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Article history: The abilities of two different estradiol esters to induce ovulation in a timed AI (TAI) synchro-
Received 12 December 2013 nization protocol in suckled Bos indicus cows were evaluated. In Experiment 1 (synchrony of
Received in revised form ovulation), 31 cows were submitted to an estradiol/progestin-based synchronization pro-
20 September 2014
tocol (Day 0) and randomly assigned to one of three treatments at the time of progestin
Accepted 22 September 2014
Available online xxx
removal on Day 8: 0.5 or 1.0 mg of estradiol cypionate (EC) at that time or 1.0 mg of estradiol
benzoate (EB) 24 h later (Day 9). To determine the timing of ovulation, ultrasound exam-
inations were performed every 12 h from ear implant removal to 96 h after the removal.
Keywords:
Orthogonal comparisons were performed to determine the effects of estradiol ester and
Reproduction
Cattle the effects of the dose of EC on reproductive parameters. Although neither the E2 ester
Progesterone (P = 0.83) nor the dose of EC (P = 0.55) affected the ovulation rate, the interval from pro-
TAI gestin removal to ovulation was longer (P = 0.04) in EC-treated cows (1.0 mg EC = 71.1 ± 3.6
Nelore and 0.5 mg EC = 78.0 ± 3.5) than EB-treated cows (EB = 66.0 ± 2.3) was detected. Ovulation
in 0.5-mg-EC-treated cows was less synchronous than that in 1.0-mg-EC-treated cows (dis-
tribution curves compared using kurtosis). In Experiment 2 (pregnancy per AI; P/AI), 660
cows at two different locations received the same synchronization protocol (n = 361 at Farm
A and n = 299 at Farm B) and were treated with estradiol esters as in Experiment 1 [0.5 mg
EC (n = 220) or 1.0 mg EC (n = 219) at the time of progestin removal or 1.0 mg EB (n = 221)
24 h later]. The cows were inseminated 54 to 56 h after progestin removal. As applied in the
Experiment 1, orthogonal comparisons were performed to evaluate the effect of estradiol
ester and the dose of EC on P/AI. Although the type of estradiol ester used did not affect the
P/AI (P = 0.57; EB – 43.0% vs. EC – 44.6%), the P/AI was higher (P = 0.03) in cows treated with
∗ Corresponding author. Tel.: +55 98 3272 9902; fax: +55 98 3272 9902.
E-mail addresses: jrtorresjr@gmail.com (J.R.S. Torres-Júnior), barusell@usp.br (P.S. Baruselli).
http://dx.doi.org/10.1016/j.anireprosci.2014.09.019
0378-4320/© 2014 Published by Elsevier B.V.
Please cite this article in press as: Torres-Júnior, J.R.S., et al., A comparison of two different esters of estradiol for the
induction of ovulation in an estradiol plus progestin-based timed artificial insemination protocol for suckled Bos indicus
beef cows. Anim. Reprod. Sci. (2014), http://dx.doi.org/10.1016/j.anireprosci.2014.09.019
G Model
ANIREP-5068; No. of Pages 6 ARTICLE IN PRESS
2 J.R.S. Torres-Júnior et al. / Animal Reproduction Science xxx (2014) xxx–xxx
1.0 mg EC (55.7%) than in those treated with 0.5 mg EC (38.6%). In summary, the adminis-
tration of 0.5 mg EC at the time of progestin removal altered the distribution of ovulation
and resulted in a lower P/AI when compared with the use of 1.0 mg EC in suckled B. indicus
cows. However, the P/AI following the administration of 1.0 mg EC at the time of progestin
removal did not differ from that after the administration of 1.0 mg EB 24 h later.
© 2014 Published by Elsevier B.V.
Please cite this article in press as: Torres-Júnior, J.R.S., et al., A comparison of two different esters of estradiol for the
induction of ovulation in an estradiol plus progestin-based timed artificial insemination protocol for suckled Bos indicus
beef cows. Anim. Reprod. Sci. (2014), http://dx.doi.org/10.1016/j.anireprosci.2014.09.019
G Model
ANIREP-5068; No. of Pages 6 ARTICLE IN PRESS
J.R.S. Torres-Júnior et al. / Animal Reproduction Science xxx (2014) xxx–xxx 3
Progestin/Progesterone
Day 0 Day 8 Day 9 Day 10
0.5 mg EC
+
EC0.5 group 2mg EB PGF2α + eCG TAI
Progestin/Progesterone
Day 0 Day 8 Day 10
1.0 mg EC
+
EC1.0 group 2mg EB PGF2α + eCG TAI
Progestin/Progesterone
Day 0 Day 8 Day 10
Fig. 1. Experimental design of Experiments 1 and 2. At the initiation of the synchronization protocol (Day 0), cows received a Progestin ear implant or a
Progesterone intravaginal device in combination with 2 mg of estradiol benzoate (EB). Eight days later (Day 8), the implants/devices were removed, and
all animals received 0.150 mg of d-cloprostenol (PGF) and 400 IU of equine chorionic gonadotropin (eCG). Cows were randomly assigned to one of three
treatments: 1.0 mg of estradiol benzoate (EB) 24 h after implant/device removal or 0.5 mg or 1.0 mg of estradiol cypionate (EC) at ear implant removal. All
females were inseminated 48 h after implants/devices withdrawal.
and Jacarezinho, Parana state (Farm B; n = 299), which apart. To evaluate the follicular dynamics and the moment
are both in Brazil. Regardless of location, the cows were of ovulation, the ovaries were scanned every 12 h from
maintained on a Brachiaria brizantha pasture with free ear implant removal to 96 h after the removal. The three
access to mineralized salt and water. largest follicles from each ovary were identified, recorded
and measured. The moment of ovulation was defined as
2.2.2. Experimental design the time of disappearance of a previously identified domi-
Suckled cows were randomly assigned to the experi- nant follicle (DF) from one ultrasound examination to the
mental treatments [0.5 of EC (n = 220), 1.0 of EC (n = 219) next, minus 6 h (Gimenes et al., 2008). In Experiment 2, the
or 1.0 mg EB (n = 221)] as described above for Experiment cows were examined for pregnancy by transrectal ultra-
1. At Farm A, the cows received the same synchroniza- sonography 30 d after TAI. Pregnancy was characterized by
tion protocol using a norgestomet ear implant that had visualization of an embryo with a heartbeat. Pregnancy per
been previously used for nine days, as described above, AI (P/AI) was calculated as the number of pregnant cows
and at Farm B, an intravaginal progesterone device (CIDR® , 30 d after AI divided by the total number of inseminated
Zoetis Animal Health, Sao Paulo, Brazil) was used. Based cows.
on previous data obtained using suckled zebu cows, a
similar response was expected following the use of a 2.4. Statistical analysis
norgestomet implant (Farm A) or an intravaginal P4 device
(Farm B) for the TAI protocol (Baruselli et al., 2002). The Statistical analyses were performed using SAS (Statisti-
TAI was performed 52–56 h after progestin/progesterone cal Analysis Software 9.3, SAS Institute Inc., Cary, NC, USA).
source removal. Frozen-thawed semen from two previ- Orthogonal comparisons were performed to determine the
ously proven fertile bulls was used. A single bull and effects of estradiol ester (1.0 mg EB vs. 1.0 mg EC or 0.5 mg
technician were used for all TAIs at each farm. EC) and the effect of the dose of EC (1.0 mg EC vs. 0.5 mg EC)
on reproductive parameters. Binary responses [Experiment
2.3. Ultrasound examination 1 (Ovulation rate) and Experiment 2 (P/AI)] were analyzed
by logistic regression fitting a binary data distribution. The
In both experiments, a real-time ultrasonic scanner evaluated response variables were the diameter of the DF,
equipped with a 5.0-7.5 MHz linear transrectal transducer time of ovulation, and ovulation rate from Experiment 1
(Chison D500VET, Chison Medical Imaging, Co, China) was and P/AI from Experiment 2, using the GLIMMIX procedure
used. of SAS for both of them. Continuous data were previously
In the Experiment 1, anestrous status was determined tested for homogeneity and normality using Guide Data
following detection of the absence of corpus luteum after Analysis and were transformed if necessary. These data
two consecutive ultrasound exams performed 10 days were analyzed with models fitting a Gaussian distribution.
Please cite this article in press as: Torres-Júnior, J.R.S., et al., A comparison of two different esters of estradiol for the
induction of ovulation in an estradiol plus progestin-based timed artificial insemination protocol for suckled Bos indicus
beef cows. Anim. Reprod. Sci. (2014), http://dx.doi.org/10.1016/j.anireprosci.2014.09.019
G Model
ANIREP-5068; No. of Pages 6 ARTICLE IN PRESS
4 J.R.S. Torres-Júnior et al. / Animal Reproduction Science xxx (2014) xxx–xxx
Table 1
Effects of estradiol esters (type and dose) as ovulatory stimuli on the ovarian follicular response and pregnancy per AI of suckled Bos indicus cows subjected
to an estradiol plus progestin/progesterone-based TAI protocol.
Experiment 1
Number of cows 10 10 11 – –
DF diameter at ear implant removal (mm)b 8.1 ± 0.1 8.1 ± 0.0 8.0 ± 0.1 0.91 0.85
DF diameter 24 h after ear implant removal (mm) 11.6 ± 0.0 11.3 ± 0.1 11.4 ± 0.1 0.64 0.79
Ovulation rate (%) 80.0 70.0 81.8 0.83 0.55
Timing of ovulation
Mean (h)c 66.0 ± 2.3 71.1 ± 3.6 78.0 ± 3.5 0.04 0.14
Kurtosis 3.5 2.4 −1.7 – –
Experiment 2
Number of cows 221 219 220 – –
Pregnancy per AI, % 43.0 50.7 38.6 0.57 0.03
a
Treatment: Cows were randomly assigned at progestin implant removal into one of three treatments. Cows from cows from 0.5 mg or 1.0 mg of EC
groups received 0.5 or 1 mg of estradiol cypionate (EC) intramuscularly at ear implant removal. Cows from the 1 mg of BE group were treated with 1 mg of
EB 24 h after ear implant removal.
b
DF = dominant follicle.
c
Time of ovulation relative to ear implant removal.
Please cite this article in press as: Torres-Júnior, J.R.S., et al., A comparison of two different esters of estradiol for the
induction of ovulation in an estradiol plus progestin-based timed artificial insemination protocol for suckled Bos indicus
beef cows. Anim. Reprod. Sci. (2014), http://dx.doi.org/10.1016/j.anireprosci.2014.09.019
G Model
ANIREP-5068; No. of Pages 6 ARTICLE IN PRESS
J.R.S. Torres-Júnior et al. / Animal Reproduction Science xxx (2014) xxx–xxx 5
(P = 0.74) of the farm [Farm A = 44.8% (134/299) and Farm or an intravaginal P4 device for the TAI protocol (Baruselli
B = 43.5% (157/361)] on the P/AI. However, the adminis- et al., 2002), it is possible that the impact of dose of EC
tration of 0.5 mg EC at the time of ear implant removal as ovulatory stimulus on P/AI could be influenced by the
promoted a lower P/AI when compared with the use of progestin source. This hypothesis requires further study.
1.0 mg EC (P = 0.03; Table 1). Among the factors that influence reproductive success
following TAI protocols in beef cows, one primary effect
4. Discussion is the time during which insemination should take place
relative to ovulation. The effect of the timing of insemina-
This study demonstrated that a similar P/AI could be tion depends primarily on the lifespan of the spermatozoa
achieved following the use of EC or EB as an inducer of and on the viability of the oocyte in the female genital
ovulation in the synchronization of ovulation protocol for tract (Hunter and Wilmut, 1984). Several experiments have
TAI in B. indicus cows, confirming the current hypothesis. demonstrated that 6 h is the minimum time needed for
However, 0.5 mg EC administered at the time of progestin a viable sperm population capable of fertilization to pass
source removal altered the distribution of ovulation after through the oviduct (Hawk, 1983; Hunter and Wilmut,
implant removal and was associated with a reduction of 1984; Hawk, 1987). Regarding the oocyte, the most desir-
the P/AI compared to the administration of 1.0 mg EC in B. able period for fertilization appears to be between 6 and
indicus cows submitted to a progestin plus estradiol-based 10 h after ovulation (Brackett et al., 1980), and the probabil-
synchronization of ovulation protocol for TAI. ity of conception decreases (Dransfield et al., 1998; Roelofs
In the present study, cows treated with EC presented et al., 2006) when AI is performed near the time of ovula-
a longer interval from ear implant removal to ovulation tion (less than 6–12 h before ovulation). Additionally, the
than cows treated with EB 24 h after implant removal. In fertilization rate exponentially decreases when AI occurs
addition, the use of 0.5 mg EC promoted a reduced syn- after ovulation (Roelofs et al., 2006).
chronization of ovulation, which was in contrast to the Therefore, the lower P/AI in cows treated with 0.5 mg
effects observed in cows treated with EB or those treated EC that was observed in the present study could be related
with 1.0 mg of EC. The induction of an LH surge upon EC to the longer interval between ear implant removal and
and EB administration in ovariectomized B. indicus cows ovulation and to the greater spread of ovulation when com-
has been previously reported (Sales et al., 2012). These pared with the other inducers of ovulation that were used
authors demonstrated that 1.0 mg EC promoted a longer (1.0 mg EC and 1.0 mg EB). Thus, the timing of TAI could be
interval between its administration and the induction of considered early (30 h before ovulation) due to the delay
an LH surge when compared to 1.0-mg-EB-treated cows. and greater dispersion of the occurrence of ovulation found
The onset of the LH peak occurred 30.9 h earlier in the in cows treated with 0.5 mg EC. In this way, delaying timed
EB group than in the EC group (19.6 ± 1.2 vs. 50.5 ± 3.6 h AI from 48 to 72 h after PGF (2alpha) in the CoSynch pro-
post administration). Moreover, animals receiving EB as an tocol associated with supplementation with EC increased
ovulation-inducing agent had a shorter (P = 0.001) LH surge the proportion of lactating dairy cows displaying estrus at
duration (8.6 ± 0.2 vs. 16.5 ± 1.0 h). AI and pregnancy per AI (Hillegass et al., 2008). In beef
Although esterification of EC prolongs the half-life of (B. indicus) cows, the moment of ovulation and timed AI
17-estradiol, it appears to reduce its efficacy for synchro- in relation to P4 device removal may be similar between
nizing follicular development and ovulation, mainly when estradiol esters, provided that EB administration is delayed
used at low doses (Thundathil et al., 1998; Colazo et al., for 24 h, because the LH peak in this group occurred 30 h
2003). Likely, the sole use of 0.5 mg EC was not sufficient earlier than that in the EC group. This delay allowed sim-
to induce a consistent preovulatory LH surge and effec- ilar growth of the ovulatory follicles and pregnancy rates
tive synchronization of ovulation. Therefore, it is suggested at timed AI between cows receiving EB or EC (Sales et al.,
that the greater variation in the interovulatory interval 2012).
for 0.5-mg-CE-treated cows was due to additional individ- In conclusion, despite the differences in the timing of
ual effects of endogenous 17-estradiol produced by the ovulation relative to progestin source removal, a similar
dominant follicle of each cow or due to follicular respon- P/AI could be achieved with the use of 1.0 mg of EC at the
siveness to estrogens and other factors that upregulate time of progestin source removal or 1 mg of EB 24 h later
ovulation. Furthermore, we believe that the action of estra- in suckled B. indicus cows subjected to an estradiol plus
diol cypionate on ovulation induction in cattle occurs in a progestin-based TAI synchronization protocol. However,
dose/time-dependent manner. the administration of 0.5 mg EC at the time of progestin
In the current study, a similar P/AI was achieved with source removal resulted in lesser synchronization of ovu-
the use of 1 mg of EC at the time of ear implant removal or lation and a lower P/AI when compared with the use of
with the use of 1 mg of EB 24 h after ear implant removal; 1.0 mg EC.
however 0.5 mg of EC promoted lower result. Additionally,
similar P/AI using EB or EC (at implant removal or 24 h Conflicts of Interest
later, respectively) have been previously reported in Bos
taurus beef heifers (Colazo et al., 2003) and in B. indicus The authors whose names are listed immediately below
suckled beef cows (Sales et al., 2012). For the present data, certify that they have NO affiliations with or involvement in
it is important to highlight the use of different progestin any organization or entity with any financial interest (such
sources at each location. Despite previous studies describ- as honoraria; educational grants; participation in speakers’
ing similar P/AI following the use of a norgestomet implant bureaus; membership, employment, consultancies, stock
Please cite this article in press as: Torres-Júnior, J.R.S., et al., A comparison of two different esters of estradiol for the
induction of ovulation in an estradiol plus progestin-based timed artificial insemination protocol for suckled Bos indicus
beef cows. Anim. Reprod. Sci. (2014), http://dx.doi.org/10.1016/j.anireprosci.2014.09.019
G Model
ANIREP-5068; No. of Pages 6 ARTICLE IN PRESS
6 J.R.S. Torres-Júnior et al. / Animal Reproduction Science xxx (2014) xxx–xxx
ownership, or other equity interest; and expert testi- Macmillan, K.L., Segwagwe, B.V.E., Pino, C.S., 2003. Associations between
mony or patent-licensing arrangements), or non-financial the manipulation of patterns of follicular development and fertility in
cattle. Anim. Reprod. Sci. 78, 327–344.
interest (such as personal or professional relationships, Martins, C.M., Castricini, E.S.C., Sá Filho, M.F., Gimenes, L.U., Baruselli, P.S.,
affiliations, knowledge or beliefs) in the subject matter or 2005. Follicular dynamics of the Nelore cows treated with estradiol
materials discussed in this manuscript. cipionate or estradiol benzoate in timed artificial insemiantion proto-
cols. Acta Sci. Vet. 33, 285.
Peres, R.F.G., Júnior, I.C., Filho, O.G.S., Nogueira, G.P., Vasconcelos, J.L.M.,
Appendix A. Supplementary data 2009. Strategies to improve fertility in Bos indicus postpubertal heifers
and nonlactating cows submitted to fixed-time artificial insemination.
Theriogenology 72, 681–689.
Supplementary material related to this article can be
Rodgers, J.C., Bird, S.L., Larson, J.E., Dilorenzo, N., Dahlen, C.R., Dicostanzo,
found, in the online version, at http://dx.doi.org/10.1016/j. A., Lamb, G.C., 2012. An economic evaluation of estrous synchroniza-
anireprosci.2014.09.019. tion and timed artificial insemination in suckled beef cows. J. Anim.
Sci. 90, 4055–4062.
Roelofs, J.B., Graat, E.A.M., Mullaart, E., Soede, N.M., Voskamp-Harkema,
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Please cite this article in press as: Torres-Júnior, J.R.S., et al., A comparison of two different esters of estradiol for the
induction of ovulation in an estradiol plus progestin-based timed artificial insemination protocol for suckled Bos indicus
beef cows. Anim. Reprod. Sci. (2014), http://dx.doi.org/10.1016/j.anireprosci.2014.09.019