Gynecological Endocrinology

ISSN: 0951-3590 (Print) 1473-0766 (Online) Journal homepage: https://www.tandfonline.com/loi/igye20

Oocyte quality in women with infertility associated

endometriosis

Mekan Rakhimberdievich Orazov, Victor Yevseyevich Radzinsky, Igor

Isaakovich Ivanov, Marina Borisovna Khamoshina & Victoriya Borisovna
Shustova

To cite this article: Mekan Rakhimberdievich Orazov, Victor Yevseyevich Radzinsky, Igor
Isaakovich Ivanov, Marina Borisovna Khamoshina & Victoriya Borisovna Shustova (2019) Oocyte
quality in women with infertility associated endometriosis, Gynecological Endocrinology, 35:sup1,
24-26, DOI: 10.1080/09513590.2019.1632088

To link to this article: https://doi.org/10.1080/09513590.2019.1632088

© 2019 The Author(s). Published by Informa Published online: 18 Sep 2019.

UK Limited, trading as Taylor & Francis
Group.

Submit your article to this journal Article views: 4006

View related articles View Crossmark data

Citing articles: 21 View citing articles

Full Terms & Conditions of access and use can be found at

https://www.tandfonline.com/action/journalInformation?journalCode=igye20
GYNECOLOGICAL ENDOCRINOLOGY
2019, VOL. 35, NO. S1, 24–26
https://doi.org/10.1080/09513590.2019.1632088

ORIGINAL ARTICLE

Oocyte quality in women with infertility associated endometriosis

Mekan Rakhimberdievich Orazova, Victor Yevseyevich Radzinskya, Igor Isaakovich Ivanovb,
Marina Borisovna Khamoshinaa and Victoriya Borisovna Shustovac
a
Department of Obstetrics and Gynecology with Course of Perinatology of the Medical Faculty, Medical Institute of the Russian University of
Friendship of Peoples, Moscow, Russian Federation; bDepartment of Obstetrics and Gynecology, Medical Academy Named S. I. Georgievskiy of
Vernadsky Crimean Federal University, Simferopol, Republic of Crimea, Russian Federation; cReproduction and Genetics Center “NOVA CLINIC”,
Moscow, Russian Federation

ABSTRACT KEYWORDS
The mechanisms of endometriosis-related infertility remain still unknown. Endometriosis and clinical Endometriosis; infertility;
markers of oocyte quality are a very important problem of reproduction. The purpose of the study is to oocyte quality
assess the quality of oocytes in women with infertility associated with endometriosis. The study included
infertile reproductive aged women, between 29 and 40 years who underwent IVF and ICSI procedures.
The patients were divided into three groups: group I involved 50 (n ¼ 50) patients with recurrent unilat-
eral endometriomas, group II included 50 patients (n ¼ 50) unilateral endometriomas after surgical treat-
ment and control group with 30 (n ¼ 30) patients with tubal factor infertility. Clinical and morphological
assessment of oocyte quality was performed in all IVF/ICSI cycles. The results of the study demonstrate a
statistically significant increase in the number of immature oocytes of metaphase MI and immature
oocytes at the GV germinal vesicle stage in patients with infertility associated with endometriosis, com-
pared with the control group (p<.005). There is deterioration in the quality of the obtained oocytes in
patients with the presence of endometrioma more than 3 cm in diameter. The results of this study allow
to conclude that endometriomas negatively affect quality of oocyte and ovarian reserve, whereas endo-
metriomas after cystectomy, have a deleterious and sustained effect on ovarian reserve.

Introduction value of these observations is limited due to the restrictions of

The association of endometriosis and fertility is the most contro-
versial issue of current reproductive medicine. The mechanisms
of endometriosis-related infertility remain largely unknown [1,2].
The causes of infertility in women with endometriosis may range
from anatomical distortions due to adhesions and fibrosis to
endocrine abnormalities and immunological disturbances.
A woman’s fertility does not depend only on the absolute
number of efficient follicles. A number of authors highlight that
multiple surgeries lead to a sharp decrease in the ovarian reserve,
insufficient blood supply, and therefore to oogenesis disruption,
which affects the quality of embryos obtained in the
IVF program.
No comprehensive evaluation of the literature supporting or
denying an effect of endometriosis on oocyte quality from both a
clinical and a biological perspective has so far been carried
out [3–6].
Knowledge on oocyte quality, as reflected by its morphologic
and molecular characteristic, is small due to the very limited
availability of MII oocytes for research. Some publications have
focused on studying the morphological changes of these imma-
ture human oocytes. There was an opinion that the use of oocyte
morphology as an indicator of embryo quality is still uncertain.
In the literature, there are data about that morphological defect
observed, including cytoplasmic granularity and/or the presence
of vacuoles, could affect fertilization; however, the predictive
noninvasive techniques as the simple transmitted light micros-
copy and the problem of subjectivity in the morphological
evaluations.
The purpose of the study is to assess the quality of oocytes in
women with infertility associated with endometriosis.
Materials and methods
Prospective study was performed in the Department of obstetrics
and gynecology with course of Perinatology of Medical Institute
of the RUDN University (eoples Friendship University of
Russia) and in the center of reproduction and genetics ‘NOVA
CLINIC’ between the 2018 and 2019 years. The study group
included infertile reproductive aged women, between 24 and
40 years who underwent IVF and ICSI procedures. The patients
were divided into three groups: group I involved 50 (n ¼ 50)
patients with recurrent unilateral endometriomas, group II
included 50 patients (n ¼ 50) after surgical treatment of unilat-
eral endometriomas and control group with 30 (n ¼ 30) patients
with tubal factor infertility. The average diameters of recurrent
endometriomas were 4 cm. All patients participating in the
study were given IVF/ICSI protocols with separate counting of
antral follicles in the ovaries, with separate collection of oocytes
into labeled Petri dishes. The diagnosis of the endometriosis
cysts was performed and confirmed twice by ultrasound

CONTACT Mekan Rakhimberdievich Orazov omekan@mail.ru Department of Obstetrics and Gynecology with Course of Perinatology of the Medical Faculty,
Medical Institute of the Russian University of Friendship of Peoples, Miklukho-Maklaya str. 6, Moscow 117198, Russian Federation
ß 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
 GYNECOLOGICAL ENDOCRINOLOGY 25

investigation. Ovarian endometriomas were defined as round- An important fact should be noted, the ability of these imma-
shaped cystic masses with more than 1 cm in diameter, with ture oocytes to undergo oocyte in vitro maturation (IVM) to
thick walls, regular margins, and homogeneous low echogenic metaphase II (MII) stage was tested, finding that a significantly
fluid content with scattered internal echoes, and without papil- lower number of GVs and metaphase I (MI) oocytes was able to
lary proliferations. Before IVF, according to ultrasound, the reach the MII stage in the endometriosis group compared to
number of visualized antral follicles in the ovary containing controls [6,8–11]. Interesting meta-analyses were demonstrated
endometriotic inclusion were taken into account, as well as in on the effect of the endometriosis on IVF outcomes as pregnancy
the contralateral ovary. During transvaginal puncture of the fol- rates, miscarriage rates, or live birth rates, but only few of them
licles, the number of oocytes obtained from the affected ovary evaluated the effect of the endometriosis on parameters directly
and not containing endometrioma was also taken into account. correlating with oocyte quality. However, it is important to
The main morphological characteristics of the ‘competent’ oocyte
were considered: the correctness of the form with a uniformly Table 2. Characteristic of patients with endometriomas.
graduated cytoplasm, with an intact first polar body. Women Size of endometriomas Group I (n ¼ 50) Group II (n ¼ 50)
carrying atypical lesions, i.e. cysts whose sonographic appearance 10 mm 18 (36%) 24 (48%)
was compatible but not distinctive for endometriosis were 10–20 mm 20 (40%) 18 (36%)
excluded. The diameter of the endometriomas was calculated as 20–30 mm 8 (16%) 6 (12%)
30–40 mm 4 (8%) 1 (2%)
the mean of three perpendicular measurements.

Results
When analyzing the age of the examined women, it was noted
that the age range in the main group was from 31 to 40 years
old, the average age was 33.36 ± 4.5, and in the control group
31.73 ± 4.21 (Table 1). In patients of groups 1 and 2, the number
of antral follicles and the number of oocytes obtained were sig-
nificantly lower in comparison with the control group. At the
same time, between the groups 1 and 2, these differences were
not identified. It is important that the absence of a statistically
significant difference (p>.005) in the number of obtained oocytes
in the cohort study is associated with the unilateral location of
the endometrioma, as well as the compensatory capabilities of
the intact ovary. The number of oocytes obtained from an ovary Figure 1. Of high-quality oocytes obtained (M II). Micrograph of oocytes on the
1st day of development (metaphase of the second division). Oocyte micro-
containing an endometrial cyst is significantly lower compared graphs 200.
to the contralateral ovary, especially when the endometrioma
diameter is more than 3 cm (Table 2). The results of a morpho-
logical analysis of the quality of oocytes using the Hoffman
modulation contrast revealed a statistically significant increase in
the number of immature oocytes of metaphase MI and immature
oocytes at the GV germinal vesicle (GV) stage in patients with
endometriosis compared with the control group (p<.005)
(Figures 1–3). Personalized study demonstrated that every fourth
oocyte extracted from the ovary containing an endometrial cyst,
had structural changes, in some patients a displacement of the
nucleus to the oocyte membrane, partial or complete absence of
the nuclear envelope and various signs of degenerative changes
were observed. The above changes were typical for patients
whose oocytes were obtained from an ovary with an endome-
trioma more than 3 cm in diameter.
According to literature, morphology itself could be influenced
by other factors, such as the ovarian stimulation or the hormonal
milieu; therefore, its potential as predictive factor of clinical out- Figure 2. This is a cell in metaphase 1 of meiosis (ΠI oocyte). Oocyte micro-
come needs further investigation [7]. graphs 200.

Table 1. Baseline characteristics of women with infertility.

Characteristics Group I (n ¼ 50) Group II (n ¼ 50) Control group (n ¼ 30)
Age, years 33.36 ± 4.5 32.64 ± 4.2 31.73 ± 4.21
Infertility duration 4.6 ± 2.4 4.2 ± 2.1 3.3 ± 2.8
AMH 2.2 ± 1.3 2.1 ± 1.8 3.0 ± 1.8
The number of antral follicles in the affected ovary 4.1 ± 1.5 5.4 ± 1.7 12.5 ± 2.9 (at both sides)
The number of antral follicles in the intact ovary 7.2 ± 2.6 7.8 ± 2.3
Total number of oocytes recovered 8.8 ± 3.9 9.2 ± 3.2 10.1 ± 6.8
The number of high-quality oocytes obtained (oocyte in metaphase II) 4.1 ± 2.8 5.2 ± 2.6 9.6 ± 3.5
26 M. R. ORAZOV ET AL.

Figure 3. The so-called germinal vesicle (GV) oocytes. Oocyte micrographs 200.
understand that around this problem, a lot of questions and
few answers.
Conclusions
The results of this study allow to conclude that endometriomas
negatively affect quality of oocyte and ovarian reserve, whereas
endometriomas after cystectomy, has a deleterious and sustained
effect on ovarian reserve.
Disclosure statement
The authors declare that there is no potential conflict of interest.
References
[1] Senapati S, Sammel MD, Morse C, et al. Impact of endometriosis on
in vitro fertilization outcomes: an evaluation of the Society for
Assisted Reproductive Technologies Database. Fertil Steril. 2016;106:
164–171.
[2] Vercellini P, Vigan o P, Somigliana E, et al. Endometriosis: pathogen-
esis and treatment. Nat Rev Endocrinol. 2014;10:261–275.
[3] Sallam HN, Garcia-Velasco JA, Dias S, et al. Long-term pituit-
ary downregulation before in vitro fertilization (IVF) for women
with endometriosis. Cochrane Database Syst Rev. 2006;1:
CD004635.
[4] Xu B, Guo N, Zhang XM, et al. Oocyte quality is decreased in
women with minimal or mild endometriosis. Sci Rep. 2015;5:
10779.
[5] Dumesic DA, Meldrum DR, Katz-Jaffe MG, et al. Oocyte environ-
ment: follicular fluid and cumulus cells are critical for oocyte health.
Fertil Steril. 2015;103:303–316.
[6] Karaer A, Tuncay G, Mumcu A, et al. Metabolomics analysis
of follicular fluid in women with ovarian endometriosis
undergoing in vitro fertilization. Syst Biol Reprod Med. 2019;
65(1):39–47.
[7] Rienzi L, Vajta G, Ubaldi F. New culture devices in ART. Placenta.
2011;32:248–251.
[8] Goud PT, Goud AP, Joshi N, et al. Dynamics of nitric oxide, altered
follicular microenvironment, and oocyte quality in women with endo-
metriosis. Fertil Steril. 2014;102:151–159.
[9] Borges E, Jr, Braga DP, Setti AS, et al. Endometriosis affects oocyte
morphology in intracytoplasmic sperm injection cycles? JBRA Assist
Reprod. 2015;19:235–240.
[10] Assidi M, Dufort I, Ali A, et al. Identification of potential markers of
oocyte competence expressed in bovine cumulus cells matured with
follicle-stimulating hormone and/or phorbol myristate acetate in
vitro. Biol Reprod. 2008;79:209–222.
[11] Younis JS, Shapso N, Fleming R, et al. Impact of unilateral versus
bilateral ovarian endometriotic cystectomy on ovarian reserve: a sys-
tematic review and meta-analysis. Hum Reprod Update. 2019;25:
375–391.

Funding
The publication has been prepared with the support of the ‘RUDN
University Program 5-100’.