Estrus Synchronization and Superovulation in Goats: A Review
The study was intended to review the recent developments
and advances of estrus synchronization and superovulation protocols in
goats with a view to improve oocytes/embryo recovery for In Vitro
Production (IVP) efficiencies. Although a number of estrus synchronizing
protocols has been developed in goat, the most widely used one is the
treatment of progesterone for 9-11 days followed by a luteolytic dose
of prostaglandin administered in the period 48h prior to removal of intravaginal
sponge. Until now, Controlled Internal Drug Release (CIDR) device and
subcutaneous implants are more preferable than sponges. Ovulation in goat
can be synchronized more precisely by administering Gonadotrophin Releasing
Hormone (GnRH) around the time of estrus that improves the success of
fixed-time Artificial Insemination (AI) and oocytes or embryos collection
at a controlled stage. Superovulation is the hormonal treatment for increasing
a large number of oocytes that ultimately accelerate genetic improvement
in any species. Generally an exogenous follicle-stimulating gonadotrophin
is administered that mimics the effect of Follicle Stimulating Hormone
(FSH) near the end of the luteal phase of the cycle (9-11 days) or around
48 h before the end of the synchronizing treatments. The major commercial
products applied are equine Chorionic Gonadotrophin (eCG) or Pregnant
Mare Serum Gonadotrophin (PMSG) and FSH. This review paper describes estrus
synchronization, ovarian superovulation as well as the normal physiology
of estrous cycle and ovulation in goats.
In this modern era Assisted Reproductive Technologies (ARTs) plays a
major role in animal reproduction and production. The estrus synchronization
and ovarian superovulation already become one of the popular ARTs in goat
industry. Estrus synchronization plays a major role in fixed time breeding,
Artificial Insemination (AI), Multiple Ovulation-Embryo Transfer (MOET),
Laparoscopic Ovum Pick-up (LOPU) for oocyte or embryo collection and Embryo
Transfer (ET). The value of estrus synchronization is vital in goats as
the duration of both estrous cycle and estrus is variable and estrus detection
cannot be accomplished safely without a buck (Jainudeen et al.,
2000; Rahman et al., 2008). On the other hand, superovulation is
the hormonal treatment for harvesting increased number of oocytes from
the ovary than normal. This will ultimately accelerate genetic improvement
in goat like any other livestock. It is a means to induce maturation,
ovulation and increase the number of follicles available for oocyte recovery.
A complete and scientifically detailed understanding of any physiological
process is vital for its successful manipulation. The basic premises of
any estrus synchronization and superovulation protocol pivots around the
predictable control of events associated with the animal`s reproductive
physiology. Control of reproductive events can be achieved through pharmacological
administration of biologically active agents. Usually the agents used
in estrus synchronization and superovulation protocols are either based
on or are the hormones that occur in the female goat or doe at various
times during her cycle. Therefore, works related to estrus synchronization
and superovulation treatments of the doe have been reviewed briefly in
this paper following a short description of estrous cycle.
This study was conducted in Animal Biotechnology-Embryo Laboratory (ABEL),
Institute of Biological Sciences, University of Malaya, Lembah Pantai,
50603 Kuala Lumpur, Malaysia from 2004 to 2008.
ESTROUS CYCLE OF THE DOE
The signs of estrus; length and duration of different phases of estrous
cycle; hormonal changes during estrous cycle; follicular dynamics, waves
and dominant follicles and ovulation in the doe are described following:
Signs of estrus: Signs of estrus are important indicators of onset
of estrus or heat and, therefore, very important for estrus detection.
These signs are mainly two types, primary and secondary signs. The primary
signs are the most reliable and well accepted for indication of estrus
behavior in most female animals. The best method of estrus detection is
the observation of primary signs exhibited by the doe in response to the
buck. However, the doe seldom mount as often as the cow, but demonstrate
some behavior when they are in heat such as seeking out bucks, waggling
of the tail when being exposed to the buck and also bleating, more frequently
if the buck is absent. Apart from the primary signs, physical signs, for
example, redness and swelling of the vulva and a clear mucous discharge
from the vulva also indicative of estrus. Restlessness, frequent urination,
isolation from others, general loss of appetite and constant vocalizations
are the secondary signs of estrus. However, secondary signs are less reliable
as they vary in length and may be confused with the symptoms of any minor
illness. Although it is possible to detect estrus signs in the doe as
described above, but a doe in heat may not exhibit all the signs at the
same time. These signs appear and disappear progressively with the onset
and termination of estrus behavior. Therefore, estrus detection is dependant
upon the careful observation and close attention of such phenomena, including
the primary and physical signs of the doe experiencing estrus. Therefore,
a routine check-up of heat twice daily (morning and evening) is indispensable
to obtain optimal results. Estrus detection is a valuable and useful tool
for natural mating, AI, predicting parturition date as well as prediction
of ovulation time for LOPU.
Length and duration of different phases of estrous cycle: Like
ewes, does are also seasonally polyestrus as their reproductive cycle
responds to changes in day length (Attwood, 2007). Sexual activity is
usually greatest during autumn and winter. Estrus activity of doe is greater
in the tropics than in temperate climates. The average length of estrous
cycle in the doe is 21 days, but can vary from 18-22 days depending on
the breed differences, stage of breeding season and environmental stress
(Jainudeen et al., 2000). The abnormally short cycles that are
observed in the doe early in the breeding season may be associated with
premature regression of the corpus luteum. The estrus lasts for 24-48
h in the doe and the duration of estrus can be influenced by breed, age,
season and presence of the buck (Jainudeen et al., 2000). Angora
does have a shorter duration of estrus (22 h) than the dairy breeds. Estrus
is of shorter duration at the end of breeding season and in the first
breeding season of young does. The characteristic events of estrous cycle
in doe are shown in Table 1. The complete estrous cycle
in doe is divided into 4 well marked phases, namely proestrus, estrus,
metestrus and diestrus. In prepubertal and aged does anoestrus (stage
of sexual quiescence characterized by lack of estrus behavior) normally
occurs. This may be due to the complete suppression of ovarian activity
or silent ovulatory cycles without behavioral signs of estrus. In all
domestic animals including the doe, anoestrus also may occur as a pathological
condition (Pineda, 2003). The duration of each event associated with the
estrus cycle and pregnancy in the doe is illustrated in Fig.
|| Duration of characteristics events of estrous cycle
|Source: Modified from Devendra and McLeroy (1982) and
Jainudeen et al. (2000)
||The estrous and reproductive cycles of the female goat.
Illustration is based on Pineda (1989) using data cited in Jainudeen
et al. (2000), Massita (2003) and Attwood (2007)
Hormonal changes during estrous cycle in doe: Like other domestic
farm animals, improvement in the efficiency of estrus synchronization
in the doe depends on a better knowledge of the endocrine patterns that
occur during induced and natural estrus (Chemineau et al., 1981).
Cyclic changes in the circulating levels of the ovarian hormones, progesterone
and estrogen have direct effects on the growth and metabolism of cells
in the reproductive tissues. Unlike the ewe, data about the endocrinology
of the estrous cycle in the doe is sparse. The main events of the estrous
cycle are related to the periods of growth of the ovarian follicles and
the corpus luteum. The sequence of hormonal events during the estrous
cycle is similar in both doe and ewe, but the doe has a longer progesterone
phase than the ewe (Jainudeen et al., 2000). During the 21 days
cycle, progesterone dominates for about 15 days and estrogen dominates
for 5-6 days.
D0 (day 0) of the cycle is generally designated as the first day of behavioral
estrus, which is the result of increasing estradiol-17β levels produced
by the developing pre-ovulatory follicle. The rise in estradiol-17β
levels and the maximum values before natural estrus in the doe are similar
to that of the ewe (Chemineau et al., 1981). The rise of estradiol-17β
is followed in less than 12 h by simultaneous peaks of Luteinizing Hormone
(LH), Follicle Stimulating Hormone (FSH) and prolactin as reported for
the ewe (Pant et al., 1977; Herriman et al., 1979; Cahill
et al., 1981). These peaks occur 8.5 h after the onset of natural
estrus (Chemineau et al., 1981). Within 48 h of the first peak,
a second FSH peak occurs (Chemineau et al., 1981) which is similar
in the ewe (Pant et al., 1977). High estradiol-17β levels
are believed to cause a surge of Gonadotrophin Releasing Hormone (GnRH)
and consequently an LH peak at estrus resulting in spontaneous ovulation
towards the end of estrus. Following ovulation the ruptured follicle becomes
a functional corpus luteum, which is the main source of progesterone in
the cycling doe. Blood levels of progesterone are low at estrus (less
than 1.0 ng mL-1) through to 2 days of diestrus and then rapidly
increase to maximal levels at 7 days and remain elevated until 13-15 days
in natural estrus (Fig. 1). Regression of the corpus
luteum (luteolysis), induced by prostaglanding F2α (PGF2α),
occurs if an embryo is not present in the uterus, resulting in a rapid
drop in plasma progesterone (reviewed in Rahman, 2006). Ovarian oxytocin
stimulates endometrial secretion and release of prostaglandins. The onset
of the follicular phase of the next cycle is characterized by low progesterone
levels and increasing GnRH and LH levels, while the FSH levels present
at the onset of this phase are progressively decreased. These events are
controlled by estrogen and inhibin, which are produced in increasing amounts
by the developing follicles (Rahman, 2006).
Follicular dynamics, waves and dominant follicles: The mature
ovary of farm animals contains varying numbers of follicles in different
stages of development. Unlike other farm animals and ruminants, reports
of caprine follicular waves and their association with hormones during
estrous cycle are limited. The term follicular wave is defined as one
or more antral follicles growing from 3 mm to ≥ 5 mm in diameter before
regression (Ginther et al., 1995; de Castro et al., 1999;
Bartlewski et al., 2000). Individual follicle emerging within a
maximum of 48 h can be regarded as a single follicular wave (Medan
et al., 2003). However, distinct differences exist in the follicular
dynamics in the ovary among different farm animals. In cow and mares,
distinct groups of follicles develop during the estrous cycle. Although
1 or 2 waves occur during the estrous cycle in mare by Pierson and Ginther
(1987a), in cow 2 or 3 waves were detected (Pierson and Ginther, 1987b).
The phenomenon called follicle dominance is generally present in each
wave of follicular development, both in mare and in cow (Pierson and Ginther,
1987a, b, 1988; Savio et al., 1988; Sirois and Fortune, 1988).
Dynamics of follicular development in ewe is a bit different and characterized
by an initial wave of follicular activity at the beginning and another
at the end of the estrous cycle (Bobes et al., 2003). However,
the growth of ovarian follicles in the ovary of doe is characterized by
the presence of 4 or more waves of follicle growth in the same cycle and
it is in the final wave where the dominant follicle ovulates (Ginther
and Kot, 1994; de Castro et al., 1999; Medan et al., 2005).
Unlike other farm animals, the subsequent follicular wave begins even
though the dominant follicle of the previous wave is still in its peak
of development. This behavior strongly suggests that follicular dominance
is less apparent in the ovary of doe (Ginther and Kot, 1994). Each follicular
wave is preceded by an increase in FSH secretion (Medan et al.,
2005). It is found that progesterone treatment affects follicular dynamics
in dairy does (Menchaca and Rubianes, 2002).
Ovulation: Ovulation can be defined as the rupture of the mature
ovarian follicle on the surface of the ovary and the release of its contents,
including the maturing oocyte (Pineda, 2003) with adhering corona radiata
cells, Cumulus Cells (CCs) and Follicular Fluid (FF). Ovulation is the
most significant event of estrus. The point of ovulation can be seen in
the resulting corpus luteum on the ovary days after ovulation. Ovulation
is controlled by gonadotrophins: FSH is predominant during the phase of
follicular growth and LH is generally regarded as ovulation inducer and
also responsible for the formation of corpus luteum (Perry, 1971). In
the doe, LH is released from the pituitary in a surge (50 ng mL-1)
(Bono et al., 1983), which induces final preparation of the follicle
24 h prior to ovulation. At ovulation, LH level in the peripheral blood
circulation of the doe reduces rapidly and FSH level begins to increase
(Bono et al., 1983). Following rupture, external part of the follicle
collapses and the follicular cavity becomes filled with clotted blood
or serous fluid. The ruptured follicle reduces in size, the granulosa
and theca internal cells begin to proliferate exuberantly under the influence
of LH and form the corpus luteum (Sanga et al., 2002). Ovulation
in the doe is spontaneous and most goat breed ovulates between 24-36 h
after onset of estrus, the Nubian goat ovulates later, which is possibly
due to a longer estrous cycle in this breed (Jainudeen et al.,
2000). The average ovulation rate in the doe is 1-3 oocytes, but can vary
from 1-5 depending upon the breeds and management conditions (Pineda,
Estrus synchronization is a key element of all the ART-protocols in livestock
animals and has a major influence to increase the overall efficiencies
of these programs (Baldassarre and Karatzas, 2004). Estrus synchronization
plays a major role in fixed time breeding, AI, LOPU for oocyte or embryo
collection and Embryo Transfer (ET). The value of estrus synchronization
is vital in does as the duration of both estrous cycle and estrus is variable
and estrus detection cannot be accomplished safely without a buck (Jainudeen
et al., 2000). This technique has been developed in the early 1960s
and since then a number of synchronizing methods has been developed for
goats. Approaches towards synchronizing estrus in livestock have to focus
on either the manipulation of the luteal or the follicular phase of the
estrous cycle. In the doe, the window of opportunity is generally greater
during the luteal phase, which is of longer duration and more responsive
to manipulation. Different approaches have been concerned with either
extending the luteal phase by supplying exogenous progesterone or with
shortening this phase through regression of the corpus luteum. Successful
techniques must not only establish synchrony, but also provide a reasonable
level of fertility in the synchronized cycle.
A number of synchronization methods for goats have been evaluated under
research conditions. The most widely used method in the doe is the treatment
of progesterone or progestagen for 9-11 days followed by a luteolytic
dose of prostaglandin (or an analogue) administered in the period 36-48h
prior to removal of intravaginal sponge (Baldassarre and Karatzas, 2004).
The progesterone or progestagen treatment can be delivered through an
intravaginal sponge, a Controlled Internal Drug Release (CIDR) device
or a subcutaneous implant (Evans and Maxwell, 1987; Ritar et al.,
1989; Freitas et al., 1997). Although sponges are widely used either
in conjunction with Pregnant Mare Serum Gonadotrophin (PMSG), FSH or prostaglandin
to more tightly synchronize and/or induce a superovulatory response, but
sponges are not preferred as these frequently cause discomfort and may
adhere to the vaginal wall causing problems with removal (Holtz, 2005).
An alternative means of supplying continuous, exogenous progesterone has
been the CIDR developed for goats in New Zealand. The CIDR device is constructed
from natural progesterone impregnated medical silicone elastomer molded
over a nylon core. Currently the CIDR and subcutaneous implants are preferable
than sponges because these are easy to use (Holtz, 2005). Ovulation in
the does can be synchronized more precisely by administering GnRH around
the time of estrus (Pierson et al., 2003), which improves the success
of fixed-time AI and the collection of oocytes or embryos at a controlled
stage of development for specific applications such as oocytes for In
Vitro Production (IVP), Intracytoplasmic Sperm Injection (ICSI) or
Somatic Cell Nuclear Transfer (SCNT) and zygotes for pronuclear microinjection
(Baldassarre and Karatzas, 2004). Although, in the past, a considerable
attention was focused in estrus synchronization, however, there is an
urgent need for additional research conducted in a well-organized and
systematic fashion to help establish guidelines for efficient breeding,
AI, oocyte or embryo recovery and ET programs. Timeline of significant
finding in estrus synchronization of does has been depicted in Table
As multiple litter bearing animals, ovulation rate and litter size have
a major impact on the reproductive efficiency of goat. Ovulation rate
is influenced by the stage of breeding season, nutrition, genotype and
parity. However, it can also be manipulated by pharmacological means which
is known as superovulation. Superovulation is the hormonal treatment for
increasing a large number of ova released by the ovary, which ultimately
accelerate genetic improvement in any species. It is a means to induce
maturation, ovulation and increase the number of ovulating or antral follicles
(>2-3 mm) on the surface of the ovary available for oocyte recovery.
Principles of inducing superovulation in doe are the same as in cow and
ewe. An exogenous follicle-stimulating gonadotrophin is administered that
mimics the effect of FSH near the end of the luteal phase of the cycle
(9-11 days) or around 48 h before the end of the synchronizing treatments.
There are a number of ways to superovulate doe, each of which has its
advantages and disadvantages. However, superovulation in goats is frequently
restricted by the cost of gonadotrophin or the handling requirements.
The major commercial products applied are equine Chorionic Gonadotrophin
(eCG) or PMSG and FSH used in higher (pharmacological) doses to elicit
a superovulatory response; commercial preparations are partly purified
from mare`s serum and porcine pituitary gland, respectively. PMSG is used
to stimulate ovarian activity during seasonal anoestrus (Gordon, 1997)
and usually used concurrently following estrus synchronization. PMSG is
available in most countries and tended to be a practical hormone to administer
for superovulation (Amoah and Gelaye, 1990). PMSG is preferred due to
its lower cost and easy availability; it can be more easily administered
than FSH, usually as a single injection of up to 1500-2000 IU, but the
superovulatory response to PMSG can be quite variable and is usually lower
than in a FSH-induced superovulation (Amoah and Gelaye, 1990). Problems
associated with PMSG-induced superovulation are a high number of non-ovulated
follicles, early regression of CL, short or irregular estrous cycles and
potential risk of embryo expulsion (Amoah and Gelaye, 1990). A combination
of eCG and human Chorionic Gonadotrphin (hCG) has also been widely used
to superovulate does (Medan et al., 2003). FSH is a better choice
of hormone for superovulating does as it provides more oocytes than PMSG.
FSH is usually administered in decreasing doses of 1-5 mg, injected in
12 h intervals over a period of 3-5 days around the time of termination
of the progestagen treatment. Like in cows and ewes, a number of experiments
have been performed to compare the superovulatory response between FSH
and PMSG, the evidence favors the use of FSH than PMSG (Tsunada and Sugie,
1989; Pendelton et al., 1992). In their study, Tsunada and Sugie
(1989) reported that average number of oocyte recovery (OR) was significantly
higher in FSH-treated does (9.4) than that in PMSG-treated ones (5.7).
Studies in our laboratory also support of this finding. Earlier in our
laboratory, PMSG alone or in combination with hCG was used to superovulate
does. However, due to higher variability of stimulation and lower OR rate,
a combination of recombinant ovine FSH (Ovagen™; ICPbio
Limited, New Zealand) and hCG (Ovidrel; Laboratories Serono, Switzerland)
as single doses was later introduced in our laboratory (Rahman et al.,
2007a; Abdullah et al., 2008).
|| Timeline of significant finding in estrus synchronization
and superovulation in the goats
Most superovulatory treatments are cumbersome and expensive and, over
and above, accompanied by endocrine repercussions that take one or more
subsequent cycles to subside (Holtz, 2005). Therefore, several attempts
have been made to devise less labor-intensive treatment regimes without
compromising oocyte or embryo yield. By applying a one shot-treatment
regimen consisting of a single dose of FSH combined with a moderate dose
of eCG (e.g., 60-80 mg FSH and 300IU eCG), Batt et al. (1993),
Baldassarre et al. (2002, 2003), Baldassarre et al. (2007)
and Gibbons et al. (2007) almost equaled the oocyte or embryo yield
obtained with the traditional multiple injection regimen. The simplicity
of this treatment is appealing. Of all the superovulation protocols in
use to date, not a single one fulfils all expectations concerning predictability
and reliability of the response. The variability in number of ovulations
and yield of viable oocytes or embryos remains the main drawback (Holtz,
2005). Both intrinsic and extrinsic factors are responsible for the variability.
Among the intrinsic factors, genetic (Nuti et al., 1987), age (Mahmood
et al., 1991) and stage of the cycle at which the treatment applied
(Wani et al., 1990) are important. A host of environmental factors
such as season, nutrition, health state, AI (Holtz, 2005) and type of
gonadotrophin administered (Gordon, 1997) are known to contribute to that
variability. Therefore, vigorous research efforts are directed for the
establishment of suitable superovulation regimes to augment the develoment
of LOPU, ET and associated technologies based on them.
Time interval between the estrus synchronization plus superovulation
treatment and LOPU may also influence the umber of oocytes recovered per
doe (Abdullah et al., 2008). While other LOPU-IVP research groups
(Baldassarre et al., 2002; Baldassarre et al., 2007) obtained
optimum OR rates (13.4-15.7 oocytes per doe) after performing LOPU at
36 h of FSH plus hCG treatment, previous OR rates in our laboratory was
always less than 7 oocytes per doe (Rahman et al., 2007b). In their
experiment, Gibbons et al. (2007) used a lower time interval of
24 h between FSH plus eCG and LOPU and recovered lower OR rates (5.6-8.0
oocytes per doe). Therefore, we speculated that 36 h time interval between
FSH plus hCG treatment and LOPU might not be optimum for proper stimulation
of the ovarian follicles with our current protocol and, thus oocytes derived
from these follicles had not acquired full meiotic competence and ooplasmic
maturation. Keeping this in mind, we increased the time interval between
FSH plus hCG treatment and the onset of LOPU from 36 h to 60 and 72 h
and obtained 8.6 and 16.1 per doe, respectively, at 60 and 72 h interval
(Abdullah et al., 2008). With slight modification of superstimulation
protocol (decreasing hCG dose rate from 500 IU to 250 IU per doe), later
we retrieved 14.9-17.6 oocytes per doe when LOPU performed 60 h post-FSH-hCG
treatment (Rahman, 2008). These recovery rates are in agreement with Baldassarre
et al. (2002), Baldassarre et al. (2003) and Baldassarre
et al. (2007), who used slightly different protocol consisting of
a single dose of FSH combined with a moderate dose of eCG (e.g., 80mg
FSH and 300IU eCG). Using 60mg FSH and 300IU eCG in their superovulation
protocol, (Gibbons et al., 2007) reported lower OR rate (5.6-8.0
oocytes per doe and 5.5-8.8 oocytes per ewe).
Dose rates of hormones for inducing superovulation might also have significant
importance. Previous superovulation protocol in our laboratory was consisted
of 70 mg FSH (Ovagen™; ICPbio Limited, New Zealand) and
1000 IU hCG (Ovidrel; Laboratories Serono, Switzerland) per doe (Rahman
et al., 2007b). Later we have lowered the hormone doses from 70 to
35 mg FSH (Ovagen™) and 500 IU hCG (Ovidrel) per doe due
to a shortage of hormones in the laboratory at that time (Abdullah
et al., 2008). However, even with lower doses of hormones similar
OR rate at 36 h and significantly higher OR rates at 60 and 72 h time
intervals were obtained. Currently we further reduced the dose rate of
hCG (Ovidrel) to 250 IU for 60 h time interval and OR rates increased
to double (Rahman, 2008). It is not clear whether this increment of OR
rates was the effect of time interval or hormonal dose rates or combined
effects of time interval and hormonal dose rates. However, decreasing
hormonal dose rates alone might not be responsible for increasing OR rates
as both higher and lower dose rates of hormones at 36 h time interval
provided similar OR rates in the previous studies in our laboratory. Timeline
of significant finding in superovulation of does has been shown in Table
The value of estrus synchronization is vital in goats as the duration
of both estrous cycle and estrus is variable and estrus detection cannot
be accomplished safely without a buck. Until now a number of studies have
been performed to synchronize the estrous cycle of goats as well as to
superovulate to increase the reproductive efficiency and genetic gain
through the use of ARTs like Artificial Insemination (AI), Laproscopic
Ovum Pick-Up (LOPU), In Vitro Production (IVP), Intracytoplasmic
Sperm Injection (ICSI) or Somatic Cell Nuclear Transfer (SCNT). Through
the application of findings from these studies reproductive performances
of goat increased in some extent. Recently, estrus synchronization and
superovulation received tremendous attention because of the rapid development
of IVP and NT technologies. However, of all the estrus synchronization
and superovulation protocols in use to date, not a single one fulfills
all expectations concerning predictability and reliability of the response.
The variability in number of ovulations and yield of viable oocytes or
embryos remains the main drawback. Therefore, more studies are required
to solve these problems.
The authors wish to thank Islamic Development Bank (IDB) for providing
an IDB Merit Scholarship to the first author. This work was supported
by grants from MOSTI Special Project (Grant Number 01-02-03-0696) and
IPPP (Grant Number Vote F-0179/2004D, 0145/2005D and P0170/2006C).
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