CHAPTER 120 Ovarian Synchronization and Induction of Ovulation in Llamas and Alpacas
Control of ovarian folliculogenesis in South American camelids would improve efficiency of supervised matings and facilitate the development of assisted breeding in all camelids. Conception due to a single mating may be maximized by inducing emergence of a new dominant follicle at a known time to allow mating to be scheduled when the dominant follicle is capable of ovulating a competent oocyte.
Real-time ultrasonography has allowed investigators to observe ovarian follicular dynamics reliably, to establish the presence of follicular waves, and to determine appropriate times of exogenous hormone treatment in domestic livestock including South American camelids.1–6 Unfortunately, it is not possible to identify whether a follicle is growing or regressing on the basis of a single ultrasonographic examination, and multiple examinations may be impractical and uneconomical. It would be an advantage to control ovarian follicular growth using exogenous hormones so that a dominant follicle develops at a specific, repeatable time after completion of a treatment protocol, which may reliably be induced to ovulate and release an oocyte of relatively high fertility.
The complex control mechanisms that regulate the development of ovarian follicles through different physiologic stages has delayed development of a simple exogenous hormonal treatment that gives a synchronized new wave emergence in animals regardless of stage of follicle wave at the time of treatment.7 The antral follicle of spontaneously ovulating mammals has a changing dependency on follicle-stimulating hormone (FSH), luteinizing hormone (LH), and other growth factors as it develops during a follicular wave.8 The development of sensitive FSH and LH assays in camelids would allow investigators to examine the characteristics of gonadotropin secretion and determine whether the assumptions that FSH and LH work in a similar fashion in induced and spontaneous ovulators are valid. If the assumptions are correct, the response of the ovary to endogenous or exogenous hormones would depend on the stage of follicular development and the physiologic status of the ovaries at the time of treatment.
Maximum fertility in female South American camelids has been proposed to occur when the dominant ovarian follicle is greater than 6 mm in diameter and capable of responding to an ovulatory stimulus, and either growing or mature but not regressing.2,9 Follicular growth is similar from day 0 to day 10 after new wave emergence in alpacas, regardless of subsequent interwave interval and the newly emerged follicle attains an average diameter of 7 mm, 6 days after new wave emergence.6 Pregnancy rates are reduced in cattle when aged oocytes are ovulated from dominant follicles that are persistent for longer than 10 days.10 Reduced fertility may also be associated with oocyte aging in camelids that ovulate when the dominant follicle is postmature.7
Removal of the existing dominant follicle may be achieved hormonally in domestic species either by inducing atresia or ovulation. Both mechanisms result in a decline in plasma estradiol and inhibin concentrations followed by a surge in FSH and emergence of a new follicular wave.7
INDUCTION OF FOLLICULAR ATRESIA
Estradiol
Exogenous 17β-estradiol and estradiol benzoate have been used in cattle and sheep to transiently suppress plasma FSH concentrations in a dose-dependent manner, thus exerting an atretogenic effect on FSH-dependent follicles early in the follicular wave and provoking synchronous emergence of a new wave.11–13
A single intramuscular dose of 0.5 mg or 2 mg 17β-estradiol apparently induced follicle regression and new wave emergence in alpacas regardless of the stage of follicular development, suggesting that estradiol has a role in gonadotropin regulation in this species.14 However, subsequent studies in alpacas treated at random stages of ovarian follicular development have shown that a single intramuscular injection of 1 mg 17β-estradiol or 2 or 5 mg estradiol benzoate (Cidirol: InterAg), with or without simultaneous injection of progesterone (Progesterone: Jurox), had no effect on follicular wave turnover.6)
Progesterone
Various doses and delivery methods of progesterone have been tested in camelids in attempts to manipulate follicular waves, based on the observations that dominant follicles in llamas are smaller in diameter, exhibit a shorter interwave interval, and produce less estradiol during the luteal phase.2,15,16 These features of follicular growth in llamas in the presence of a corpus luteum may be due to the negative feedback effects of progesterone on LH secretion, as demonstrated in female cattle, in which follicular growth may be suppressed in a dose-dependent manner using exogenous progesterone.10,17
Intravaginal Progestagen Devices
Different intravaginal devices such as progesterone-releasing intravaginal devices (PRID), controlled internal drug releasing (CIDR) devices, and sponges have been used to deliver progesterone or progestagen to camelids (Table 120-1).
Table 120-1 Exogenous Progesterone Treatments Used in Llamas and Alpacas
| Reference | Species | Source of Progesterone |
|---|---|---|
| Bourke et al. 199218 | Llama | (a) endogenous progesterone (corpus luteum) |
| (b) 3 mg norgestamet implant SC for 7 days | ||
| (c) 2 × CIDR 0.3 g progesterone for 9 days | ||
| Correa et al. 199419 | Llama/alpaca | 12.5 mg progesterone IM once a day for 12 days |
| Bourke et al. 199520 | Llama | (a) endogenous progesterone (corpus luteum) |
| (b) 3 mg norgestamet implant SC for 7 days | ||
| Aba et al. 199921 | Llama | 120 mg MPA intravaginal sponge for 9 days |
| Cancino et al. 199922 | Llama | 6 mg norgestomet implant SC 9 days plus |
| 3 mg norgestomet and 5 mg estradiolvalerate IM on day 0 | ||
| Ferrer et al. 199923 | Llama | 120 mg or 240 mg MPA intravaginal sponge for 13 days |
| Aba et al. 200016 | Llama | 120 mg MPA intravaginal sponge for 9 days |
| Vaughan 20016 | Alpaca | 25 mg twice a day, 50 mg once a day, 100 mg every other day, or 200 mg every other day progesterone IM 4–21 days |
| Chaves et al. 200224 | Llama | 330 mg progesterone CIDR 8 or 16 days |
| Aller et al. 200225 | Llama | 1.9 g progesterone CIDR-B 8 days |
CIDR, controlled internal drug releasing; IM, intramuscular; MPA, medroxyprogesterone acetate; SC, subcutaneous.
However, only one study has been conducted on the plasma progesterone levels obtained in South American camelids after device insertion. CIDRs (CIDR: InterAg) containing 330 mg progesterone were used in llamas for 8 or 16 days.24 Plasma progesterone concentrations were similar to luteal-phase levels in llamas for the first 3 days after CIDR insertion, and subluteal thereafter. Variation in plasma progesterone following CIDR insertion was evident in the llamas studied, possibly due to wide variations in ability to metabolize progesterone rather than variation in amount of progesterone released from the device.26
During the intravaginal presence of some PRIDs and sponges, some camelids have ovulated in the absence of mating. These devices have been implicated in inducing ovulation or luteinization by their physical presence, usually at the time of insertion or removal.21,27,28 Endogenous progesterone production may then potentially compromise exogenous hormone protocols. There have also been problems with device retention. CIDRs were expelled by some llamas, or caused vaginal discharges severe enough to necessitate their removal.18 PRIDs were expelled by some camels and one failed to retain the device at all.27 Sponges containing 0, 120, and 240 mg of medroxyprogesterone caused severe hemorrhagic, purulent, ulcerated vaginitis in llamas.23
CIDR devices.
In a recent study, llamas were each treated with a CIDR device containing 330 mg of progesterone (CIDR-G: InterAg) for 16 (n = 6) or 8 (n = 16) days.24 In animals with follicles greater than 6 mm prior to device insertion, a significant decrease in follicular diameter resulting in minima (mean 4–6 mm) between days 5 and 7. Follicular diameter began increasing on day 10 in those animals treated with a device for 16 days, but was not reported in females with a device for 8 days. In 3 of 4 animals with a follicle less than 6 mm at CIDR insertion, follicle size remained small and relatively unchanged in the presence of the device.
Follicular waves generally overlap in camelids,2 but Chaves and co-workers also demonstrated that a CIDR device inserted into each of 6 llamas for 16 days apparently prevented emergence of a new follicle until day 12 after insertion.24 This suggested that progesterone may exert a suppressive effect on FSH secretion, but FSH assays need to be improved before this can be shown.
Sponges.
Intravaginal sponges containing 120 or 240 mg medroxyprogesterone acetate (MPA) have been used in llamas to synchronize follicle growth with mixed success. Aba and co-workers inserted one 120 mg MPA sponge (120 mg MPA: Syntex SA) for 9 days with 100% ovulation rates in 22 animals treated with the gonadotropin-releasing hormone (GnRH) analogue, given buserelin (Receptal: Hoechst), or mated with a vasectomized or intact male 6 days after sponge removal.21 Plasma estradiol declined to basal levels 3 days after sponge insertion, then steadily increased thereafter until ovulation induction on day 16. No ultrasonography was performed to monitor follicular growth patterns in response to the progestagen, but 5 out of the 10 females conceived after mating.
Ferrer and co-workers used intravaginal sponges containing 0, 120, or 240 mg MPA in llamas for 13 days and monitored follicle activity using transrectal ultrasonography.23 Neither dose of MPA inhibited follicular development as follicles of 7 mm diameter were observed in each group. Every llama in the group in which a 240 mg MPA sponge was used developed hemorrhagic follicles 9 days after sponge removal.23
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