Theriogenology 109 (2018) 22e30

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Theriogenology
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Monitoring and controlling follicular activity in camelids

Ahmed Tibary
Comparative Theriogenology, Department of Veterinary Clinical Science, College of Veterinary Medicine, Center for Reproductive Biology, Washington State
University, USA

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

Article history: This paper reviews that state of our knowledge concerning follicular wave dynamics, monitoring and
Received 1 December 2017 manipulation. All camelids have overlapping follicular waves in absence of ovulation which is induced by
Accepted 1 December 2017 a seminal plasma factor (bNGF). The interval between follicular waves varies. The size of the ovulatory
Available online 8 December 2017
follicle varies between 11 and 25 mm in camels and between in 6 and 13 mm in South American
Camelids. The interval between induction of ovulation and next ovulatory follicle is 15 ± 1 day for all
Keywords:
camelids. Follicular activity is best monitored by transrectal ultrasonography. Progesterone therapy for 7
Camelidae
e15 days seems to suppress follicular dominance but does not completely inhibit follicular recruitment.
Ovarian activity
Nutrition
Combination of estradiol and progesterone seems to provide better control of follicular activity. Both
Artificial breeding methods have provided variable results in the synchronization of follicular waves. Combination of in-
duction of ovulation with GnRH and luteolysis at predetermined times shows some promise in syn-
chronization of follicular dominance. These synchronization protocols require further investigation in
order to provide practical approaches for fixed-time breeding. Ovarian superstimulation with FSH and
eCG alone or in combination is somewhat successful. The best results are obtained when treatment is
initiated at the emergence of a new follicular wave after induction of ovulation or following treatment
with progesterone for 7e14 days. However, response remains extremely variable particularly in terms of
ovulation rate and number of recovered embryos. Sources of this variability need to be studied including
the effects of season, nutrition, doses and frequency of administration of gonadotropin.
© 2017 Elsevier Inc. All rights reserved.

1. Introduction biotechnologies, such as artificial insemination (AI) and embryo

The camelidae family includes 6 major species traditionally
subdivided into Old-world camelids (OWC) or camels (Camelus
dromedarius and Camelus bactrianus) and New-world camelids
(NWC) (Lama glama, Lama guanicoe, Vicugna pacos and Vicugna
vicugna). Domestic camelids (camels, llamas and alpacas) are
important livestock in several parts of the word. It is predicted that
these species will be increasingly important for animal production
in harsh environments due to their adaptive characteristics to
desert (camelids) or altiplano (llamas and alpacas). Wild camelids
(vicugna, guanaco and some Bactrian camels) are important re-
sources that are increasingly threatened due to habitat degrada-
tion. Reproductive management and multiplication of wild
camelids through the use of interspecies embryo transfer has been
investigated as a mean for the preservation of these species [1,2].
Efficient reproductive management and use of reproductive
transfer (ET), require a thorough understanding of follicular dy-
namics and factors governing ovarian activity. Prior to 1990's, most
studies on ovarian activity in camelids relied on behavioral and
hormonal observation [3]. Effort to characterize follicular wave
dynamics was mostly driven by the desire to develop AI and ET
technologies. The widespread use of ultrasonography allowed in
situ observation of ovarian follicular activity and better character-
ization of follicular dynamics, ovulation and monitoring of re-
sponses to treatments [4]. The present paper discusses the state of
our knowledge on ovarian follicular dynamics in camelids, factors
governing it, and its monitoring and manipulation.
2. Follicular dynamics in camelids
2.1. Follicular dynamics in absence of ovulation

Ultrasonographic and hormonal studies in the mid to late 1990's

helped define follicular dynamics in several domestic camelids
E-mail address: tibary@vetmed.wsu.edu. species [5e8]. Field and experimental observations demonstrated

https://doi.org/10.1016/j.theriogenology.2017.12.011
0093-691X/© 2017 Elsevier Inc. All rights reserved.
 A. Tibary / Theriogenology 109 (2018) 22e30 23

that ovarian activity in the female camelid is not seasonal under

optimal nutritional condition [9]. However, under some conditions,
female camels may display seasonal variation in follicular activity
that may be partly regulated by photoperiod. All camelid species
are induced ovulators, thus in absence of ovulatory stimulus
(mating or hormonal induction), follicular waves occur in an
overlapping manner [6,10]. Follicular waves present the typical
phases of recruitment, growth, maturation and regression. The
duration of each of these stages of the follicular waves is variable
(Table 1).
Follicles that surpass a certain diameter (25 mm in camels,
12 mm in alpacas, 13 mm llama) have decreased ovulatory
response. Some of these follicles may continue to grow and develop
into large anovulatory follicles that may become hemorrhagic or
luteinized (Fig. 1). Anovulatory hemorrhagic follicles (AHF) seems
to be more frequent in camels [4,6] and llamas [11] than in other
camelids species. The tendency for development of AHF seems to
be dependent on individual female. The pathophysiology of AHF is
poorly understood [6]. Clinical observations suggest that some of
these AHF may be triggered by metabolic disorders in the female as
well as adverse climatic conditions. Presence of AHF does not seem
to disturb follicular wave patterns.
Follicular dynamic is dependent on FSH and LH stimulation
[12e14]. Presence of 2 or more co-dominant follicles is not un-
common in camelids and may occur in up to 40% of follicular wave
(Camels [4,15,16], NWC [17]). Behavioral changes during the
follicular wave are not strongly correlated to size of the follicle and
readiness for ovulation (Camels [4,18]; NWC [19e22]). Therefore
the best method for monitoring follicular dynamics is transrectal
ultrasonography. At peak follicular development (pre-ovulatory
stage), the uterus is toned and present characteristic edema pattern
on ultrasonography (Fig. 2). Color-Doppler ultrasonography can be Fig. 1. Ultrasonographic appearance of anovulatory follicles in the dromedary. A)
used to monitor blood flow to the follicle during various stages of 48.6 mm thin-walled anovulatory follicle with anechoic fluid, b) 80 mm thick-walled
development. Blood flow to the dominant follicle increased with anovulatory follicle with echogenic fluid, c) 42 mm anovulatory follicle showing
follicular growth [23]. some hemorrhage and intralumunal fibrin, d) 83.3 mm anovulatory hemorrhagic fol-
licle (AHF) with characteristic multiloculated appearance, e) and f) AHF with varying
degrees of luteinization.
2.2. Ovulation

following mating in presence of a mature follicle in OWC [31,32]

The induced nature of ovulation in camelids has long been
and NWC [12,13]. The second group of studies led to the hypothe-
suspected based on clinical and hormonal studies [30]. However,
sis of the presence of an ovulation-inducing factor (OIF) within the
the major breakthroughs in defining the mechanisms of induction
seminal plasma [33]. Recent studies identified the OIF as b nerve
of ovulation came in two main groups of studies. The first
growth factor (bNGF) in llamas and alpacas [34,35] and in camels
demonstrated the hypothalamo-pituitary response to mating rep-
[36]. Both bNGF and endometrial inflammation are required to
resented by a sharp increase in luteinizing hormone within minutes

Table 1
Characteristics of follicular dynamics and corpus luteum development in camelids Dromedary [4,5,24,25]; Alpaca and llama [7,26]; Bactrian camel [27,28]; Vicuna [17];
Guanoco [29].

Parameter C. dromedarius C. bactrianus V. pacos L. glama V. vicugna L. guanacoe

a
Follicular wave phases duration
Growth (days) 10.5 ± 0.5 10.9 ± 3 3e9 3e9 3.0 ± 0.2 7.0 ± 2.4
Maturation (days) 7.6 ± 0.8 7 ± 4.2 2e8 2e8 1.4 ± 0.1 3.0 ± 1.2
Regression (days) 11.9 ± 0.8 11.9 ± 4.2 3e8 3e8 2.0 ± 0.3 5.2 ± 2.1
Ovulatory follicle characteristica
Minimum size (mm) 9 9 6 7 6.2 7.2
Growth rate (mm/day) 1.8 0.7e1.8 0.43 0.5e0.9 1.8 ± 0.1 1.0 ± 0.3
Average size (mm) 10e18 10e18 8e10 9e12 8.4 ± 0.9 10.2 ± 2.1
Maximum size (mm) 25 25 12 13 11.2 16.1
Incidence of anovulatory follicles (%) 40e50 ? 5 10e40 ? ?
Anovulatory follicle regression (days) 8e45 ? ? 4e22 ? ?
Corpus luteum characteristics
Interval from mating to ovulation (hours) 32 to 40 30 to 48 28 to 30 27e36 e e
Size (mm) 15e25 15e25 11e15 11e18 e e
Day at CL maximum size 7.2 ± 1.7 7.3 7e8 8 e e
Days post-ovulation to complete luteolysis 10 ± 1.2 10.5 10e12 10e12 e e
a
Extreme variation in onset of postpartum ovarian follicular activity is primarily due to nutritional condition and effect on lactation anestrus and seasonality.
24 A. Tibary / Theriogenology 109 (2018) 22e30
Fig. 2. Maximum uterine edema and ontrcation at the peak follicular growth (arrow
indicated cranial aspect of the uterus).
maximize ovulation rate [34]. Mating in absence of seminal plasma
(urethrotomized males) does not induce ovulation [37]. Adminis-
tration of bNGF by various routes (IV, IM or intrauterine) induced
LH surge however the dose required is higher with the intrauterine
route [38]. The bNGF seems to have a luteotrophic effect on the
corpus luteum in llamas [39e41]. However, this effect was not
observed after intrauterine administration [42].
In absence of copulation, ovulation can be reliably induced by
GnRH (Buserelin 8 mg NWC, 20 mg camels; GnRH 20e50 mg NWC,
100 mg camels) or hCG (NWC 500e750 IU IV, Camels 1500e3000 IU
IV) as long as a growing or mature follicle is present (Fig. 3). In
llamas, there is no difference in ovulation rate, interval to ovulation
and luteal development whether ovulation is induced by copula-
tion, im administration of LH or GnRH [43]. In camels, optimal
ovulation rate is achieved when the dominant follicle is at least
11 mm in diameter [44].
Ovulation occurs on average 30 h after mating. Both ovaries are
equally active and alternation of ovulation between ovaries occurs
Fig. 3. Effect of follicular size on ovulatory response after GnRH intramuscular GnRH injection in camels (100 mg) and alpacas (50 mg) (12e25 females per group) (Tibary A,
unpublished).
frequently but not systematically [6]. Double ovulations are com-
mon in most domestic camelids in good health and nutritional
status [15]. Triple and quadruple ovulations have also been docu-
mented in the dromedary camel [4,16]. Spontaneous ovulation has
been described in up to 5% of the follicular wave in llamas and
camels [45]. This phenomenon seems to be more common in
lactating animals [25].
Follicular recruitment in mated females start 2e4 days
following ovulation and results in an available mature follicle
within 2e4 days of completion of luteolysis which occurs around
day 10 post-ovulation. This short luteal phase results in a single
follicular wave per cycle in the majority of the females. Preliminary
data in our laboratory show that 90% of the female (camels and
alpacas) have only one follicular wave per ovulatory cycle. Thus
after a sterile mating or hormonal induction of ovulation, the
average interval between two consecutive ovulatory follicles is 14
days in all camelids [6,46].
2.3. Factors affecting follicular dynamics
The major factors influencing follicular dynamics are puberty,
season, postpartum, lactation and nutrition. Studies on age at pu-
berty in the female camelids are very scarce and limited to field
observation. In well fed animals, follicular wave start as early as 4
months in alpacas, 6 months in llamas and 18 months in camels.
However, under traditional management, puberty may be delayed
until 3 or 4 years in camels [6,47].
Seasonal variation of ovarian activity of female camelids has
been described in both OWC [6] and NWC [48]. However, the
control of this apparent seasonality of reproduction in camelids
remains poorly studied. In camels, slaughterhouse studies show a
significantly lower follicular activity (number and size) and oocyte
quality during the non-breeding season [49]. However, some fe-
males continue to have normal follicular activity outside of the
defined breeding season [50]. Although some studies in camels
have shown some degree of control of ovarian follicular activity by
photoperiod [51], several aspects of the interaction between
photoperiod, temperature and nutrition remain to be elucidated
[52,53]. In the dromedary, seasonal variation in follicular activity
may be exacerbated by lactation. In one study, lactating dromedary
 A. Tibary / Theriogenology 109 (2018) 22e30
females had smaller dominant follicles at the beginning of the
breeding season than non-lactating females [54].
Postpartum resumption of follicular activity occurs in NWC
within 5 days of delivery and good conception rates are obtained by
2e3 weeks postpartum [55,56]. There seem to be an interaction
between lactation and ovarian activity. In llamas, lactation was
associated with decreased diameter of the dominant follicle [57]
and CL size and pregnancy rate following embryo transfer were
lower in lactating female alpacas [58]. OWC have a slightly delayed
postpartum resumption of ovarian activity and adequate concep-
tion rate which occurs between 30 and 45 days postpartum
[3,59,60]. However, prolonged lactational anestrus is frequent in
camels reared under desert conditions and may last several
months. This long lactational anestrus is one of the reason why
MOET has a great impact on the generation interval and genetic
improvement in camels [6,47]. Early weaning in camels hastens
postpartum follicular activity and shorten the inter-calving in-
tervals in intensive camel production systems [47,61].
Clinical and experimental observations show a pronounced ef-
fect of nutrition on ovarian activity. In llamas, females under
nutritional restriction (BCS ¼ 2.5) experience follicular suppression,
lower CL development and lower concentration of progesterone
after ovulation than females averaging a BCS of 3.9 [62]. In alpacas,
administration of leptin prior to induction of ovulation improved CL
size and progesterone levels [63]. These studies as well as the ef-
fects of lactation on ovarian follicular dynamics confirm the effect
of negative energy balance on follicular dynamics and CL quality.
3. Synchronization of follicular waves
Synchronization of follicular waves is important for develop-
ment of fixed time artificial insemination and embryo transfer
programs [14,64]. Methods used in ruminant species have been
adapted to camelids with varying degrees of success. Several ap-
proaches have been used to control ovarian follicular dynamics and
eliminate dominant follicles prior to gonadotropin treatment.
These include manual ablation, ultrasound guided aspiration of the
dominant follicles or initiation of treatment following a period
progestogen treatment [65e69]. There are limited observations on
hormonal inhibition of follicular activity. In one study on alpacas,
daily administration of Buserelin (50 mg/female SQ) for 10 days
results in suppression of follicular activity starting on the 6th day of
treatment [70].
3.1. Follicular ablation
Dominant follicles can be eliminated by follicular aspiration or
induction of ovulation. Removal of the dominant follicle by
ultrasound-guided aspiration provides consistent results for
ovarian superstimulation 48 h after [64]. Studies in llamas and al-
pacas, show improved embryo recovery rates when gonadotropin
treatment is started after administration of LH to synchronize
follicular wave emergence [71,72]. Initiation of gonadotropin
treatment at a specific time (2e4 days) following induction of
ovulation has been shown to be more reliable in Bactrian [1] and
dromedary camels [73,74]. In camels, follicular wave emergence
occur about 70.6 ± 1.4 h (range 60e84 h) after GnRH injection to
induce ovulation and follicular deviation occurs 58.6 ± 2.7 h (range
36e84 h) from emergence [16]. In one study on dromedary camels,
there was not difference in the percentage of females that ovulated
14 days (47% vs 40%) after follicular ablation by ultrasound-guided
transvaginal aspiration or control (saline injection), whereas 80 and
87% of females that received receptively GnRH or GnRH followed by
a luteolytic dose of cloprostenol a week later ovulated after GnRH
treatment 14 days later [75]. In llamas, follicular ablation by
25
aspiration or LH treatment are effective in inducing follicular wave
synchronization [57].
Ovulation synchronization using a combination of GnRH and
PGF2a was investigated in camels. Timed breeding on day 22
following a series of treatment (GnRH on Day 0, PGF2a on day 7,
GnRH on Day 10, PGF2a on day 17) resulted in pregnancy rates of
46e60%. However, this study lacked a control group [76]. In Bac-
trian camels, two injections of GnRH at 14 days interval provided a
better synchronization of follicular waves and response to super-
stimualtion with eCG and FSH [77].
A study in our laboratory did not show any advantage any
advantage in terms of synchronization of follicular wave, ovulation
rate and pregnancy rate with a treatment consisting of 2 injection
of GnRH at one week interval followed by PGF2a at 14 days (Fig. 4)
[78].
3.2. Progesterone treatment
Progestogen treatments that have been tested in camelids
include daily progesterone injection (50e100 mg in SAC and
100e150 mg in camels), intravaginal devices PRIDs or CIDRs with
1.38 g or 1.9 g progesterone in camels, CIDRs 0.3 g progesterone and
Medroxyprogesterone acetate (MAP) sponges in llamas and alpacas
or subcutaneous implants of norgestomet (3 mg) in llamas and
alpacas. The length of treatment varies generally from 7 to 14 days
(OWC [30,64,68]; camels [14,30,79]).
A 9 day treatment with MAP vaginal sponges (60 mg) was
shown to synchronize follicular activity in llamas and produce a
preovulatory follicle 6 days after treatment [80]. In llamas, CIDRs
(0.33 mg progesterone) treatment for 16 days reduced follicular
diameter from day 5 [81]. Similar results were obtained in our
laboratory in llamas and alpacas with a 14 day treatment
(Figs. 5e7). In vicunas, treatment with CIDRs for 5 days exerted a
negative effect on follicular development and allowed a better
superstimulation response to eCG [82].
In llamas, intravaginal devices containing 0.5 mg of progester-
one seem to provide better control of follicular activity and provide
better response to superovulation with eCG. The shape and area of
contact of the vaginal device for progesterone delivery may affect
absorption of progesterone [83]. Vaginal devices containing 0.78 g
progesterone (Cue-mate®) inserted for 7 days reduced follicular
development. A new dominant follicle was available in all females 6
days after removal of the device [84].
In camels, there are conflicting reports on the efficacy of PRIDs
Fig. 4. Proportion of female llamas that were mated, ovulated and their pregnancy rate
at 45 days. Treatment: Females (n ¼ 31) received a synchronization treatment protocol
consisting of 2 GnRH injections at 7 days interval followed by an injection of clo-
prostenol 7 days after the second injection and mated on day 25 (Day 0 ¼ First GnRH
injection). Control: females (n ¼ 10) mated based on receptivity on the same day [78].
26 A. Tibary / Theriogenology 109 (2018) 22e30
Fig. 5. Serum progesterone level in alpacas (n ¼ 7) and llamas (n ¼ 7) during and following a 14 day treatment with vaginal CIDR (0.33 mg progesterone) [78].
[85] and CIDRs [9] in synchronization of follicular waves. In addi-
tion, these devices have been associated with increased sponta-
neous ovulation in some studies. Treatment with PRIDs containing
1.55 g of progesterone for 7 days did not synchronize follicular
waves [85,86]. However camels treated for 17 days with PRIDs
containing 1.9 g progesterone and receiving a large dose of eCG
(3000 IU) had a better synchrony of follicular growth [87]. Treat-
ment with CIDRs containing 1.38 g of progesterone for 10 days did
not synchronize follicular waves in the non-breeding season [9]. In
a recent study, 70 and 75% of camels had a preovulatory follicle on
days 16 and 18 respectively after treatment with CIDRs containing
1.9 g of progesterone for 14 days [88]. However in there was no
control (untreated) group in this study. Nogestomet implant were
not efficacious in synchronizing follicular wave in Bactrian camels
[77].
Daily injection of progesterone (50 mg, IM) for 12 days induced
reduction follicular diameter on day 7 in llamas [89]. In camels,
daily injections of progesterone (100 mg/day) for 10e16 days pro-
vided promising results in MOET programs [66]. A recent study in
our laboratory showed that long-acting progesterone injection can
be used in camels and may be more advantageous then daily in-
jections (Fig. 8) [90].
Fig. 6. Serum estradiol 17b levels in alpacas and llamas with and without a 14 day
treatment with CIDRs (Group 1 ¼ 7 treated llamas, Group 2 ¼ 7 treated alpacas, Group
3 ¼ 7 untreated llamas, Group 4 ¼ 9 untreated alpacas) [78].
In summary, progesterone therapy in camelid suppresses the
growth of large follicles but does not completely suppress follicular
activity and therefore is not efficient in synchronizing follicular
wave emergence and fixed time breeding [6,69,79,86].
The combination of estradiol and progesterone has been shown
to be more effective in the control of follicular wave in OWC in some
studies [91] but not others [68]. In llamas, daily pretreatment with
100 or 150 mg progesterone for 5 days after a single injection of
estradiol benzoate (1 mg) resulted in a higher embryo recovery rate
following superstimulation in some trials [92]. In our laboratory,
daily administration of estradiol and progesterone for 7e10 days to
alpacas produced a more uniform response however the ovulatory
response was poor [93].
In llamas, a single injection of combined estradiol-17b (1 mg)
and progesterone (25 mg) provided some synchronization of
follicular wave but not as good as induction of ovulation or follicle
aspiration [57]. In camels, a single injection of estradiol benzoate
(5 mg) and progesterone (100 mg) was not effective in synchroni-
zation of follicular wave [75].
4. Ovarian superstimulation
4.1. Induction of follicular activity in anestrous females
Induction of follicular activity with eCG or FSH in prepubertal
animals and during lactational and seasonal anestrus is possible
and was demonstrated in dromedaries [94]. However, this is not a
viable management option for natural mating and may only be
useful for in vitro or in vitro (follicular aspiration) embryo
production.
4.2. Superstimulation for MOET programs
Approaches to ovarian superstimulation in camelids have been
largely adapted from protocols used in ruminants. The primary
hormones used are FSH and eCG alone or in combination. As for
other species, response to these hormones depends on timing of
initiation of treatment in relationship to follicular dynamics, dose
and schedule on administration, and individual variation. Response
to gonadotropin treatment is largely affected by the stage of
follicular wave recruitment and the presence of a dominant folli-
cles. Although FSH and eCG treatments have been initiated during
 A. Tibary / Theriogenology 109 (2018) 22e30 27

Fig. 7. Proportion of females with ovulatory follicles (9e12 mm in llamas; 8e11 mm in alpacas) following a 14 days CIDR (0.33 mg progesterone). Group 1 ¼ 7 treated llamas, Group
2 ¼ 7 treated alpacas, Group 3: 7 untreated llamas, Group 4: 9 untreated alpacas [78].

the receptive or luteal phase of the cycle with some success, better
results are obtained when the treatment is initiated in absence of
any follicles greater than 2 mm [14].
4.2.1. Follicle stimulating hormone (FSH)
Both ovine (oFSH) and porcine (pFSH) FSH, have been for
ovarian superstimulation with variable success [6]. The manner of
administration of FSH (dose, frequency and timing during the cycle)
has been investigated to some degree. Unfortunately detailed
description of the treatment protocol is often not clearly presented
in publications.
In the dromedary, a total dose of 20e30 mg units of oFSH is
given over 6 days (two injections daily) starting 2 days before and
up to 1 day after completion of a 7-day course of progesterone
treatment by intravaginal device (PRID) [85]. FSH was also given in
a single small dose (3.3 units) followed by an injection of 3500 IU of
eCG, resulting in an average of 7 embryos recovered per treated
female [86]. In another study, oFSH was given twice a day (1e3 mg
per injection) during 3e5 days following a 10e15 day course of
progesterone treatment (100 mg per day during 10e15 days) [66].
Single subcutaneous dose of oFSH has been tested with variable
results.
Porcine FSH given twice daily in decreasing doses over 3, 5, or 7
days after a 10e15 day progesterone treatment resulted also in
superstimulation of dromedary female [14,66]. The interval from
pFSH treatment to development of a mature follicle (10e16 mm in
diameter) varies between 6 and 8 days [6,69]. Similar protocols
have been used for superstimulation of Bactrian camels [1,77].
In llamas and alpacas, FSH alone or in combination with eCG, has
been used following a 12 day progesterone treatment [95,96]. The
best superovulation and embryo collection results were obtained
following administration of pFSH twice a day for 5 days in
decreasing doses (32, 27, 22, 17 and 12 mg, im) [68,96]. The number
of embryos obtained after pFSH stimulation is generally low. Al-
pacas reportedly produce a more variable response to super-
stimulation protocols than llamas [68].
4.2.2. Equine chorionic gonadotropin (eCG)
Superstimulation with eCG has been extensively used in cam-
elids. In general, a single dose is administered intramuscularly one

Fig. 8. Mean (±SEM) serum progesterone concentration in female camels (n ¼ 12) following intramuscular injection of 5 mL of BioRelease P4 LA 300 containing 300 mg or
progesterone/ml on day 0 [90].
28 A. Tibary / Theriogenology 109 (2018) 22e30
day before or on the day of completion of a 5e15 days progesterone
regime. The dose of eCG used vary from 1500 to 6000 in camels,
500e2000 IU in the llama and 500 to 750 in alpaca and vicun ~ as
[30].
In the dromedary, eCG given as a single injection of 2000 IU,
2500 IU or 4000 IU, one day before or one day after PRID removal,
resulted in ovulation in 40% of treated animals. Only 42% of ovu-
lating females yielded one or more embryos. The interval from PRID
removal to mating was 5 and 4.5 days respectively for females
receiving 2500 IU and 4000 IU of eCG. This interval was one day
shorter in females treated with eCG one day before removal of PRID
[85,86]. When eCG (2000e3000 IU) is administered to females
with no dominant follicle, the interval from treatment to mating
(follicular diameter of 12 mm) is relatively constant (8 days) [30].
Follicular response is variable (0e19) with about 20% of the females
not responding [14].
In the llama, eCG (1000 IU) was used following progesterone
priming either in the form of natural corpus luteum (ovulation
induced by hCG or GnRH injection), CIDR's or subcutaneous im-
plants [97]. Follicular response was variable (0e13 follicles) and the
number of ovulations ranged from 0 to 7 with a mean number of
embryos collected of 1.3e2.3 per donor (range 0e6). Follicles
reached the mature size (9e13 mm) 5e11 days following eCG
treatment. Several treated females show premature luteinization
7e9 days following eCG treatment. Increasing the dose of eCG to
2000 IU results in an increase in incidence of anovulatory follicles.
In the alpaca, injection of 750 IU of eCG resulted in average 3.7
embryos per ovulating female [95,96].
The main disadvantage of eCG is the high incidence of follicular
luteinization and disturbance of ovulation probably due to its long
half-life. Dromedary females tend to become refractory to eCG
following multiple use. This suggests that at least in the camel, the
risk of inducing anti-eCG antibodies is real [69].
Superstimulation protocols combining both FSH and eCG have
been published in alpacas, llamas [68], vicunas [98] and camels
[69]. In general, these protocols do not provide much superiority to
protocols using FSH alone.
Superstimulation treatments of the female camelidae are far
from being perfect. Ovulation response and embryo yield remain
highly variable [6,14,64,68]. The major problems that need to be
addressed are: the high incidence of non-responsive females
(20e30%), incidence of follicular luteinization, hyperstimulation in
some females and loss of efficacy after multiple treatments. In
addition, the recovery rate number of embryos recovery/number of
corpora lutea is low (40%). Sources of variations that need to be
investigate in response to superstimulation include species, breed,
and individual animal variation.
4.2.3. Immunization against inhibin
Immunization again inhibin results in very high levels of
circulating FSH and consequently an increase in the number or
recruited follicles which will continue to grow until maturation. In
the dromedary, immunization against inhibin resulted in encour-
aging ovulatory response. An increase in ovulation number (4e10)
was observed in 60% of the immunized females [69]. Recent studies
showed a high rate of triple of ovulations up to 5 months from the
initial immunization [99,100].
5. Conclusion
In the last 3 decades, research on camelids reproduction has
helped further our knowledge on follicular dynamics in these
species. Transrectal ultrasonographic monitoring of follicular waves
is now current practice in all species of camelids. This has been an
effective tool in the management of breeding and to monitoring
effects of various factors on ovarian activity. This technique has
replaced the need for laborious endocrine assays. Factors affecting
follicular dynamics and in particular season and nutrition need
more investigation. Multiple approaches to synchronize follicular
wave have been adapted from other species but met with variable
results. Progesterone therapy alone or in combination with estra-
diol shows some efficacy for superstimulation in MOET programs
but is not sufficient for fixed time mating or artificial insemination.
Ovulation synchronization protocol may be more suitable for timed
breeding and artificial insemination.
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