Investigação, 15(4):47-53, 2016
PAPER REVIEW
| ANIMAL REPRODUCTION
PUBERTY IN HEIFERS AND
PREMATURE LUTEOLYSIS IN THE
FIRST ESTROUS CYCLE
UNESP – Universidade Estadual Paulista “Júlio de Mesquita Filho” – UNESP Jaboticabal, São Paulo, Brasil.
1
Universidade Estadual do Centro-Oeste – UNICENTRO Guarapuava, Paraná, Brasil.
2
Universidade de Franca – UNIFRAN Franca, São Paulo, Brasil.
3
M.V. Dayane P. Vrisman , M.V. Eliza M. de S. R. Pedroso , M.V. Augusto R. Taira , Aulo H. Araújo , M.V.
Luisa P. B. Borges3, M.V. MsCc. Dr. Felipe F. P. da C. Barros3, M.V. Msc. Dr. Maria Emilia F. Oliveira1, M.V.
Msc. Dr. Pedro Paulo Maia Teixeira4.
1*
2
1
3
Universidade Federal do Pará – UFPA Pará, Belém, Brasil.
4
Departamento de Medicina Veterinária Preventiva e Reprodução Animal, Via de Acesso Prof. Paulo Donato Castellane s/n, CEP:14884-900,
Jaboticabal – SP. Email: [email protected]
*
RESUMO
ABSTRACT
A puberdade é o marco inicial do processo reprodutivo e produtivo, sendo um processo gradual de aquisição de
competência reprodutiva, iniciando-se durante o período gestacional e terminando com o início da puberdade da fêmea.
Sob o ponto de vista hormonal, corresponde ao primeiro sinal de comportamento de estro da novilha acompanhado
de desenvolvimento de fase lútea com duração normal para a espécie. O 17β estradiol tem sido visto como o principal
hormônio regulador do início da puberdade. O processo de luteólise ocorre devido a secreção de prostaglandina F2α
pelo endométrio em padrão pulsátil, atingindo o CL por meio do sistema de transporte local veno-arterial contracorrente, onde produz vasoconstrição e, consequentemente luteólise. Normalmente esse processo ocorre por volta
do 17º dia do ciclo estral, mas se ocorrer antes do 16º dia, acontece o fenômeno chamado luteólise prematura. Na
luteólise prematura o intervalo interestros é mais curto nos animais, sendo este denominado ciclo estral curto, comum
no primeiro ciclo estral da novilha após a puberdade.
Puberty is the beginning of the reproductive and productive process, and a gradual process of acquiring reproductive
competence, starting during pregnancy and continues until the female reaches puberty. Corresponds to the first
oestrus behavior signal heifer accompanied by development luteal phase of normal duration for the species. The 17β
estradiol has been seen as the main regulator hormone onset of puberty. The luteolysis process occurs due to the
secretion of prostaglandins F2α by the endometrium in a pulsatile pattern, reaching CL through the venous-arterial
local transportation counter-current system, which produces vasoconstriction and thus luteolysis. Usually this process
takes place around the 17th day of the estrous cycle, but if it occurs before the 16th day, happens the phenomenon
called premature luteolysis. In the premature luteolysis, interestros interval is shorter in animals, and is called short
cycle, common in the first estrous cycle of the heifer after puberty.
Keywords: short cycle, corpus luteum, estradiol, progesterone, prostaglandin.
Palavras-chave: ciclo curto, corpo lúteo, estradiol, progesterona, prostaglandina.
ISSN 21774080
47
Investigação, 15(4):47-53, 2016
INTRODUÇÃO
Commercial breeding of beef cattle is an economic activity
of great impact in Brazil, once the country counts with the
largest commercial herd in the world. However, the predominant
breeding systems are known for their low zootechnical rates,
mainly as a result of failures in nutritional, reproductive and
health managements (QUADROS, 2005).
The reproductive efficiency of animals on a property is one
of the main factors that contribute to improve the productive
and reproductive results (AZEREDO, 2008). Sexual precocity of
the bovine female, evaluated by age at puberty or age at first
calving, consists in one of the most reliable parameters when
it comes to measure and enhance the reproductive efficiency
of the herd, because it expresses the best index for assessing
female fertility (MARSON et al., 2004).
A management alternative to anticipate the heifers
conception rate would be anticipate the calving season, this
being very useful for the reproductive life of the female. This
would result in increase in calf weaning weight and increase
the possibility of this heifer to become pregnant in the next
breeding season (AZEREDO, 2008). However, after puberty, there
is a high probability of a short first estrous cycle, indicating early
luteal regression, which is followed by regulated estrous cycles
(NOGUEIRA, 2004).
In the last years hormonal therapy has been used to
induce puberty. Some hormones are capable of inducing and
synchronizing the estrus, however the progesterone used in
the beginning of the treatment is capable of initiating cyclical
ovarian activity. Other hormones such as gonadotropinreleasing hormone (GnRH), human chorionic gonadotropin
(hCG) and equine chorionic gonadotropin (eCG), estrogens and
prostaglandins are also used in association in the treatment
(SILVA FILHO, 2007).
The aim of this review is to inform the neuroendocrine
mechanisms responsible for the onset of puberty in heifers,
the main induction protocols used in commercial breeding, as
well as the mechanisms that lead to the first estrous cycle of the
heifer present premature luteolysis.
DEVELOPMENT
From birth to puberty
According to Day and Anderson (1998), the corresponding
period from birth to puberty of a heifer can be separated into
four phases: infantile period, development, statistical phase and
prepubertal.
The infantile period starts from birth until approximately
two months of age. Low levels of luteinizing hormone (LH)
are observed, and increase gradually, showing that there is an
increase in the pituitary response to GnRH. The development
period begins approximately from the second to the sixth
month of age and in this interval, higher concentrations of
gonadotropins are noticed when compared to the previous
period. In the statistical phase (approximately from the sixth
to the tenth month old) an inhibition of gonadotropins release
occurs, due to an increased production of estrogens by the
gonads in the previous period. Circulating LH concentrations
remain low until the next phase, which is called prepubescent
phase. In this last period there is a higher GnRH release by the
hypothalamus and consequently a greater LH release by the
ISSN 21774080
48
pituitary. These changes in the hormonal secretion pattern occur
approximately 50 days before puberty onset (DAY et al., 1984).
Neuroendocrine mechanisms involved in the puberty
of the heifer
Puberty is the beginning of the reproductive and productive
process, and a gradual process of acquiring reproductive
competence, starting during pregnancy and continues until the
female reaches puberty (McDONALD, 2003). According to the
hormonal point of view, it corresponds to the first sign of estrus
behavior of the heifer accompanied by the development of the
luteal phase with regular duration for the species (ALMEIDA et al.,
2013). The main factors that have been reported as determinant
for the onset of puberty are the nutritional level, growth rate,
social interaction and treatment with exogenous hormones
(EMERICK et al., 2009).
When it comes to sexual maturity, it is considered a
process that succeeds puberty, occurring two or three estrous
cycles after the first ovulation. It is represented by the presence
of clinical signs of estrus and by the fertility of the heifer in
the subsequent estrous cycles, so it can acquire the capacity
to conceive and carry the pregnancy to term (SANTOS and SÁ
FILHO, 2006). Byerley et al. (1987) described lower conception
rates in heifers covered on the first estrous compared to those
covered on the third estrous cycle (57% vs. 78%). Therefore, that
is why it is important that heifers reach puberty one to three
months before the first breeding season, so they can improve
their chances of conception (AZEREDO, 2008).
The most accepted theory to explain how puberty occurs
is the gonadostatic hypothesis, in which the hypothalamic-
Investigação, 15(4):47-53, 2016
pituitary-ovarian axis would already be functionally competent.
This hypothesis describes desensitization of hypothalamus to
gonadal steroids, with a decreased number of hypothalamic
receptors during the period of sexual maturation, allowing
the increase of gonadotropins secretion. After birth, the small
quantity of estradiol secreted by the follicles is responsible for
suppression of pulsatile LH secretion (CARDOSO and NOGUEIRA,
2007). These pulses increase with age and body score, two of
the fundamental requirements for heifers to enter puberty
(AZEREDO, 2008).
The 17β estradiol (E2) has been seen as the main regulator
hormone in the beginning of puberty. During the prepubertal
phase, a negative feedback occurs in the hypothalamus due to
E2, causing a low secretion of GnRH and an insufficient stimulus
to raise the LH pulsatility and lead to ovulation. This negative
feedback happens due to a high sensibility of the hypothalamus
to E2. As the heifer grows older this hypothalamic sensibility
decreases, triggering an increase in the GnRH secretion and also
an increase in the frequency of LH pulsatile release, resulting in
the first ovulation (DAY et al., 2010).
The pulsatile LH secretion is established in heifers between
one and two months old, increasing around the 3rd to 5th month.
After this period, LH secretion decreases and is maintained
in a static stage, until it is increased in the peripuberal phase
(approximately 50 days before puberty), culminating in puberty
(DAY et al., 2010).
Other mechanisms may be responsible for controlling the
secretion and pulsatility of LH, such as excitatory and inhibitory
neurotransmitters. Among the excitatory ones, two amino acids
(glutamate and aspartate), Y neuropeptide, norepinephrine,
noradrenaline and aspartic acid can be cited; and among the
inhibitory ones it is described the alpha-aminobutyric acid,
dopamine, endogenous opioides and endorphins (CARDOSO
and NOGUEIRA, 2007).
Hormonal puberty induction
In all species, there is a critical need for the development of
threshold body size to start puberty. In beef heifers, the average
weight recommended for the onset of puberty is 60% to 65% of
the adult body weight for taurine and Zebu breeds, respectively.
If this requirement is not attended, mainly due to a deficient
nutritional management, there is a delay on the development
and consequently on the age at puberty (NRC, 1996).
Management alternatives that aim to induce puberty in
heifers tend to increase their reproductive efficiency by providing
the first estrous, which is subfertile, before the beginning of the
breeding season. Therefore, hormonal treatments directed to
puberty induction allow heifers covered in the beginning of the
breeding season to have their parturition in the beginning of the
production season. This will promote a longer time for them to
reestablish their body reserves in the postpartum (PATTERSON
et al., 1990).
Many hormonal substances can be used to induce puberty
in heifers and increase the reproductive efficiency in these
animals. Among these hormones, progesterone (ANDERSON
et al., 1996), estradiol and their association (RASBY et al., 1998;
VOGG et al., 2004), and GnRH and its analogs (RODRIGUES et al.,
2013) are described.
Using only protocols with progesterone implants, Anderson
et al. (1996), induced puberty in 86% of evaluated heifers. To
ISSN 21774080
49
Rasby et al. (1998), the heifer’s treatment with progesteronereleasing intravaginal device increased the percentage of animals
with corpus luteum (CL) with normal duration. Additionally,
progesterone also decreased the occurrence of short estrous
cycles, increased the estrous rate and decreased the frequency
of silent estrus.
To Day and Anderson (1998), treatments with progesterone
decreased the number of E2 receptors in the hypothalamus,
reducing the negative feedback of E2 on GnRH secretion, leading
to an increased level of LH after the removal of the implant and
higher rates of follicular development (SILVA FILHO et al., 2007).
According to Rasby et al. (1998), combining the progesterone
implant with the injection of 1mg of estradiol benzoate (EB) 24
to 30 hours after the removal of the implant, it was possible
to induce estrous with the development of a functional CL in
a greater number of animals (68% vs. 44%) and it provided
synchrony in the appearance of clinical signs of estrus 2 to 4
days after the end of treatment (81% vs. 37%).
Vogg et al. (2004), used a protocol to induce puberty in
beef heifers using two applications of exogenous estrogen:
one application (5mg of EB) after placement of progesterone
implant and another 24 hours after the removal of the device
(0.5mg and 1mg of EB), having a group that did not receive
this second application (control group). It was noticed that the
animals that received the second application of estrogen had a
higher percentage of estrus incidence when compared to control
group (96% vs. 84%). However, pregnancy rates evaluated
subsequently to the treatment were higher after injection of 0.5
mg of EB and a higher percentage of animals returning to estrus
was observed after treatment with 1mg.
Investigação, 15(4):47-53, 2016
Cabral (2013) also developed a study with two applications
of exogenous estrogen, one in the beginning of the protocol
and one in the end. In this study, it was utilized progesterone
implants of 4th use and different doses of estrogen. At the
moment of the progesterone implant placement, it was applied
2mg of EB and 1mg of EB at the day of the removal of the implant.
As a result it was noticed a higher number of inseminated
heifers in the subsequent breeding season when compared to
the data presented by other authors using 1st use progesterone
implants. Valentim (2004) noticed an increase in the fertility rate
in animals using 4th use implants (42.11%) when compared to
animals using new implants (25.81%). Claro Júnior et al. (2010),
had as a result a greater follicular diameter when compared
to animals that received 1st and 4th use implants (9.72mm vs.
11.42mm) and a higher pregnancy rate at 45 days (39.2% vs.
47.7%).
According to Bridgez et al. (1999), the EB use in the
beginning of the treatment is capable to increase estrous,
fertility and pregnancy rates in heifers close to puberty. When
used in the end of the protocol, EB induces posteriorly estrous,
ovulation and appearance of a functional CL in a higher number
of animals, also providing synchronization of estrus signs
(CABRAL, 2013).
Rodrigues et al. (2013), held four different protocols to
induce puberty in Nelore heifers. In the first one, they compared
the 1st and 4th use progesterone implants. In animals which the
4th use implants were used, there was an increase in the uterine
tract score when compared to the other animals and a smaller
interval onset of estrus after implant removal, however, the
conception rate was higher in animals which received the 1st
use implant. In the second experiment all animals were tested
with the 4th use implants and evaluated the application of 200
international units (IU) of eCG on the day of the implant removal.
Animals who received the application of eCG had an increase in
the estrus detection from day 1 to 7 after the removal of the
implant. This probably happened due to action of the applied
hormone, which led to an increase in the follicular growth,
diameter of the dominant follicle and ovulation rate. In the third
evaluation, also applying implants of 4th use, animals were
divided into three groups: (1) control; (2) 200 IU of eCG in the day
of implant removal and (3) 200 IU of eCG and 0.5 mg of estradiol
cypionate (ECP) on withdrawal. In groups 2 and 3, the eCG was
able to induce ovulation and animals that received ECP had an
increase in estrus detection. In the last assessments, animals
were divided into four groups. The first three were identical
to the previous protocol. In group 4, heifers only received the
application of 0.5 mg of ECP. No improvement was found with
only the application of ECP.
The success rate to induce puberty through steroids
treatments is variable, but suggests that the treatments might
be effective. Some of the variations in responses between the
studies may be due to differences between races, environment
and growth rates of heifers (WHISNANT and BURNS, 2002).
Luteolysis mechanism
In cycling cows, CL will have morphological and functional
regressions usually from 17 to 20 days after ovulation (SÁ
FILHO and VASCONCELOS, 2008). This process is known as
luteolysis, which determinates the duration of the estrous cycle
and it is characterized by ceasing production of progesterone
and fragmented cellular components, including reduction of
vascular support, proliferation of connective tissue, cellular
ISSN 21774080
50
disorganization, degeneration and phagocytosis of luteal cells
(MILVAE et al., 1996).
Luteolysis occurs due to prostaglandin F2α (PGF2α)
secretion by the endometrium in a pulsatile pattern, reaching
the CL by a local venoarterial countercurrent system of
transportation (FERREIRA, 2010), producing vasoconstriction
and therefore luteolysis (CUNNINGHAM, 2004).
Around the 17th day of the estrous cycle there is an increase
in endometrial release of PGF2α in the absence of a viable
embryo. Approximately 98% of this PGF2α is transformed into
PGFM (13,14 dihydro-15 keto prostaglandin F2α) in the first
passage through the lungs, and which is a measurement form
in vivo. In the beginning of the luteolysis there are secretion
peaks of PGF2α, which promotes an increase in the plasmatic
concentration of PGFM to levels higher than 100-125 pg/mL
and posteriorly reaching values around 550 pg/mL. When this
occurs, the ovarian blood flow and the progesterone synthesis
are already declining, until they reach levels lower than 1ng/
mL (TREVISOL et al., 2013). All this process lasts approximately
30 hours (GINTHER et al., 2007).
PGF2α is connected to receptors in the membrane of
the luteal steroidogenic cells and stimulates the activity of
protein kinase C, which decreases cholesterol capitation
and transportation to the cytoplasm and mitochondria, also
decreasing the progesterone production and increasing the
expression and activation of apoptotic proteins (BERTAN et al.,
2006).
In ruminants, there is a synthesis of oxytocin by the
CL. PGF2α stimulates the secretion of this hormone, which
Investigação, 15(4):47-53, 2016
stimulates the secretion of PGF2α by the uterus. These two
hormones operate between the uterus and the CL, reinforcing
luteal regression (SHIRASUNA et al., 2007). Estradiol also
participates in the luteolysis, increasing the frequency of pulses
of oxytocin via the hypothalamus as well as oxytocin receptors
expression in the endometrium (McCRACKEN et al., 1999).
Nitric oxide (NO) is an important factor for the onset of
luteolysis. It is a potent vasodilator, promoting an increase
in the luteal blood flow. According to Acosta and Miyamoto
(2004), there is an increase in the blood flow to the CL in the
beginning of the luteolysis, which is crucial for endothelial
cells CL to synthesize and release vasoactive substances
(endothelin-1 and angiotensin II). These substances will later
cause vasoconstriction, reducing the blood flow supply to the
CL (LEVY et al., 2000).
Premature luteolysis in the first estrous cycle after
puberty
Premature luteolysis is considered when the regression
of the CL happens before the day 16th of the estrous cycle. This
event is common in heifers after their first ovulation in puberty
and in postpartum cows (SÁ FILHO and VASCONCELOS, 2008).
In this case, the interestrus interval is shorter than the average
observed, being named short estrous cycle (SÁ FILHO, 2007).
Evans et al. (1994), noticed an average of seven days in the
duration of the short estrous cycle. Similarly, Sharma et al. (2012)
described a variation of eight to twelve days and Sá Filho (2007),
a variation of five to seven days.
These cycles are usually accompanied by low rates of
conception because the CL regresses when the embryo is still
not capable of producing sufficient interferon τ (IFN-τ, hormone
responsible by maternal-fetal recognition) to block luteolysis,
leading to early embryonic death (MANN and LAMMING, 2001).
Several assumptions have been proposed to explain the
occurrence of premature luteal regression in cattle, such as: (1)
inadequate development of the ovulatory follicle (RAMIREZGODINEZ et al., 1981). Taponen et al. (2003) assigned that
ovulation of follicles with small diameter can be responsible
for a shorter duration of the estrous cycle. The ovulation of
a small dominant follicle results in the creation of a small CL,
with low concentration of progesterone, low rates of pregnancy
and therefore short estrous cycles; (2) inadequate support of
gonadotropic hormones (MANNS et al., 1983); (3) CL unresponsive
to gonadotropins (KESLER et al., 1981); (4) premature luteolitic
stimulus (PUGLISI et al. 1979), due to endometrial secretion of
PGF2α, in which luteolysis will occur as soon as the CL acquires
receptors to PGF2α, that is, around the sixth day of the estrous
cycle (FERREIRA, 2010); (5) CL higher sensibility to luteolytic
substances (TROXEL and KESLER, 1984); (6) ovulation without
previous exposure to progesterone. To Sá Filho et al. (2009), the
preexposure to exogenous progesterone in heifers increases
the rate of estrus manifestation and the percentage of animals
with normal duration of CL after preexposure, minimizing
early luteolysis (RASBY et al., 1998). According to Sá Filho and
Vasconcelos (2008), the mechanism in which progesterone
prevents the occurrence of short cycles involves inhibition of
oxytocin receptors in the endometrium after ovulation; (7)
consequence of low concentrations of pre-ovulatory estradiol.
Short estrous cycles can result from inadequade preovulatory
estrogen secretion, so no sign is strong enough to block
oxytocin receptors in the endometrium, allowing early secretion
of PGF2α (SÁ FILHO and VASCONCELOS, 2008). Garverick et al.
ISSN 21774080
51
(1988) noticed that the pretreatment with progesterone in
postpartum animals also resulted in higher concentrations of
preovulatory estrogen.
CONCLUSION
Puberty induction in beef heifers has been used in
recent years in the Brazilian livestock in order to reduce the
age at first calving and improve performance parameters.
Additionally, the anticipation of the estrous cycle increases
calves production, as well income for the producer. However,
all the neuroendocrine process that triggers puberty is very
complex, and there are some points that are still obscure to
this physiology, being of great value and importance more
studies in this regard.
ACKNOWLEDGEMENTS
FAPESP (grant 2015/13079-0) and Ouro Fino.
REFERENCES
Acosta TJ, Miyamoto A. 2004. Vascular control of ovarian function: ovulation, corpus
luteum formation and regression. Animal Reproduction Science. 82: 127-140.
Almeida OM, Pinho RO, Lima, DMA, et al. 2013. Endocrinologia da puberdade em
fêmeas bovinas. Revista Científica Eletrônica de Medicina Veterinária. 20: 1-33.
Anderson LH, McDowell CM, Day ML. 1996. Progestin-induced puberty and
secretion or luteinizing hormone in heifers. Biology of Reproduction. 54: 1025-1031.
Azeredo DM. 2008. Alternativas para indução da ovulação e do estro em novilhas de
corte peripúberes. 139f. Porto Alegre, RS. Tese (Doutorado em Ciências Veterinárias)
– Curso de Pós-graduação em Ciências Veterinárias, Universidade Federal do Rio
Grande do Sul.
Bertan CM, Binelli M, Madureira EH, et al. 2006. Mecanismos endócrinos e
moleculares envolvidos na formação de corpo lúteo e na luteólise – revisão de
literatura. Brazilian Journal of Veterinary Research and Animal Science. 43: 824-840.
Investigação, 15(4):47-53, 2016
Byerley DJ, Staigmiller RB, Berardinelli JG, et al. 1987. Pregnancy rates of beef heifers
bred either on puberal or third estrus. Journal Animal Science. 65: 645-650.
Cardoso D, Nogueira GP. 2007. Mecanismos neuroendócrinos envolvidos na
puberdade de novilhas. Arquivos de Ciências Veterinárias e Zoologia. 10(1): 59-67.
Ginther OJ, Silva LA, Araujo RR, et al. 2007. Temporal associations among pulses of 13,
14-Dihydro-15-keto-PGF2alpha, luteal blood flow, and luteolysis in cattle. Biology of
Reproduction. 76: 506-513.
Patterson DJ, Corah LR, Brethour JR. 1990. Response of prepubertal Bos taurus
and Bos indicus x Bos taurus heifers to melengestrol acetate with or without
gonadotropin-releasing hormone. Theriogenology. 33(3): 661-668.
Hafez ESE. 1993. Reproduction in farm animals. Lea e Febiger, Philadelphia, p.585.
Puglisi TA, Rampacek GB, Kraeling RR, et al. 1979. Corpus luteum susceptibility to
prostaglandin F2α (PGF2α) luteolysis in hysterectomysed prepubertal and mature
gilts. Prostaglandins. 18: 257-264.
Claro Júnior I, Sá Filho OG, Peres RFG, et al. 2010. Reproductive performance
of prepubertal Bos indicus heifers after progesterone-based treatments.
Theriogenology. 74: 90-911.
Kesler DJ, Weston PG, Pimentel CA, et al. 1981. Diminution of the in vitro response to
luteinizing hormone by corpora lutea induced by gonadotropin releasing hormone
treatment of post-partum suckled beef cows. Journal Animal Science. 53: 749-754.
Cunningham JG. 2004. Tratado de fisiologia veterinária. Guanabara Koogan, Rio de
Janeiro, 3ª ed.
Levy N, Kobayashi S, Roth Z, et al. 2000. Administration of prostaglandin F2α during
the early bovine luteal phase does not alter the expression of ET-1 and its type A
receptor: A possible cause of corpus luteum refractoriness. Biology of Reproduction.
63: 377-382.
Day ML, Imakawa K, Garcia-Winder M, et al. 1984. Endocrine mechanisms of puberty
in heifers. Estradiol negative feedback regulation of luteinizing hormone secretion.
Biology of Reproduction. 31: 332-341.
Day ML, Anderson LH. 1998. Current concepts on the control of puberty in cattle.
Journal of Animal Science. 76: 1-15.
Day ML, Gasser CL, Grum DE, et al. 2010. Fatores que afetam a idade na puberdade
em novilhas de corte. In: Pires AV. Bovinocultura de corte. Piracicaba: Fealq. pp.637652.
Diancourt MA. 2001. Regulation of ovarian follicular dynamics in farms animals.
Implications for manipulation of reproduction. Theriogenology. 55: 1211-1239.
Emerick LL, Dias JC, Gonçalves PEM, et al. 2009. Retorno da atividade ovariana luteal
cíclica de vacas de corte no pós-parto: uma revisão. Revista Brasileira de Reprodução
Animal. 33(1): 11-19.
Evans ACO, Adams GP, Rawlings NC. 1994. Endocrine and ovarian follicular changes
leading up to the first ovulation in prepubertal heifers. Journal of Reproduction and
Fertility. 100: 187-194.
FERREIRA, A.M. 2010. Reprodução da Fêmea Bovina: Fisiologia aplicada e Problemas
mais comuns. Editar, Juiz de Fora.
Fortune JE. 2001. Ovarian follicular growth and development in mammals. Biology
of Reproduction. 65: 648-654.
Lucy MC, Savio JD, Badinga L, et al. 1992. Factors that affect ovarian follicular dynamics
in cattle. Journal of Animal Science. 70: 3615-3626.
MacMillian KL, Burke CR. 1996. Effects of oestrus cycle control on reproductive
efficiency. Animal Reproduction Science. 42: 307-320.
Mann GE, Lamming GE. 2001. Relationship between maternal endocrine environment,
early embryo development and inhibition of the luteolytic mechanism in cows.
Reproduction. 121: 175-180.
Manns JG, Humphrey WD, Flood PF, et al. 1983. Endocrine profiles and functional
characteristics of corpora lutea following onset of postpartum ovarian activity in beef
cows. Canadian Journal of Animal Science. 63: 331-347.
Marson EP, Guimarães JD, Neto TM. 2004. Puberdade e maturidade sexual em novilhas
de corte. Revista Brasileira de Reprodução Animal. 28: 1-64.
Quadros DG. 2005. Sistemas de produção de bovinos de corte. Disponível em: <http://
www.neppa.uneb.br/textos/publicacoes/cursos/sistemas_producao_gado_corte.
pdf>. Acesso em: 14 de abril de 2015.
Ramirez-Godinez JA, Kiracofe GH, McKee RM, et al. 1981. Reducing the incidence of
short estrous cycles in beef cows with norgestomet. Theriogenology. 15: 613-623.
Rasby RJ, Day ML, Johnson SK, et al. 1998. Luteal function and estrus in peripubertal
beef heifers treated with an intravaginal progesterone releasing device with or
without a subsequente injection of estradiol. Theriogenology. 50; 55-63.
Sá Filho OG, Vasconcelos JLM. 2008. Regressão prematura do corpo lúteo em
bovinos. Veterinária e Zootecnia. 15: 220-233.
Sá Filho OG. 2007. Efeito de tratamentos com progesterona e/ou estradiol na
incidência de regressão prematura do corpo lúteo após a primeira ovulação em
vacas Nelore pós-parto. 137 f. Botucatu, SP. Dissertação (Mestrado em Medicina
Veterinária) – Universidade Estadual Paulista.
Sá Filho OG, Thatcher WW, Vasconcelos JLM. 2009. Effect of progesterone and/or
estradiol treatments prior to induction of ovulation on subsequent luteal lifespan
in anestrous Nelore cows. Animal Reproduction Science. 112: 95-106.
McCracken JA, Custer EE, Lamsa JC. 1999. Luteolysis: A neuroendocrine-mediated
event. Physiological Reviews. 79(2): 264-323.
Santos JEP, Sá Filho MF. 2006. Nutrição e reprodução em bovinos. Biotecnologias da
Reprodução em Bovinos. In. Simpósio Internacional de Reprodução Animal aplicada.
Londrina, Brasil, p. 30-54.
McDonald LE. 2003. Veterinary endocrinology and reproduction. Lea e Febiger,
Philadelphia. p.597.
Sharma RK, Singh JK, Khanna S, et al. 2012. Ovarian response of prepubertal Murrah
heifers to exogenous GnRH. Animal Reproduction Science. 133: 153-158.
Milvae RA, Hinckley ST, Carlson JC. 1996. Luteotropic and luteolytic mechanisms in
the bovine corpus luteum. Theriogenology. 45: 1327-1349.
Shirasuna K, Shimizu T, Hayashi K, et al. 2007. Positive association, in local release, of
luteal oxytocin with endothelin 1 and prostaglandina F2alpha during spontaneous
luteolysis in the cow: A possible intermediatory role for luteolytic cascade within
the corpus luteum. Biology of Reproduction. 76: 965-970.
Garverick HA, Parfet JR, Lee CN, et al. 1988. Relationship of pre and post-ovulatory
gonadotropin concentrations to subnormal luteal function in postpartum beef
cattle. Journal Animal Science. 66: 104-111.
National Research Council - NRC. 1996. Nutrient requirements of beef cattle. National
Academy Press, 7ª ed, p.249.
Ginther OJ, Bergfelt DR, Kulick LJ, et al. 2000. Selection of the dominant follicle in
the cattle: role of estradiol. Biology of Reproduction. 63: 383-389.
Nogueira GP 2004. Puberty in South America Bos indicus (Zebu) cattle. Animal
Reproduction Science. 82: 361-372.
ISSN 21774080
52
Silva Filho AHS, Araújo AA, Rodrigues APR. 2007. Indução da puberdade em novilhas
com uso de hormonioterapia. Ciência Animal. 2(17): 83-89.
Investigação, 15(4):47-53, 2016
Taponen J, Hjerppe P, Kopra E, et al. 2003. Premature prostaglandin F2α secretion
causes luteal regression in GnRH-induced short estrous cycles in cyclic dairy heifers.
Theriogenology. 60: 379-393.
Trevisol E, Ferreira JCP, Ackermann CL, et al. 2013. Luteólise em bovinos: revisão.
Revista Brasileira de Reprodução Animal. 37(1): 29-36.
Troxel TR, Kesler DJ. 1984. Ability of indomethacin to alter prostaglandin metabolite
concentrations and to enhance the function of corpora lutea induced in postpartum
suckled beef cows. Journal Animal Science. 59: 177-181.
Whisnant CS, Burns PJ. 2002. Evaluation of steroid microspheres for control of estrus
in cows and induction of puberty in heifers. Theriogenology. 58(6): 1229-1235.
ISSN 21774080
53