Follicle vascularity coordinates corpus luteum blood flow and progesterone production
S. G. S. de Tarso A , G. D. A. Gastal A , S. T. Bashir A , M. O. Gastal A , G. A. Apgar A and E. L. Gastal A B
+ Author Affiliations
- Author Affiliations
A Department of Animal Science, Food and Nutrition, Southern Illinois University, 1205 Lincoln Drive, MC 4417, Carbondale, IL 62901, USA.
B Corresponding author. Email: egastal@siu.edu
Reproduction, Fertility and Development 29(3) 448-457 https://doi.org/10.1071/RD15223
Submitted: 4 June 2015 Accepted: 24 July 2015 Published: 7 September 2015
Abstract
Colour Doppler ultrasonography was used to compare the ability of preovulatory follicle (POF) blood flow and its dimensions to predict the size, blood flow and progesterone production capability of the subsequent corpus luteum (CL). Cows (n = 30) were submitted to a synchronisation protocol. Follicles ≥7 mm were measured and follicular wall blood flow evaluated every 12 h for approximately 3.5 days until ovulation. After ovulation, cows were scanned daily for 8 days and similar parameters were evaluated for the CL. Blood samples were collected and plasma progesterone concentrations quantified. All parameters were positively correlated. Correlation values ranged from 0.26 to 0.74 on data normalised to ovulation and from 0.31 to 0.74 on data normalised to maximum values. Correlations between calculated ratios of both POF and CL in data normalised to ovulation and to maximum values ranged from moderate (0.57) to strong (0.87). Significant (P < 0.0001) linear regression analyses were seen in all comparisons. In conclusion, higher correlations were observed between the dimensions of POF and/or CL and blood flow of both structures, as well as POF and/or CL blood flow with plasma progesterone concentrations of the resultant CL. These findings indicate that follicle vascularity coordinates CL blood flow and progesterone production in synchronised beef cows.
Additional keywords: colour Doppler ultrasonography, cows, preovulatory follicle, ovary.
References
Acosta, T. J. (2007). Studies of follicular vascularity associated with follicle selection and ovulation in cattle. J. Reprod. Dev. 53, 39–44.| Studies of follicular vascularity associated with follicle selection and ovulation in cattle.Crossref | GoogleScholarGoogle Scholar | 17332698PubMed |
Acosta, T. J., and Miyamoto, A. (2004). Vascular control of ovarian function: ovulation, corpus luteum formation and regression. Anim. Reprod. Sci. 82–83, 127–140.
| Vascular control of ovarian function: ovulation, corpus luteum formation and regression.Crossref | GoogleScholarGoogle Scholar | 15271448PubMed |
Acosta, T. J., Yoshizawa, N., Ohtani, M., and Miyamoto, A. (2002). Local changes in blood flow within the early and midcycle corpus luteum after prostaglandin F(2 alpha) injection in the cow. Biol. Reprod. 66, 651–658.
| Local changes in blood flow within the early and midcycle corpus luteum after prostaglandin F(2 alpha) injection in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVeitb0%3D&md5=461e7b4e7176385042640edbd99181c2CAS | 11870071PubMed |
Acosta, T. J., Hayashi, K. G., Ohtani, M., and Miyamoto, A. (2003). Local changes in blood flow within the preovulatory follicle wall and early corpus luteum in cows. Reproduction 125, 759–767.
| Local changes in blood flow within the preovulatory follicle wall and early corpus luteum in cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVKmu7k%3D&md5=b3dc1e8c553c5a095c94992bfbf3b57fCAS | 12713439PubMed |
Acosta, T. J., Gastal, E. L., Gastal, M. O., Beg, M. A., and Ginther, O. J. (2004a). Differential blood flow changes between the future dominant and subordinate follicles precede diameter changes during follicle selection in mares. Biol. Reprod. 71, 502–507.
| Differential blood flow changes between the future dominant and subordinate follicles precede diameter changes during follicle selection in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgtbo%3D&md5=2f83ae36c377324d22b31b9fd07d69eaCAS | 15070831PubMed |
Acosta, T. J., Beg, M. A., and Ginther, O. J. (2004b). Aberrant blood flow area and plasma gonadotropin concentrations during the development of dominant-sized transitional anovulatory follicles in mares. Biol. Reprod. 71, 637–642.
| Aberrant blood flow area and plasma gonadotropin concentrations during the development of dominant-sized transitional anovulatory follicles in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgu78%3D&md5=3c94e96e77462483055bf49f817263adCAS | 15084481PubMed |
Acosta, T. J., Hayashi, K. G., Matsui, M., and Miyamoto, A. (2005). Changes in follicular vascularity during the first follicular wave in lactating cows. J. Reprod. Dev. 51, 273–280.
| Changes in follicular vascularity during the first follicular wave in lactating cows.Crossref | GoogleScholarGoogle Scholar | 15699584PubMed |
Atkins, J. A., Smith, M. F., Wells, K. J., and Geary, T. W. (2010). Factors affecting preovulatory follicle diameter and ovulation rate after gonadotropin-releasing hormone in postpartum beef cows. Part I: cycling cows. J. Anim. Sci. 88, 2300–2310.
| Factors affecting preovulatory follicle diameter and ovulation rate after gonadotropin-releasing hormone in postpartum beef cows. Part I: cycling cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1Kmsb4%3D&md5=f65124e3de09f01ce1e35497fa1f2212CAS | 20228240PubMed |
Bhal, P. S., Pugh, N. D., Chui, D. K., Gregory, L., Walker, S. M., and Shaw, R. W. (1999). The use of transvaginal power Doppler ultrasonography to evaluate the relationship between perifollicular vascularity and outcome in in-vitro fertilization treatment cycles. Hum. Reprod. 14, 939–945.
| The use of transvaginal power Doppler ultrasonography to evaluate the relationship between perifollicular vascularity and outcome in in-vitro fertilization treatment cycles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3jslGrsw%3D%3D&md5=d1c3aa1fb608ee13674564aed86fcb29CAS | 10221224PubMed |
Bollwein, H., Prost, D., Ulbrich, S. E., Niemann, H., and Honnens, A. (2010). Effects of a shortened preovulatory follicular phase on genital blood flow and endometrial hormone receptor concentrations in Holstein–Friesian cows. Theriogenology 73, 242–249.
| Effects of a shortened preovulatory follicular phase on genital blood flow and endometrial hormone receptor concentrations in Holstein–Friesian cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGrs77M&md5=6fe81a8e278a6d1fd7fcd4dcac767f6aCAS | 19897233PubMed |
Brännström, M., Zackrisson, U., Hagström, H. G., Josefsson, B., Granberg, S., Collins, W. P., and Bourne, T. (1998). Preovulatory changes of blood flow in different regions of the human follicle. Fertil. Steril. 69, 435–442.
| Preovulatory changes of blood flow in different regions of the human follicle.Crossref | GoogleScholarGoogle Scholar | 9531873PubMed |
El-Sherry, T. M., Derar, R., and Bakry, R. (2013). Changes in blood flow in ovine follicles and serum concentration of estradiol 17 beta (E2) and nitric oxide (NO) around the time of ovulation in Ossimi ewes. Anim. Reprod. Sci. 138, 188–193.
| Changes in blood flow in ovine follicles and serum concentration of estradiol 17 beta (E2) and nitric oxide (NO) around the time of ovulation in Ossimi ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVChtb4%3D&md5=38db7d47d73ccc51c4b7fdddcc1ba33dCAS | 23582607PubMed |
Eversole, D. E., Browne, M. F., Hall, J. B., and Dietz, R. E. (2009). ‘Body Condition Scoring Beef Cows.’ (Publications and Educational Resources, Virginia Tech: Blacksburg, VA.) Available at: https://pubs.ext.vt.edu/400/400-795/400-795.html [verified 4 August 2015].
Gastal, E. L., and Gastal, M. O. (2011). Equine preovulatory follicle: blood flow changes, prediction of ovulation and fertility. Rev. Bras. Reprod. Anim. 35, 239–252.
Gastal, E. L., Gastal, M. O., and Ginther, O. J. (2006). Relationships of changes in B-mode echotexture and colour-Doppler signals in the wall of the preovulatory follicle to changes in systemic oestradiol concentrations and the effects of human chorionic gonadotrophin in mares. Reproduction 131, 699–709.
| Relationships of changes in B-mode echotexture and colour-Doppler signals in the wall of the preovulatory follicle to changes in systemic oestradiol concentrations and the effects of human chorionic gonadotrophin in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jtrg%3D&md5=a39671956ade25ee4a2452133263e0faCAS | 16595721PubMed |
Geary, T. W., Smith, M. F., Macneil, M. D., Day, M. L., Bridges, G. A., Perry, G. A., Abreu, F. M., Atkins, J. A., Pohler, K. G., Jinks, E. M., and Madsen, C. A. (2013). Influence of follicular characteristics at ovulation on early embryonic survival. J. Anim. Sci. 91, 3014–3021.
| Influence of follicular characteristics at ovulation on early embryonic survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFChsLzI&md5=d4f98c088a01fa7b15de985938cc14c5CAS | 23230106PubMed |
Ginther, O. J. (1995). ‘Ultrasonic Imaging and Animal Reproduction: Book 2, Horses.’ (Equiservices Publishing: Cross Plains, WI.)
Ginther, O. J. (2007). ‘Ultrasonic Imaging and Animal Reproduction: Book 4, Color-Doppler Ultrasonography.’ (Equiservices Publishing: Cross Plains, WI.)
Ginther, O. J., Knopf, L., and Kastelic, J. P. (1989). Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves. J. Reprod. Fertil. 87, 223–230.
| Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7ls1WrsQ%3D%3D&md5=e00c4b2b251dd138a79036f242a9812dCAS | 2621698PubMed |
Ginther, O. J., Gastal, E. L., Gastal, M. O., Siddiqui, M. A. R., and Beg, M. A. (2007a). Relationships of follicle versus oocyte maturity to ultrasound morphology, blood flow, and hormone concentrations of the preovulatory follicle in mares. Biol. Reprod. 77, 202–208.
| Relationships of follicle versus oocyte maturity to ultrasound morphology, blood flow, and hormone concentrations of the preovulatory follicle in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1OnsLo%3D&md5=ddd656aad3c050d958981f573a25bc96CAS | 17475927PubMed |
Ginther, O. J., Gastal, E. L., Gastal, M. O., Utt, M. D., and Beg, M. A. (2007b). Luteal blood flow and progesterone production in mares. Anim. Reprod. Sci. 99, 213–220.
| Luteal blood flow and progesterone production in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1GmsL4%3D&md5=5a5207728b30b97c52c08bb66510e828CAS | 16815650PubMed |
Herzog, K., and Bollwein, H. (2007). Application of Doppler ultrasonography in cattle reproduction. Reprod. Domest. Anim. 42, 51–58.
| Application of Doppler ultrasonography in cattle reproduction.Crossref | GoogleScholarGoogle Scholar | 17688602PubMed |
Herzog, K., Brockhan-Lüdemann, M., Kaske, M., Beindorff, N., Paul, V., Niemann, H., and Bollwein, H. (2010). Luteal blood flow is a more appropriate indicator for luteal function during the bovine estrous cycle than luteal size. Theriogenology 73, 691–697.
| Luteal blood flow is a more appropriate indicator for luteal function during the bovine estrous cycle than luteal size.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOhsrg%3D&md5=20e913e8fda063e553508542f259868fCAS | 20071016PubMed |
Herzog, K., Voss, C., Kastelic, J. P., Beindorff, N., Paul, V., Niemann, H., and Bollwein, H. (2011). Luteal blood flow increases during the first three weeks of pregnancy in lactating dairy cows. Theriogenology 75, 549–554.
| Luteal blood flow increases during the first three weeks of pregnancy in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2Fps1yqtA%3D%3D&md5=831cdb36b086543bf1a4b5b9da913c07CAS | 20965557PubMed |
Honnens, A., Voss, C., Herzog, K., Niemann, H., Rath, D., and Bollwein, H. (2008). Uterine blood flow during the first 3 weeks of pregnancy in dairy cows. Theriogenology 70, 1048–1056.
| Uterine blood flow during the first 3 weeks of pregnancy in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFajurjL&md5=9a081095761c32d1c090cff8edd942d2CAS | 18675450PubMed |
Janson, P. O., Damber, J. E., and Axén, C. (1981). Luteal blood flow and progesterone secretion in pseudopregnant rabbits. J. Reprod. Fertil. 63, 491–497.
| Luteal blood flow and progesterone secretion in pseudopregnant rabbits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtVWnu7Y%3D&md5=9aa7289692f1f6bc2479d99182b30c3dCAS | 7299751PubMed |
Khan, F. A., Pinaffi, F. L. V., Beg, M. A., and Ginther, O. J. (2012). Unilateral ablation of follicles ≥4 mm leads to compensatory follicle response from the contralateral ovary in heifers. Theriogenology 77, 1605–1614.
| Unilateral ablation of follicles ≥4 mm leads to compensatory follicle response from the contralateral ovary in heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vjt1OnsQ%3D%3D&md5=3e34034e1e78a9d2e52616da3a2f09dbCAS | 22341711PubMed |
Lüttgenau, J., Beindorff, N., Ulbrich, S. E., Kastelic, J. P., and Bollwein, H. (2011). Low plasma progesterone concentrations are accompanied by reduced luteal blood flow and increased size of the dominant follicle in dairy cows. Theriogenology 76, 12–22.
| Low plasma progesterone concentrations are accompanied by reduced luteal blood flow and increased size of the dominant follicle in dairy cows.Crossref | GoogleScholarGoogle Scholar | 21529918PubMed |
MacNeil, M. D., Geary, T. W., Perry, G., Roberts, A., and Alexander, L. J. (2006). Genetic partitioning of variation in ovulatory follicle size and probability of pregnancy in beef cattle. J. Anim. Sci. 84, 1646–1650.
| Genetic partitioning of variation in ovulatory follicle size and probability of pregnancy in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aqsbs%3D&md5=1326a31e43d08bd270873ffef22b0755CAS | 16775047PubMed |
Mann, G. E. (2009). Corpus luteum size and plasma progesterone concentration in cows. Anim. Reprod. Sci. 115, 296–299.
| Corpus luteum size and plasma progesterone concentration in cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2iu7s%3D&md5=4e07b41a9b6ef1b72aa8ae15045007eaCAS | 19121900PubMed |
Mann, G. E., and Lamming, G. E. (2001). Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121, 175–180.
| Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslaqsw%3D%3D&md5=eacebfac4a9077c312223ef6fe1728a5CAS | 11226041PubMed |
Matsui, M., and Miyamoto, A. (2009). Evaluation of ovarian blood flow by colour Doppler ultrasound: practical use for reproductive management in the cow. Vet. J. 181, 232–240.
| Evaluation of ovarian blood flow by colour Doppler ultrasound: practical use for reproductive management in the cow.Crossref | GoogleScholarGoogle Scholar | 18693121PubMed |
Miyamoto, A., Shirasuna, K., and Sasahara, K. (2009). Local regulation of corpus luteum development and regression in the cow: impact of angiogenic and vasoactive factors. Domest. Anim. Endocrinol. 37, 159–169.
| Local regulation of corpus luteum development and regression in the cow: impact of angiogenic and vasoactive factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKgt77O&md5=a256fc96e51a90928bc0174b5dd99030CAS | 19592192PubMed |
Miyazaki, T., Tanaka, M., Miyakoshi, K., Minegishi, K., Kasai, K., and Yoshimura, Y. (1998). Power and colour Doppler ultrasonography for the evaluation of the vasculature of the human corpus luteum. Hum. Reprod. 13, 2836–2841.
| Power and colour Doppler ultrasonography for the evaluation of the vasculature of the human corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FhvFertQ%3D%3D&md5=06c175a47581050e8fbaef8b682e6faeCAS | 9804242PubMed |
Murdoch, W. J., and Van Kirk, E. A. (1998). Luteal dysfunction in ewes induced to ovulate early in the follicular phase. Endocrinology 139, 3480–3484.
| 1:CAS:528:DyaK1cXkvVGrtro%3D&md5=c3722ff3fec697f3e8cfc18e9e958046CAS | 9681498PubMed |
Perry, G. A., Smith, M. F., Roberts, A. J., MacNeil, M. D., and Geary, T. W. (2007). Relationship between size of the ovulatory follicle and pregnancy success in beef heifers. J. Anim. Sci. 85, 684–689.
| Relationship between size of the ovulatory follicle and pregnancy success in beef heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1WktL8%3D&md5=230ebbec9de229c9d4669adddf264896CAS | 17060416PubMed |
Pfeifer, L. F. M., Mapletoft, R. J., Kastelic, J. P., Small, J. A., Adams, G. P., Dionello, N. J., and Singh, J. (2009). Effects of low versus physiologic plasma progesterone concentrations on ovarian follicular development and fertility in beef cattle. Theriogenology 72, 1237–1250.
| Effects of low versus physiologic plasma progesterone concentrations on ovarian follicular development and fertility in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlCgtr3L&md5=8f4d6a55be7a6c134efb8cddbb14bf44CAS |
Sartori, R., Rosa, G. J. M., and Wiltbank, M. C. (2002). Ovarian structures and circulating steroids in heifers and lactating cows in summer and lactating and dry cows in winter. J. Dairy Sci. 85, 2813–2822.
| Ovarian structures and circulating steroids in heifers and lactating cows in summer and lactating and dry cows in winter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptlagsbk%3D&md5=c894487ed14d1af100fe73f8e19f0d69CAS | 12487448PubMed |
Shirasuna, K., Asahi, T., Sasaki, M., and Shimizu, T. (2010). Distribution of arteriolovenous vessels, capillaries and eNOS expression in the bovine corpus luteum during the estrous cycle: a possible implication of different sensitivity by luteal phase to PGF2α in the increase of luteal blood flow. J. Reprod. Dev. 56, 124–130.
| Distribution of arteriolovenous vessels, capillaries and eNOS expression in the bovine corpus luteum during the estrous cycle: a possible implication of different sensitivity by luteal phase to PGF2α in the increase of luteal blood flow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVymtro%3D&md5=931777c9f47b67496c4bbe0f05128ad9CAS | 19893278PubMed |
Siddiqui, M. A. R., Gastal, E. L., Gastal, M. O., Almamun, M., Beg, M. A., and Ginther, O. J. (2009a). Relationship of vascular perfusion of the wall of the preovulatory follicle to in vitro fertilisation and embryo development in heifers. Reproduction 137, 689–697.
| Relationship of vascular perfusion of the wall of the preovulatory follicle to in vitro fertilisation and embryo development in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2ntb0%3D&md5=fb0766bf217b63bd46692525d06e3702CAS |
Siddiqui, M. A. R., Almamun, M., and Ginther, O. J. (2009b). Blood flow in the wall of the preovulatory follicle and its relationship to pregnancy establishment in heifers. Anim. Reprod. Sci. 113, 287–292.
| Blood flow in the wall of the preovulatory follicle and its relationship to pregnancy establishment in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFelurw%3D&md5=f18cbf5b9447ed86eb786b81603131c4CAS |
Siddiqui, M. A. R., Gastal, E. L., Gastal, M. O., Beg, M. A., and Ginther, O. J. (2009c). Effect of hCG in the presence of hCG antibodies on the follicle, hormone concentrations, and oocyte in mares. Reprod. Domest. Anim. 44, 474–479.
| Effect of hCG in the presence of hCG antibodies on the follicle, hormone concentrations, and oocyte in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslKrtL0%3D&md5=62f6e838c0523bdf6b078248efa1b273CAS |
Siddiqui, M. A. R., Ferreira, J. C., Gastal, E. L., Beg, M. A., Cooper, D. A., and Ginther, O. J. (2010). Temporal relationships of the LH surge and ovulation to echotexture and power Doppler signals of blood flow in the wall of the preovulatory follicle in heifers. Reprod. Fertil. Dev. 22, 1110–1117.
| Temporal relationships of the LH surge and ovulation to echotexture and power Doppler signals of blood flow in the wall of the preovulatory follicle in heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjnvVSnuw%3D%3D&md5=124effd87a200699ba5ade78a711b897CAS |
Silva, L. A., Gastal, E. L., Gastal, M. O., Beg, M. A., and Ginther, O. J. (2006). Relationship between vascularity of the preovulatory follicle and establishment of pregnancy in mares. Anim. Reprod. 3, 339–346.
Taylor, R. (1990). Interpretation of the correlation coefficient: a basic review. J. Diagn. Med. Sonogr. 6, 35–39.
| Interpretation of the correlation coefficient: a basic review.Crossref | GoogleScholarGoogle Scholar |
Thijssen, J. M., Herzog, K., Weijers, G., Brockhan-Luedemann, M., Starke, A., Niemann, H., Bollwein, H., and de Korte, C. L. (2011). Ultrasound image analysis offers the opportunity to predict plasma progesterone concentrations in the estrous cycle in cows: a feasibility study. Anim. Reprod. Sci. 127, 7–15.
| Ultrasound image analysis offers the opportunity to predict plasma progesterone concentrations in the estrous cycle in cows: a feasibility study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKis7nF&md5=84b247c22126c14a78e1ce7d0c818d78CAS | 21835565PubMed |
Varughese, E. E., Brar, P. S., Honparkhe, M., and Ghuman, S. P. S. (2014). Correlation of blood flow of the preovulatory follicle to its diameter and endocrine profile in dairy buffalo. Reprod. Domest. Anim. 49, 140–144.
| Correlation of blood flow of the preovulatory follicle to its diameter and endocrine profile in dairy buffalo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVKqtb4%3D&md5=33996df4a7d8287a5d3eb96524678fefCAS | 24188698PubMed |
Vasconcelos, J. L. M., Sartori, R., Oliveira, H. N., Guenther, J. G., and Wiltbank, M. C. (2001). Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate. Theriogenology 56, 307–314.
| Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mvjt1ymtA%3D%3D&md5=3fd168994904d01ee93f6638fd0287adCAS |
Vasconcelos, J. L. M., Pereira, M. H. C., Meneghetti, M., Dias, C. C., Sá Filho, O. G., Peres, R. F. G., Rodrigues, A. D. P., and Wiltbank, M. C. (2013). Relationships between growth of the preovulatory follicle and gestation success in lactating dairy cows. Anim. Reprod. 10, 206–214.
Yung, M. C., Vandehaar, M. J., Fogwell, R. L., and Sharma, B. K. (1996). Effect of the energy balance and somatotropin on insulin-like growth factor I in serum and on weight and progesterone of corpus luteum in heifers. J. Anim. Sci. 74, 2239–2244.
| Effect of the energy balance and somatotropin on insulin-like growth factor I in serum and on weight and progesterone of corpus luteum in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xls1OmtLk%3D&md5=11289c6615aee321bbd9396c10c2ec7bCAS | 8880428PubMed |
