Theriogenology 136 (2019) 10e14

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Theriogenology
journal homepage: www.theriojournal.com

Relationships between antral follicle count, body condition, and

pregnancy rates after timed-AI in Bos indicus cattle

bio Lucas Zito de Moraes, Fa
Fa
bio Morotti, Camila Bortoliero Costa,
Paula Alvares Lunardelli, Marcelo Marcondes Seneda*
University of Londrina (UEL), Laboratory of Animal Reproduction, Londrina, PR, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: An experiment was performed to evaluate the association between the antral follicle count (AFC) plus
Received 12 December 2018 body condition score (BCS) and the pregnancy rate in Bos indicus undergoing timed artificial insemi-
Received in revised form nation (TAI). A total of 736 Nelore cows with BCSs ranging from 2 to 4 received a conventional protocol
9 June 2019
for TAI. On a random day of the estrous cycle (Day 0), all cows received an intravaginal P4 device and an
Accepted 10 June 2019
Available online 17 June 2019
intramuscular (i.m.) injection of 2.0 mg estradiol benzoate. On Day 8, the P4 device was removed, and
150 mg sodium D-cloprostenol, 300 IU equine chorionic gonadotrophin and 1.0 mg estradiol cypionate
were administered by i.m. injection. TAI was performed 48 h after P4 device removal, and pregnancy
Keywords:
Antral follicle count
diagnosis was performed by ultrasonography after 30 days. On Day 0, all cows were examined by ul-
Pregnancy rate trasonography to determine the AFC by counting the number of follicles >3 mm in diameter that were
TAI present in both ovaries and to evaluate the BCS (scale of 1e5). The cows were then classified based on
Body condition score their AFCs as those with low (
10 follicles), intermediate (11e29 follicles) and high AFC (30 follicles).
Furthermore, cows were classified as having low (2.0 to
2.9) and high (3.0 to
4.0) BCSs. The AFCs
and BCSs were analyzed using the generalized linear model, and the pregnancy rate was assessed with
the binary logistic regression model (P
0.05). The pregnancy rate was influenced (P < 0.05) by AFC and
BCS classification and by interactions (P ¼ 0.034) between these factors. Cows with a low AFC exhibited
higher a pregnancy rate than did cows with a high or an intermediate AFC (57.7% a, 47.9% b and 49.7% b,
P ¼ 0.008). Low BCS resulted in a higher pregnancy rate than did high BCS (55.2% vs. 50.4%, P ¼ 0.008).
Cows with a high BCS and a low AFC had a higher pregnancy rate (P < 0.05) than did those with a high
BCS and an intermediate or a high AFC (59.8%a, 48.0%b, and 38.0%b, respectively). An interaction (P < 0.05)
was observed between the AFC and BCS, and the pregnancy rate decreased significantly in cows with an
AFC > 30 and a BCS between 3 and 4. In conclusion, AFC and BCS classifications influence the pregnancy
rate of Bos indicus beef cattle subjected to TAI. In addition, an important interaction between these factors
was observed, namely, the lowest pregnancy rates were found in cows with high BCSs and high AFCs.
© 2019 Elsevier Inc. All rights reserved.

1. Introduction progesterone and estrogen than do indicus [6,7]. However, despite

In Bos indicus cattle three to four waves of follicular develop-
ment per estrous cycle are evident [1,2], whereas in Bos taurus,
there is a higher occurrence of two to three waves per estrous cycle
[3]. Bos indicus cattle also have more antral follicles in each follic-
ular wave than do Bos taurus [4,5]. In addition, taurine females have
exhibited greater ovulatory follicle diameter, mean corpus luteum
volume and serum concentrations of steroid hormones, namely,
* Corresponding author.
E-mail address: marcelo.seneda@uel.br (M.M. Seneda).
these characteristics, the antral follicle count (AFC) in Bos taurus
cattle appears to have a well-established positive relationship with
fertility [8e10], but this relationship is not yet well understood in
Bos indicus [11,12].
The AFC has been investigated in many studies, which have
described the relationship between the AFC classification and the
fertility, reproductive performance, and biotechnological efficiency
in cattle [8,12e16]. Thus, a high degree of reproducibility in the
number of antral follicles count has been observed in the same
individual through successive ultrasound evaluations [13,17,18].
However, there are variations in follicle populations between
individuals from the same subspecies [19], and follicles can be

https://doi.org/10.1016/j.theriogenology.2019.06.024
0093-691X/© 2019 Elsevier Inc. All rights reserved.
 F.L.Z. de Moraes et al. / Theriogenology 136 (2019) 10e14
measured and classified as low, intermediate or high AFC [13,14]. In
addition to individual variations, body conditions and sanitary
conditions, a high AFC is directly related to a high pregnancy rate in
Bos taurus cows [8,10]. Nonetheless, the results obtained with Bos
indicus appear to be contradictory with respect to this correlation
[11e13,20], and the same is true for Bos taurus cattle [16]. Therefore,
more research is needed to investigate the relationship between
the AFC and body condition score (BCS) on the reproductive per-
formance of Bos indicus cattle and reproductive biotechnologies.
The aim of this study was to evaluate whether AFC and BCS
variability can be related to the pregnancy rate of Bos indicus cows
(Nelore) subjected to an ovulation synchronization protocol for
timed artificial insemination (TAI).
2. Materials and methods
The present study was conducted in accordance with the ethics
and experimentation committee of the State University of Londrina
based on the federal law nº 11.794 as of October 08, 2008.
2.1. Location, animals and management
A total of 736 multiparous Nelore cows (Bos indicus), ranging in
age from 36 to 96 months and that had calved (up to 40 days
postpartum) were used. These cows were from a rural property
located at a latitude of 21 590 5500 S and a longitude of 49 270 2600
W at 486 m above sea level. All cows were pasture (Brachiaria bri-
zantha) raised with mineral salt ad libitum.
All females were subjected to a conventional ovulation syn-
chronization protocol for TAI, which started on a random day of the
estrous cycle, denoted Day 0 (D0).
2.2. Antral follicle count and experimental design
The AFC of each female was assessed at the beginning of the TAI
protocol by ultrasound with a transrectal linear transducer of
5 MHz (Aloka SSD-500, Aloka Co. Ltda., Tokyo, Japan). Both the right
and left ovaries (the pair) were evaluated to determine the total
number of antral follicles (follicles with diameters  3 mm), as
previously described [18,19].
To standardize the AFC, every ovary surface was evaluated from
the extremity towards the pedicle to more precisely determine the
number of antral follicles. On the same day as the AFC evaluation
and by the same technician, each animal was classified according to
its BCS on a scale of 1e5 [21], and only females with scores ranging
from 2 to 4 were selected.
2.3. Hormonal protocol for TAI and pregnancy diagnosis
The TAI protocol was started on a random day of the estrous
cycle (D0) by inserting an intravaginal P4 device (Cronipres® Mono
Dose M-24, Bioge
nesis Bago
, Buenos Aires, Argentina) associated
with 2.0 mg estradiol benzoate (EB; Bioestrogen®, Bioge
nesis Bago
,
Buenos Aires, Argentina) by intramuscular (i.m.) injection. After 8
days (D8), the P4 device was removed, and 150 mg sodium D-clo-
prostenol (PGF2a; Croniben® Bioge
nesis Bago
, Buenos Aires,
Argentina), 300 IU equine chorionic gonadotrophin (eCG, Novor-
mon®, MSD Animal Health, Sao Paulo, Brazil) and 1.0 mg estradiol
cypionate (EC; ECP®, Pfizer, Sao Paulo, Brazil) were administered by
i.m. injection. The TAI was performed 48 h after P4 device removal,
as shown in Fig. 1.
For pregnancy diagnosis, cows were evaluated by transrectal
ultrasound examination after 30 days of TAI, and pregnancy was
confirmed by visualizing the embryo vesicle containing a viable
embryo (with heartbeat). The pregnancy rate was calculated as the
11
total number of pregnant cows divided by the number of insemi-
nated cows.
2.4. Statistical analysis
For statistical analysis, groups were established from the mean
number (M) and standard deviation (SD) extracted from the total
antral follicle population of the 736 cows in this study. Cows with
low counts were defined as the population mean (approximately 20
follicles) minus 1 SD (approximately 10 follicles). A low AFC was
defined as
10 follicles (n ¼ 305). Cows exhibiting AFCs ranging
from 11 to
29 follicles constituted the intermediate group
(n ¼ 312). A high AFC was defined based on the population mean
plus 1 SD:  30 follicles (n ¼ 119).
The number of antral follicles and BCSs were analyzed using the
generalized linear model (GLM), including all variables and possible
interactions. These values are presented as mean and standard
deviation (M ± SD). Nominal categorical variables (e.g., the preg-
nancy rate from AFC and BCS groups) were analyzed with a binary
logistic regression model and were included as fixed effects; the
bull and management lot were included as random effects. All
possible interactions were considered. The pregnancy rates are
expressed as proportions. All statistical analyses were performed
using Minitab® 18.1.1 statistical software, adopting P
0.05 to
indicate significant effects of the categorical variables and their
interactions.
3. Results and discussion
The distribution frequency and classification of the AFCs and
BCSs groups observed in the present study are shown in Fig. 2. The
pregnancy rate in Nelore cows after conventional TAI was influ-
enced (P < 0.05) not only by the AFC classification (low, 57.7%a;
intermediate, 49.7%b; and high, 47.9%b) but also by the BCS classi-
fication (low, 55.2% and high, 50.4%; Table 1). Additionally, a sig-
nificant interaction (P < 0.05) between AFC and BCS resulted in
variations in the pregnancy rates of the groups (Table 2).
Data from the present study have confirmed that the pregnancy
rate in beef cattle (Bos indicus) can be affected (P < 0.05) not only by
AFC variability but also by BCS variation. However, to the best of our
knowledge, these data reflect a significant interaction between the
AFC and BCS classifications that may determine an important
variation in the pregnancy rate of cows subjected to TAI. Therefore,
from this interaction, we observed that the classification of AFCs
has a greater influence on cows with high BCSs (above 3) than on
those with low BCSs (less than 3). Although a larger follicles
diameter has been indicated for females with low AFC, the bio-
logical justification for the BCS interaction is not yet known, but
some metabolic influences may occur depending on the nutritional
status. Finally, from a practical standpoint, interactive assessment
of AFC and BCS can be strategically evaluated by determining the
variability in the pregnancy rate of cows subjected to TAI programs.
The data in the present study are very similar to those data
presented by Morotti et al. [13] and are different to those published
previously in terms of the relationship between AFC and female
fertility in TAI. In the last decade, a large number of studies have
been published on this subject [8,9,13,16,22]. In Bos taurus cattle,
there seems to be a consensus that a high AFC is highly advanta-
geous because a high number of antral follicles is correlated with
several characteristics that are linked to high female fertility
[8e10], such as a higher pregnancy rate following artificial
insemination (AI) and TAI [22,23], a higher number of embryos
produced in vivo and in vitro [14,15,17], better oocyte quality [8,18],
a higher progesterone concentration [24] and benefits with respect
to herd productivity [25].
12 F.L.Z. de Moraes et al. / Theriogenology 136 (2019) 10e14

Fig. 1. Hormonal protocol for timed artificial insemination (TAI) and experimental design used for the evaluation of pregnancy rate in Nelore cows with different antral follicle count
(AFC) and body condition score (BCS).
P4 - progesterone, EB - estradiol benzoate, PGF2a - sodium D-cloprostenol, eCG - equine chorionic gonadotrophin, EC - estradiol cypionate.

A number of studies in Bos indicus and crossed Bos indicus-
taurus animals have produced results that are consistent with the
findings in Bos taurus, at least with respect to embryonic produc-
tion. In other words, the performance of high-AFC donors has been
superior in donors with intermediate or low counts with respect to
the number of oocytes recovered or the number of embryos pro-
duced [14,17,18,26]. However, one study on the pregnancy rate
following TAI revealed that the AFC has no effect, showing similar
pregnancy rates among AFC groups (58.5, 48.6 and 51.9% for low,
intermediate or high AFC, respectively) [14], while others studies
have reported contradictory findings, showing a better reproduc-
tive performance with low AFC [12,13,16].
In the present study, the increase in the pregnancy rate of 8e10%
for cows with low AFC compared with those with an intermediate
or a high AFC is consistent with the data reported by Morotti et al.
[13], who reported pregnancy rates of 61.7%, 52.9% and 49.5% for
their low-, intermediate- and high-AFC groups, respectively.
Furthermore, by examining ovarian follicular dynamics, these au-
thors revealed that cows with low AFCs exhibited larger follicular
diameters at specific times of the TAI protocol (e.g., from Day 8 to
Day 10), and this factor may explain the higher pregnancy rate in
this group. Larger dominate follicles for TAI have been associated
with higher pregnancy rates, as dsecribed by Sa Filho et al. [27] and
Pfeifer et al. [28]. On the other hand, it is worth noting that these
studies were performed on Bos indicus cattle, and it is possible that
these conflicting data may result from differences between sub-
species [6,7,29,30], as the first studies of AFC were conducted with
Bos taurus animals. However, a recent study [16] with Holstein
cows also revealed higher fertility and productivity rates for low
AFC females. Therefore, despite the controversies on this subject
[11,12], at least with respect to pregnancy following insemination,
the results of the present study closely resemble the latest research
on the AFC.
Another factor that requires attention is the methodologies used
in published studies for classifications of subjects into low-, inter-
mediate- and high-AFC groups. There is no consensus on the nu-
merical limits for the number of antral follicles that determine the
AFC groups. For example, Burns et al. [19] and Jimenez-Krassel et al.
[16] used the following definitions for Bos taurus: low,
15 follicles;
intermediate, 16 to 24 follicles; and high,  25 follicles. Martinez
et al. [22] defined
20, 21 to 29, and 30 follicles as low, inter-
mediate, and high AFCs, respectively, and Santos et al. [14] applied

Fig. 2. Distribution frequency and classification of groups according to the antral follicle count (AFC) range and body condition score (BCS) in Bos indicus cows undergoing treatment
per an ovulation synchronization protocol for timed artificial insemination.
 F.L.Z. de Moraes et al. / Theriogenology 136 (2019) 10e14 13

Table 1
Effect of low (
10 follicles), intermediate (11e29 follicles) or high (30 follicles) antral follicle count (AFC) and low (2.0 to
2.9) or high (3.0 to
4.0) body condition score
(BCS) on the pregnancy rate of Bos indicus cows subjected to timed artificial insemination.

Groups AFC (mean ± SD) BCS (mean ± SD Pregnancy rate % (n/N)

AFC Low 7.7 ± 2.6c 2.6 ± 0.5b 57.7a (176/305)

Intermediate 18.0 ± 3.4b 2.7 ± 0.4a 49.7b (155/312)
High 38.0 ± 12.4a 2.8 ± 0.4a 47.9b (57/119)
P-value <0.0001 <0.001 0.008
BCS Low 15.2 ± 9.8 2.3 ± 0.3 55.2 (195/353)
High 18.3 ± 13.0 3.1 ± 0.2 50.4 (193/383)
P-value <0.0001 <0.0001 0.008

Values followed by superscripted lowercase letters (a, b) within the same column and the same variable indicate statistically significantly differences between groups (low,
intermediate and high AFC).

the following classification for Bos indicus: low,
10 follicles; in-
termediate, 16 to 20 follicles; and high,  25 follicles. However,
Morotti et al. [13] used a different classification, as follows: low,

15 follicles; intermediate, 20 to 40 follicles; and high,  45 follicles.
These variations in AFC groups among studies are a natural
result of differences in the herds being studied and reflect signifi-
cant variability in ovarian follicle counts. In the Brazil, one criterion
that has been used for the classification of groups is the calculation
of the mean and standard deviation from the number of antral
follicles evaluated throughout the herd [13,14]. Then, the value of
the mean plus one standard deviation is defined as the high-AFC
group, the mean minus one standard deviation is defined as the
low-AFC group, and the intervals between these are the limits for
the intermediate-AFC group. In contrast, studies outside of Brazil
have used <15, 16 to 24 and > 25 follicles for their low-, interme-
diate- and high-AFC groups, respectively [8,10,17,18,24,25]. This
divergence is certainly a challenge and reflects the need to develop
a standardized methodology so that the AFC can be widely used as a
reproducible and consistent reproductive tool.
In this study, postpartum cows with 2.0 to
2.9 BCSs exhibited
higher pregnancy rates than did those with 3.0 to
4.0 BCSs.
Curiously, this reproductive behavior does not follow the patterns
described by most reports in the literature regarding beef cattle. For
example, BCS is reported to have a positive effect on pregnancy
rates in lactating Nelore cows [31]. Some studies on beef cattle (Bos
indicus) subjected to TAI have reported that cows with a
score < 2.75 have lower pregnancy rates than those with a
BSC > 2.75 [27,32]. However, studies that were conducted specif-
ically with dairy cattle have reported a greater challenge to health
and fertility in cows with high BCSs during the postpartum period
due to metabolic changes [33,34]. Ingestion disorders and the high
metabolic rates of postpartum dairy cows are two of the primary
factors contributing to the negative energy balance [35,36]. Addi-
tionally, the associations among BCS, negative energy balance,
oocyte quality, hormone production, and metabolism, as well as
their relationships with low reproductive performance, are well
documented [33,35,37]. On the other hand, these associations are
poorly understood, particularly the relationship between BCS and
energy balance.
Considering the data of the present study, it is unclear why cows
with a high AFC and high BCS showed the worst result pregnancy
results. This may suggest that cows with the highest BCSs are less
able to maintain an adequate nutritional balance during the post-
partum period. Thus, as the large pastures in Brazil may be limited
in quantity and quality of forage, they can lead to challenges in
maintaining an appropriate energy balance in cows, depending on
their BCSs. This hypothesis needs to be tested, and these ideas just
speculations. Nevertheless, in this study, it is clear from the inter-
action between these factors (AFC and BCS) that the group of cows
with high AFCs and high BCSs have a drastically reduced pregnancy
rate, representing a drop of more than 20% compared to the group
with low AFCs and low BCSs. This relationship between AFC and
BCS has not been reported previously, but the challenges of having
a high AFC plus a high with BCSs and maintaining energy balance
may compromise reproductive performance in postpartum beef
cattle.
The proportion of animals in each AFC category is another factor
that should be considered. The high-AFC group was the least
populated in our study (16.17%; 119/736). Therefore, proportionally,
the number of animals in this group was small relative to those in
the other BCS groups for the comparison of the pregnancy rates
between the different groups. This proportion follows the same
pattern reported in other studies. Morotti et al. [9] found high AFCs
in 23.26% of indicus cattle (high: 119/834; intermediate: 397/834;
and low: 234/834) and Martinez et al. [22] found high AFCs 23.58%
of taurus cattle (high: 104/441; intermediate: 137/441; and low:
200/441). On the other hand, although the present study included a
smaller number of animals, the findings are biological relevant in
that the proportion of animals in the group with low BCSs and high
AFCs was almost 25% points higher than that of group with high
BCSs and high AFCs. More research on this subject is needed to
clarify the relationship between AFC and BCS.
4. Conclusion
In conclusion, the antral follicle count and body condition score

Table 2
Pregnancy rate from the interaction between antral follicle count (AFC; low, intermediate and high count) and body condition score (BCS; low and high) in Bos indicus cows
subjected to timed artificial insemination.

Group interaction for the pregnancy rate BCS % (n/N)

Low (2.0 to
2.9) High (3.0 to
4.0) P-value

AFC % (n/N) Low (
10 follicles) 55.9 (94/168) 59.8a (82/137) 0.492
Intermediate (11e29 follicles) 51.8 (71/137) 48.0b (84/175) 0.502
High (30 follicles) 62.5 (30/48) 38.0b (27/71) 0.008
P-value 0.424 0.008

Values followed by superscripted lowercase letters (a, b) within the same column indicate statistically significant differences between groups (low, intermediate and high
AFC).
14 F.L.Z. de Moraes et al. / Theriogenology 136 (2019) 10e14
classification have been shown to influence the pregnancy rate in
beef cattle submitted to TAI. In addition; AFC and BCS represents
important sources of variation for pregnancy rate, with the lowest
rate observed in cows with high condition scores and higher follicle
counts.
Conflicts of interest
The authors declare no conflicts of interest.
Acknowledgments
This work was supported by National Council for Scientific and
Technological Development CNPq 311129/2014-5.
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