Associations of antral follicle count with fertility in cattle: A review

K.J. Alward,* R.R. Cockrum, and A.D. Ealy

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Graphical Abstract

Summary: Ultrasonic determination of antral follicle count (AFC) is used to classify animals into high or low AFC categories. These categories have a wide range and animals classified as low on one study may be considered high by another study based on the population. Associations with high AFC cows include greater follicular vasculature, blastocyst rates, hatched blastocyst rates, 12-d embryonic cell growth and cleavage rates, along with a lower number of embryonic apoptotic cells. More high AFC cows cycled as heifers at 15 months, had a greater pregnancy rate and conception rate and progesterone concentration after breeding, and fewer days to conception. However, other studies have found that low AFC animals had greater pregnancy and conception rates and progesterone concentration after breeding compared with high AFC cows. Low AFC cows also showed greater preovulatory follicle blood flow, greater blastocyst cell number, and greater area of the corpus luteum.

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Highlights

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  Antral follicle count is highly correlated with superovulatory response in cattle.

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  Antral follicle count is more heritable than any other reproductive traits thus far identified.

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  There is a positive relationship between AFC and embryo production.

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  Antral follicle count is related to pregnancy and conception rates, but data are conflicting.

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Abstract

Ovarian antral follicle count (AFC) is a marker of ovarian stimulatory response to superovulation protocols in cattle. This article reviews novel research from the past 10 years, focusing on the relationship between AFC and embryo production and cow fertility. Substantial evidence indicates a positive relationship between AFC with embryo production; however, conflicting findings exist regarding the relationship of AFC with conception and pregnancy rates. This lack of consistent association with pregnancy outcomes is perplexing given the differences detected in oocytes, embryos, and endometria from high- versus low-AFC animals. Those differences include markers of embryonic viability such as protein level, blastocyst development rates, cleavage rates, and blastocyst cell numbers that differ between high- and low-AFC groups, as well as differential gene expression at the cow and embryo level with genes associated with fertility. In addition, Bos indicus and Bos taurus cattle appear to have different fertility responses based on their AFC category. In summary, clearly more studies are needed to elucidate the true associations between AFC and cow fertility, but the data that have been accumulated thus far indicate that AFC has the potential to be a useful marker of lifetime cow fertility.

Subfertility is the number-one reason for culling on US dairy operations (USDA/NAHMS, 2018). Regardless of herd size or region of the US, approximately 25% of a dairy farm's cull cows are due to reproductive problems. It is very interesting to consider that this culling rate is so high even though our definition of “normal” fertility has changed from 50 years ago to today. For example, first-service conception rate is reduced from 55% (Casida, 1961) to an average of 30 to 40% (Norman et al., 2020). More recently, days to first breeding after calving has increased by 3.5 d, and the calving interval has increased by 2.5 d since 2010 (Norman et al., 2020). This can be partially attributed to increased selection for high-producing animals without co-selection for fertility traits (Windig et al., 2006). High-producing dairy cows pose management challenges that compromise fertility. One example of this is the rapid breakdown of steroid hormones (namely estradiol and progesterone) that occurs within the liver of high-producing dairy cows due to increased blood flow through the gastrointestinal tract to digest feedstuffs (Sangsritavong et al., 2002; Wiltbank et al., 2006). This causes decreased duration and intensity of estrus and reduced GnRH and LH surges at ovulation, which can lead to larger, older follicles at ovulation (Lopez et al., 2004). Lowering circulating progesterone limits uterine support for embryo and conceptus development (Gábor et al., 2016) and alters follicular recruitment in ways that promote follicle persistence and increase the incidence of multiple dominant follicle ovulations and twinning (Lopez et al., 2005). The economic consequences of poor fertility are substantial. A decrease in conception rate from 40 to 50% to 30 to 40% has an estimated value of $42 per cow per year (Krpálková et al., 2020). On the average 300-cow farm in the US, this amounts to just over $12,600 in losses. The fertility parameters of today's dairy farms demonstrate a clear need for new technologies and tools to overcome these obstacles and improve reproductive efficiency. This mini-review will explore the potential use of antral follicle count (AFC) as an indicator of lifelong fertility in dairy cattle.

Antral follicle count, or antral follicle population, refers to the total number of antral follicles present on the ovaries at any one time. This parameter is determined via transrectal or intravaginal ultrasonography by counting all follicles 2 to 3mm in diameter or greater on both ovaries (Burns et al., 2005; Gobikrushanth et al., 2017). Although variations in AFC exist based on the day of the estrous cycle (Ireland et al., 2008), age (Burns et al., 2005), body condition (de Moraes et al., 2019), and other parameters such as dam nutritional status (Cushman et al., 2013), the repeatability of this measurement is surprisingly high, generally ranging from 0.8 to 0.9 (Burns et al., 2005). Substantial variation in AFC occurs between animals (e.g., range from 11 to 54 follicles in one study; Burns et al., 2005), but this high repeatability permits use of AFC as a reliable indicator of an animal's follicular reserve, or entire antral follicle population present. The best use of AFC in cattle is as a predictor of an animal's superovulatory response. Animals with greater AFC produce more embryos in response to a superovulation protocol compared with low-AFC animals (Center et al., 2018). In addition, Walsh and colleagues (2014) found AFC to be moderately heritable, with heritability estimates averaging 0.31 ± 0.14 in lactating dairy cows and 0.25 ± 0.13 in dairy heifers. The heritability of Nelore cows, a Bos indicus beef breed, are roughly similar to that of dairy cattle, with an estimated heritability of 0.30 ± 0.09 (Grigoletto et al., 2020). These outcomes are significant, because many other female fertility indicators contain heritabilities <5% (Cammack et al., 2009).

The correlation of AFC with superovulatory response in cattle has prompted work focusing on the discovery of relationships between AFC and the health and competency of the oocyte and with the ability of the embryo to generate and maintain a pregnancy. This article reviews novel research from the past 10 years, focusing on the relationship between AFC and oocyte and embryo production and cow fertility. Applicability of these findings to identify high-fertility animals and managing cows for improved conception and pregnancy rates, embryo quality, and in vitro embryo production will be examined.

The benefits of high AFC on embryo production can be observed by collecting oocytes and completing in vitro embryo production. A study evaluating ovaries obtained from dairy cows with high (>10 follicles) versus low AFC (<10 follicles) observed greater blastocyst development and hatched blastocyst development rates along with lower apoptotic cell numbers in the high-AFC group than in the low-AFC group (Tessaro et al., 2011). Another study in Holstein cows detected increases in ova viability and granulosa cell numbers in ovaries from high- (>25 follicles) versus low-AFC animals (<25 follicles; Nagai et al., 2016). In addition, there was a greater proportion of matured oocytes in the high-AFC group, and those oocytes had greater mitochondrial activity before maturation began. Cleavage rate and blastocyst development rate were also greater in the high-AFC group (Nagai et al., 2016). Another study using 143 Senepol cows found that high-AFC animals (>36 follicles) had a greater numbers of viable oocytes, average number of embryos, and cleaved embryos compared with either mid-AFC (23–26 follicles) or low-AFC cows (<22 follicles; Fagundes Faria et al., 2021). An additional study found that high-AFC (>25 follicles) Nelore cows had increased blastocyst development rates on d 7 compared with low-AFC (<15 follicles) blastocyst rates (Garcia et al., 2020). Although one study found no differences in blastocyst and cleavage development rates from high (>91) or low (<30) cattle in 1,143 oocytes from Nelore cows, yet another study of 66 Nelore cows found that blastocyst and cleavage rates were greatest in high-AFC animals (>39 follicles) compared with intermediate (18–25 follicles) or low-AFC cows (<8 follicles). Collectively, this indicates that more oocytes can be recovered from high-AFC animals, and those oocytes have greater developmental competency to advance to blastocyst stages. These findings are summarized in Figure 1.

Figure 1

Differences in blastocyst and cleavage development rate by antral follicle count classification for each study summarized in this review. Author and year of study, as well as species and heifer versus cow used in study, are indicated above each graph. Different lowercase letters (a–e) indicate significant differences. P-values and numbers of oocytes used are provided. Error bars indicate SE.

There are several reasons for improvements in embryo production in high-AFC cattle. One may be attributed to blood flow rates in developing follicles. Tessaro and colleagues observed increases in both endothelial nitric oxide synthase protein content, a potent vasodilator, and increases in follicular vasculature in follicles from high-AFC dairy cows (Tessaro et al., 2011). However, another study found conflicting results, with reduced blood flow to the pre-ovulatory follicle noted in high-AFC Holstein cows (Bonato et al., 2022). The reasons for this disparity remain unresolved. Another possible reason why high-AFC cattle produce higher-quality embryos is because of changes in lipid content. Nelore cows with high AFC had greater concentrations of triglyceride and lower cholesterol and diacylglycerol concentrations in their embryos compared with embryos from low-AFC cattle (Rosa et al., 2021). Elevated triglyceride and reduced diacylglycerol concentrations are prominent in grade 1 bovine embryos (Janati Idrissi et al., 2021). This phenomenon probably occurs because either oocytes from high-AFC cows contained this preferred lipid composition before they were collected and fertilized, or embryos generated from these oocytes are better able to produce this lipid profile. It is interesting, however, that no differences in cleavage and blastocyst development rates were observed in this study. Thus, further research is needed to determine why embryos from high- versus low-AFC animals perform differently.

Based on available evidence, it appears that high AFC improves embryo production efficiency by some means that likely involves control over follicle vascularization or improving oocyte quality, or both. It is strange, however, that no clear connection has been found between AFC and pregnancy per AI. Several studies found inverse relationship between AFC and fertility. Morotti and colleagues collected data from 834 Nelore cows and found that those with a lower AFC (<15 follicles) had greater pregnancy per AI than cows with either intermediate (20–40 follicles) or high AFC (>45 follicles) after breeding to a timed AI (TAI) protocol (Morotti et al., 2018). Another study in Nelore cows had similar results when cows were classed as low (<10 follicles), intermediate (11–29 follicles), or high AFC (>30 follicles). After TAI, low-AFC animals had the highest pregnancy per AI compared with intermediate or high-AFC cows (de Moraes et al., 2019). They also found an interaction of body condition score with AFC and pregnancy per AI, with pregnancy per AI decreasing significantly in cows with a high AFC and high BCS. A third study in Nelore cows also evaluated pregnancy per AI post-TAI in cows with very low AFC (<16 follicles), low AFC (16–30 follicles), intermediate (31–44 follicles), and high AFC (>46 follicles). Cows with very low, low, and intermediate AFC had increased pregnancy per AI compared with the high-AFC cows (de Lima et al., 2020). Other studies in Bos indicus breeds found no differences in pregnancy per AI by AFC classification (dos Santos et al., 2016; Fagundes Faria et al., 2021). It is interesting, however, that evidence suggests that embryos from high-AFC cattle may still be more competent to establish a pregnancy than those from low-AFC cattle, evidenced by one study that identified a positive association between AFC and pregnancy per AI following embryo transfer in Nelore cows (Garcia et al., 2020). Therefore, it appears that embryo competency is not an issue with the lower fertility observed in high-AFC Bos indicus cattle. More work is needed to define the mechanisms at play.

Data in Bos taurus breeds is also conflicting regarding the relationship between AFC and fertility. When high-producing Holsteins were classed as high (>24 follicles) or low AFC (<14 follicles), the low-AFC cows had greater blood flow to the preovulatory follicle, greater corpus luteum area, and greater progesterone levels (Bonato et al., 2022). This would indicate healthier or more robust follicles and corpora lutea in the low-AFC animals. However, a second study on Holsteins showed that high-AFC animals (≥15 follicles) had a shorter interval from calving to conception, greater pregnancy per AI to first AI and overall, as well as greater progesterone concentration during diestrus compared with low-AFC animals (<15 follicles; Martinez et al., 2016). These factors indicate greater fertility in the high-AFC animals. Clearly, additional studies are needed to interpret the relationship between AFC and fertility. Figure 2 summarizes the data regarding pregnancy per AI by AFC group.

Figure 2

Differences in pregnancy per AI by antral follicle count classification for each study summarized in this review. Author, year of study, species, and heifer versus cow used in study are indicated above each graph. Different lowercase letters (a, b) indicate significant differences. P-values and numbers of animals used are provided.

An additional set of factors that have not yet been accounted for in the previously described studies are those that have a genetic linkage. One study evaluated 944 Nelore cattle and identified several candidate genes responsible for the variation in phenotypic AFC with roles in follicular development, steroidogenesis, and ovulation (Grigoletto et al., 2020). At least 5 additional genes linked to expression of reproductive traits were also found to be related to AFC. A second study on 257 Angus cows evaluated AFC and associated SNPs and identified genes involved with protein encoding, regulation of primordial germ cells, and cellular maintenance, as well as those linked with body weight and height in cattle as different by AFC group (Oliveira Júnior et al., 2021). These studies indicate that several downstream genes and processes are linked with a cow's AFC.

Gene expression also varies at the oocyte and embryonic level, potentially contributing to the differences seen in embryo production. de Lima and colleagues identified the top and bottom 20% by AFC of 50 Nelore cows and performed ovum pick-up for genetic sequencing. They found 11 genes differentially expressed in oocytes from high- and low-AFC animals. In the low-AFC group, upregulated genes included those involved in intercellular communication, meiotic control, epigenetic modification, and follicular growth, with one gene associated with cell stress and apoptosis downregulated (de Lima et al., 2020). This indicates that oocytes and cumulus cells from high- and low-AFC animals experience different epigenetic, cell growth, and cellular processes, and low-AFC oocytes may display increased competency (de Lima et al., 2020). A second study in Nelore cows found conflicting gene expression patterns in oocytes from low- (<31 follicles) or high-AFC (>92) animals. Low-AFC oocytes had higher expression of some genes involved in meiosis resumption, cumulus cell expansion, and transcription factor for regulating oocyte maturation and cell proliferation, but lower expression of other genes that are also involved in meiosis resumption and cumulus cell expansion (Rosa et al., 2018). This conflicting data shows less discernable difference in developmental competency between high- and low-AFC oocytes and contradicts the previously outlined results showing higher viability via greater blastocyst and cleavage rates in high-AFC oocytes.

The conflicting data between Bos taurus and Bos indicus breeds regarding the relationship of AFC and both oocyte competency and pregnancy per AI indicates factors other than the animals' AFC must differ and contribute to differences in fertility. A portion of these differences can be explained genetically, as outlined above. However, it is also important to note that inherent differences in physiology exist between Bos taurus and Bos indicus breeds. Bos indicus animals ovulate a smaller follicle and develop a smaller corpus luteum (Sartori et al., 2016). Despite this, Bos indicus have greater circulating concentrations of estradiol and progesterone than Bos taurus breeds (Sartori et al., 2016). These differences in physiology and cyclicity parameters have resulted in tailored TAI programs that are specific for each species (Sartori et al., 2001; Gimenes et al., 2008). Therefore, differences in species and AI protocol may be a factor. Bos indicus also average a substantially greater AFC than Bos taurus animals (Bastos et al., 2010). This may indicate that the high-AFC Bos indicus animals and low-AFC Bos taurus animals represent the extremes in AFC range and that, rather than high or low being ideal, the intermediary group (low-AFC Bos indicus and high-AFC Bos taurus) may be the most fertile. However, these theories need to be investigated to determine their contribution toward the differences seen in fertility by AFC category.

In summary, AFC is correlated with a cow's superovulation response. The AFC is also moderately heritable, and this level of heritability provides much better selection opportunities than most other reproductive traits. Good evidence suggests that AFC is positively correlated with embryo production efficiency. However, conflicting findings exist when applying these findings to fertility status, and more evidence actually suggests that high-AFC cattle are less fertile than intermediate and low-AFC cattle. Gene expression in high- versus low-AFC animals at the cow level find that numerous downstream processes related to reproduction are differentially expressed. At the embryonic level, embryos from high- versus low-AFC animals also exhibit differential gene expression; however, these mostly indicate greater fertility and health in low-AFC oocytes and embryos. One factor that has not been standardized across studies is the threshold for “high” AFC. Some studies show that extreme AFC animals, both high and low, have reduced fertility compared with the median groups (Gobikrushanth et al., 2017; Akbarinejad et al., 2020). Therefore, studies that classify their high-AFC groups more broadly may be capturing the mid group and the extreme high group, negating any differences between them. In addition, breed differences may exist. Differences certainly exist between bovid subspecies, with Bos indicus and Bos taurus breeds exhibiting different fertility responses by AFC category. More studies are required to confirm these theories and elucidate the true associations between AFC and embryo production and fertility. Collectively, these data indicate a relationship between AFC and measures of cow fertility and the potential to use AFC as a genetic selection and management tool to improve reproductive efficiency on dairy farms.

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Notes

Funding for this work was provided by Agriculture and Food Research Initiative Competitive Grant numbers 2017-67015-2646 and 2021-67015-34485 from the USDA National Institute of Food and Agriculture (Washington, DC).

No human or animal subjects were used, so this analysis did not require approval by an Institutional Animal Care and Use Committee or Institutional Review Board.

The authors have not stated any conflicts of interest.

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References

• Akbarinejad V., Gharagozlou F., Vojgani M., Ranji A. Evidence for quadratic association between serum anti-Müllerian hormone (AMH) concentration and fertility in dairy cows. Anim. Reprod. Sci. 2020;218 doi: 10.1016/j.anireprosci.2020.106457. 32507251. [PubMed] [CrossRef] [Google Scholar]

• Bastos M.R., Mattos M.C.C., Meschiatti M.A.P., Surjus R.S., Guardieiro M.M., Ferreira J.C.P., Mourão G.B., Pires A.V., Biehl M.V., Pedroso A.M., Santos F.A.P., Sartori R. Ovarian function and circulating hormones in nonlactating Nelore versus Holstein cows. Acta Sci. Vet. 2010;38:776. [Google Scholar]

• Bonato D.V., Ferreira E.B., Gomes D.N., Bonato F.G.C., Droher R.G., Morotti F., Seneda M.M. Follicular dynamics, luteal characteristics, and progesterone concentrations in synchronized lactating Holstein cows with high and low antral follicle counts. Theriogenology. 2022;179:223–229. doi: 10.1016/j.theriogenology.2021.12.006. 34896744. [PubMed] [CrossRef] [Google Scholar]

• Burns D.S., Jimenez-Krassel F., Ireland J.L.H., Knight P.G., Ireland J.J. Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle-stimulating hormone concentrations. Biol. Reprod. 2005;73:54–62. doi: 10.1095/biolreprod.104.036277. 15744026. [PubMed] [CrossRef] [Google Scholar]

• Cammack K.M., Thomas M.G., Enns R.M. Reproductive traits and their heritabilities in beef cattle. Prof. Anim. Sci. 2009;25:517–528. doi: 10.15232/S1080-7446(15)30753-1. [CrossRef] [Google Scholar]

• Casida L.E. Present status of the repeat breeder cow problem. J. Dairy Sci. 1961;44:2323–2329. doi: 10.3168/jds.S0022-0302(61)90063-7. [CrossRef] [Google Scholar]

• Center K., Dixon D., Looney C., Rorie R. Anti-Mullerian hormone and follicle counts as predictors of superovulatory response and embryo production in beef cattle. Adv. Reprod. Sci. 2018;6:22–33. doi: 10.4236/arsci.2018.61003. [CrossRef] [Google Scholar]

• Cushman R.A., McNeel A.K., Freetly H.C. The impact of cow nutrient status during the second and third trimesters on age at puberty, antral follicle count, and fertility of daughters. Livest. Sci. 2014;162:252–258. doi: 10.1016/j.livsci.2014.01.033. [CrossRef] [Google Scholar]

• de Lima M.A., Morotti F., Bayeux B.M., de Rezende R.G., Botigelli R.C., De Bem T.H.C., Fontes P.K., Nogueira M.F.G., Meirelles F.V., Baruselli P.S., da Silveira J.C., Perecin F., Seneda M.M. Ovarian follicular dynamics, progesterone concentrations, pregnancy rates and transcriptional patterns in Bos indicus females with a high or low antral follicle count. Sci. Rep. 2020;10 doi: 10.1038/s41598-020-76601-5. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

• de Moraes F.L.Z., Morotti F., Costa C.B., Lunardelli P.A., Seneda M.M. Relationships between antral follicle count, body condition, and pregnancy rates after timed-AI in Bos indicus cattle. Theriogenology. 2019;136:10–14. doi: 10.1016/j.theriogenology.2019.06.024. [PubMed] [CrossRef] [Google Scholar]

• dos Santos G.M.G., Silva-Santos K.C., Barreiros T.R.R., Morotti F., Sanches B.V., de Moraes F.L.Z., Blaschi W., Seneda M.M. High numbers of antral follicles are positively associated with in vitro embryo production but not the conception rate for FTAI in Nelore cattle. Animal Reprod. Sci. 2016;165:17–21. doi: 10.1016/j.anireprosci.2015.11.024. [PubMed] [CrossRef] [Google Scholar]

• Fagundes Faria A.C., Faria de Moraes G., Silva Pereira L., Ribeiro Cunha R., dos Santos R.M. Influence of antral follicle count on in vitro embryo production, sexual precocity and conception rate of Senepol cattle. Anim. Prod. Sci. 2021;61:1418–1424. doi: 10.1071/AN20355. [CrossRef] [Google Scholar]

• Gábor G., Kastelic J.P., Abonyi-Tóth Z., Gábor P., Endrődi T., Balogh O.G. Pregnancy loss in dairy cattle: Relationship of ultrasound, blood pregnancy-specific protein B, progesterone and production variables. Reprod. Domest. Anim. 2016;51:467–473. doi: 10.1111/rda.12703. 27198072. [PubMed] [CrossRef] [Google Scholar]

• Garcia S.M., Morotti F., Cavalieri F.L.B., Lunardelli P.A., Santos A.O., Membrive C.M.B., Castilho C., Puelker R.Z., Silva J.O.F., Zangirolamo A.F., Seneda M.M. Synchronization of stage of follicle development before OPU improves embryo production in cows with large antral follicle counts. Anim. Reprod. Sci. 2020;221 doi: 10.1016/j.anireprosci.2020.106601. 32961391. [PubMed] [CrossRef] [Google Scholar]

• Gimenes L.U., Sá Filho M.F., Carvalho N.A.T., Torres-Júnior J.R.S., Souza A.H., Madureira E.H., Trinca L.A., Sartorelli E.S., Barros C.M., Carvalho J.B.P., Mapletoft R.J., Baruselli P.S. Follicle deviation and ovulatory capacity in Bos indicus heifers. Theriogenology. 2008;69:852–858. doi: 10.1016/j.theriogenology.2008.01.001. 18316116. [PubMed] [CrossRef] [Google Scholar]

• Gobikrushanth M., Dutra P.A., Bruinjé T.C., Colazo M.G., Butler S.T., Ambrose D.J. Repeatability of antral follicle counts and anti-Müllerian hormone and their associations determined at an unknown stage of follicular growth and an expected day of follicular wave emergence in dairy cows. Theriogenology. 2017;92:90–94. doi: 10.1016/j.theriogenology.2017.01.018. 28237349. [PubMed] [CrossRef] [Google Scholar]

• Grigoletto L., Santana M.H.A., Bressan F.F., Eler J.P., Nogueira M.F.G., Kadarmideen H.N., Baruselli P.S., Ferraz J.B.S., Brito L.F. Genetic parameters and genome-wide association studies for anti-Müllerian hormone levels and antral follicle populations measured after estrus synchronization in Nelore cattle. Animals (Basel) 2020;10 doi: 10.3390/ani10071185. 32668804. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

• Ireland J.L.H., Scheetz D., Jimenez-Krassel F., Themmen A.P.N., Ward F., Lonergan P., Smith G.W., Perez G.I., Evans A.C.O., Ireland J.J. Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol. Reprod. 2008;79:1219–1225. doi: 10.1095/biolreprod.108.071670. 18768912. [PubMed] [CrossRef] [Google Scholar]

• Janati Idrissi S., Le Bourhis D., Lefevre A., Emond P., Le Berre L., Desnoes O., Joly T., Buff S., Maillard V., Schibler L., Salvetti P., Elis S. Lipid profile of bovine grade-1 blastocysts produced either in vivo or in vitro before and after slow freezing process. Sci. Rep. 2021;11 doi: 10.1038/s41598-021-90870-8. 34078963. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

• Krpálková L., O'Mahony N., Carvalho A., Campbell S., Walsh J. Evaluating the economic profit of reproductive performance through the integration of a dynamic programming model on a specific dairy farm. Czech J. Anim. Sci. 2020;65:124–134. doi: 10.17221/38/2020-CJAS. [CrossRef] [Google Scholar]

• Lopez H., Caraviello D.Z., Satter L.D., Fricke P.M., Wiltbank M.C. Relationship between level of milk production and multiple ovulations in lactating dairy cows. J. Dairy Sci. 2005;88:2783–2793. doi: 10.3168/jds.S0022-0302(05)72958-1. 16027192. [PubMed] [CrossRef] [Google Scholar]

• Lopez H., Satter L.D., Wiltbank M.C. Relationship between level of milk production and estrous behavior of lactating dairy cows. Anim. Reprod. Sci. 2004;81:209–223. doi: 10.1016/j.anireprosci.2003.10.009. [PubMed] [CrossRef] [Google Scholar]

• Martinez M.F., Sanderson N., Quirke L.D., Lawrence S.B., Juengel J.L. Association between antral follicle count and reproductive measures in New Zealand lactating dairy cows maintained in a pasture-based production system. Theriogenology. 2016;85:466–475. doi: 10.1016/j.theriogenology.2015.09.026. 26489910. [PubMed] [CrossRef] [Google Scholar]

• Morotti F., Moretti R., Dos Santos G., Silva-Santos K.C., Ramos Cerqueira P.H., Seneda M.M. Ovarian follicular dynamics and conception rate in Bos indicus cows with different antral follicle counts subjected to timed artificial insemination. Anim. Reprod. Sci. 2018;188:170–177. doi: 10.1016/j.anireprosci.2017.12.001. 29224967. [PubMed] [CrossRef] [Google Scholar]

• Nagai K., Yanagawa Y., Katagiri S., Nagano M. The relationship between antral follicle count in a bovine ovary and developmental competence of in vitro-grown oocytes derived from early antral follicles. Biomed. Res. 2016;37:63–71. doi: 10.2220/biomedres.37.63. 26912141. [PubMed] [CrossRef] [Google Scholar]

• Norman H.D., Guinan F.L., Megonigal J.H., Durr J.W. Council on Dairy Cattle Breeding; 2020. Reproductive Status of Cows in Dairy Herd Improvement Programs and Bred Using Artificial Insemination. [Google Scholar]

• Oliveira G.A., Júnior, Pinheiro V.G., Fonseca P.A.S., Costa C.B., Pioltine E.M., Botigelli R.C., Razza E.M., Ereno R.L., Ferraz J.B.S., Seneda M.M., Nogueira M.F.G. Genomic and phenotypic analyses of antral follicle count in Aberdeen Angus cows. Livest. Sci. 2021;249 doi: 10.1016/j.livsci.2021.104534. [CrossRef] [Google Scholar]

• Rosa C.O., Costa C.B., de Lima C.B., da Silva C.B., Zangirolamo A.F., Ferreira C.R., Seneda M.M. Lipid profile of in vitro embryos produced from Bos indicus cows with low and high antral follicle counts. Livest. Sci. 2021;250 doi: 10.1016/j.livsci.2021.104586. [CrossRef] [Google Scholar]

• Rosa C.O., Marinho L.S.R., da Rosa P.R.A., De Cesaro M.P., Lunardelli P.A., Silva-Santos K.C., Basso A.C., Bordignon V., Seneda M.M. Molecular characteristics of granulosa and cumulus cells and oocyte competence in Nelore cows with low and high numbers of antral follicles. Reprod. Domest. Anim. 2018;53:921–929. 29770509. [PubMed] [Google Scholar]

• Sangsritavong S., Combs D.K., Sartori R., Armentano L.E., Wiltbank M.C. High feed intake increases liver blood flow and metabolism of progesterone and estradiol-17β in dairy cattle. J. Dairy Sci. 2002;85:2831–2842. doi: 10.3168/jds.S0022-0302(02)74370-1. 12487450. [PubMed] [CrossRef] [Google Scholar]

• Sartori R., Fricke P.M., Ferreira J.C.P., Ginther O.J., Wiltbank M.C. Follicular deviation and acquisition of ovulatory capacity in bovine follicles. Biol. Reprod. 2001;65:1403–1409. doi: 10.1095/biolreprod65.5.1403. 11673256. [PubMed] [CrossRef] [Google Scholar]

• Sartori R., Monteiro P.L.J., Wiltbank M.C. Endocrine and metabolic differences between Bos taurus and Bos indicus cows and implications for reproductive management. Anim. Reprod. 2016;13:168–181. doi: 10.21451/1984-3143-AR868. [CrossRef] [Google Scholar]

• Tessaro I., Luciano A.M., Franciosi F., Lodde V., Corbani D., Modina S.C. The endothelial nitric oxide synthase/nitric oxide system is involved in the defective quality of bovine oocytes from low mid-antral follicle count ovaries. J. Animal Sci. 2011;89:2389–2396. doi: 10.2527/jas.2010-3714. [PubMed] [CrossRef] [Google Scholar]

• USDA/NAHMS . USDA; 2018. Health and Management Practices on U.S. Dairy Operations 2014. February 2018, Report 3. [Google Scholar]

• Walsh S.W., Mossa F., Butler S.T., Berry D.P., Scheetz D., Jimenez-Krassel F., Tempelman R.J., Carter F., Lonergan P., Evans A.C.O., Ireland J.J. Heritability and impact of environmental effects during pregnancy on antral follicle count in cattle. J. Dairy Sci. 2014;97:4503–4511. doi: 10.3168/jds.2013-7758. 24835969. [PubMed] [CrossRef] [Google Scholar]

• Wiltbank M., Lopez H., Sartori R., Sangsritavong S., Gümen A. Changes in reproductive physiology of lactating dairy cows due to elevated steroid metabolism. Theriogenology. 2006;65:17–29. doi: 10.1016/j.theriogenology.2005.10.003. 16290258. [PubMed] [CrossRef] [Google Scholar]

• Windig J.J., Calus M.P.L., Beerda B., Veerkamp R.F. Genetic correlations between milk production and health and fertility depending on herd environment. J. Dairy Sci. 2006;89:1765–1775. doi: 10.3168/jds.S0022-0302(06)72245-7. 16606748. [PubMed] [CrossRef] [Google Scholar]