ealy 2023

Prévia do material em texto

<p>School of Animal Science, Virginia Tech, Blacksburg 24060. *Corresponding author: kalward@ vt .edu. © 2023, The Authors. Published by Elsevier Inc. and Fass</p><p>Inc. on behalf of the American Dairy Science Association®. This is an open access article under the CC BY license (http: / / creativecommons .org/ licenses/ by/ 4</p><p>.0/ ). Received June 18, 2022. Accepted October 31, 2022.</p><p>JDS</p><p>Communications®</p><p>2023; 4:132–137• AMERI</p><p>CA</p><p>N</p><p>D</p><p>AIR</p><p>Y SCIENCE ASSO</p><p>C</p><p>IATION •</p><p>®</p><p>https: / / doi .org/ 10 .3168/ jdsc .2022 -0283</p><p>Mini-Review</p><p>Physiology</p><p>Associations of antral follicle count with fertility</p><p>in cattle: A review</p><p>K. J. Alward,* R. R. Cockrum, and A. D. Ealy</p><p>Graphical Abstract</p><p>Summary</p><p>Ultrasonic determination of antral follicle count (AFC) is used to classify animals into high or low AFC</p><p>categories. These categories have a wide range and animals classified as low on one study may be considered</p><p>high by another study based on the population. Associations with high AFC cows include greater follicular</p><p>vasculature, blastocyst rates, hatched blastocyst rates, 12-d embryonic cell growth and cleavage rates, along</p><p>with a lower number of embryonic apoptotic cells. More high AFC cows cycled as heifers at 15 months, had a</p><p>greater pregnancy rate and conception rate and progesterone concentration after breeding, and fewer days to</p><p>conception. However, other studies have found that low AFC animals had greater pregnancy and conception</p><p>rates and progesterone concentration after breeding compared with high AFC cows. Low AFC cows also</p><p>showed greater preovulatory follicle blood flow, greater blastocyst cell number, and greater area of the corpus</p><p>luteum.</p><p>Highlights</p><p>• Antral follicle count is highly correlated with superovulatory response in cattle.</p><p>• Antral follicle count is more heritable than any other reproductive traits thus far identified.</p><p>• There is a positive relationship between AFC and embryo production.</p><p>• Antral follicle count is related to pregnancy and conception rates, but data are conflicting.</p><p>mailto:kalward@vt.edu</p><p>https://orcid.org/0000-0002-7584-5759</p><p>https://orcid.org/0000-0002-0040-238X</p><p>https://orcid.org/0000-0002-8507-6578</p><p>School of Animal Science, Virginia Tech, Blacksburg 24060. *Corresponding author: kalward@ vt .edu. © 2023, The Authors. Published by Elsevier Inc. and Fass</p><p>Inc. on behalf of the American Dairy Science Association®. This is an open access article under the CC BY license (http: / / creativecommons .org/ licenses/ by/ 4</p><p>.0/ ). Received June 18, 2022. Accepted October 31, 2022.</p><p>JDS</p><p>Communications®</p><p>2023; 4:132–137• AMERI</p><p>CA</p><p>N</p><p>D</p><p>AIR</p><p>Y SCIENCE ASSO</p><p>C</p><p>IATION •</p><p>®</p><p>https: / / doi .org/ 10 .3168/ jdsc .2022 -0283</p><p>Mini-Review</p><p>Physiology</p><p>Abstract: Ovarian antral follicle count (AFC) is a marker of ovarian stimulatory response to superovulation protocols in cattle. This</p><p>article reviews novel research from the past 10 years, focusing on the relationship between AFC and embryo production and cow fertil-</p><p>ity. Substantial evidence indicates a positive relationship between AFC with embryo production; however, conflicting findings exist</p><p>regarding the relationship of AFC with conception and pregnancy rates. This lack of consistent association with pregnancy outcomes is</p><p>perplexing given the differences detected in oocytes, embryos, and endometria from high- versus low-AFC animals. Those differences</p><p>include markers of embryonic viability such as protein level, blastocyst development rates, cleavage rates, and blastocyst cell numbers</p><p>that differ between high- and low-AFC groups, as well as differential gene expression at the cow and embryo level with genes associated</p><p>with fertility. In addition, Bos indicus and Bos taurus cattle appear to have different fertility responses based on their AFC category. In</p><p>summary, clearly more studies are needed to elucidate the true associations between AFC and cow fertility, but the data that have been</p><p>accumulated thus far indicate that AFC has the potential to be a useful marker of lifetime cow fertility.</p><p>Subfertility is the number-one reason for culling on US dairy</p><p>operations (USDA/NAHMS, 2018). Regardless of herd size or</p><p>region of the US, approximately 25% of a dairy farm’s cull cows</p><p>are due to reproductive problems. It is very interesting to consider</p><p>that this culling rate is so high even though our definition of “nor-</p><p>mal” fertility has changed from 50 years ago to today. For example,</p><p>first-service conception rate is reduced from 55% (Casida, 1961)</p><p>to an average of 30 to 40% (Norman et al., 2020). More recently,</p><p>days to first breeding after calving has increased by 3.5 d, and the</p><p>calving interval has increased by 2.5 d since 2010 (Norman et al.,</p><p>2020). This can be partially attributed to increased selection for</p><p>high-producing animals without co-selection for fertility traits</p><p>(Windig et al., 2006). High-producing dairy cows pose manage-</p><p>ment challenges that compromise fertility. One example of this is</p><p>the rapid breakdown of steroid hormones (namely estradiol and</p><p>progesterone) that occurs within the liver of high-producing dairy</p><p>cows due to increased blood flow through the gastrointestinal tract</p><p>to digest feedstuffs (Sangsritavong et al., 2002; Wiltbank et al.,</p><p>2006). This causes decreased duration and intensity of estrus and</p><p>reduced GnRH and LH surges at ovulation, which can lead to larger,</p><p>older follicles at ovulation (Lopez et al., 2004). Lowering circulat-</p><p>ing progesterone limits uterine support for embryo and conceptus</p><p>development (Gábor et al., 2016) and alters follicular recruitment</p><p>in ways that promote follicle persistence and increase the incidence</p><p>of multiple dominant follicle ovulations and twinning (Lopez et al.,</p><p>2005). The economic consequences of poor fertility are substantial.</p><p>A decrease in conception rate from 40 to 50% to 30 to 40% has an</p><p>estimated value of $42 per cow per year (Krpálková et al., 2020).</p><p>On the average 300-cow farm in the US, this amounts to just over</p><p>$12,600 in losses. The fertility parameters of today’s dairy farms</p><p>demonstrate a clear need for new technologies and tools to over-</p><p>come these obstacles and improve reproductive efficiency. This</p><p>mini-review will explore the potential use of antral follicle count</p><p>(AFC) as an indicator of lifelong fertility in dairy cattle.</p><p>Antral follicle count, or antral follicle population, refers to the</p><p>total number of antral follicles present on the ovaries at any one</p><p>time. This parameter is determined via transrectal or intravaginal</p><p>ultrasonography by counting all follicles 2 to 3mm in diameter or</p><p>greater on both ovaries (Burns et al., 2005; Gobikrushanth et al.,</p><p>2017). Although variations in AFC exist based on the day of the</p><p>estrous cycle (Ireland et al., 2008), age (Burns et al., 2005), body</p><p>condition (de Moraes et al., 2019), and other parameters such as</p><p>dam nutritional status (Cushman et al., 2013), the repeatability of</p><p>this measurement is surprisingly high, generally ranging from 0.8</p><p>to 0.9 (Burns et al., 2005). Substantial variation in AFC occurs</p><p>between animals (e.g., range from 11 to 54 follicles in one study;</p><p>Burns et al., 2005), but this high repeatability permits use of AFC</p><p>as a reliable indicator of an animal’s follicular reserve, or entire</p><p>antral follicle population present. The best use of AFC in cattle</p><p>is as a predictor of an animal’s superovulatory response. Animals</p><p>with greater AFC produce more embryos in response to a super-</p><p>ovulation protocol compared with low-AFC animals (Center et al.,</p><p>2018). In addition, Walsh and colleagues (2014) found AFC to be</p><p>moderately heritable, with heritability estimates averaging 0.31 ±</p><p>0.14 in lactating dairy cows and 0.25 ± 0.13 in dairy heifers. The</p><p>heritability of Nelore cows, a Bos indicus beef breed, are roughly</p><p>similar to that of dairy cattle, with an estimated heritability of 0.30</p><p>± 0.09 (Grigoletto et al., 2020). These outcomes are significant,</p><p>because many other female fertility indicators contain heritabilities</p><p>of AFC with superovulatory response in cattle</p><p>has prompted work focusing on the discovery of relationships be-</p><p>tween AFC and the health and competency of the oocyte and with</p><p>the ability of the embryo to generate and maintain a pregnancy.</p><p>This article reviews novel research from the past 10 years, focusing</p><p>on the relationship between AFC and oocyte and embryo produc-</p><p>tion and cow fertility. Applicability of these findings to identify</p><p>high-fertility animals and managing cows for improved conception</p><p>Associations of antral follicle count with fertility</p><p>in cattle: A review</p><p>K. J. Alward,* R. R. Cockrum, and A. D. Ealy</p><p>mailto:kalward@vt.edu</p><p>https://orcid.org/0000-0002-7584-5759</p><p>https://orcid.org/0000-0002-0040-238X</p><p>https://orcid.org/0000-0002-8507-6578</p><p>JDS Communications 2023; 4: 132–137</p><p>and pregnancy rates, embryo quality, and in vitro embryo produc-</p><p>tion will be examined.</p><p>The benefits of high AFC on embryo production can be observed</p><p>by collecting oocytes and completing in vitro embryo production.</p><p>A study evaluating ovaries obtained from dairy cows with high</p><p>(>10 follicles) versus low AFC (25 follicles) versus low-AFC</p><p>animals (36 fol-</p><p>licles) had a greater numbers of viable oocytes, average number</p><p>of embryos, and cleaved embryos compared with either mid-AFC</p><p>(23–26 follicles) or low-AFC cows (25 fol-</p><p>licles) Nelore cows had increased blastocyst development rates</p><p>on d 7 compared with low-AFC (91) or low</p><p>(39 follicles) compared with in-</p><p>termediate (18–25 follicles) or low-AFC cows (45</p><p>follicles) after breeding to a timed AI (TAI) protocol (Morotti et</p><p>al., 2018). Another study in Nelore cows had similar results when</p><p>cows were classed as low (30 follicles). After TAI, low-AFC animals</p><p>had the highest pregnancy per AI compared with intermediate or</p><p>high-AFC cows (de Moraes et al., 2019). They also found an in-</p><p>teraction of body condition score with AFC and pregnancy per AI,</p><p>with pregnancy per AI decreasing significantly in cows with a high</p><p>AFC and high BCS. A third study in Nelore cows also evaluated</p><p>pregnancy per AI post-TAI in cows with very low AFC (46 follicles). Cows with very low, low, and inter-</p><p>mediate AFC had increased pregnancy per AI compared with the</p><p>high-AFC cows (de Lima et al., 2020). Other studies in Bos indicus</p><p>breeds found no differences in pregnancy per AI by AFC classi-</p><p>fication (dos Santos et al., 2016; Fagundes Faria et al., 2021). It</p><p>is interesting, however, that evidence suggests that embryos from</p><p>high-AFC cattle may still be more competent to establish a preg-</p><p>nancy than those from low-AFC cattle, evidenced by one study that</p><p>identified a positive association between AFC and pregnancy per</p><p>AI following embryo transfer in Nelore cows (Garcia et al., 2020).</p><p>Therefore, it appears that embryo competency is not an issue with</p><p>the lower fertility observed in high-AFC Bos indicus cattle. More</p><p>work is needed to define the mechanisms at play.</p><p>Data in Bos taurus breeds is also conflicting regarding the</p><p>relationship between AFC and fertility. When high-producing</p><p>Holsteins were classed as high (>24 follicles) or low AFC (</p><p>2 summarizes the data regarding pregnancy per</p><p>AI by AFC group.</p><p>An additional set of factors that have not yet been accounted</p><p>for in the previously described studies are those that have a ge-</p><p>netic linkage. One study evaluated 944 Nelore cattle and identified</p><p>several candidate genes responsible for the variation in phenotypic</p><p>AFC with roles in follicular development, steroidogenesis, and</p><p>ovulation (Grigoletto et al., 2020). At least 5 additional genes</p><p>linked to expression of reproductive traits were also found to be</p><p>related to AFC. A second study on 257 Angus cows evaluated AFC</p><p>and associated SNPs and identified genes involved with protein</p><p>encoding, regulation of primordial germ cells, and cellular mainte-</p><p>nance, as well as those linked with body weight and height in cattle</p><p>as different by AFC group (Oliveira Júnior et al., 2021). These</p><p>studies indicate that several downstream genes and processes are</p><p>linked with a cow’s AFC.</p><p>Gene expression also varies at the oocyte and embryonic level,</p><p>potentially contributing to the differences seen in embryo produc-</p><p>tion. de Lima and colleagues identified the top and bottom 20% by</p><p>AFC of 50 Nelore cows and performed ovum pick-up for genetic</p><p>sequencing. They found 11 genes differentially expressed in oo-</p><p>cytes from high- and low-AFC animals. In the low-AFC group,</p><p>upregulated genes included those involved in intercellular commu-</p><p>nication, meiotic control, epigenetic modification, and follicular</p><p>growth, with one gene associated with cell stress and apoptosis</p><p>downregulated (de Lima et al., 2020). This indicates that oocytes</p><p>and cumulus cells from high- and low-AFC animals experience</p><p>different epigenetic, cell growth, and cellular processes, and low-</p><p>AFC oocytes may display increased competency (de Lima et al.,</p><p>2020). A second study in Nelore cows found conflicting gene</p><p>expression patterns in oocytes from low- (92) animals. Low-AFC oocytes had higher expression of</p><p>some genes involved in meiosis resumption, cumulus cell expan-</p><p>sion, and transcription factor for regulating oocyte maturation and</p><p>cell proliferation, but lower expression of other genes that are also</p><p>involved in meiosis resumption and cumulus cell expansion (Rosa</p><p>et al., 2018). This conflicting data shows less discernable differ-</p><p>ence in developmental competency between high- and low-AFC</p><p>oocytes and contradicts the previously outlined results showing</p><p>higher viability via greater blastocyst and cleavage rates in high-</p><p>AFC oocytes.</p><p>The conflicting data between Bos taurus and Bos indicus breeds</p><p>regarding the relationship of AFC and both oocyte competency and</p><p>pregnancy per AI indicates factors other than the animals’ AFC</p><p>must differ and contribute to differences in fertility. A portion of</p><p>these differences can be explained genetically, as outlined above.</p><p>However, it is also important to note that inherent differences in</p><p>physiology exist between Bos taurus and Bos indicus breeds. Bos</p><p>indicus animals ovulate a smaller follicle and develop a smaller</p><p>corpus luteum (Sartori et al., 2016). Despite this, Bos indicus have</p><p>greater circulating concentrations of estradiol and progesterone</p><p>than Bos taurus breeds (Sartori et al., 2016). These differences in</p><p>physiology and cyclicity parameters have resulted in tailored TAI</p><p>programs that are specific for each species (Sartori et al., 2001;</p><p>Gimenes et al., 2008). Therefore, differences in species and AI</p><p>protocol may be a factor. Bos indicus also average a substantially</p><p>greater AFC than Bos taurus animals (Bastos et al., 2010). This</p><p>may indicate that the high-AFC Bos indicus animals and low-AFC</p><p>Bos taurus animals represent the extremes in AFC range and that,</p><p>rather than high or low being ideal, the intermediary group (low-</p><p>AFC Bos indicus and high-AFC Bos taurus) may be the most fer-</p><p>tile. However, these theories need to be investigated to determine</p><p>their contribution toward the differences seen in fertility by AFC</p><p>category.</p><p>In summary, AFC is correlated with a cow’s superovulation</p><p>response. The AFC is also moderately heritable, and this level</p><p>of heritability provides much better selection opportunities than</p><p>most other reproductive traits. Good evidence suggests that AFC</p><p>is positively correlated with embryo production efficiency. How-</p><p>ever, conflicting findings exist when applying these findings to</p><p>fertility status, and more evidence actually suggests that high-AFC</p><p>cattle are less fertile than intermediate and low-AFC cattle. Gene</p><p>expression in high- versus low-AFC animals at the cow level find</p><p>that numerous downstream processes related to reproduction are</p><p>134Alward et al. | Associations of AFC with cattle fertility</p><p>JDS Communications 2023; 4: 132–137</p><p>differentially expressed. At the embryonic level, embryos from</p><p>high- versus low-AFC animals also exhibit differential gene ex-</p><p>pression; however, these mostly indicate greater fertility and health</p><p>in low-AFC oocytes and embryos. One factor that has not been</p><p>standardized across studies is the threshold for “high” AFC. Some</p><p>studies show that extreme AFC animals, both high and low, have</p><p>reduced fertility compared with the median groups (Gobikrushanth</p><p>et al., 2017; Akbarinejad et al., 2020). Therefore, studies that clas-</p><p>sify their high-AFC groups more broadly may be capturing the</p><p>mid group and the extreme high group, negating any differences</p><p>between them. In addition, breed differences may exist. Differ-</p><p>ences certainly exist between bovid subspecies, with Bos indicus</p><p>and Bos taurus breeds exhibiting different fertility responses by</p><p>AFC category. More studies are required to confirm these theories</p><p>and elucidate the true associations between AFC and embryo pro-</p><p>duction and fertility. Collectively, these data indicate a relationship</p><p>between AFC and measures of cow fertility and the potential to</p><p>use AFC as a genetic selection and management tool to improve</p><p>reproductive efficiency on dairy farms.</p><p>References</p><p>Akbarinejad, V., F. Gharagozlou, M. Vojgani, and A. Ranji. 2020. Evidence</p><p>for quadratic association between serum anti-Müllerian hormone (AMH)</p><p>concentration and fertility in dairy cows. Anim. Reprod. Sci. 218:106457.</p><p>https: / / doi .org/ 10 .1016/ j .anireprosci .2020 .106457.</p><p>Bastos, M. R., M. C. C. Mattos, M. A. P. Meschiatti, R. S. Surjus, M. M.</p><p>Guardieiro, J. C. P. Ferreira, G. B. Mourão, A. V. Pires, M. V. Biehl, A.</p><p>M. Pedroso, F. A. P. Santos, and R. Sartori. 2010. Ovarian function and</p><p>circulating hormones in nonlactating Nelore versus Holstein cows. Acta</p><p>Sci. Vet. 38:776.</p><p>Bonato, D. V., E. B. Ferreira, D. N. Gomes, F. G. C. Bonato, R. G. Droher,</p><p>F. Morotti, and M. M. Seneda. 2022. Follicular dynamics, luteal char-</p><p>acteristics, and progesterone concentrations in synchronized lactating</p><p>Holstein cows with high and low antral follicle counts. Theriogenology</p><p>179:223–229. https: / / doi .org/ 10 .1016/ j .theriogenology .2021 .12 .006.</p><p>Burns, D. S., F. Jimenez-Krassel, J. L. H. Ireland, P. G. Knight, and J. J. Ire-</p><p>land. 2005. Numbers of antral follicles during follicular waves in cattle:</p><p>evidence for high variation among animals, very high repeatability in</p><p>individuals, and an inverse association with serum follicle-stimulating</p><p>hormone concentrations. Biol. Reprod. 73:54–62. https: / / doi .org/ 10 .1095/</p><p>biolreprod .104 .036277.</p><p>135Alward et al. | Associations of AFC with cattle fertility</p><p>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</p><p>heifer versus cow used in study are indicated above each graph. Different lowercase letters (a, b) indicate significant differences. P-values and numbers of</p><p>animals used are provided.</p><p>https://doi.org/10.1016/j.anireprosci.2020.106457</p><p>https://doi.org/10.1016/j.theriogenology.2021.12.006</p><p>https://doi.org/10.1095/biolreprod.104.036277</p><p>https://doi.org/10.1095/biolreprod.104.036277</p><p>JDS Communications 2023; 4: 132–137</p><p>Cammack, K. M., M. G. Thomas, and R. M. Enns.</p><p>2009. Reproductive traits</p><p>and their heritabilities in beef cattle. Prof. Anim. Sci. 25:517–528. https: / /</p><p>doi .org/ 10 .15232/ S1080 -7446(15)30753 -1.</p><p>Casida, L. E. 1961. Present status of the repeat breeder cow problem. J. Dairy</p><p>Sci. 44:2323–2329. https: / / doi .org/ 10 .3168/ jds .S0022 -0302(61)90063 -7.</p><p>Center, K., D. Dixon, C. Looney, and R. Rorie. 2018. Anti-Mullerian hormone</p><p>and follicle counts as predictors of superovulatory response and embryo</p><p>production in beef cattle. Adv. Reprod. Sci. 6:22–33. https: / / doi .org/ 10</p><p>.4236/ arsci .2018 .61003.</p><p>Cushman, R. A., A. K. McNeel, and H. C. Freetly. 2014. The impact of cow</p><p>nutrient status during the second and third trimesters on age at puberty,</p><p>antral follicle count, and fertility of daughters. Livest. Sci. 162:252–258.</p><p>https: / / doi .org/ 10 .1016/ j .livsci .2014 .01 .033.</p><p>de Lima, M. A., F. Morotti, B. M. Bayeux, R. G. de Rezende, R. C. Botigelli,</p><p>T. H. C. De Bem, P. K. Fontes, M. F. G. Nogueira, F. V. Meirelles, P. S.</p><p>Baruselli, J. C. da Silveira, F. Perecin, and M. M. Seneda. 2020. Ovar-</p><p>ian follicular dynamics, progesterone concentrations, pregnancy rates and</p><p>transcriptional patterns in Bos indicus females with a high or low antral</p><p>follicle count. Sci. Rep. 10:19557. https: / / doi .org/ 10 .1038/ s41598 -020</p><p>-76601 -5.</p><p>de Moraes, F. L. Z., F. Morotti, C. B. Costa, P. A. Lunardelli, and M. M.</p><p>Seneda. 2019. Relationships between antral follicle count, body condition,</p><p>and pregnancy rates after timed-AI in Bos indicus cattle. Theriogenology</p><p>136:10–14. https: / / doi .org/ 10 .1016/ j .theriogenology .2019 .06 .024.</p><p>dos Santos, G. M. G., K. C. Silva-Santos, T. R. R. Barreiros, F. Morotti, B. V.</p><p>Sanches, F. L. Z. de Moraes, W. Blaschi, and M. M. Seneda. 2016. High</p><p>numbers of antral follicles are positively associated with in vitro embryo</p><p>production but not the conception rate for FTAI in Nelore cattle. Animal</p><p>Reprod. Sci. 165:17–21. https: / / doi .org/ 10 .1016/ j .anireprosci .2015 .11 .024.</p><p>Fagundes Faria, A. C., G. Faria de Moraes, L. Silva Pereira, R. Ribeiro Cunha,</p><p>and R. M. dos Santos. 2021. Influence of antral follicle count on in vitro</p><p>embryo production, sexual precocity and conception rate of Senepol cattle.</p><p>Anim. Prod. Sci. 61:1418–1424. https: / / doi .org/ 10 .1071/ AN20355.</p><p>Gábor, G., J. P. Kastelic, Z. Abonyi-Tóth, P. Gábor, T. Endrődi, and O. G.</p><p>Balogh. 2016. Pregnancy loss in dairy cattle: Relationship of ultrasound,</p><p>blood pregnancy-specific protein B, progesterone and production variables.</p><p>Reprod. Domest. Anim. 51:467–473. https: / / doi .org/ 10 .1111/ rda .12703.</p><p>Garcia, S. M., F. Morotti, F. L. B. Cavalieri, P. A. Lunardelli, A. O. Santos,</p><p>C. M. B. Membrive, C. Castilho, R. Z. Puelker, J. O. F. Silva, A. F. Zan-</p><p>girolamo, and M. M. Seneda. 2020. Synchronization of stage of follicle</p><p>development before OPU improves embryo production in cows with large</p><p>antral follicle counts. Anim. Reprod. Sci. 221:106601. https: / / doi .org/ 10</p><p>.1016/ j .anireprosci .2020 .106601.</p><p>Gimenes, L. U., M. F. Sá Filho, N. A. T. Carvalho, J. R. S. Torres-Júnior, A. H.</p><p>Souza, E. H. Madureira, L. A. Trinca, E. S. Sartorelli, C. M. Barros, J. B.</p><p>P. Carvalho, R. J. Mapletoft, and P. S. Baruselli. 2008. Follicle deviation</p><p>and ovulatory capacity in Bos indicus heifers. Theriogenology 69:852–858.</p><p>https: / / doi .org/ 10 .1016/ j .theriogenology .2008 .01 .001.</p><p>Gobikrushanth, M., P. A. Dutra, T. C. Bruinjé, M. G. Colazo, S. T. Butler, and D.</p><p>J. Ambrose. 2017. Repeatability of antral follicle counts and anti-Müllerian</p><p>hormone and their associations determined at an unknown stage of fol-</p><p>licular growth and an expected day of follicular wave emergence in dairy</p><p>cows. Theriogenology 92:90–94. https: / / doi .org/ 10 .1016/ j .theriogenology</p><p>.2017 .01 .018.</p><p>Grigoletto, L., M. H. A. Santana, F. F. Bressan, J. P. Eler, M. F. G. Nogueira, H.</p><p>N. Kadarmideen, P. S. Baruselli, J. B. S. Ferraz, and L. F. Brito. 2020. Ge-</p><p>netic parameters and genome-wide association studies for anti-Müllerian</p><p>hormone levels and antral follicle populations measured after estrus syn-</p><p>chronization in Nelore cattle. Animals (Basel) 10:1185. https: / / doi .org/ 10</p><p>.3390/ ani10071185.</p><p>Ireland, J. L. H., D. Scheetz, F. Jimenez-Krassel, A. P. N. Themmen, F. Ward,</p><p>P. Lonergan, G. W. Smith, G. I. Perez, A. C. O. Evans, and J. J. Ireland.</p><p>2008. Antral follicle count reliably predicts number of morphologically</p><p>healthy oocytes and follicles in ovaries of young adult cattle. Biol. Reprod.</p><p>79:1219–1225. https: / / doi .org/ 10 .1095/ biolreprod .108 .071670.</p><p>Janati Idrissi, S., D. Le Bourhis, A. Lefevre, P. Emond, L. Le Berre, O. Desnoes,</p><p>T. Joly, S. Buff, V. Maillard, L. Schibler, P. Salvetti, and S. Elis. 2021. Lipid</p><p>profile of bovine grade-1 blastocysts produced either in vivo or in vitro</p><p>before and after slow freezing process. Sci. Rep. 11:11618. https: / / doi .org/</p><p>10 .1038/ s41598 -021 -90870 -8.</p><p>Krpálková, L., N. O’Mahony, A. Carvalho, S. Campbell, and J. Walsh. 2020.</p><p>Evaluating the economic profit of reproductive performance through the</p><p>integration of a dynamic programming model on a specific dairy farm.</p><p>Czech J. Anim. Sci. 65:124–134. https: / / doi .org/ 10 .17221/ 38/ 2020 -CJAS.</p><p>Lopez, H., D. Z. Caraviello, L. D. Satter, P. M. Fricke, and M. C. Wiltbank.</p><p>2005. Relationship between level of milk production and multiple ovula-</p><p>tions in lactating dairy cows. J. Dairy Sci. 88:2783–2793. https: / / doi .org/ 10</p><p>.3168/ jds .S0022 -0302(05)72958 -1.</p><p>Lopez, H., L. D. Satter, and M. C. Wiltbank. 2004. Relationship between level</p><p>of milk production and estrous behavior of lactating dairy cows. Anim. Re-</p><p>prod. Sci. 81:209–223. https: / / doi .org/ 10 .1016/ j .anireprosci .2003 .10 .009.</p><p>Martinez, M. F., N. Sanderson, L. D. Quirke, S. B. Lawrence, and J. L. Juengel.</p><p>2016. Association between antral follicle count and reproductive measures</p><p>in New Zealand lactating dairy cows maintained in a pasture-based pro-</p><p>duction system. Theriogenology 85:466–475. https: / / doi .org/ 10 .1016/ j</p><p>.theriogenology .2015 .09 .026.</p><p>Morotti, F., R. Moretti, G. Dos Santos, K. C. Silva-Santos, P. H. Ramos Cer-</p><p>queira, and M. M. Seneda. 2018. Ovarian follicular dynamics and concep-</p><p>tion rate in Bos indicus cows with different antral follicle counts subjected</p><p>to timed artificial insemination. Anim. Reprod. Sci. 188:170–177. https: / /</p><p>doi .org/ 10 .1016/ j .anireprosci .2017 .12 .001.</p><p>Nagai, K., Y. Yanagawa, S. Katagiri, and M. Nagano. 2016. The relationship</p><p>between antral follicle count in a bovine ovary and developmental compe-</p><p>tence of in vitro-grown oocytes derived from early antral follicles. Biomed.</p><p>Res. 37:63–71. https: / / doi .org/ 10 .2220/ biomedres .37 .63.</p><p>Norman, H. D., F. L. Guinan, J. H. Megonigal, and J. W. Durr. 2020. Reproduc-</p><p>tive Status of Cows in Dairy Herd Improvement Programs and Bred Using</p><p>Artificial Insemination. Council on Dairy Cattle Breeding.</p><p>Oliveira Júnior, G. A., V. G. Pinheiro, P. A. S. Fonseca, C. B. Costa, E. M.</p><p>Pioltine, R. C. Botigelli, E. M. Razza, R. L. Ereno, J. B. S. Ferraz, M. M.</p><p>Seneda, and M. F. G. Nogueira. 2021. Genomic and phenotypic analyses</p><p>of antral follicle count in Aberdeen Angus cows. Livest. Sci. 249:104534.</p><p>https: / / doi .org/ 10 .1016/ j .livsci .2021 .104534.</p><p>Rosa, C. O., C. B. Costa, C. B. de Lima, C. B. da Silva, A. F. Zangirolamo,</p><p>C. R. Ferreira, and M. M. Seneda. 2021. Lipid profile of in vitro embryos</p><p>produced from Bos indicus cows with low and high antral follicle counts.</p><p>Livest. Sci. 250:104586. https: / / doi .org/ 10 .1016/ j .livsci .2021 .104586.</p><p>Rosa, C. O., L. S. R. Marinho, P. R. A. da Rosa, M. P. De Cesaro, P. A. Lu-</p><p>nardelli, K. C. Silva-Santos, A. C. Basso, V. Bordignon, and M. M. Seneda.</p><p>2018. Molecular characteristics of granulosa and cumulus cells and oocyte</p><p>competence in Nelore cows with low and high numbers of antral follicles.</p><p>Reprod. Domest. Anim. 53:921–929.</p><p>Sangsritavong, S., D. K. Combs, R. Sartori, L. E. Armentano, and M. C. Wilt-</p><p>bank. 2002. High feed intake increases liver blood flow and metabolism of</p><p>progesterone and estradiol-17β in dairy cattle. J. Dairy Sci. 85:2831–2842.</p><p>https: / / doi .org/ 10 .3168/ jds .S0022 -0302(02)74370 -1.</p><p>Sartori, R., P. M. Fricke, J. C. P. Ferreira, O. J. Ginther, and M. C. Wiltbank.</p><p>2001. Follicular deviation and acquisition of ovulatory capacity in</p><p>bovine follicles. Biol. Reprod. 65:1403–1409. https: / / doi .org/ 10 .1095/</p><p>biolreprod65 .5 .1403.</p><p>Sartori, R., P. L. J. Monteiro, and M. C. Wiltbank. 2016. Endocrine and meta-</p><p>bolic differences between Bos taurus and Bos indicus cows and implica-</p><p>tions for reproductive management. Anim. Reprod. 13:168–181. https: / / doi</p><p>.org/ 10 .21451/ 1984 -3143 -AR868.</p><p>Tessaro, I., A. M. Luciano, F. Franciosi, V. Lodde, D. Corbani, and S. C. Mo-</p><p>dina. 2011. The endothelial nitric oxide synthase/nitric oxide system is</p><p>involved in the defective quality of bovine oocytes from low mid-antral</p><p>follicle count ovaries. J. Animal Sci. 89:2389–2396. https: / / doi .org/ 10</p><p>.2527/ jas .2010 -3714.</p><p>USDA/NAHMS. 2018. Health and Management Practices on U.S. Dairy Op-</p><p>erations 2014. February 2018, Report 3. USDA.</p><p>Walsh, S. W., F. Mossa, S. T. Butler, D. P. Berry, D. Scheetz, F. Jimenez-Krassel,</p><p>R. J. Tempelman, F. Carter, P. Lonergan, A. C. O. Evans, and J. J. Ireland.</p><p>2014. Heritability and impact of environmental effects during pregnancy</p><p>on antral follicle count in cattle. J. Dairy Sci. 97:4503–4511. https: / / doi</p><p>.org/ 10 .3168/ jds .2013 -7758.</p><p>Wiltbank, M., H. Lopez, R. Sartori, S. Sangsritavong, and A. Gümen. 2006.</p><p>Changes in reproductive physiology of lactating dairy cows due to elevated</p><p>steroid metabolism. Theriogenology 65:17–29. https: / / doi .org/ 10 .1016/ j</p><p>.theriogenology .2005 .10 .003.</p><p>Windig, J. J., M. P. L. Calus, B. Beerda, and R. F. Veerkamp. 2006. Genetic</p><p>correlations between milk production and health and fertility depending on</p><p>herd environment. J. Dairy Sci. 89:1765–1775. https: / / doi .org/ 10 .3168/ jds</p><p>.S0022 -0302(06)72245 -7.</p><p>136Alward et al. | Associations of AFC with cattle fertility</p><p>https://doi.org/10.15232/S1080-7446(15)30753-1</p><p>https://doi.org/10.15232/S1080-7446(15)30753-1</p><p>https://doi.org/10.3168/jds.S0022-0302(61)90063-7</p><p>https://doi.org/10.4236/arsci.2018.61003</p><p>https://doi.org/10.4236/arsci.2018.61003</p><p>https://doi.org/10.1016/j.livsci.2014.01.033</p><p>https://doi.org/10.1038/s41598-020-76601-5</p><p>https://doi.org/10.1038/s41598-020-76601-5</p><p>https://doi.org/10.1016/j.theriogenology.2019.06.024</p><p>https://doi.org/10.1016/j.anireprosci.2015.11.024</p><p>https://doi.org/10.1071/AN20355</p><p>https://doi.org/10.1111/rda.12703</p><p>https://doi.org/10.1016/j.anireprosci.2020.106601</p><p>https://doi.org/10.1016/j.anireprosci.2020.106601</p><p>https://doi.org/10.1016/j.theriogenology.2008.01.001</p><p>https://doi.org/10.1016/j.theriogenology.2017.01.018</p><p>https://doi.org/10.1016/j.theriogenology.2017.01.018</p><p>https://doi.org/10.3390/ani10071185</p><p>https://doi.org/10.3390/ani10071185</p><p>https://doi.org/10.1095/biolreprod.108.071670</p><p>https://doi.org/10.1038/s41598-021-90870-8</p><p>https://doi.org/10.1038/s41598-021-90870-8</p><p>https://doi.org/10.17221/38/2020-CJAS</p><p>https://doi.org/10.3168/jds.S0022-0302(05)72958-1</p><p>https://doi.org/10.3168/jds.S0022-0302(05)72958-1</p><p>https://doi.org/10.1016/j.anireprosci.2003.10.009</p><p>https://doi.org/10.1016/j.theriogenology.2015.09.026</p><p>https://doi.org/10.1016/j.theriogenology.2015.09.026</p><p>https://doi.org/10.1016/j.anireprosci.2017.12.001</p><p>https://doi.org/10.1016/j.anireprosci.2017.12.001</p><p>https://doi.org/10.2220/biomedres.37.63</p><p>https://doi.org/10.1016/j.livsci.2021.104534</p><p>https://doi.org/10.1016/j.livsci.2021.104586</p><p>https://doi.org/10.3168/jds.S0022-0302(02)74370-1</p><p>https://doi.org/10.1095/biolreprod65.5.1403</p><p>https://doi.org/10.1095/biolreprod65.5.1403</p><p>https://doi.org/10.21451/1984-3143-AR868</p><p>https://doi.org/10.21451/1984-3143-AR868</p><p>https://doi.org/10.2527/jas.2010-3714</p><p>https://doi.org/10.2527/jas.2010-3714</p><p>https://doi.org/10.3168/jds.2013-7758</p><p>https://doi.org/10.3168/jds.2013-7758</p><p>https://doi.org/10.1016/j.theriogenology.2005.10.003</p><p>https://doi.org/10.1016/j.theriogenology.2005.10.003</p><p>https://doi.org/10.3168/jds.S0022-0302(06)72245-7</p><p>https://doi.org/10.3168/jds.S0022-0302(06)72245-7</p><p>JDS Communications 2023; 4: 132–137</p><p>Notes</p><p>K. J. Alward https: / / orcid .org/ 0000 -0002 -7584 -5759</p><p>R. R. Cockrum https: / / orcid .org/ 0000 -0002 -0040 -238X</p><p>A. D. Ealy https: / / orcid .org/ 0000 -0002 -8507 -6578</p><p>Funding for this work was provided by Agriculture and Food Research Ini-</p><p>tiative Competitive Grant numbers 2017-67015-2646 and 2021-67015-34485</p><p>from the USDA National Institute of Food and Agriculture (Washington, DC).</p><p>No human or animal subjects were used, so this analysis did not require ap-</p><p>proval by an Institutional Animal Care and Use Committee or Institutional</p><p>Review Board.</p><p>The authors have not stated any conflicts of interest.</p><p>137Alward et al. | Associations of AFC with cattle fertility</p><p>https://orcid.org/0000-0002-7584-5759</p><p>https://orcid.org/0000-0002-0040-238X</p><p>https://orcid.org/0000-0002-8507-6578</p><p>Associations of antral follicle count with fertility</p><p>in cattle: A review</p><p>Graphical Abstract</p><p>References</p>