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Monitoring and Controlling Follicular Activity in Camelids Tibary2017
Monitoring and Controlling Follicular Activity in Camelids Tibary2017
Theriogenology
journal homepage: www.theriojournal.com
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.
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
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].
Fig. 2. Maximum uterine edema and ontrcation at the peak follicular growth (arrow 2.3. Factors affecting follicular dynamics
indicated cranial aspect of the uterus).
The major factors influencing follicular dynamics are puberty,
season, postpartum, lactation and nutrition. Studies on age at pu-
maximize ovulation rate [34]. Mating in absence of seminal plasma berty in the female camelids are very scarce and limited to field
(urethrotomized males) does not induce ovulation [37]. Adminis- observation. In well fed animals, follicular wave start as early as 4
tration of bNGF by various routes (IV, IM or intrauterine) induced months in alpacas, 6 months in llamas and 18 months in camels.
LH surge however the dose required is higher with the intrauterine However, under traditional management, puberty may be delayed
route [38]. The bNGF seems to have a luteotrophic effect on the until 3 or 4 years in camels [6,47].
corpus luteum in llamas [39e41]. However, this effect was not Seasonal variation of ovarian activity of female camelids has
observed after intrauterine administration [42]. been described in both OWC [6] and NWC [48]. However, the
In absence of copulation, ovulation can be reliably induced by control of this apparent seasonality of reproduction in camelids
GnRH (Buserelin 8 mg NWC, 20 mg camels; GnRH 20e50 mg NWC, remains poorly studied. In camels, slaughterhouse studies show a
100 mg camels) or hCG (NWC 500e750 IU IV, Camels 1500e3000 IU significantly lower follicular activity (number and size) and oocyte
IV) as long as a growing or mature follicle is present (Fig. 3). In quality during the non-breeding season [49]. However, some fe-
llamas, there is no difference in ovulation rate, interval to ovulation males continue to have normal follicular activity outside of the
and luteal development whether ovulation is induced by copula- defined breeding season [50]. Although some studies in camels
tion, im administration of LH or GnRH [43]. In camels, optimal have shown some degree of control of ovarian follicular activity by
ovulation rate is achieved when the dominant follicle is at least photoperiod [51], several aspects of the interaction between
11 mm in diameter [44]. photoperiod, temperature and nutrition remain to be elucidated
Ovulation occurs on average 30 h after mating. Both ovaries are [52,53]. In the dromedary, seasonal variation in follicular activity
equally active and alternation of ovulation between ovaries occurs may be exacerbated by lactation. In one study, lactating dromedary
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).
A. Tibary / Theriogenology 109 (2018) 22e30 25
females had smaller dominant follicles at the beginning of the aspiration or LH treatment are effective in inducing follicular wave
breeding season than non-lactating females [54]. synchronization [57].
Postpartum resumption of follicular activity occurs in NWC Ovulation synchronization using a combination of GnRH and
within 5 days of delivery and good conception rates are obtained by PGF2a was investigated in camels. Timed breeding on day 22
2e3 weeks postpartum [55,56]. There seem to be an interaction following a series of treatment (GnRH on Day 0, PGF2a on day 7,
between lactation and ovarian activity. In llamas, lactation was GnRH on Day 10, PGF2a on day 17) resulted in pregnancy rates of
associated with decreased diameter of the dominant follicle [57] 46e60%. However, this study lacked a control group [76]. In Bac-
and CL size and pregnancy rate following embryo transfer were trian camels, two injections of GnRH at 14 days interval provided a
lower in lactating female alpacas [58]. OWC have a slightly delayed better synchronization of follicular waves and response to super-
postpartum resumption of ovarian activity and adequate concep- stimualtion with eCG and FSH [77].
tion rate which occurs between 30 and 45 days postpartum A study in our laboratory did not show any advantage any
[3,59,60]. However, prolonged lactational anestrus is frequent in advantage in terms of synchronization of follicular wave, ovulation
camels reared under desert conditions and may last several rate and pregnancy rate with a treatment consisting of 2 injection
months. This long lactational anestrus is one of the reason why of GnRH at one week interval followed by PGF2a at 14 days (Fig. 4)
MOET has a great impact on the generation interval and genetic [78].
improvement in camels [6,47]. Early weaning in camels hastens
postpartum follicular activity and shorten the inter-calving in- 3.2. Progesterone treatment
tervals in intensive camel production systems [47,61].
Clinical and experimental observations show a pronounced ef- Progestogen treatments that have been tested in camelids
fect of nutrition on ovarian activity. In llamas, females under include daily progesterone injection (50e100 mg in SAC and
nutritional restriction (BCS ¼ 2.5) experience follicular suppression, 100e150 mg in camels), intravaginal devices PRIDs or CIDRs with
lower CL development and lower concentration of progesterone 1.38 g or 1.9 g progesterone in camels, CIDRs 0.3 g progesterone and
after ovulation than females averaging a BCS of 3.9 [62]. In alpacas, Medroxyprogesterone acetate (MAP) sponges in llamas and alpacas
administration of leptin prior to induction of ovulation improved CL or subcutaneous implants of norgestomet (3 mg) in llamas and
size and progesterone levels [63]. These studies as well as the ef- alpacas. The length of treatment varies generally from 7 to 14 days
fects of lactation on ovarian follicular dynamics confirm the effect (OWC [30,64,68]; camels [14,30,79]).
of negative energy balance on follicular dynamics and CL quality. A 9 day treatment with MAP vaginal sponges (60 mg) was
shown to synchronize follicular activity in llamas and produce a
3. Synchronization of follicular waves preovulatory follicle 6 days after treatment [80]. In llamas, CIDRs
(0.33 mg progesterone) treatment for 16 days reduced follicular
Synchronization of follicular waves is important for develop- diameter from day 5 [81]. Similar results were obtained in our
ment of fixed time artificial insemination and embryo transfer laboratory in llamas and alpacas with a 14 day treatment
programs [14,64]. Methods used in ruminant species have been (Figs. 5e7). In vicunas, treatment with CIDRs for 5 days exerted a
adapted to camelids with varying degrees of success. Several ap- negative effect on follicular development and allowed a better
proaches have been used to control ovarian follicular dynamics and superstimulation response to eCG [82].
eliminate dominant follicles prior to gonadotropin treatment. In llamas, intravaginal devices containing 0.5 mg of progester-
These include manual ablation, ultrasound guided aspiration of the one seem to provide better control of follicular activity and provide
dominant follicles or initiation of treatment following a period better response to superovulation with eCG. The shape and area of
progestogen treatment [65e69]. There are limited observations on contact of the vaginal device for progesterone delivery may affect
hormonal inhibition of follicular activity. In one study on alpacas, absorption of progesterone [83]. Vaginal devices containing 0.78 g
daily administration of Buserelin (50 mg/female SQ) for 10 days progesterone (Cue-mate®) inserted for 7 days reduced follicular
results in suppression of follicular activity starting on the 6th day of development. A new dominant follicle was available in all females 6
treatment [70]. days after removal of the device [84].
In camels, there are conflicting reports on the efficacy of PRIDs
3.1. Follicular ablation
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- In summary, progesterone therapy in camelid suppresses the
tion, these devices have been associated with increased sponta- growth of large follicles but does not completely suppress follicular
neous ovulation in some studies. Treatment with PRIDs containing activity and therefore is not efficient in synchronizing follicular
1.55 g of progesterone for 7 days did not synchronize follicular wave emergence and fixed time breeding [6,69,79,86].
waves [85,86]. However camels treated for 17 days with PRIDs The combination of estradiol and progesterone has been shown
containing 1.9 g progesterone and receiving a large dose of eCG to be more effective in the control of follicular wave in OWC in some
(3000 IU) had a better synchrony of follicular growth [87]. Treat- studies [91] but not others [68]. In llamas, daily pretreatment with
ment with CIDRs containing 1.38 g of progesterone for 10 days did 100 or 150 mg progesterone for 5 days after a single injection of
not synchronize follicular waves in the non-breeding season [9]. In estradiol benzoate (1 mg) resulted in a higher embryo recovery rate
a recent study, 70 and 75% of camels had a preovulatory follicle on following superstimulation in some trials [92]. In our laboratory,
days 16 and 18 respectively after treatment with CIDRs containing daily administration of estradiol and progesterone for 7e10 days to
1.9 g of progesterone for 14 days [88]. However in there was no alpacas produced a more uniform response however the ovulatory
control (untreated) group in this study. Nogestomet implant were response was poor [93].
not efficacious in synchronizing follicular wave in Bactrian camels In llamas, a single injection of combined estradiol-17b (1 mg)
[77]. and progesterone (25 mg) provided some synchronization of
Daily injection of progesterone (50 mg, IM) for 12 days induced follicular wave but not as good as induction of ovulation or follicle
reduction follicular diameter on day 7 in llamas [89]. In camels, aspiration [57]. In camels, a single injection of estradiol benzoate
daily injections of progesterone (100 mg/day) for 10e16 days pro- (5 mg) and progesterone (100 mg) was not effective in synchroni-
vided promising results in MOET programs [66]. A recent study in zation of follicular wave [75].
our laboratory showed that long-acting progesterone injection can
be used in camels and may be more advantageous then daily in- 4. Ovarian superstimulation
jections (Fig. 8) [90].
4.1. Induction of follicular activity in anestrous females
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 Single subcutaneous dose of oFSH has been tested with variable
results are obtained when the treatment is initiated in absence of results.
any follicles greater than 2 mm [14]. Porcine FSH given twice daily in decreasing doses over 3, 5, or 7
days after a 10e15 day progesterone treatment resulted also in
4.2.1. Follicle stimulating hormone (FSH) superstimulation of dromedary female [14,66]. The interval from
Both ovine (oFSH) and porcine (pFSH) FSH, have been for pFSH treatment to development of a mature follicle (10e16 mm in
ovarian superstimulation with variable success [6]. The manner of diameter) varies between 6 and 8 days [6,69]. Similar protocols
administration of FSH (dose, frequency and timing during the cycle) have been used for superstimulation of Bactrian camels [1,77].
has been investigated to some degree. Unfortunately detailed In llamas and alpacas, FSH alone or in combination with eCG, has
description of the treatment protocol is often not clearly presented been used following a 12 day progesterone treatment [95,96]. The
in publications. best superovulation and embryo collection results were obtained
In the dromedary, a total dose of 20e30 mg units of oFSH is following administration of pFSH twice a day for 5 days in
given over 6 days (two injections daily) starting 2 days before and decreasing doses (32, 27, 22, 17 and 12 mg, im) [68,96]. The number
up to 1 day after completion of a 7-day course of progesterone of embryos obtained after pFSH stimulation is generally low. Al-
treatment by intravaginal device (PRID) [85]. FSH was also given in pacas reportedly produce a more variable response to super-
a single small dose (3.3 units) followed by an injection of 3500 IU of stimulation protocols than llamas [68].
eCG, resulting in an average of 7 embryos recovered per treated
female [86]. In another study, oFSH was given twice a day (1e3 mg 4.2.2. Equine chorionic gonadotropin (eCG)
per injection) during 3e5 days following a 10e15 day course of Superstimulation with eCG has been extensively used in cam-
progesterone treatment (100 mg per day during 10e15 days) [66]. 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 effects of various factors on ovarian activity. This technique has
regime. The dose of eCG used vary from 1500 to 6000 in camels, replaced the need for laborious endocrine assays. Factors affecting
500e2000 IU in the llama and 500 to 750 in alpaca and vicun ~ as follicular dynamics and in particular season and nutrition need
[30]. more investigation. Multiple approaches to synchronize follicular
In the dromedary, eCG given as a single injection of 2000 IU, wave have been adapted from other species but met with variable
2500 IU or 4000 IU, one day before or one day after PRID removal, results. Progesterone therapy alone or in combination with estra-
resulted in ovulation in 40% of treated animals. Only 42% of ovu- diol shows some efficacy for superstimulation in MOET programs
lating females yielded one or more embryos. The interval from PRID but is not sufficient for fixed time mating or artificial insemination.
removal to mating was 5 and 4.5 days respectively for females Ovulation synchronization protocol may be more suitable for timed
receiving 2500 IU and 4000 IU of eCG. This interval was one day breeding and artificial insemination.
shorter in females treated with eCG one day before removal of PRID
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