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Embryo and cow factors affecting pregnancy per embryo transfer for multiple-service, lactating Holstein recipients

Embryo and cow factors affecting pregnancy per embryo transfer for multiple-service, lactating... Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 Embryo and cow factors affecting pregnancy per embryo transfer for multiple- service, lactating Holstein recipients ,† ,‡ Eliab Estrada-Cortés,* William G. Ortiz,* Ricardo C. Chebel,* Elizabeth A. Jannaman,* James I. Moss,* Fernanda Cavallari de Castro,|| Adriana M. Zolini,* Charles R. Staples,* and ,1, Peter J. Hansen* *Department of Animal Sciences, University of Florida, Gainesville, FL 32611-0910; Campo Experimental Centro Altos de Jalisco, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Tepatitlán de Morelos, Jalisco 47600, México; Department of Large Animal Clinical Sciences, University of Florida, || Gainesville, FL 32611-0910; and Departamento de Medicina Veterinária, Universidade de São Paulo, Pirassununga, São Paulo 13635-900, Brazil ABSTRACT: The objective was to determine and characteristics of recipients (average of 190 d whether pregnancy success after embryo transfer in milk at transfer) were evaluated. Pregnancy per (ET) during heat stress in multi-service Holstein ET was lower for cows receiving frozen embryos cows depends upon characteristics of the embryo or (7.0%; 3/43) than for cows receiving fresh embryos recipient. Female embryos produced in vitro were (26.7%; 32/120) but there were no differences cultured with either 0.0 (control) or 1.8 mM choline between various types of fresh embryo. Pregnancy chloride and transferred fresh. Fresh embryos of per ET was lower for cows diagnosed with metritis undetermined breed and frozen Holstein embryos in the early postpartum period (7.1%; 2/28) than were used when experimental embryos were insuf- for cows without metritis (24.4%; 33/135). In con- ficient. Embryos were transferred 8 d after the last clusion, the use of frozen/thawed embryos pro- GnRH injection of an ovulation synchronization duced in vitro and recipients which had metritis in program. Embryo type [frozen vs. fresh, choline the early postpartum period reduced the success of vs. control, unknown breed vs. (control + choline)] ET in multiple-service Holstein cows. Key words: embryo transfer, lactating cows, metritis © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For com- mercial re-use, please contact journals.permissions@oup.com Transl. Anim. Sci. 2019.3:60–65 doi: 10.1093/tas/txz009 cows (Tanabe et al., 1985; Rodriques et al., 2007; INTRODUCTION Block et al., 2010). Pregnancy success depends on Embryo transfer (ET) can be a valuable genetic characteristics of the embryo and the recipient. selection tool (Kaniyamattam et  al., 2017) and Embryos produced in vitro, for example, are less can enhance fertility during heat stress (Ambrose likely to establish pregnancy after transfer than et  al., 1999; Drost et  al., 1999; Stewart et  al., embryos produced in vivo (Ferraz et al., 2016) and 2010; Baruselli et  al., 2011) or in repeat-breeder culture of embryos with embryokines can increase pregnancies per transfer (Loureiro et  al., 2009; Corresponding author: pjhansen@ufl.edu Denicol et al., 2014). Cryopreservation can lower Received October 31, 2018. embryo survival (Drost et al., 1999; Stewart et al., Accepted February 2, 2019. 60 Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 ET success in multi-service cows 61 2010; Ferraz et al., 2016). Success of ET also may in milk. Pregnancy diagnosis was performed at 33 depend upon the incidence of disease among recip- d after AI by ultrasound. Cows diagnosed as non- ients (Ferraz et al., 2016; Ribeiro et al., 2016). pregnant received an injection of GnRH (100 µg; Herein, we describe an experiment to evaluate Fertagyl, Merck, Kenilworth, NJ), an injection of embryo and cow factors that affect pregnancy per PGF α (25  mg; Lutalyse, Zoetis, Kalamazoo, MI) ET in cows predisposed to infertility. The study pop- at day 7 and 8, a second injection of GnRH (100 µg) ulation was a group of lactating Holsteins insem- at day 9 (considered as day 0 of the new estrous inated unsuccessfully at least two times prior to cycle), and timed AI 24 h later. Cows enrolled in the enrollment. The experiment was performed during experiment were not inseminated. Rather, ET was heat stress. Embryos were produced in vitro using performed 8 d after last GnRH injection (day 17 ovaries obtained at an abattoir. The main embryo of the protocol). Only cows with a corpus luteum factors considered were whether the embryo was (≥15 mm) detected by ultrasonography (Easy Scan; transferred fresh or after freezing/thawing and BCF Technology, Livingston, Scotland) received an whether the culture medium used to produce embryo. Selected cows received an epidural injection embryos contained choline chloride. We tested of 5  mL of 2% (w/v) lidocaine (Aspen Veterinary choline chloride because it is a precursor of mem- Resources, Liberty, MO) and a single embryo was brane phospholipids and the methyl donor betaine randomly transferred transcervically into the uter- (Glier et  al., 2014) and because feeding ruminally ine horn ipsilateral to the corpus luteum. Pregnancy protected choline has been reported to improve fer- diagnosis was performed by transrectal ultrasonog- tility in Holstein cows (Ardalan et al., 2010; Zenobi raphy at day 33 after last GnRH. et  al., 2018). To date, effects of choline on preim- Each week, embryos were produced in vitro by plantation embryonic development have not been fertilization of oocytes with X-sorted semen. Media assessed. The cow factors considered were parity, (Ortega et  al., 2017) and procedures for in vitro milk production, days in milk, and previous occur- maturation, fertilization, and embryo culture were rence in the current lactation of metritis, retained done as described by Siqueira and Hansen (2016). placenta, mastitis, and other diseases. Exceptions to previously published procedures included addition of 50  µg/mL amikacin (Sigma- Aldrich, Saint Louis, MO) to prevent bacterial con- MATERIALS AND METHODS tamination caused by use of sexed-sorted semen. The medium for embryo culture was a proprietary All procedures involving cows were approved medium called BBH7 (Cooley Biotech, Gainesville, by the Animal Care and Use Committee of the FL; Block et  al., 2010) or synthetic oviduct fluid University of Florida and all methods were per- bovine embryo 2 (Ortega et al., 2017). formed in accordance with the relevant guidelines To test the effects of choline on embryo compe- and regulations. The experiment was conducted tence for establishment of pregnancy, embryos were between July 27 and October 12, 2017 at a commer- produced using cumulus-oocyte complexes (COC) cial dairy farm located in north Florida (Trenton, harvested from abattoir-derived ovaries of Holstein FL; 29°35′N, 82°51′W). Meteorological condi- cows located in California or Idaho (J. R. Simplot, tions during the experiment were characteristic of Boise, ID). The COC were shipped overnight in heat stress. Average temperature-humidity index at a portable incubator at 38.5  °C in groups of 30 1500 h (calculated using the formula of Ravagnolo in 2  mL tubes with Simplot maturation medium. and Misztal, 2000) at a nearby weather station for Upon arrival, COC were allowed to complete mat- 14-d intervals from July 14 to October 14 ranged uration for 24 h. Following maturation, COC were from 80.5 to 83.3. Cows enrolled in the experi- fertilized with X-sorted semen using one of three ment were multiparous and primiparous lactating Holstein sires (STGenetics, Navosota, TX) and for a Holstein cows with at least two previous insemina- coincubation period of 17 to 18 h. A single sire was tions (3.8 ± 0.8; range of 3 to 5). The average days used each week for both treatments. Embryos were in milk at the time of transfer were 190 d (range 117 produced on different occasions (n = 7 replicates). to 253 d). Cows were fed a total mixed ration ad Putative zygotes (i.e., oocytes exposed to sperm) libitum, were milked three times per day, and were were then cultured in groups of 30 in 50 µL drops housed in sand-bedded free-stall barns equipped of BBH7 culture medium at 38.5  °C in a humidi- with fans and sprinklers. fied atmosphere of 5% CO (v/v), 5% O (v/v), and The reproductive management involved use of 2 2 90% N (v/v). Putative zygotes were assigned ran- the DoubleOvsynch regimen (Souza et  al., 2008) domly to culture in medium containing 1.8  mM for first timed artificial insemination (AI) at 81 d Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 62 Estrada-Cortés et al. choline chloride (Sigma-Aldrich, Saint Louis, MO) blastocyst stage were analyzed by logistic regres- or medium with 1.8 mM sodium chloride (Sigma- sion fitted to a binomial distribution, using the Aldrich) as a control to ensure osmolarity was the GLIMMIX procedure of the Statistical Analysis same for both treatments. The concentration of cho- System version 9.4 (SAS Institute, Cary, NC). The line chloride tested was chosen because it is equiv- model included effects of choline treatment as a alent to the sum of concentrations of all forms of fixed effect and sire as a random effect. Pregnancy choline in blood plasma of lactating Holstein cows outcome (pregnant or nonpregnant) on day 33 after at 1  wk after calving (~1.3  mM; Artegoitia et  al., presumptive ovulation also was considered a bino- 2014) plus the incremental increase in total cho- mial variable and analyzed by logistic regression line concentration in blood plasma (0.5 mM) when using the GLIMMIX procedure of SAS. Factors Holstein cows were supplemented with ruminally evaluated from recipients were parity (≤2 vs. >2), protected choline during the transition period (M. days in milk (≤192 vs. >192 d), milk production at Zenobi and C.R.S., personal communication). The the test day closest to ET (≤40.8 vs. >40.8  kg/d), number of embryos transferred was 48 for choline diagnosis of metritis (presence of foul-smelling, and 56 for vehicle treatments. watery vaginal discharge, with or without fever, When the number of Holstein embryos pro- during the first 21 d in milk of the current lacta - duced for choline experiment were insufficient for tion), retained placenta, mastitis diagnosed within the number of synchronized recipients, recipients 30 d of ET, and other diseases (ketosis, digestive received either a frozen/thawed, in vitro produced and respiratory diseases) diagnosed at any point Holstein embryo produced by fertilization using between calving and pregnancy diagnosis. Embryo X-sorted semen (frozen; n = 43) or a fresh in vitro type included fresh control, fresh choline, embryos produced embryo (n = 16) produced using conven- of unknown breed, and frozen embryos. Sources tional semen from beef bulls (Angus, Simental, of variation with a P-value greater than 0.100 were and Polled Hereford) and oocytes from abattoir excluded from the final model. Orthogonal con - ovaries from cattle of undetermined breed. Both trasts were used to investigate the effects of embryo types of embryos were cultured in synthetic oviduct type [frozen vs. others, choline vs. control, unknown fluid bovine embryo 2. For frozen/thawed embryos, breed vs. (control + choline)]. blastocysts were washed in Vigro Holding Plus To further examine the effect of previous diag- Medium (Vetoquinol, Fort Worth, TX), immersed nosis of metritis on pregnancy outcome, an addi- in Vigro Ethylene Glycol Freeze Plus with Sucrose tional analysis was conducted using fresh embryos (Vetoquinol, Fort Worth, TX) for 10 to 15  min at only (to avoid potential confounding effect of cry- room temperature and individually loaded into a opreservation). The effect of previous diagnosis of 0.25  mL straw. Subsequently, straws were frozen metritis was analyzed using a one-tailed Wilcoxon’s as described by Valente et  al. (2016) using a pro- test with the NPAR1WAY procedure of SAS. grammable freezing machine (CL-5500, Cryologic, Victoria, Australia). RESULTS AND DISCUSSION Cleavage rate was evaluated at day 3 post-in- semination and blastocysts were evaluated at day The two major determinants of pregnancy suc- 7.5 post-insemination. Blastocysts were evaluated cess after ET were whether the embryo was fresh or according to the guidelines of the International frozen (P  =  0.007) and whether the recipient had Embryo Technology Society (Robertson and been previously diagnosed with metritis (P = 0.059; Nelson, 1998). Only blastocyst-stage embryos Fig. 1). Recipients that received a frozen embryo graded as 1 or 2 were transferred. Selected blasto- had a lower pregnancy per ET (3/43; 7.0%) than cysts were loaded into 0.25  mL straws containing recipients receiving a fresh embryo (32/120; 26.7%). transfer medium [HEPES-TALP + 10% (v/v) fetal Lower pregnancy success after transfer of fro- bovine serum + 50  µM dithithreitol from Sigma- zen/thawed embryos was expected because of the Aldrich], placed in a portable incubator (Biotherm often-reported poor survival of in vitro produced INC-12v; Cryologic) at 38.5 °C, and transported to embryos frozen using ethylene glycol (Ambrose the farm for transfer into recipients. Frozen embryos et  al., 1999; Drost et  al., 1999) or glycerol (Wurth were thawed for 5 s in air, 20 s in water at 29 °C, and et  al., 1994). There is, however, great variation in transferred directly while in the original straw. pregnancy success following transfer of frozen Effect of choline on percent of oocytes that embryos produced in vitro, probably due to differ- cleaved after fertilization, and the percent of ences in molecular characteristics of in vitro pro- oocytes and cleaved embryos that developed to the duced embryos between laboratories. For example, Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 ET success in multi-service cows 63 40.2% of in vitro produced embryos cryopreserved uterine disease was still present at the time of ET. in ethylene glycol established pregnancy after trans- One implication of these results is that use of ET fer (Valente et  al., 2016). Pregnancy per ET also to improve fertility of repeat-breeder cows (Tanabe was lower for recipients that had been diagnosed et  al., 1985; Rodriques et  al., 2007; Block et  al., previously with metritis (2/28; 7.1%) compared 2010) is likely to depend on the cause of the inher- with those that had not been diagnosed with metri- ent fertility and may not be effective for cows which tis (33/135; 24.4%). The negative effect of previous experienced metritis. diagnosis of metritis on pregnancy success was There were no effects (P > 0.10) on pregnancy observed regardless of whether a recipient received outcome when other recipient characteristics were a fresh or frozen embryo (Fig. 1). Further analysis examined (parity, days in milk, milk production, of pregnancy outcomes for cows receiving a fresh retained placenta, mastitis, and other diseases), embryo indicated that pregnancy per ET was lower possibly due to the small number of observations. (P = 0.027) for recipients that had been diagnosed In a study involving over 10,000 transfers, preg- previously with metritis (2/21; 9.5%) compared nancy per ET was lower for multiparous cows than with those that had not been diagnosed with metri- primiparous cows, lower for cows diagnosed with tis (30/99; 30.3%). metritis, slightly lower for recipients which expe- Ribeiro et al. (2016) reported that diagnosis of rienced calving problems and not associated with uterine or nonuterine diseases in the early postpar- milk yield at ET (Ferraz et al., 2016). tum period was associated with reduced pregnancy As shown in Table 1, there was no effect of addi- success after the first breeding by either AI or ET. tion of choline chloride to the culture medium on However, all recipients in the present study had the percent of oocytes that cleaved after fertiliza- at least two previous unsuccessful services before tion (P = 0.290), percent of oocytes becoming blas- enrollment in ET and were further in the post- tocysts (P = 0.490), or percent of cleaved embryos partum period (average  =  190 d in milk) than the that developed to the blastocyst stage (P = 0.326). cows in the study of Ribeiro et al. (2016). Thus, it is Pregnancy per ET was not affected (P = 0.284) by likely that metritis can either create a uterine envi- the presence of choline in culture medium (Table ronment hostile for the establishment of pregnancy 2). Numerically, pregnancy per ET was slightly for weeks after diagnosis or else that undiagnosed higher for cows receiving an embryo treatment with choline but the small number of cows precludes definitive conclusions. The absence of effects of choline on the com- petence of embryos to develop to blastocyst stage was striking because choline is a precursor of mem- brane phospholipids and its metabolite betaine is involved in DNA methylation (Glier et  al., 2014). The preimplantation embryo undergoes extensive cell proliferation and the eight-cell stage embryo undergoes re-methylation of DNA (Dobbs et  al., 2013), making phospholipids and methyl groups 0/7 30/99 2/21 33/135 2/28 3/36 critical for its development and pregnancy establish- No Metritis Metritis No Metritis Metritis No Metritis Metritis ment. Perhaps stores of choline and its metabolites Frozen embryosFresh embryos Total in the oocyte or de novo synthesis are adequate for Figure 1. Effects of previous diagnosis of metritis in the recipient the embryo to meet its needs. In mice, betaine is syn- and cryopreservation of the embryo on pregnancy per embryo transfer. thesized during oocyte development and is present Pregnancy outcome was affected by the comparison of fresh vs. frozen in the preimplantation embryo (McClatchie et  al., (P = 0.007) and whether the recipient had been previously diagnosed with metritis (P = 0.059). 2017). It also has been observed that transcripts Table 1. Effect of choline supplementation of embryo culture medium on in vitro production of blastocysts Variable Control Choline P-value Oocytes undergoing cleavage, % 72.9 ± 1.3 69.2 ± 1.3 0.290 Oocytes becoming blastocyst, % 17.2 ± 1.1 18.8 ± 1.1 0.490 Cleaved embryos becoming a blastocyst, % 24.6 ± 1.5 28.8 ± 1.6 0.326 Data are least-squares means ± SEM of results from seven replicates representing 1,335 (control) or 1,332 (choline) cumulus-oocyte complexes (choline). Translate basic science to industry innovation Pregnancy rate (%) Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 64 Estrada-Cortés et al. Artegoitia, V . M., J. L. Middleton, F. M. Harte, S. R. Campagna, Table 2.  Pregnancy per embryo transfer (fraction and M. J. de Veth. 2014. Choline and choline metabolite of cows pregnant) for recipients receiving fresh patterns and associations in blood and milk during lac- embryos produced in control medium or medium tation in dairy cows. PLoS One 9:e103412. doi:10.1371/ containing 1.8 mM choline chloride journal.pone.0103412 Baruselli,  P.  S., R.  M.  Ferreira, J.  N.  Sales, L.  U.  Gimenes, Treatment Metritis No metritis Total M.  F.  Sá  Filho, C.  M.  Martins, C.  A.  Rodrigues, Control 0% (0/11) 24.4% (11/45) 19.6% (11/56) and G.  A.  Bó. 2011. Timed embryo transfer pro- Choline 25% (2/8) 30.0% (12/40) 29.2% (14/48) grams for management of donor and recipient cat- tle. Theriogenology 76:1583–1593. doi:10.1016/j. theriogenology.2011.06.006 coding for enzymes involved in betaine and phos- Block, J., L. Bonilla, and P. J. Hansen. 2010. Efficacy of in vitro phatidylcholine synthesis are present during the embryo transfer in lactating dairy cows using fresh or vitri- preimplantation period in bovine embryos (Jiang fied embryos produced in a novel embryo culture medium. et al., 2014). In the present study, choline chloride J. Dairy Sci. 93:5234–5242. doi:10.3168/jds.2010-3443 was used to provide choline to the embryo but the Denicol, A. C., J. Block, D. E. Kelley, K. G. Pohler, K. B. Dobbs, main metabolite in the blood plasma of dairy cows C.  J.  Mortensen, M.  S.  Ortega, and P.  J.  Hansen. 2014. The WNT signaling antagonist Dickkopf-1 directs lineage is phosphatidylcholine (Artegoitia et  al., 2014). commitment and promotes survival of the preimplantation Perhaps, phosphatidylcholine is utilized differently embryo. FASEB J. 28:3975–3986. doi:10.1096/fj.14-253112 by the embryo than choline chloride. Dobbs, K. B., M. Rodriguez, M. J. Sudano, M. S. Ortega, and In conclusion, the use of frozen embryos pro- P. J. Hansen. 2013. Dynamics of DNA methylation during duced in vitro and recipients which had metritis in early development of the preimplantation bovine embryo. PLoS One 8:e66230. doi:10.1371/journal.pone.0066230 the early postpartum period reduced the success of Drost,  M., J.  D.  Ambrose, M.  J.  Thatcher, C.  K.  Cantrell, ET during the heat stress season in multiple-service K.  E.  Wolfsdorf, J.  F.  Hasler, and W.  W.  Thatcher. Holstein cows. The negative effect of metritis on 1999. Conception rates after artificial insemination or the success of ET was still present after long period embryo transfer in lactating dairy cows during summer from the diagnosis in the early postpartum. in Florida. Theriogenology 52:1161–1167. doi:10.1016/ S0093-691X(99)00208-3 Ferraz,  P.  A., C.  Burnley, J.  Karanja, A.  Viera-Neto, ACKNOWLEDGMENTS J.  E.  Santos, R.  C.  Chebel, and K.  N.  Galvão. 2016. The authors acknowledge the owners of Alliance Factors affecting the success of a large embryo transfer program in Holstein cattle in a commercial herd in the Dairies, Trenton, FL, for allowing us to conduct the Southeast region of the United States. Theriogenology embryo transfer trial, and the reproduction staff 86:1834–1841. doi:10.1016/j.theriogenology.2016.05.032 for support and assistance, especially N. Francisco Glier,  M.  B., T.  J.  Green, and A.  M.  Devlin. 2014. Methyl and B.  Velasquez. Thanks also are extended to nutrients, DNA methylation, and cardiovascular dis- M. Zenobi, C. Coriano, G. Adiyaman, S. Dikmen, ease. Mol. Nutr. Food Res. 58:172–182. doi:10.1002/ mnfr.201200636 P.  Tribulo, C.  Lopera, E.  Obesso, V.  Rocha, and Jiang,  Z., J.  Sun, H.  Dong, O.  Luo, X.  Zheng, C.  Obergfell, T. Vilar for technical assistance. Research was sup- Y.  Tang, J.  Bi, R.  O’Neill, Y.  Ruan, et  al. 2014. ported by the L.E. “Red” Larson Endowment and Transcriptional profiles of bovine in vivo pre-im - funding for E.E.-C. by CONACyT-México. plantation development. BMC Genomics 15:756. doi:10.1186/1471-2164-15-756 Conflict of interest statement: P.J.H.  has an Kaniyamattam,  K., J.  Block, P.  J.  Hansen, and A.  De  Vries. 2017. Economic and genetic performance of various ownership interest in Cooley Biotech, manufactur- combinations of in vitro-produced embryo transfers ers of BBH7 culture medium. and artificial insemination in a dairy herd. J. Dairy Sci. 101:1540–1553. doi:10.3168/jds.2017-13475 Loureiro, B., L. Bonilla, J. Block, J. M. Fear, A. Q. Bonilla, and LITERATURE CITED P.  J.  Hansen. 2009. 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Sex differences in 1284. doi:10.1016/0093-691X(94)90247-G response of the bovine embryo to colony-stimulating factor Zenobi,  M.  G., R.  Gardinal, J.  E.  Zuniga, A.  L.  G.  Dias, 2. Reproduction 152:645–654. doi:10.1530/REP-16-0336 C.  D.  Nelson, J.  P.  Driver, B.  A.  Barton, J.  E.  P.  Santos, Souza, A. H., H. Ayres, R. M. Ferreira, and M. C. Wiltbank. and C. R. Staples. 2018. Effects of supplementation with 2008. A new presynchronization system (Double- ruminally protected choline on performance of multip- Ovsynch) increases fertility at first postpartum timed arous Holstein cows did not depend upon prepartum AI in lactating dairy cows. Theriogenology 70:208–215. caloric intake. J. Dairy Sci. 101:1088–1110. doi:10.3168/ doi:10.1016/j.theriogenology.2008.03.014 jds.2017-13327 Translate basic science to industry innovation http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Translational Animal Science Oxford University Press

Embryo and cow factors affecting pregnancy per embryo transfer for multiple-service, lactating Holstein recipients

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Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 Embryo and cow factors affecting pregnancy per embryo transfer for multiple- service, lactating Holstein recipients ,† ,‡ Eliab Estrada-Cortés,* William G. Ortiz,* Ricardo C. Chebel,* Elizabeth A. Jannaman,* James I. Moss,* Fernanda Cavallari de Castro,|| Adriana M. Zolini,* Charles R. Staples,* and ,1, Peter J. Hansen* *Department of Animal Sciences, University of Florida, Gainesville, FL 32611-0910; Campo Experimental Centro Altos de Jalisco, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Tepatitlán de Morelos, Jalisco 47600, México; Department of Large Animal Clinical Sciences, University of Florida, || Gainesville, FL 32611-0910; and Departamento de Medicina Veterinária, Universidade de São Paulo, Pirassununga, São Paulo 13635-900, Brazil ABSTRACT: The objective was to determine and characteristics of recipients (average of 190 d whether pregnancy success after embryo transfer in milk at transfer) were evaluated. Pregnancy per (ET) during heat stress in multi-service Holstein ET was lower for cows receiving frozen embryos cows depends upon characteristics of the embryo or (7.0%; 3/43) than for cows receiving fresh embryos recipient. Female embryos produced in vitro were (26.7%; 32/120) but there were no differences cultured with either 0.0 (control) or 1.8 mM choline between various types of fresh embryo. Pregnancy chloride and transferred fresh. Fresh embryos of per ET was lower for cows diagnosed with metritis undetermined breed and frozen Holstein embryos in the early postpartum period (7.1%; 2/28) than were used when experimental embryos were insuf- for cows without metritis (24.4%; 33/135). In con- ficient. Embryos were transferred 8 d after the last clusion, the use of frozen/thawed embryos pro- GnRH injection of an ovulation synchronization duced in vitro and recipients which had metritis in program. Embryo type [frozen vs. fresh, choline the early postpartum period reduced the success of vs. control, unknown breed vs. (control + choline)] ET in multiple-service Holstein cows. Key words: embryo transfer, lactating cows, metritis © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For com- mercial re-use, please contact journals.permissions@oup.com Transl. Anim. Sci. 2019.3:60–65 doi: 10.1093/tas/txz009 cows (Tanabe et al., 1985; Rodriques et al., 2007; INTRODUCTION Block et al., 2010). Pregnancy success depends on Embryo transfer (ET) can be a valuable genetic characteristics of the embryo and the recipient. selection tool (Kaniyamattam et  al., 2017) and Embryos produced in vitro, for example, are less can enhance fertility during heat stress (Ambrose likely to establish pregnancy after transfer than et  al., 1999; Drost et  al., 1999; Stewart et  al., embryos produced in vivo (Ferraz et al., 2016) and 2010; Baruselli et  al., 2011) or in repeat-breeder culture of embryos with embryokines can increase pregnancies per transfer (Loureiro et  al., 2009; Corresponding author: pjhansen@ufl.edu Denicol et al., 2014). Cryopreservation can lower Received October 31, 2018. embryo survival (Drost et al., 1999; Stewart et al., Accepted February 2, 2019. 60 Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 ET success in multi-service cows 61 2010; Ferraz et al., 2016). Success of ET also may in milk. Pregnancy diagnosis was performed at 33 depend upon the incidence of disease among recip- d after AI by ultrasound. Cows diagnosed as non- ients (Ferraz et al., 2016; Ribeiro et al., 2016). pregnant received an injection of GnRH (100 µg; Herein, we describe an experiment to evaluate Fertagyl, Merck, Kenilworth, NJ), an injection of embryo and cow factors that affect pregnancy per PGF α (25  mg; Lutalyse, Zoetis, Kalamazoo, MI) ET in cows predisposed to infertility. The study pop- at day 7 and 8, a second injection of GnRH (100 µg) ulation was a group of lactating Holsteins insem- at day 9 (considered as day 0 of the new estrous inated unsuccessfully at least two times prior to cycle), and timed AI 24 h later. Cows enrolled in the enrollment. The experiment was performed during experiment were not inseminated. Rather, ET was heat stress. Embryos were produced in vitro using performed 8 d after last GnRH injection (day 17 ovaries obtained at an abattoir. The main embryo of the protocol). Only cows with a corpus luteum factors considered were whether the embryo was (≥15 mm) detected by ultrasonography (Easy Scan; transferred fresh or after freezing/thawing and BCF Technology, Livingston, Scotland) received an whether the culture medium used to produce embryo. Selected cows received an epidural injection embryos contained choline chloride. We tested of 5  mL of 2% (w/v) lidocaine (Aspen Veterinary choline chloride because it is a precursor of mem- Resources, Liberty, MO) and a single embryo was brane phospholipids and the methyl donor betaine randomly transferred transcervically into the uter- (Glier et  al., 2014) and because feeding ruminally ine horn ipsilateral to the corpus luteum. Pregnancy protected choline has been reported to improve fer- diagnosis was performed by transrectal ultrasonog- tility in Holstein cows (Ardalan et al., 2010; Zenobi raphy at day 33 after last GnRH. et  al., 2018). To date, effects of choline on preim- Each week, embryos were produced in vitro by plantation embryonic development have not been fertilization of oocytes with X-sorted semen. Media assessed. The cow factors considered were parity, (Ortega et  al., 2017) and procedures for in vitro milk production, days in milk, and previous occur- maturation, fertilization, and embryo culture were rence in the current lactation of metritis, retained done as described by Siqueira and Hansen (2016). placenta, mastitis, and other diseases. Exceptions to previously published procedures included addition of 50  µg/mL amikacin (Sigma- Aldrich, Saint Louis, MO) to prevent bacterial con- MATERIALS AND METHODS tamination caused by use of sexed-sorted semen. The medium for embryo culture was a proprietary All procedures involving cows were approved medium called BBH7 (Cooley Biotech, Gainesville, by the Animal Care and Use Committee of the FL; Block et  al., 2010) or synthetic oviduct fluid University of Florida and all methods were per- bovine embryo 2 (Ortega et al., 2017). formed in accordance with the relevant guidelines To test the effects of choline on embryo compe- and regulations. The experiment was conducted tence for establishment of pregnancy, embryos were between July 27 and October 12, 2017 at a commer- produced using cumulus-oocyte complexes (COC) cial dairy farm located in north Florida (Trenton, harvested from abattoir-derived ovaries of Holstein FL; 29°35′N, 82°51′W). Meteorological condi- cows located in California or Idaho (J. R. Simplot, tions during the experiment were characteristic of Boise, ID). The COC were shipped overnight in heat stress. Average temperature-humidity index at a portable incubator at 38.5  °C in groups of 30 1500 h (calculated using the formula of Ravagnolo in 2  mL tubes with Simplot maturation medium. and Misztal, 2000) at a nearby weather station for Upon arrival, COC were allowed to complete mat- 14-d intervals from July 14 to October 14 ranged uration for 24 h. Following maturation, COC were from 80.5 to 83.3. Cows enrolled in the experi- fertilized with X-sorted semen using one of three ment were multiparous and primiparous lactating Holstein sires (STGenetics, Navosota, TX) and for a Holstein cows with at least two previous insemina- coincubation period of 17 to 18 h. A single sire was tions (3.8 ± 0.8; range of 3 to 5). The average days used each week for both treatments. Embryos were in milk at the time of transfer were 190 d (range 117 produced on different occasions (n = 7 replicates). to 253 d). Cows were fed a total mixed ration ad Putative zygotes (i.e., oocytes exposed to sperm) libitum, were milked three times per day, and were were then cultured in groups of 30 in 50 µL drops housed in sand-bedded free-stall barns equipped of BBH7 culture medium at 38.5  °C in a humidi- with fans and sprinklers. fied atmosphere of 5% CO (v/v), 5% O (v/v), and The reproductive management involved use of 2 2 90% N (v/v). Putative zygotes were assigned ran- the DoubleOvsynch regimen (Souza et  al., 2008) domly to culture in medium containing 1.8  mM for first timed artificial insemination (AI) at 81 d Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 62 Estrada-Cortés et al. choline chloride (Sigma-Aldrich, Saint Louis, MO) blastocyst stage were analyzed by logistic regres- or medium with 1.8 mM sodium chloride (Sigma- sion fitted to a binomial distribution, using the Aldrich) as a control to ensure osmolarity was the GLIMMIX procedure of the Statistical Analysis same for both treatments. The concentration of cho- System version 9.4 (SAS Institute, Cary, NC). The line chloride tested was chosen because it is equiv- model included effects of choline treatment as a alent to the sum of concentrations of all forms of fixed effect and sire as a random effect. Pregnancy choline in blood plasma of lactating Holstein cows outcome (pregnant or nonpregnant) on day 33 after at 1  wk after calving (~1.3  mM; Artegoitia et  al., presumptive ovulation also was considered a bino- 2014) plus the incremental increase in total cho- mial variable and analyzed by logistic regression line concentration in blood plasma (0.5 mM) when using the GLIMMIX procedure of SAS. Factors Holstein cows were supplemented with ruminally evaluated from recipients were parity (≤2 vs. >2), protected choline during the transition period (M. days in milk (≤192 vs. >192 d), milk production at Zenobi and C.R.S., personal communication). The the test day closest to ET (≤40.8 vs. >40.8  kg/d), number of embryos transferred was 48 for choline diagnosis of metritis (presence of foul-smelling, and 56 for vehicle treatments. watery vaginal discharge, with or without fever, When the number of Holstein embryos pro- during the first 21 d in milk of the current lacta - duced for choline experiment were insufficient for tion), retained placenta, mastitis diagnosed within the number of synchronized recipients, recipients 30 d of ET, and other diseases (ketosis, digestive received either a frozen/thawed, in vitro produced and respiratory diseases) diagnosed at any point Holstein embryo produced by fertilization using between calving and pregnancy diagnosis. Embryo X-sorted semen (frozen; n = 43) or a fresh in vitro type included fresh control, fresh choline, embryos produced embryo (n = 16) produced using conven- of unknown breed, and frozen embryos. Sources tional semen from beef bulls (Angus, Simental, of variation with a P-value greater than 0.100 were and Polled Hereford) and oocytes from abattoir excluded from the final model. Orthogonal con - ovaries from cattle of undetermined breed. Both trasts were used to investigate the effects of embryo types of embryos were cultured in synthetic oviduct type [frozen vs. others, choline vs. control, unknown fluid bovine embryo 2. For frozen/thawed embryos, breed vs. (control + choline)]. blastocysts were washed in Vigro Holding Plus To further examine the effect of previous diag- Medium (Vetoquinol, Fort Worth, TX), immersed nosis of metritis on pregnancy outcome, an addi- in Vigro Ethylene Glycol Freeze Plus with Sucrose tional analysis was conducted using fresh embryos (Vetoquinol, Fort Worth, TX) for 10 to 15  min at only (to avoid potential confounding effect of cry- room temperature and individually loaded into a opreservation). The effect of previous diagnosis of 0.25  mL straw. Subsequently, straws were frozen metritis was analyzed using a one-tailed Wilcoxon’s as described by Valente et  al. (2016) using a pro- test with the NPAR1WAY procedure of SAS. grammable freezing machine (CL-5500, Cryologic, Victoria, Australia). RESULTS AND DISCUSSION Cleavage rate was evaluated at day 3 post-in- semination and blastocysts were evaluated at day The two major determinants of pregnancy suc- 7.5 post-insemination. Blastocysts were evaluated cess after ET were whether the embryo was fresh or according to the guidelines of the International frozen (P  =  0.007) and whether the recipient had Embryo Technology Society (Robertson and been previously diagnosed with metritis (P = 0.059; Nelson, 1998). Only blastocyst-stage embryos Fig. 1). Recipients that received a frozen embryo graded as 1 or 2 were transferred. Selected blasto- had a lower pregnancy per ET (3/43; 7.0%) than cysts were loaded into 0.25  mL straws containing recipients receiving a fresh embryo (32/120; 26.7%). transfer medium [HEPES-TALP + 10% (v/v) fetal Lower pregnancy success after transfer of fro- bovine serum + 50  µM dithithreitol from Sigma- zen/thawed embryos was expected because of the Aldrich], placed in a portable incubator (Biotherm often-reported poor survival of in vitro produced INC-12v; Cryologic) at 38.5 °C, and transported to embryos frozen using ethylene glycol (Ambrose the farm for transfer into recipients. Frozen embryos et  al., 1999; Drost et  al., 1999) or glycerol (Wurth were thawed for 5 s in air, 20 s in water at 29 °C, and et  al., 1994). There is, however, great variation in transferred directly while in the original straw. pregnancy success following transfer of frozen Effect of choline on percent of oocytes that embryos produced in vitro, probably due to differ- cleaved after fertilization, and the percent of ences in molecular characteristics of in vitro pro- oocytes and cleaved embryos that developed to the duced embryos between laboratories. For example, Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 ET success in multi-service cows 63 40.2% of in vitro produced embryos cryopreserved uterine disease was still present at the time of ET. in ethylene glycol established pregnancy after trans- One implication of these results is that use of ET fer (Valente et  al., 2016). Pregnancy per ET also to improve fertility of repeat-breeder cows (Tanabe was lower for recipients that had been diagnosed et  al., 1985; Rodriques et  al., 2007; Block et  al., previously with metritis (2/28; 7.1%) compared 2010) is likely to depend on the cause of the inher- with those that had not been diagnosed with metri- ent fertility and may not be effective for cows which tis (33/135; 24.4%). The negative effect of previous experienced metritis. diagnosis of metritis on pregnancy success was There were no effects (P > 0.10) on pregnancy observed regardless of whether a recipient received outcome when other recipient characteristics were a fresh or frozen embryo (Fig. 1). Further analysis examined (parity, days in milk, milk production, of pregnancy outcomes for cows receiving a fresh retained placenta, mastitis, and other diseases), embryo indicated that pregnancy per ET was lower possibly due to the small number of observations. (P = 0.027) for recipients that had been diagnosed In a study involving over 10,000 transfers, preg- previously with metritis (2/21; 9.5%) compared nancy per ET was lower for multiparous cows than with those that had not been diagnosed with metri- primiparous cows, lower for cows diagnosed with tis (30/99; 30.3%). metritis, slightly lower for recipients which expe- Ribeiro et al. (2016) reported that diagnosis of rienced calving problems and not associated with uterine or nonuterine diseases in the early postpar- milk yield at ET (Ferraz et al., 2016). tum period was associated with reduced pregnancy As shown in Table 1, there was no effect of addi- success after the first breeding by either AI or ET. tion of choline chloride to the culture medium on However, all recipients in the present study had the percent of oocytes that cleaved after fertiliza- at least two previous unsuccessful services before tion (P = 0.290), percent of oocytes becoming blas- enrollment in ET and were further in the post- tocysts (P = 0.490), or percent of cleaved embryos partum period (average  =  190 d in milk) than the that developed to the blastocyst stage (P = 0.326). cows in the study of Ribeiro et al. (2016). Thus, it is Pregnancy per ET was not affected (P = 0.284) by likely that metritis can either create a uterine envi- the presence of choline in culture medium (Table ronment hostile for the establishment of pregnancy 2). Numerically, pregnancy per ET was slightly for weeks after diagnosis or else that undiagnosed higher for cows receiving an embryo treatment with choline but the small number of cows precludes definitive conclusions. The absence of effects of choline on the com- petence of embryos to develop to blastocyst stage was striking because choline is a precursor of mem- brane phospholipids and its metabolite betaine is involved in DNA methylation (Glier et  al., 2014). The preimplantation embryo undergoes extensive cell proliferation and the eight-cell stage embryo undergoes re-methylation of DNA (Dobbs et  al., 2013), making phospholipids and methyl groups 0/7 30/99 2/21 33/135 2/28 3/36 critical for its development and pregnancy establish- No Metritis Metritis No Metritis Metritis No Metritis Metritis ment. Perhaps stores of choline and its metabolites Frozen embryosFresh embryos Total in the oocyte or de novo synthesis are adequate for Figure 1. Effects of previous diagnosis of metritis in the recipient the embryo to meet its needs. In mice, betaine is syn- and cryopreservation of the embryo on pregnancy per embryo transfer. thesized during oocyte development and is present Pregnancy outcome was affected by the comparison of fresh vs. frozen in the preimplantation embryo (McClatchie et  al., (P = 0.007) and whether the recipient had been previously diagnosed with metritis (P = 0.059). 2017). It also has been observed that transcripts Table 1. Effect of choline supplementation of embryo culture medium on in vitro production of blastocysts Variable Control Choline P-value Oocytes undergoing cleavage, % 72.9 ± 1.3 69.2 ± 1.3 0.290 Oocytes becoming blastocyst, % 17.2 ± 1.1 18.8 ± 1.1 0.490 Cleaved embryos becoming a blastocyst, % 24.6 ± 1.5 28.8 ± 1.6 0.326 Data are least-squares means ± SEM of results from seven replicates representing 1,335 (control) or 1,332 (choline) cumulus-oocyte complexes (choline). Translate basic science to industry innovation Pregnancy rate (%) Downloaded from https://academic.oup.com/tas/article-abstract/3/1/60/5373008 by Ed 'DeepDyve' Gillespie user on 18 October 2019 64 Estrada-Cortés et al. Artegoitia, V . M., J. L. Middleton, F. M. Harte, S. R. Campagna, Table 2.  Pregnancy per embryo transfer (fraction and M. J. de Veth. 2014. Choline and choline metabolite of cows pregnant) for recipients receiving fresh patterns and associations in blood and milk during lac- embryos produced in control medium or medium tation in dairy cows. PLoS One 9:e103412. doi:10.1371/ containing 1.8 mM choline chloride journal.pone.0103412 Baruselli,  P.  S., R.  M.  Ferreira, J.  N.  Sales, L.  U.  Gimenes, Treatment Metritis No metritis Total M.  F.  Sá  Filho, C.  M.  Martins, C.  A.  Rodrigues, Control 0% (0/11) 24.4% (11/45) 19.6% (11/56) and G.  A.  Bó. 2011. Timed embryo transfer pro- Choline 25% (2/8) 30.0% (12/40) 29.2% (14/48) grams for management of donor and recipient cat- tle. Theriogenology 76:1583–1593. doi:10.1016/j. theriogenology.2011.06.006 coding for enzymes involved in betaine and phos- Block, J., L. Bonilla, and P. J. Hansen. 2010. Efficacy of in vitro phatidylcholine synthesis are present during the embryo transfer in lactating dairy cows using fresh or vitri- preimplantation period in bovine embryos (Jiang fied embryos produced in a novel embryo culture medium. et al., 2014). In the present study, choline chloride J. Dairy Sci. 93:5234–5242. doi:10.3168/jds.2010-3443 was used to provide choline to the embryo but the Denicol, A. C., J. Block, D. E. Kelley, K. G. Pohler, K. B. Dobbs, main metabolite in the blood plasma of dairy cows C.  J.  Mortensen, M.  S.  Ortega, and P.  J.  Hansen. 2014. The WNT signaling antagonist Dickkopf-1 directs lineage is phosphatidylcholine (Artegoitia et  al., 2014). commitment and promotes survival of the preimplantation Perhaps, phosphatidylcholine is utilized differently embryo. FASEB J. 28:3975–3986. doi:10.1096/fj.14-253112 by the embryo than choline chloride. Dobbs, K. B., M. Rodriguez, M. J. Sudano, M. S. Ortega, and In conclusion, the use of frozen embryos pro- P. J. Hansen. 2013. Dynamics of DNA methylation during duced in vitro and recipients which had metritis in early development of the preimplantation bovine embryo. PLoS One 8:e66230. doi:10.1371/journal.pone.0066230 the early postpartum period reduced the success of Drost,  M., J.  D.  Ambrose, M.  J.  Thatcher, C.  K.  Cantrell, ET during the heat stress season in multiple-service K.  E.  Wolfsdorf, J.  F.  Hasler, and W.  W.  Thatcher. Holstein cows. The negative effect of metritis on 1999. Conception rates after artificial insemination or the success of ET was still present after long period embryo transfer in lactating dairy cows during summer from the diagnosis in the early postpartum. in Florida. Theriogenology 52:1161–1167. doi:10.1016/ S0093-691X(99)00208-3 Ferraz,  P.  A., C.  Burnley, J.  Karanja, A.  Viera-Neto, ACKNOWLEDGMENTS J.  E.  Santos, R.  C.  Chebel, and K.  N.  Galvão. 2016. The authors acknowledge the owners of Alliance Factors affecting the success of a large embryo transfer program in Holstein cattle in a commercial herd in the Dairies, Trenton, FL, for allowing us to conduct the Southeast region of the United States. Theriogenology embryo transfer trial, and the reproduction staff 86:1834–1841. doi:10.1016/j.theriogenology.2016.05.032 for support and assistance, especially N. Francisco Glier,  M.  B., T.  J.  Green, and A.  M.  Devlin. 2014. Methyl and B.  Velasquez. Thanks also are extended to nutrients, DNA methylation, and cardiovascular dis- M. Zenobi, C. Coriano, G. Adiyaman, S. Dikmen, ease. Mol. Nutr. Food Res. 58:172–182. doi:10.1002/ mnfr.201200636 P.  Tribulo, C.  Lopera, E.  Obesso, V.  Rocha, and Jiang,  Z., J.  Sun, H.  Dong, O.  Luo, X.  Zheng, C.  Obergfell, T. Vilar for technical assistance. Research was sup- Y.  Tang, J.  Bi, R.  O’Neill, Y.  Ruan, et  al. 2014. ported by the L.E. “Red” Larson Endowment and Transcriptional profiles of bovine in vivo pre-im - funding for E.E.-C. by CONACyT-México. plantation development. BMC Genomics 15:756. doi:10.1186/1471-2164-15-756 Conflict of interest statement: P.J.H.  has an Kaniyamattam,  K., J.  Block, P.  J.  Hansen, and A.  De  Vries. 2017. Economic and genetic performance of various ownership interest in Cooley Biotech, manufactur- combinations of in vitro-produced embryo transfers ers of BBH7 culture medium. and artificial insemination in a dairy herd. J. Dairy Sci. 101:1540–1553. doi:10.3168/jds.2017-13475 Loureiro, B., L. Bonilla, J. Block, J. M. Fear, A. Q. Bonilla, and LITERATURE CITED P.  J.  Hansen. 2009. 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