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Effect of season on follicular population, quality and nuclear maturation of bovine oocytes under tropical conditions ⁎

Jorge Alonso Peralta-Torresa, , Jesús Ricardo Aké-Lópezb, José Candelario Segura-Correab, Jesús Ricardo Aké-Villanuevab a

División Académica de Ciencias Agropecuarias. Universidad Juárez Autónoma de Tabasco, Carretera Villahermosa-Teapa Km. 25, R/A La Huasteca 2ª Sección, ZP 86280 Villahermosa, Tabasco, Mexico b Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Carretera Mérida-Xmatkuil Km. 15.5, ZP, 97100 Mérida, Yucatán, Mexico



Keywords: Season Follicular population Viable oocytes Metaphase II Corpus luteum Bovine

The aim was to determine the effect of season of the year and the presence of a corpus luteum (CL) on follicular population (FP) and the quality of the oocytes, and of season on nuclear maturation of the bovine oocytes under tropical conditions. Three seasons were evaluated: hot-dry (March–June), hot-humid (July–October) and fresh-humid (November–February). In a first study, 1112 bovine ovaries were obtained from a local slaughterhouse. Follicles were classified as small (≤4 mm), middle (4.1–8 mm) and large (≥8.1 mm); and the maximum diameter of the follicle (MDF) and CL (MDCL) were also recorded. The oocytes were collected by aspiration and classified as viable (grade I and II) and damaged (grade III and IV). In the second study, 2261 viable oocytes were matured in vitro, and then fixed and stained with Lacmoid to classify the stage of development as mature (metaphase II), immature or degenerate. Data were analyzed using analysis of variance and chi-square procedures. The largest FP of large follicles (0.67), MDF (1.18 mm), MDCL (1.87 mm), and the highest proportion of viable oocytes (34.19%) were obtained during the hot-humid season (P < 0.05). The ovaries without CL had the greatest FP (10.34) with more viable oocytes (24.44%). The highest proportion of mature oocytes (76.92%) was also obtained in the hot-humid season. In conclusion, season influenced FP, MDF, MDCL, and the quality and nuclear maturation of oocytes. The presence of a CL in the ovary resulted in a decrease of FP and viability of oocytes.

1. Introduction It is known that in tropical and subtropical regions, environmental conditions such as high temperature and high relative humidity are associated with a decrease in the reproductive efficiency of cattle (Al-Katanani et al., 1999). There are reports that indicate that environmental conditions during the hot season cause a reduction in the fertility of cows due to modifications in the estrous cycle and in endocrine secretions (Shehab-El-Deen et al., 2010). In addition, it causes changes in the follicular dynamic decreasing the population of small (3–5 mm) and middle (6–9 mm) follicles (Wilson et al., 1998; Wolfenson et al., 1995), influence the production of follicular steroids (Bilego et al., 2013) and cause a reduction of the diameter of the dominant follicle (Roth et al., 2001). It is known also that in cattle, the environmental temperature alters the ovulatory process (Siddiqui et al., 2010) and affects the formation and development of the next corpus luteum (Burke et al., 2001; Wolfenson et al., 1995). ⁎

Corresponding author. E-mail addresses: [email protected], [email protected] (J.A. Peralta-Torres). Received 15 March 2017; Received in revised form 12 September 2017; Accepted 4 October 2017 0378-4320/ © 2017 Published by Elsevier B.V.

Please cite this article as: Peralta-Torres, J.A., Animal Reproduction Science (2017),

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Furthermore, high temperatures and humidity may influence the quality of oocytes causing premature aging (Andreu-Vázquez et al., 2010; Roth and Hansen, 2004; Roth, 2008), abnormal nuclear maturation (Maya-Soriano et al., 2013), effects on survivability, growth and development of the embryos in vivo or in vitro (Eberhardt et al., 2009; Putney et al., 1989; Silva et al., 2006). Therefore, the micro-environment of oocytes development is a cue for the success of in vitro maturation and posterior development of embryos (Rizos et al., 2002; Sutton et al., 2003). Nutrition is another important factor for cattle kept under tropical conditions. Animals in the tropics are fed mainly in pasture, which quality and availability depends on the season of the year, characterized by variations in rainfall and temperature. Therefore, determining the effects of season on reproductive performance of cows is very relevant task. The aim of this study was to determine the effect of season of the year and the presence of a corpus luteum on follicular population and the quality of oocytes, and of season on nuclear maturation of bovine oocytes under tropical conditions. 2. Materials and methods All chemicals were purchased from Sigma Chemical Company (Sigma-Aldrich Corp., St. Louis, MO, USA), unless otherwise indicated. 2.1. Localization and study periods Two studies were conducted, from April 2015 to January 2016 (first study) and from December 2015 to September 2016 (second study), in the laboratory of Animal Reproduction of the “Facultad de Medicina Veterinaria y Zootecnia de la Universidad Autónoma de Yucatán (FMVZ-UADY)”, located in Merida, Yucatan, Mexico (20° 58′ 04′′ N and 89° 37′ 18′′ W). The FMVZ-UADY is 10 m above sea level and has a hot-sub humid climate with rain in summer, and average temperature and rainfall of 26.1 °C and 1022 mm, respectively (INEGI, 2015). Based on climatological records (temperature and relative humidity) of the last 15 years in Yucatán, three seasons were established: hot-dry (March–June), hot-humid (July–October) and fresh-humid (November–February). Climatological information during the periods of study is shown in Table 1. The ambient temperature (T, °C) and relative humidity (RH, %) were used to calculate the temperature humidity index (THI) based on Mader et al. (2006) formula:

THI = (0.8xT) + [(RH/100)x(T−14.4) + 46.4] 2.2. First study: follicle population and quality of oocytes 2.2.1. Ovaries collection One thousand one-hundred and twelve ovaries from Bos indicus and F1 (Bos indicus × Bos taurus) cows (364 in the hot-dry, 374 in the hot-humid and 374 in the fresh-humid seasons), were collected from a slaughterhouse in Mérida, Yucatán, México. Ovaries were transported in a thermo with 0.9% NaCl containing 70 μg mL−1 kanamycin at 37 °C. The period between the collection of the ovaries and their transport to the laboratory did not exceed 2 h. Once in the laboratory, ovaries were washed with a saline solution with kanamycin at 37 °C. 2.2.2. Follicle and corpus luteum diameters According to Bó et al. (2003), follicles were counted (FP), measured and classified as small (≤4 mm), middle (4.1–8 mm) and large (≥8.1 mm) using a real time ultrasound (Mindray-DP-50Vet, USA), equipped with a 5 MHz probe. In addition, the maximum diameter of the follicle (MDF) and maximum diameter of the corpus luteum (MDCL) were obtained. 2.2.3. Collection and selection of oocytes Oocytes were collected by puncture and aspiration of antral follicles (≥3 mm), using a 10 ml syringe (Air tite) with an 18 g needle. The extracted follicular liquid was collected in Falcon tubes of 50 ml, and let it sediment during 15 min at 37 °C. Later, the supernatant was removed and the sediment with oocytes and follicular cells was re-suspended in 10 ml of a modified Dulbecco's phosphate buffered saline solution (PBS), at 37 °C. The tube content was deposited in a Petri dish (90 × 14 mm) to next classify the Table 1 Mean of ambient temperature, relative humidity, rainfall and temperature humidity index (THI) during periods of study (CONAGUA, 2015, 2016). Season a

Hot-dry (April–May 2015) Hot-humid (Aug–Sept 2015)a Fresh-humid (Dec 2015–Jan 2016)a,b Hot-dry (April–May 2016)b Hot-humid (Aug–Sept 2016)b a b

Temperature (°C)

Relative humidity (%)

Rainfall (mm)


30.1 28.7 25.0 30.0 28.7

68.0 86.0 91.0 81.5 89.5

10.6 342.0 26.5 45.8 221.6

81.1 81.6 76.0 83.1 82.1

Seasons of the first study. Seasons of the second study.


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oocytes with the help of a stereomicroscope equipped with a thermal plate at 38.5 °C. Quality of the oocytes was evaluated according to cumulus-oocyte complexes as described by Walters et al. (2002). Grade I: were compact oocytes with three or more layers of cumulus-oocyte cells and a homogeneous cytoplasm. Grade II: were compact oocytes with two cumulus-oocyte cells and a less homogeneous cytoplasm than grade I. Grade III: were irregular oocytes with few cumulusoocyte cells and dark agglomerations in the cytoplasm. Grade IV: were oocytes without cumulus-oocyte cells and evident dark cytoplasm agglomerations. According to Penitente-Filho et al. (2015), oocytes were further classified as viable (Grade I and II) and damaged (Grade III and IV). 2.3. Second study: nuclear maturation of oocytes 2.3.1. Oocyte collection Two thousand and two-hundred and sixty-one oocytes (754 in the fresh-humid, 753 in the hot-dry and 754 in the hot-humid seasons) obtained from the ovaries of Bos indicus and F1 (Bos indicus × Bos taurus) cows at a local slaughterhouse were used. Aspiration of follicles, collection, transport, management, and classification of oocytes was as described previously. 2.3.2. In vitro maturation The maturation medium consisted of TCM-199 (Gibco-BRL, NY, USA) supplemented with 10% (v/v) fetal calf serum, 0.2 mM sodium pyruvate, 25 μM sodium bicarbonate, 1.0 μg/ml estradiol, 0.5 μg/ml eCG (Folligon, Intervet, Holland) and 100 UI/ml hCG (Chorulon, Intervet, Holland). Viable oocytes (Grade I and II) were used, which were washed three times in a maturation medium. Afterwards, droplets of 100 μl (25–30 oocytes per droplet) of the same medium were covered with mineral oil and incubated during 24 h at 38.5 °C, in a 5% CO2 and humidity saturated atmosphere. 2.3.3. Assessment of oocyte nuclear maturation At the end of the maturation process, oocytes were denuded in 0.1% hyaluronidase in a maturation medium during 2 min using a vortex at 1660 rpm. Then oocytes were washed in PBS and placed in micro drops of the same medium in a slide (1 oocyte/micro drop: 10 oocytes per slide) in which previously two parallel lines of vaseline were placed and were covered with a coverslip pressing until get contact with the micro drops. The oocytes were fixed in a solution of acetic acid:ethanol (1:3, v/v) per 48–72 h at ambient temperature (24–26 °C). Past the time of oocytes fixation, they were stained with 1% Lacmoid in 45% (v:v) acetic acid. Afterwards, oocytes were assessed under a microscope of contrast phase at 400X and classified as suggested by Brisard et al. (2014). Mature. Oocytes with chromosomes in metaphase II and extrusion of polar body. Immature. Oocytes in the germinal vesicle or germinal vesicle breakdown stage. Degenerate. Oocytes with vacuolar or fragmented cytoplasm, disperse chromatin and marked enlargement of the perivitelline space. 2.4. Statistical analysis Data on FP, MDF, MDCL were analyzed using analysis of variance. The model for FP and MDF included the fixed effects of season of the year, presence or not of a corpus luteum (CL) and their interaction; whereas the model for MDCL only included the effect of season. Chi-squares tests were used to determine the effect of season or the presence of a CL on the quality, viability and maturation of oocytes. All analyses were carried out using the SAS package (SAS, 2009). 3. Results 3.1. First study: follicle population and quality of oocytes The season of the year and the presence of a CL in the ovary had significant effects (P < 0.05) on FP (Table 2). Total FP was greatest in the fresh-humid season (10.45); however, more follicles of large size were obtained in the hot-humid season (Table 2). With respect to the presence or not of a CL, more follicles of all sizes were observed in the ovaries without a CL (Table 2). In addition, no season x CL interaction was found (P < 0.05). The ovaries in the hot-humid season presented larger MDF (1.18 ± 0.02 mm; n = 196) than those evaluated in the hot-dry (1.12 ± 0.02 mm; n = 171) and fresh-humid (1.10 ± 0.02 mm; n = 175) seasons (P < 0.05). The greatest MDCL mean was also observed in the hot-humid season (1.87 ± 0.03 mm; n = 160) in comparison to the hot-dry (1.55 ± 0.03 mm; n=181) and freshhumid (1.69 ± 0.03 mm; n = 161) seasons (P < 0.05). Ovaries with or without CL had similar MDF (1.15 and 1.12 mm, respectively). The greatest proportion of grade I oocytes was found in the hot-humid season (11.39%; P < 0.05), and in the ovaries without a CL (8.10%; P < 0.05) (Table 3). With respect to the viability of the oocytes, the greatest proportion of viable oocytes (Grade I and II) was observed in the hot-humid season (34.19%; P < 0.05) and in the ovaries without a CL (24.44%; P < 0.05) (Fig. 1). 3

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Table 2 Least square means ( ± SE) by season of the year and the presence or not of a corpus luteum for the follicular population (size and total) per ovary. Factor

Season Hot-dry Hot-humid Fresh-humid Corpus luteum Without With abc

Follicular population Small




6.81 ± 0.20a 7.25 ± 0.20a 8.10 ± 0.20b

1.49 ± 0.08a 1.77 ± 0.08b 1.82 ± 0.08b

0.50 ± 0.03a 0.67 ± 0.03b 0.53 ± 0.03a

8.80 ± 0.21a 9.68 ± 0.20b 10.45 ± 0.21c

7.80 ± 0.16a 6.97 ± 0.17b

1.87 ± 0.06a 1.51 ± 0.07b

0.66 ± 0.03a 0.47 ± 0.03b

10.34 ± 0.16a 8.95 ± 0.18b

Different literals between categories of a factor, mean significant differences (P < 0.05).

Table 3 Proportion (%) by season of the year and the presence or not of a corpus luteum for bovine oocytes of different quality. Factor/Grade

Season Hot-dry Hot-humid Fresh-humid Corpus luteum Without With

Oocytes quality (n=9542) I




9.33a (230)* 11.39b (376) 2.28c (86)

21.23a (523) 22.80a (753) 7.23b (273)

33.97a (837) 24.71b (816) 17.00c (642)

35.47a (874) 41.10b (1357) 73.49c (2775)

8.10a (430) 6.19b (262)

16.34a (867) 16.10a (682)

23.63a (1254) 24.58a (1041)

51.93a (2756) 53.13a (2250)


Different literals between categories of a factor, means significant differences (P < 0.05). * Values within parenthesis refer to the number of oocytes.

Fig. 1. Proportion of viable oocytes (grade I and II) in different season of the year and for ovaries with and without a corpus luteum. abc Bars with different literals were significant (P < 0.05).

3.2. Second study: Nuclear maturation of oocytes The major proportion of mature oocytes (76.92%) and in consequence the minor proportions of immature and degenerated oocytes (19.10 and 3.98%, respectively) were found in the hot-humid season, as compared with the other two seasons (Table 4).


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Table 4 Proportion (%) of nuclear maturation of the oocytes in different season of the year. Season

Stage of oocyte (n = 2261) Mature

Hot-dry Hot-humid Fresh-humid


52.19 (393) 76.92b (580) 39.12c (295)

Immature *


31.21 (235) 19.10b (144) 38.46c (290)

Degenerate 16.60a (125) 3.98b (30) 22.41c (169)


Different literals between categories of a factor, means significant differences (P < 0.05). * Values in the parenthesis refer to the number of oocytes.

4. Discussion The greater FP obtained during the fresh-humid season agrees with the results of Zeron et al. (2001), who working with Holstein cows, found that the highest FP was obtained during winter (19.6 follicles per ovary) versus the summer season (12 follicles per ovary). Badinga et al. (1993) reported that high temperatures compromise the follicular dynamic, which support the results of this study (Table 2). Furthermore, the observed performance of large follicles agrees with the results of Peralta-Torres et al. (2017) who found in Brahman y F1 (Simmental × Brahman) heifers that the greatest FP of large follicles (≥8.1 mm) corresponded to the hothumid season. The increase in FP during the hot-humid season could be due to an increase in the availability and quality of pasture associated with more rainfall in that season, which could have improved the body condition score (BCS) of cows. In this regard, there are reports, which indicate that better nutrition improves BCS and increases the number and diameter of follicles (Diskin et al., 2003; Domínguez, 1995). The greatest FP in the ovaries without a CL, agrees with the results of Contreras-Solis et al. (2008), who working with ewes reported greater mean of follicles ≥ 2 mm (3.3 ± 0.1 vs 2.5 ± 0.1) and > 4.5 mm (2.7 ± 0.3 vs 0.9 ± 0.5) in the ovaries without a CL. Shabankareh et al. (2010) also in ewes reported a greater FP in the ovaries without a CL. The greatest FP in ovaries without a CL can be explained by the own function of the CL, which in addition to secrete progesterone, produce also inhibin, which together affect the growth of follicles during the luteal phase (Fukuda et al., 1997). In addition, Acosta and Miyamoto (2004) indicated that the follicles of ovaries without a CL have more gonadotrophins, and other biochemical and hormonal factors needed for the follicular development. The largest MDF mean found in the hot-humid season, agrees with the results of Satheshkumar et al. (2015), who reported, in crossbred Jersey cows, that the largest diameter of follicles (12.8 mm) was observed in the hot season (April-June), in comparison to the cool season (December-February; 11.2 mm). On the other hand, the largest MDCL was also found in the hot-humid season, result that disagree from those of Howell et al. (1994), who observed that in Holstein cows, the size of the CL was greater in spring than in summer (384.1 vs 327.9 mm2). In this study, it was found that both MDF and MDCL means were observed in the hot-humid season; therefore, it could be speculated a possible association between the size of the follicle and the size of the CL. Vasconcelos et al. (2001) reported a relationship between the follicles with large diameter (≥15 mm) and large CL, in the day 14 of the estrous cycle (7.10 vs 5.89 mm3). The largest proportion of oocytes grade I and II in the hot-humid season (Table 3, Fig. 1) differ from the results by Alves et al. (2014), who, in Girolando cows, did not find influence of season on oocytes of grade I (4.3 vs 6.8%) and II (11.4 vs 10.1%). However, the proportion of viable oocytes (Grades I and II), in our study, agree with the results of Chrenek et al. (2015), who reported, in Holstein cows, more viable oocytes in summer (63.26%) than in fall (50.07%) and spring (49.45%). The increase in viable oocytes during the hot-humid season could be due to the fact that in that season were found the largest FP of large (≥8.1 mm) follicles, which are associated to a better oocyte quality (Machatkova et al., 2004). The highest proportion of viable oocytes observed in the ovaries without a CL differ from the results of Penitente-Filho et al. (2015), who did not find differences in the quality of the oocytes obtained from ovaries with or without a CL (33.7 vs 29.0%). Hajarian et al. (2016) reported that the quality of the oocytes is better when there is not a CL, and they observed that a greater proportion of oocytes reached the blastocyst phase, as compared to oocytes from ovaries without a CL (43.0 vs 22.5%; P < 0.05). The major proportion of viable oocytes obtained from the ovaries without a CL, probably was due to a better follicular environment as result of a greater concentration of gonadotrophins and other biochemical factors, due to the lack of progesterone and inhibin secreted by the CL (Fukuda et al., 1997; Shabankareh et al., 2015). On the other hand, with respect to nuclear maturation, in this study, the greatest proportion of mature oocytes occurred during the hot-humid season. A similar result was found by Chrenek et al. (2015), who reported that the major proportion of mature oocytes was observed during summer (85.00%; P < 0.05) as compared to fall and spring (73.42 y 80.55%, respectively). The results of our study; however, disagree with those of Pavani et al. (2015), who reported that in Holstein cows, the major proportion of mature oocytes was observed in the cool season as compared to the hot season (78.4 vs 44.3%; P < 0.05). The increase in the proportion of mature oocytes during the hot-humid season could be due to various factors; it is probable that a relationship exists with follicular growth observed in the same season of this study, where the major population of large follicles, MFD and oocytes of better quality were obtained. Furthermore, it is possible that the large photoperiod of the hot-humid season may have induce a greater secretion of IGF-1, which resulted in a better quality and better developmental competence of the oocytes (Dahl et al., 2000; Machatkova et al., 2004). 5

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Finally, probably the type of cow used (Bos indicus and F1) could have influenced the better response obtained in the season of greatest THI (hot-humid), due to the fact that those breed groups are better adapted to the high temperatures and high humidity characteristics of the region (Hansen, 2004). In conclusion, under the conditions of the present study, it was observed an important effect of the season of year on the reproductive activity of cows. More follicles of large size, MDF, MDCL, viable and mature oocytes were found in the hot-humid season. Ovaries without a CL had more follicles and more viable oocytes. Conflict of interest The authors declare no conflict of interest. Acknowledgements Programa para el desarrollo profesional docente (PRODEP) is acknowledged for providing the PhD scholarship for the first author. References Acosta, T.J., Miyamoto, A., 2004. Vascular control of ovarian function: ovulation, corpus luteum formation and regression. Anim. Reprod. 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Effect of season on follicular population, quality and nuclear maturation of bovine oocytes under tropical conditions.

The aim was to determine the effect of season of the year and the presence of a corpus luteum (CL) on follicular population (FP) and the quality of th...
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