https://doi.org/10.52973/rcfcv-e33212
Received: 07/06/2023 Accepted: 01/08/2023 Published: 17/08/2023
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Revista Científica, FCV-LUZ / Vol. XXXIII, rcfcv-e33212
ABSTRACT
Oocyte maturation is a critical step for in vitro embryo production.
In female cats, ndings on the inuence of the estrous cycle stage
on oocyte quality and maturation are contradictory. Little is known
about this phenomenon in female cats in the tropics. This study aimed
to assess the effect of the estrous cycle stage on oocyte quality and
subsequent capacity to complete nuclear maturation in cats in a
tropical environment. Ovaries from 18 sexually matured cats were
collected during ovariohysterectomy. Cumulus–oocyte complexes
(COCs) were released from follicles by slicing and fragmentation of
the ovarian cortex. According to morphological characteristics, COCs
were classied into grades I–II (suitable) and III–IV (no suitable). Only
suitable COCs from each cat were cultured for in vitro maturation.
Nuclear oocyte maturation was assessed by the presence of a
telophase I or metaphase II plate with extrusion of the rst polar
corpuscle. A signicantly greater number of oocytes per ovary were
collected from queens in inactive than in follicular or luteal phase.
Proportions of suitable COCs were similar among groups. Rate of
oocyte maturation did not differ among stages of the estrous cycle,
nor did the proportion of non–matured or degenerated oocytes. The
age of the queens did not affect the percentage of oocyte maturation.
In conclusion, the quality and rate of oocytes maturation were similar
in the three stages of estrous cycle examined.
Key words: Cat, reproduction; biotechnology; in vitro system;
tropics
RESUMEN
La maduración de los ovocitos es un paso crítico para la producción
de embriones in vitro. En las gatas, los hallazgos sobre la inuencia de
la fase del ciclo estral en la calidad y maduración de los ovocitos son
contradictorios. Se sabe poco sobre este fenómeno en las gatas en los
trópicos. El objetivo de este estudio fue evaluar el efecto de la fase del
ciclo estral sobre la calidad de los ovocitos y la posterior capacidad de
completar la maduración nuclear en gatas de un ambiente tropical.
Se recogieron ovarios de 18 gatas sexualmente maduras durante la
ovariohisterectomía. Los complejos cúmulo–ovocito (COCs) fueron
obtenidos de los folículos mediante el corte y la fragmentación de la
corteza ovárica. Según sus características morfológicas, los COCs se
clasicaron en grados I–II (aptos) y III–IV (no aptos). Sólo los COCs de
buena calidad de cada gata se cultivaron para su maduración in vitro.
La maduración nuclear de los ovocitos se evaluó por la presencia
de una placa en telofase I o metafase II con extrusión del primer
corpúsculo polar. Se obtuvo un número signicativamente mayor
de ovocitos por ovario en las gatas en fase inactiva que en fase
folicular o lútea. Las proporciones de COCs fueron similares entre
los grupos. La tasa de maduración de los ovocitos no dirió entre
las fases del ciclo estral, ni tampoco la proporción de ovocitos no
maduros o degenerados. La edad de las gatas no afectó al porcentaje
de maduración de los ovocitos. En conclusión, la calidad y la tasa de
maduración de los ovocitos fueron similares en las tres etapas del
ciclo estral examinadas.
Palabras clave: Gata; reproducción; biotecnología; sistema in vitro;
trópico
Effect of estrous cycle stage on oocyte in vitro maturation of domestic cats
reared under tropical conditions
Efecto de la fase del ciclo estral en la maduración in vitro de ovocitos de gatas domésticas
criadas en condiciones tropicales
Enmar Monasterio–Alemán
1
, Luis Monasterio–Oquendo
1
, Liset Zambrano–Vivas
2
, Verónica Arboleda–Caldera
2
, Carla Osorio–Melendez
2
,
José Aranguren–Méndez
1
, Fernando Perea–Ganchou
3
* , Hugo Hernández–Fonseca
4
1
Universidad del Zulia, Facultad de Ciencias Veterinarias. Maracaibo, Venezuela.
2
Universidad del Zulia, Facultad de Ciencias Veterinarias, Unidad de Investigación en Biotecnología Animal. Maracaibo, Venezuela.
3
Universidad de Cuenca, Facultad de Ciencias Agropecuarias. Cuenca, Ecuador.
4
Saint George's University, School of Veterinary Medicine, Anatomy, Physiology and Pharmacology Department. True Blue, St. George's, Grenada, WI.
*Corresponding author: fernando.perea@ucuenca.edu.ec
Estrous cycle stage and in vitro maturation of cat oocytes in tropical countries/ Monasterio-Alemán et al. ________________________
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INTRODUCTION
Domestic cats (Felis catus) are very prolic and fertile animals, so
the main efforts to develop an ecient in vitro system for embryo
production have been the multiplication and preservation of wild
species of felines threatened by extinction [1]. Thus, domestic cats
have been used as an experimental model [2, 3] for the development
of an in vitro embryo production system to generate information
applicable to the reproduction of wild cats [4, 5].
In vitro studies in small animals are scarce, particularly in domestic
cats. In felines, as in other domestic species, in vitro oocyte
maturation has been considered a critical step for the advancement
of this biotechnology in terms of production of transferable embryos
[6]. Different methodologies and media for in vitro maturation (IVM)
and in vitro fertilization (IVF) in cat oocytes have been described [3,
7, 8, 9, 10, 11, 12, 13].
The goal of an optimal in vitro maturation media is to allow the
developmental competence of the oocytes to be fully expressed.
Oocyte competence is crucial for the success of in vitro maturation
and subsequent embryo development. This capacity is inuenced
by several factors such as the presence of cumulus cells around the
oocyte [14], reproductive season [15], the diameter of the follicle
from which the oocyte is derived [16] and stage of the estrous cycle
at the time of oocyte retrieval [13].
In cats, the estrous cycle progresses throughout different phases:
proestrus, estrus, interestrus, diestrus (if copulation and induced
ovulation occur), and anestrus [17]. In each phase, there is absence
(anestrus), low (interestrus) or high concentration of estrogens
(proestrus, estrus), and high (diestrus) or low (proestrus, estrus)
concentration of Progesterone. These gonadal hormones modulate
the physiological characteristics of the ovaries, oviduct and uterus,
and determine changes in the cellular morphology of the vagina [17].
The variation in the developmental capacity of cat oocytes by the
influence of the estrous cycle stage has been poorly studied and
controversial. Progesterone and or other substances produced by the
corpus luteum (CL) seem to affect the ability of oocytes to complete
nuclear maturation. Oocytes retrieved during the follicular phase
completed metaphase II in a greater proportion, to those recovered
from ovaries with a luteal structure [13, 18]. However, other studies found
no effects of the stage of the estrous cycle on the maturation rate of
cat oocytes, or the cleavage rate and blastocyst development [19, 20].
The studies mentioned above were conducted in regions where
cats exhibit seasonal polyestrous reproductive conduct [21]. In
the tropics, daylight hours do not vary greatly throughout the year,
and cat reproduction is continuously polyestrous [22]. There is no
published information about the inuence of estrous cycle stages
on oocyte quality and nuclear maturation in tropical regions in cats.
Therefore, this study aimed to assess the effect of the estrous cycle
stage on oocyte quality and subsequent capacity to complete nuclear
maturation in cats under a tropical environment.
MATERIAL AND METHODS
All chemicals were purchased from Sigma (St Louis, MO, USA),
unless otherwise mentioned.
Animals and surgery
It was studied 18 domestic cat females, sexually matured, aged
between 8 and 30 months, of different breeds and crossbreeds. Cats
(2.4 kg weight) were in satisfactory physical and health condition
before being included in the study. The surgical procedure was
performed at the Veterinary Polyclinic of the University of Zulia,
Maracaibo, Venezuela. For surgery was used the Hedlund's surgical
technique [23]. The study was conducted between March and May
2017. Vaginal smears were taken before surgery to corroborate the
stage of the estrous cycle. Ovaries were collected from each female
during ovariohysterectomy. Cats were allocated to one of three stages
of the estrus cycle, according to the structures found in the ovaries:
1) follicular stage: one or more follicles greater than or equal to 2 mm
in diameter in one or both ovaries; 2) luteal stage: presence of one or
more CL in one or both ovaries; 3) inactive stage: ovaries without CL
and with no follicles greater than or equal to 2 mm in diameter [20].
Ovary collection and oocyte recovery were transported to the
in vitro fertilization (IVF) laboratory in sterile saline (0.9% NaCl) at
38°C within one h after surgery. Immediately after arriving at the
laboratory, ovaries were rinsed twice in a sterile warmed washing
medium (NaHCO
3
0.55 g; Heparin 0.00277 g; TCM–199 3.9 g; Gentamicin
sulphate 50 mg·mL
-1
, 0.4 % Bovine Serum Albumin (BSA), Sodium
Pyruvate 20 µL; embryo tested ultra–pure water 250 mL). Surrounding
tissues were removed from the ovaries. Ovaries were placed in a
sterile 100 mm petri dish containing washing medium, and cumulus
oocytes complexes (COCs) were released from follicles by slicing and
fragmentation of the ovarian cortex.
COCs were classied according to morphological features under
stereoscopic magnication 20X (Nikon, SMZ–2B, Tokyo, Japan) into
four categories [24]: 1) Grade I: oocytes with uniform, dark cytoplasm,
eccentric spherical nuclei, and five or more compact layers of
cumulus cells; 2) Grade II: oocytes with uniform, dark cytoplasm,
less than ve compact layers of cumulus cells; 3) Grade III: oocytes
with inhomogeneous cytoplasm, partially surrounded by not so
compact cumulus cells; 4) Grade IV: oocytes with heterogeneous or
fragmented cytoplasm, with few or no cumulus cells around them.
Grade I and II oocytes were considered suitable and grades III and IV
were unsuitable. Only the former group of oocytes (grades I and II)
was submitted to Maturation in vitro (IVM).
In vitro maturation
Cumulus oocytes complexes from each cat were cultured separately
for IVM in groups no greater than 20 structures in 90–µL droplets,
covered with mineral oil. IVM medium was composed of TCM–199
supplemented with 1 µg·mL
-1
of estradiol 17–ß; 0.02 UI·mL
-1
of FSH;
0.02 UI·mL
-1
of LH 50 µL; 0.3 mM sodium pyruvate; 4 mg·mL
-1
BSA; 5%
fetal bovine serum; and 50 μg·mL
-1
of Gentamicin. Incubation (Thermo
Scientic, modelo 3010, Waltham, MA, USA) was performed for 30 h
at 38.5 °C in a humidied atmosphere of 5% CO
2
.
Oocyte nuclear maturation
After maturation, COCs from each cat were denuded from cumulus
cells by gentle pipetting in the maturation medium. Denuded oocytes
were xed in a solution of acetic acid–ethanol (1:3) for 24–48 h at
4°C and then placed on a sterile slide covered with a cover slide
setting. Oocytes stained with 1% aceto–orcein solution for 30
min, were rinsed in acetic acid and glycerol solution and left to
dry. Nuclear oocyte maturation was assessed by the presence of
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a telophase I or metaphase II plate and the extrusion of the rst
polar corpuscle. Oocytes without the above characteristics were
considered immature. Fragmented or irregularly shaped oocytes
were considered degenerated [25].
Statistical analysis
The number of oocytes recovered per ovary was analyzed by the
general linear model of SAS (SAS
®
; Version 9.3; SAS Institute, Inc.,
Cary, NC, USA). Means differences were compared by Tukey’s multiple
comparison test. Proportions of suitable, matured or immatured/
degenerated oocytes were analyzed by Chi–square of SAS.
RESULTS AND DISCUSSION
In general, 601 COCs were recovered from female cats in follicular
(n=7), luteal (n=9) or inactive (n=2) stage. A signicantly greater
(P<0.05) number of oocytes per ovary were obtained from queens
in inactive than in the follicular or luteal phases. This difference was
because one queen in the inactive stage yielded 100 COCs and the
other 21. Similar proportions of suitable COCs were quantied among
groups of ovaries (TABLE I).
Proportionally more COCs per ovary were retrieved from ovaries in
the inactive than in the luteal or follicular stages. Although only two
queens with inactive phase ovaries were part of the current study,
and the ovaries from one of them produced 5 fold more COCs than
the second, the average number of oocytes recovered was close to
doubling the average number of oocytes recovered from the other
groups. In relation to this issue, there are opposite ndings. Naoi et al.
[20] reported obtaining a greater number of COCs from inactive than
from follicular or luteal ovaries, which agrees with the outcomes of
Freistedt et al. [26] and the present study in South America. However,
no difference was found in the number of COC retrieved in different
stages of the reproductive cycle [19]. It was found similar proportions
of suitable (grade I and II) COCs among groups of ovaries; however,
signicant differences in the proportions of grade I oocytes was
observed between the follicular and luteal stages [20].
In this study conducted in a tropical region, where cats exhibit
reproductive cyclicity throughout the entire year, maturation
rates were statistically similar among stages of the estrous cycle.
However, it is important to note that the maturation rate was 5 and 9.7
percentage points greater (P>0.05) in oocytes obtained in luteal than
in follicular or inactive phase, respectively. The rate of maturation in
this study was considerably lower than that found in other studies [13,
19]. There is no precise explanation for this nding; however, the donor
cats included in this study came from widely varied households with
varying levels of medical care, husbandry, and nutrition. In general,
cats in tropical environments are freer to be outside the house and,
therefore, are more exposed to stressful situations and environmental
cues that may affect the oocyte developmental competence [27, 28].
The outcomes of previously published studies in felines about
oocyte competence and how it is affected by the stages of the
reproductive cycle have been variables, but not enough evidence
has been gathered. For instance, noticeable differences in oocyte
maturation between follicular and luteal stages were found, with
maturation rates of 50 percentage points greater in the former than
in the later stage [13]. This difference did not change by adding IGF–I,
EGF, or both growth factors, in the maturation media [13].
Supporting the previous nding, substances produced by luteal
tissue, likely Progesterone, seem to have adverse effects on oocyte
competence, because maturation rate was lower when the oocytes
were collected during the luteal stage or from ovaries of pregnant
cats than in the follicular or inactive stage [18]. However, in ruminants,
the CL had favorable effects on oocyte competence and embryonic
development [29, 30].
On the other hand, other studies found no difference in the
maturation rate [19] or blastocyst development [20] from cat
oocytes collected at different stages of the estrous cycle. However,
proportionally more oocytes obtained from the luteal or inactive or
TABLE I
Effect of stage of estrous cycle on the quantity and
quality of oocytes recovered from cat ovaries
Estrous cycle
stage
No. oocytes
recovered
Oocytes/ovary
(mean ± EE)
Suitable
oocytes n (%)
Follicular 228 16.3 ± 6.7
a
173 (75.9)
a
Luteal 252 14.0 ± 6.2
a
188 (74.6)
a
Inactive 121 30.2 ± 27.9
b
90 (74.4)
a
Total 601 16.7 ± 10.2
a, b
: Values with different letters in the same column differ. P<0.05
TABLE II
Effect of stage of estrous cycle on nuclear maturation
of oocytes recovered from cat ovaries
Estrous cycle
stage
No. oocytes
examined
Matured
oocytes n (%)
Immature/
degenerated
oocytes n (%)
Follicular 89 11 (12.4) 78 (87.6)
a
Luteal 144 25 (17.4) 119 (82.6)
a
Inactive 65 5 (7.7) 60 (92.3)
a
Total 298 41 (13.7) 257 (86.2)
TABLE III
Chi–square value and odds ratios for oocyte
maturation among stages of estrous cycle
Estrous cycle
stage
Χ
2
P–value
Odds ratio
(95% CI)
Luteal × Follicular 1.05 0.305 1.49 (0.69–3.19)
Luteal × Inactive 0.87 0.349 1.69 (0.56–5.13)
Luteal × Inactive 3.40 0.065 2.52 (0.91–6.91)
Maturation rate was greater (P>0.05) in oocytes from cats in luteal
than in follicular or inactive stage (TABLE II). A similar proportion of
immature/degenerated oocyte was observed among groups. The
odds ratios for oocyte maturation between two groups in different
stages of the estrous cycle showed a greater probability of oocyte
maturation in luteal than in follicular phase, and in follicular or in
luteal than in inactive stage (TABLE III). According to the cat’s age,
categorized as ≤ 12 (10.1 ± 1.7; n=8) and >12 (20.4 ± 4.2; n=10) months,
the rate of maturation did not differ among stages of estrous cycle
(data not shown).
Estrous cycle stage and in vitro maturation of cat oocytes in tropical countries/ Monasterio-Alemán et al. ________________________
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intermediate phase cleaved and became blastocysts after IVF than
those recovered in the follicular stage [19, 28].
At different stages of the estrous cycle, oocytes are exposed to
varying concentrations of gonadal steroids and other substances
produced inside or outside the ovary [31, 32, 33, 34]. Therefore,
it is plausible that the developmental competence of the oocytes
changes throughout the reproductive cycle. Progesterone is essential
in determining uterine receptivity in mammals but also plays a relevant
role in oocyte maturation and subsequent embryo development [29,
35, 36]. Follicular size, which is related to the stage of the estrous
cycle, may affect maturation and blastocyst rates [37, 38]. Even
varying rates of oocyte maturation, cleavage, and embryo production
in cats in the same stages of the estrous cycle may be supported by
numerous factors modifying the oocyte developmental capacity [26,
27, 39, 40, 41, 42, 43].
CONCLUSION
The quality and rate of oocyte maturation were not affected by the
estrous cycle stage. Nonetheless there was a greater probability for
oocytes obtained from queens in the luteal phase to reach maturation
after IVM . Eventhough, there is some indication that the number of
recovered COCs increased in the inactive than in the follicular or luteal
stage, it cannot at this time conclude this due to the small number
of cats in this group and further research should be conducted using
cats between 12–24 months of known parity.
Conicts of Interest
The authors have no potential conicts of interest with respect to
the research, authorship or publication of this article.
BIBLIOGRAPHICS REFERENCES
[1] Veraguas D, Echeverry D, Castro FO, Rodriguez–Alvarez Ll.
Applied biotechnologies in the conservation of wild felids: In
vitro embryo production and cellular regenerative therapies. In:
Shrivastav AB, Singh KP, editors. Big Cats [Internet]. London:
Intech. Open. 2017. p. 47–71. doi: https://doi.org/kpcj
[2] Pope CE. Aspects of in vivo oocyte production, blastocyst
development, and embryo transfer in the cat. Theriogenol.
[Internet]. 2014; 81(1):126–37. doi: https://doi.org/kpck
[3] Pope CE. Thirty years of assisted reproductive technology in the
domestic cat: A selected summary. Rev. Bras. Reprod. Anim.
2019; 43(2):129–136.
[4] Farstad W. Current state in biotechnology in canine and feline
reproduction. Anim. Reprod. Sci. [Internet]. 2000; 60–61:375–
387. doi: https://doi.org/cmfnmk
[5] Luvoni GC. Current progress on assisted reproduction in
dogs and cats: in vitro embryo production. Reprod. Nutr. Dev.
[Internet]. 2000; 40:505–512. doi: https://doi.org/bd9sqp
[6] Sánchez A; López L; Silva M; Berland M. Maduración in vitro de
ovocitos de gatas tratadas con hormona folículo estimulante
(FSH). Rev. Cientif. FCV–LUZ. 2006; 26(2):124–128.
[7] Goodrowe KL, Hay M, King W. Nuclear maturation of domestic cat
ovarian oocytes in vitro. Biol. Reprod. [Internet]. 1991; 45:466–
470. doi: https://doi.org/bhz65s
[8] Johnston L, Donoghue A, O´Brien S, Wildt D. Culture medium
and protein supplementation inuence in vitro fertilization
and embryo development in the domestic cat. J. Exp. Zool.
[Internet]. 1991; 257:350–359. doi: https://doi.org/bfpvkg
[9] Roth T, Swanson W, Wildt D. Development competence of
domestic cat embryos fertilized in vivo versus in vitro. Biol.
Reprod. [Internet]. 1994; 51:441–451. doi: https://doi.org/c9ss9b
[10] Prochowska S, Nizanski W, Partyka A, Kochan J, Młodawska W,
Nowak A, Skotnicki J, Grega T, Pałys M. The use of human and
bovine commercial media for oocyte maturation and embryo
development in the domestic cat (Felis catus). Reprod. Domest.
Anim. [Internet]. 2019; 54(4):719–726. doi: https://doi.org/kpcm
[11] Wlodarczyk R, Bukowska D, Jackowska M, Mucha S, Jaskowski
JM. In vitro maturation and degeneration of domestic cat oocytes
collected from ovaries stored at various temperatures. Vet. Med.
[Internet]. 2009; 54(10):491–497. doi: https://doi.org/kpcn
[12] Wolfe B, Wildt D. Development to blastocyst of domestic cat
oocytes matured and fertilized in vitro after prolonged cold
storage. J. Reprod. Fert. [Internet]. 1996; 106:135–141. doi:
https://doi.org/bb5g96
[13] Yildirim K, Vural MR, Küplülü S, Ozcan Z, Polat I.M. The effects of
EGF and IGF–1 on FSH–mediated in vitro maturation of domestic
cat oocytes derived from follicular and luteal stages. Reprod.
Biol. [Internet]. 2014; 14(2):122–127. doi: https://doi.org/f59bxx
[14] Sowińska N, Frankowska K, Filipczyk A, Adamaszek A, Nalik K,
Fic K, Pietsch–Fulbiszewska A. The effect of cumulus cells on
domestic cat (Felis catus) oocytes during in vitro maturation and
fertilization. Reprod. Domest. Anim. [Internet]. 2017; 52(Suppl
2):108–113. doi: https://doi.org/kpcq
[15] Martins LM, Fernandes CB, Villaverde A, Landim–Alveranga
FC, Lopes MD. The seasonal and ovarian status effects on in
vitro production of domestic cat embryos between Equator
and Tropic of Capricorn. Pesq. Vet. Bras. 2014; 34(3):277–280.
[16] Uchikura K, Nagano M, Hishinuma M. The effect of ovarian status
and follicular diameter on maturational ability of domestic cat
oocytes. J. Vet. Med. Sci. [Internet]. 2011; 73(5):561–566. doi:
https://doi.org/cjw2nz
[17] Feldman EC, Nelson RW, Reusch C, Scott–Moncrieff, JC. Canine and
Feline Endocrinology. 4th ed. Philadelphia: Saunders; 2014. 688 p.
[18] Johnston LA, O'brien SJ, Wildt DE. In vitro maturation and
fertilization of domestic cat follicular oocytes. Gamete Res.
[Internet]. 1989; 24(3):343–56. doi: https://doi.org/bhrqrg
[19] Karja N, Otoi T, Murakami M, Fahrudin M, Suzuki T. In vitro
maturation, fertilization and development of domestic cat
oocytes recovered from ovaries collected at three stages of the
reproductive cycle. Theriogenol. [Internet]. 2002; 57(9):2289–
2298. doi: https://doi.org/d2bzdr
[20] Naoi H, Agung B, Karja NW, Wongsrikeao P, Shimizu R, Taniguchi
M, Otoi T. Effects of the reproductive status on morphological
oocyte quality and developmental competence of oocytes after
in vitro fertilization and somatic cell nuclear transfer in cat.
Reprod. Domest. Anim. 2008; 43(2):157–161.
______________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIII, rcfcv-e33212
5 of 5
[21] Schmidt PM. Feline breeding management. Vet. Clin. North Am.
Small Anim. Pract. [Internet]. 1986; 16(3):435–451. doi: https://
doi.org/bj54bs
[22] Hurni H. Daylength and breeding in the domestic cat. Lab. Anim.
[Internet]. 1981; 15(3):229–233. doi: https://doi.org/b739d7
[23] Hedlund CH. Surgery of the reproductive and genital systems.
In: Fossun TW, editor. Small Animal Surgery. 2nd ed. St Louis,
USA: Mosby. 2002. 122 p.
[24] Wood T, Wildt D. Effect of the quality of the cumulus–oocyte
complex in the domestic cat on the ability of oocytes to mature,
fertilize and develop into blastocysts in vitro. J. Reprod.
[Internet]. Fert. 1997; 110:355–360. doi: https://doi.org/dhfqw8
[25] Wood T, Montali R, Wildt D. Follicle–oocyte atresia and temporal
taphonomy in cold–stored domestic cat ovaries. Mol. Reprod.
Dev. [Internet]. 1997; 46:190–200. doi: https://doi.org/cgzcs6
[26] Freistedt P, Stojkovic M, Wolf E. Ecient in vitro production
of cat embryos in modied synthetic oviduct uid medium:
effects of season and ovarian status. Biol. Reprod. [Internet].
2001; 65(1):9–13. doi: https://doi.org/fnjjwk
[27] Brevini TA, Cillo F, Antonini S, Gandol F. Effects of endocrine
disrupters on the oocytes and embryos of farm animals. Reprod.
Dom. Anim. [Internet]. 2005; 40(4):291–299. doi: https://doi.
org/d69j7p
[28] Gao Y, Chen F, Kong Qq, Ning Sf, Yuan Hj, Lian Hy, Luo Mj, Tan Jh.
Stresses on female mice impair oocyte developmental potential:
effects of stress severity and duration on oocytes at the growing
follicle stage. Reprod. Sci. [Internet]. 2016; 23(9):1148–1157. doi:
https://doi.org/kpcw
[29] Argudo DE, Tenemaza MA, Merchán Sl, Balvoa JA, Méndez MS,
Soria ME, Galarza LR, Ayala LE, Hernández–Fonseca HJ, Perea
MS, Perea FP. Intraovarian inuence of bovine corpus luteum on
oocyte morphometry and developmental competence, embryo
production and cryotolerance. Theriogenol. [Internet]. 2020;
155:232–239. doi: https://doi.org/kpcx
[30] Gonzalez–Bulnes A, Berlinguer F, Cocero MJ, Garcia–Garcia RM,
Leoni G, Naitana S, Rosati I, Succu S., Veiga–Lopez A. Induction
of the presence of corpus luteum during superovulatory
treatments enhances in vivo and in vitro blastocysts output in
sheep. Theriogenol. [Internet]. 2005; 64:1392–1403. doi: https://
doi.org/fds7zc
[31] Cotterill M, Catt Sl, Picton HM. Characterisation of the cellular
and molecular responses of ovine oocytes and their supporting
somatic cells to pre–ovulatory levels of LH and FSH during in
vitro maturation. Reprod. [Internet]. 2012; 144(2):195–207. doi:
https://doi.org/kpcz
[32] Knight PG, Satchell L, Glister C. Intra–ovarian roles of activins and
inhibins. Mol. Cell Endocrinol. [Internet]. 2012; 359(1–2):53–65.
doi: https://doi.org/fpxg4x
[33] Richani D, Gilchrist RB. The epidermal growth factor network: role
in oocyte growth, maturation and developmental competence.
Hum. Reprod. Update. [Internet]. 2018; 24(1):1–14. doi: https://
doi.org/gczkxr
[34] Webb R, Garnsworthy PC, Campbell B, Hunter MG. Intra–ovarian
regulation of follicular development and oocyte competence in
farm animals. Theriogenol. [Internet]. 2007; 68 (Suppl.1):S22–29.
doi: https://doi.org/ctd9v8
[35] Fair T, Lonergan P. The role of progesterone in oocyte acquisition
of developmental competence. Reprod. Domest. Anim. [Internet].
2012; 47(Suppl 4):142–147. doi: https://doi.org/f36jgn
[36] Menchaca A, Cuadro F, Dos Santos–Neto Pc, Bosolasco D, Barrera
N, De Brun V, Crispo M. Oocyte developmental competence
is improved by relatively greater circulating progesterone
concentrations during preovulatory follicular growth. Anim.
Reprod. Sci. 2018; 195:321–328. doi: https://doi.org/gd2hgh
[37] Manjunatha BM, Gupta PS, Ravindra JP, Devaraj M, Ramesh HS,
Nandi S. In vitro developmental competence of buffalo oocytes
collected at various stages of the estrous cycle. Theriogenol.
2007; 68(6):882–88.
[38] Rosen MP, Shen S, Dobson AT, Rinaudo PF, Mcculloch CE,
Cedars MI. A quantitative assessment of follicle size on oocyte
developmental competence. Fertil. Steril. [Internet]. 2008;
90(3):684–690. doi: https://doi.org/bns4wz
[39] Ahmadi E, Nazari H, Hossini–Fahraji H. Low developmental
competence and high tolerance to thermal stress of ovine oocytes
in the warm compared with the cold season. Trop. Anim. Health
Prod. [Internet]. 2019; 51(6):1611–1618. doi: https://doi.org/kpc2
[40] Almeida FR, Mao J, Novak S, Cosgrove JR, Foxcroft GR. Effects
of different patterns of feed restriction and insulin treatment
during the luteal phase on reproductive, metabolic, and
endocrine parameters in cyclic gilts. J. Anim. Sci. [Internet].
2001; 79(1):200–212. doi: https://doi.org/kpc3
[41] Armstrong DT. Effects of maternal age on oocyte developmental
competence. Theriogenol. [Internet]. 2001; 55(6):1303–1322.
doi: https://doi.org/btrmzc
[42] Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchee
MR, Mcconnell J. Maternal diet–induced obesity alters mitochondrial
activity and redox status in mouse oocytes and zygotes. Plos One.
[Internet]. 2010; 5(4):e10074. doi: https://doi.org/c6pqw7
[43] Magata F, Shimizu T. Effect of lipopolysaccharide on
developmental competence of oocytes. Reprod. Toxicol.
[Internet]. 2017; 71:1–7. doi: https://doi.org/gbrqb4