickness and volume were larger among women with

endometrial polyps and hyperplasia; endometrial VI, FI, and VFI were lower among

women with intrauterine adhesions.

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 Conclusion: Three-dimensional PD has value for the differential diagnosis of

endometrial lesions among infertile women.

Accepted Article
Clinical trial registration: The trial is registered in the Chinese Clinical Trial Registry

as ChiCTR1800015799.

1 INTRODUCTION

Endometrial pathology, including endometrial polyps, hyperplasia, intrauterine

adhesions, endometritis, endometrial cancer, and submucosal fibroids, is common in

cases of infertility. These pathologies affect embryo implantation and may lead to

infertility or early pregnancy loss [1]. Diagnosis and treatment of these abnormalities

are advocated to optimize the condition of the uterine environment and improve

pregnancy outcomes in cases of infertility.

Hysteroscopy is recommended as a routine procedure for assessing endometrial

lesions among infertile women. Although it offers direct visualization and real-time

treatment for intrauterine pathology [2, 3], it is an invasive procedure. As an

alternative, two-dimensional transvaginal ultrasound (TVUS) has been widely used to

detect endometrial lesions. The addition of power Doppler (PD) has further increased

the sensitivity and specificity of TVUS to diagnose endometrial polyps [4]. However,

few studies have described how to distinguish complex endometrial lesions in

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 infertility using color Doppler [5]. Furthermore, the prevalence of different endometrial

pathologies in cases of infertility has not been fully documented.

Accepted Article
Different types of endometrial lesion have different blood flow characteristics, which

can be used as tools to differentiate focal endometrial pathology [6]. Furthermore,

combined with three-dimensional (3D) ultrasound, PD provides a unique noninvasive

tool to examine the blood supply in the whole endometrium and the subendometrial

region, facilitating calculations of endometrial thickness, volume, vascularization

index (VI), flow index (FI), and vascularization flow index (VFI), and subendometrial

VI, FI, and VFI. The aim of the present study was to compare 3D PD characteristics

among different endometrial lesions and to assess whether these characteristics can

help to differentially diagnose endometrial pathologies among asymptomatic infertile

women.

2 MATERIALS AND METHODS

The present prospective study enrolled consecutive women who attended the

outpatient clinic of the Reproductive Medical Center of Luoyang Center Hospital,

Luoyang, China, for the assessment and treatment of infertility between January 1

and December 31, 2015. Study approval was obtained from the ethics committee of

the Luoyang Center Hospital of Zhengzhou University. All women provided specific

consent to participation in the study and to the publication of identifying information

and images.

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 The inclusion criteria were asymptomatic infertility with normal endometrium or

specific endometrial lesions. Asymptomatic was defined as infertility without abnormal

Accepted Article
bleeding symptoms, menorrhagia, or intermenstrual spotting. Specific endometrial

lesions included endometrial polyps, hyperplasia, intrauterine adhesions, and

endometritis confirmed by hysteroscopy. Women with severe endometriosis, uterine

fibroids, uterine anomalies, premature ovary failure, or hydrosalpinx, which might

affect PD characteristics, were excluded.

All methods were carried out in accordance with appropriate guidelines and

regulations. As part of the pretreatment assessment, TVUS, 3D PD, and

hysteroscopy were performed in the follicular phase (3–7 days after menstruation)

because it has been reported that better ultrasound images of intrauterine lesions can

be obtained in this phase [7]. Diagnosis of endometrial lesions was confirmed by

hysteroscopy and pathologic analysis.

For the ultrasound examination, women were placed in the dorsal lithotomy position.

TVUS was performed with a Voluson E6 (GE Tiefenbach, Zipf, Austria) and a

5–9-MHz endocavitary transducer to evaluate the pelvis, endometrial thickness,

endometrial–myometrial interface, and endometrial echogenicity. For the 3D PD

examination, the 3D PD box was positioned to cover the whole uterus completely in

order to evaluate endometrial volume, VI, FI, and VFI, and subendometrial VI, FI, and

VFI. The following settings were used: quality, high; wall motion filter, low 1; pulse

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 repetition frequency, 0.9 kHz; sweep angle, 120°. The women were asked to remain

still and the 3D transvaginal probe was kept as still as possible during the evaluation.
Accepted Article
Imaging was done by using the Virtual Organ Computer Aided Analysis (VOCAL)

imaging program that is integral to the Voluson E6 sonography system. Endometrial

thickness was measured at the point of maximum thickness at the highly reflective

interface of the endometrial–myometrial junction. Endometrial volume was estimated

by manually tracing the outline of the endometrium in multiple views. The longitudinal

view was used as the reference and a rotation step of 15° was used, resulting in 12

defined contours for the endometrium. From these contours, the endometrial volume,

VI, FI, and VFI were calculated automatically by VOCAL. The subendometrial region

was defined as the region 10 mm beneath the endometrial–myometrial junction [8],

and the subendometrial VI, FI, and VFI were calculated in the same way.

The VI is a measure of the ratio of color voxels to all voxels in the region of interest,

and represents the density of vessels in the tissue. The FI is the mean PD signal

intensity inside the endometrium and represents the mean intensity of flow. The VFI

represents a combination of vascularity and flow intensity [9]. All measurements were

performed by the same research (NJ) to avoid the inter-operator variation.

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 The endometrium of all women was assessed by hysteroscopy 3–7 days after

menstruation. The procedure was performed under anesthesia in an outpatient

Accepted Article
setting. All diagnoses of endometrial lesions were confirmed by pathologic analysis.

Endometritis was diagnosed on the basis of plasma cells in the endometrial stroma

[10]. The diagnostic criteria for hyperplasia were focal or diffuse polypoid or papillary

endometrial thickening, abnormal vascular patterns, presence of glandular cysts, and

glandular outlets [11].

For the present analysis, participants were subdivided into two groups in accordance

with their hysteroscopic and endometrial pathology: the first group had normal

endometrium and was included in the analysis as the control, whereas the second

group had endometrial lesions. The second group was further subdivided into women

with endometrial polyps, endometrial hyperplasia, intrauterine adhesions, and

endometritis. The 3D PD characteristics in each of these subgroups were compared

with those of control women.

The data were analyzed by using SPSS version 16.0 (IBM, Armonk, NY, USA). Data

were reported as mean ± SD or number (percentage). Two-tailed, independent

samples t test and 2 test were used to compare differences as appropriate. A P value

of less than 0.05 was considered statistically significant.

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 3 RESULTS

Among 555 women invited to participate in the study, 90 were excluded because of
Accepted Article
uterine anomalies (n=68), uterine fibroids (n=12), endometriosis (n=4), and

hydrosalpinx (n=6). Thus, 465 women underwent the 3D PD examination and

hysteroscopy. Subsequently, a further 9 women were excluded because of cervix

polyps (n=8) and submucosal fibroids (n=1) (Figure 1).

Among the 456 women included in the final analysis, 357 had normal endometrium

(Figure 2a), and 99 had endometrial lesions. Among the 99 women with endometrial

lesions, the incidence of endometrial polyps (Figure 2b), hyperplasia (Figure 2c),

intrauterine adhesions (Figure 2d), and endometritis was 61 (13.1%), 23 (4.9%), 8

(1.7%), and 7 (1.5%), respectively. The overall prevalence of endometrial lesions

among the infertile women was 99/456 (21.3%).

Table 1 summarizes the general characteristics, endometrial thickness, volume, VI,

FI, and VFI, and subendometrial VI, FI, and VFI of the study women by the presence

of normal endometrium and endometrial lesions. There was no difference between

the two groups in age, duration of infertility, cause of infertility, endometrial VI, FI, or

VFI, or subendometrial VI, FI, or VFI. However, the proportion of primary infertility (68

[68.7%] vs 190 [53.2%], P=0.008), endometrial thickness (9.96 ± 3.24 mm vs

8.15 ± 2.50 mm, P<0.001), and endometrial volume (3.70 ± 2.54 cm3 vs

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 2.42 ± 1.64 cm3, P<0.001) were higher for women with normal endometrium than for

those with endometrial lesions.

Accepted Article
Table 2 summarizes the general characteristics, endometrial thickness, volume, VI,

FI, and VFI, and subendometrial VI, FI, and VFI of the study women by the presence

of normal endometrium or type of endometrial lesion (Figure 3). Age and the

proportion of primary infertility were similar between each of the four types of lesion

and normal endometrium. As compared with those with normal endometrium, women

with hyperplasia had a higher duration of infertility and women with endometritis had a

larger proportion of female factors. Significantly larger endometrial thickness and

volume were observed among women with polyps (respectively, 10.57 ± 3.57 mm vs

8.15 ± 2.50 mm, P<0.001; and 4.04 ± 2.84 cm3 vs 2.42 ± 1.64 cm3, P<0.001) and

hyperplasia (respectively, 9.35 ± 2.19 mm vs 8.15 ± 2.50 mm, P=0.026; and

3.45 ± 1.77 cm3 vs 2.42 ± 1.64 cm3, P=0.044) as compared with normal endometrium.

Endometrial VI, FI, and VFI were significantly lower for women with uterine adhesions

than for those with normal endometrium (respectively, 0.33 ± 0.41 vs 1.38 ± 2.01,

P=0.040; 20.22 ± 2.72 vs 23.23 ± 3.88, P=0.030; and 0.06 ± 0.06 vs 0.37 ± 0.61,

P=0.045).

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 4 DISCUSSION

The present results indicate that endometrial thickness and volume have clinical
Accepted Article
value in diagnosing different endometrial pathologies, such as endometrial polyps,

hyperplasia, intrauterine adhesions, and endometritis. As compared with women with

normal endometrium, those with endometrial lesions had a larger endometrial

thickness and volume (9.96 ± 3.24 mm vs 8.15 ± 2.50 mm, P<0.001; 3.70 ± 2.54 cm3

vs 2.42 ± 1.64 cm3, P<0.001). Therefore, we recommend that hysteroscopy should

be performed if endometrial thickness and volume are greater than 10.0 mm and 3.7

cm3, respectively, in the follicular phase. Furthermore, significantly lower endometrial

VI, FI, and VFI values were observed for women with intrauterine adhesions than for

women with normal endometrium. On the basis of these findings, we suggest that 3D

PD should be performed before hysteroscopy for infertility assessment, especially for

women with endometrial lesions.

Few studies have used 3D PD to assess endometrial and subendometrial

vascularization during the evaluation of endometrial lesions [6, 12]. Cil et al. [6]

reported that a single-vessel pattern was characteristic of endometrial polyps,

whereas a rim-like vessel pattern was typical of a submucosal fibroid. However, those

indicators were subjective. Furthermore, few studies have assessed the association

of these characteristics with infertility. To our knowledge, the present study is the first

to use 3D PD to assess the characteristics of different endometrial lesions among

infertile women.

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 The prevalence of endometrial lesions among infertile women was found to be 99

(21.3%), indicating that endometrial lesions might be a principal cause of infertility.

Accepted Article
Furthermore, the proportion of primary infertility was higher among women with

endometrial lesions than among those with normal endometrium, indicating that

endometrial lesions can directly affect infertility.

Ait et al. [13] reported that intrauterine lesions were present among 40%–50% of

infertile women, whereas Fatemi et al. [14] noted an 11% prevalence of intrauterine

abnormalities among asymptomatic patients. The present incidence of 21.3% is

similar to the findings of Karayalcin et al. [15], who reported that 22.9% of infertile

women had endometrial lesions on hysteroscopy. In terms of the types of lesion

observed, the incidence of endometrial polyps was highest (13.1%), followed by

hyperplasia (4.9%), intrauterine adhesions (1.7%), and endometritis (1.5%).

The present study demonstrated that there are some differences in endometrial

thickness, volume, VI, FI, and VFI and subendometrial VI, FI, and VFI between

women with normal endometrium and those with endometrial lesions. Endometrial

thickness is commonly used to estimate endometrial function, and some studies have

shown that endometrial thickness, volume and VI, FI, and VFI can be used to

evaluate endometrial receptivity among women undergoing assisted reproduction

[16-18]. However, whether endometrial volume and 3D PD characteristics can be

used to evaluate endometrial function is largely unknown. In the present study,

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 endometrial thickness and volume differed between women with normal endometrium

and those with endometrial lesions, but endometrial and subendometrial VI, FI, and
Accepted Article
VFI were similar between the two groups.

Regarding the different types of lesion, larger endometrial thickness and volume were

found among women with polyps (10.57 ± 3.5 mm and 4.04 ± 2.84 cm3, respectively)

and hyperplasia (9.35 ± 2.19 mm and 3.45 ± 1.77 cm3, respectively) than among

those with normal endometrium (8.15 ± 2.50 mm and 2.42 ± 1.64 cm3, respectively),

whereas endometrial and subendometrial VI, FI, and VFI were similar. It has been

reported that endometrial polyps include endometrial glands, stroma, and blood

vessels, similar to normal endometrium [19], and hyperplasia has been defined as

abnormal proliferation of the uterine endometrial glands [20]. Both endometrial polyps

and hyperplasia are derived from the endometrium, which might explain why these

two types of lesion had similar vascularization characteristics.

More interestingly, endometrial VI, FI, and VFI were significantly lower among women

with intrauterine adhesions than among those with normal endometrium, indicating

that adhesions might affect vascularization of the endometrium. In addition,

endometrial FI was slightly higher among women with endometritis than among those

with normal endometrium. Although the difference was not significant, this might

suggest a higher intensity of blood flow. Collectively, these data indicate that different

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 endometrial lesions have different 3D PD characteristics, which might be helpful for

making a differential diagnosis.

Accepted Article
The main limitation of this study is the small sample size, and studies with larger

sample sizes are needed to confirm these findings and provide further insight. An

additional limitation is that we did not analyze the vascularization characteristics of

the endometrium after surgical treatment for patients with endometrium lesions,

which is something we hope to do in future work.

In conclusion, endometrial thickness and volume calculated by 3D PD were found to

have value in the differential diagnosis of endometrial lesions among women affected

by infertility.

Author contributions

NJ and HBB contributed to study design and analysis. NJ and LJB performed the

evaluations and prepared the figures and tables. HBB and WF collected the data and

performed the statistical analysis. All authors contributed to manuscript writing.

Conflicts of interest

The authors have no conflicts of interest.

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Accepted Article
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Figure legends

Figure 1: Flowchart showing the study participants.

Figure 2: Types of endometrial pathology. (a) Normal endometrium. (b) Single

endometrial polyp. (c) Hyperplasia. (d) Intrauterine adhesions.

Figure 3 Endometrial and subendometrial vascularization of the different types of

endometrial pathology: (a) Normal endometrium. (b) Single endometrial polyp. (c)

Hyperplasia. (d) Intrauterine adhesion.

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 Table 1 Characteristics of the study women by presence of endometrial lesions a.
Characteristic Normal endometrium Endometrial P value
(n=357) lesions (n=99)
Accepted Article
Age, y 30.15 ± 4.84 30.94 ± 4.76 0.148
Primary infertility 190 (53.2) 68 (68.7) 0.008
Infertility duration, y 3.96 ± 3.26 4.74 ± 3.65 0.058
Cause of infertility
Female b 194 (54.3) 53 (53.5) 0.977
c
Male 81 (22.7) 17 (17.2) 0.296
Mixed 61 (17.1) 19 (19.2) 0.735
Unexplained 20 (5.6) 10 (10.1) 0.171
Endometrial thickness, mm 8.15 ± 2.50 9.96 ± 3.24 <0.001
3
Endometrial volume, cm 2.42 ± 1.64 3.70 ± 2.54 <0.001
Endometrial VI 1.38 ± 2.01 1.29 ± 1.84 0.675
Endometrial FI 23.23 ±3.88 23.00 ± 3.19 0.594
Endometrial VFI 0.37 ± 0.61 0.32 ± 0.49 0.549
Subendometrial VI 4.42± 4.29 4.12 ± 3.78 0.520
Subendometrial FI 27.06 ± 3.36 27.11 ± 3.03 0.901
Subendometrial VFI 1.27 ± 1.31 1.23 ± 1.22 0.797
Abbreviations: FI, flow index; VI, vascularization index; VFI, vascularization flow index.
a
Values are given as mean ± SD or number (percentage).
b
Mainly tuboperitoneal, ovulation failure or mild endometriosis
c
Oligoasthenoteratospermia or azoospermia.

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ccepted Articl
Table 2 Characteristics of the study women by type of endometrial lesion a.
Characteristic Normal (n=357) Polyps (n=61) Hyperplasia (n=23) Adhesions (n=8) Endometritis (n=7)
b b b
Value Value P value Value P value Value P value Value P
value b
Age, y 30.15 ± 4.84 30.41 ± 4.28 31.13 ± 4.81 32.65 ± 3.92 33.0 ± 8.45
Primary infertility 190 (53.2) 43 (70) 17 (74) 3 5
Infertility duration, y 3.96 ± 3.26 4.44 ± 3.38 6.00 ± 4.45 0.011 4.47 ± 3.91 3.57 ± 2.15
Cause of infertility
Female 194 (54.3) 29 (48) 11 (48) 6 7 <0.001
Male 81 (22.7) 14 (23) 3 (13) 0 0
Mixed 61 (17.1) 10 (16) 8 (35) 1 0
Unexplained 20 (5.6) 8 (13) 1 (4) 1 0
Endometrial 8.15 ± 2.50 10.57 ± 3.57 <0.001 9.35 ± 2.19 0.026 8.62 ± 2.77 8.14 ± 2.41
thickness, mm
Endometrial 2.42 ± 1.64 4.04 ± 2.84 <0.001 3.45 ± 1.77 0.044 2.46 ± 2.04 2.96 ± 2.16
3
volume, cm
Endometrial VI 1.38 ± 2.01 1.36 ± 3.29 1.41 ± 1.76 0.33 ± 0.41 0.040 1.35 ± 2.39
Endometrial FI 23.23 ± 3.88 23.19 ± 3.29 22.85 ± 2.48 20.22 ± 2.72 0.030 24.98 ± 3.37
Endometrial VFI 0.37 ± 0.61 0.35 ± 0.53 0.34 ± 0.45 0.06 ± 0.06 0.045 0.37 ± 0.59
Subendometrial VI 4.42 ± 4.29 4.21 ± 3.64 4.48 ± 4.38 2.27 ± 1.61 4.21 ± 4.67
Subendometrial FI 27.06 ± 3.36 27.27 ± 3.16 27.34 ± 2.81 25.58 ± 2.63 26.72 ± 3.12
Subendometrial VFI 1.27 ± 1.31 1.26 ± 1.12 1.40 ± 1.58 0.62 ± 0.45 1.21 ± 1.38
a
Values are given as mean ±SD, absolute number, or number (percentage) unless stated otherwise.
b
As compared with normal endometrium.

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Accepted Article

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 Figure 2: Different endometrial pathologies: (a). normal endometrium; (b). single
endometrial polyp; (c). hyperplasia; (d). intrauterine adhesions.
Accepted Article

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 Figure 3: The endometrial and subendometrial vascularization of different
endometrial pathologies: (a). normal endometrium; (b). single endometrial polyp; (c).
hyperplasia; (d). intrauterine adhesion.
Accepted Article

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