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. 2024;25(1):3–7. doi: 10.22099/IJVR.2024.49344.7239

Comparing CIDR with progesterone injections and eCG with human recombinant FSH for synchronizing estrous cycle in ewes

A Alijani 1, A Niasari-Naslaji 2,3,*, N Sayyah 4, M Baninajar 3, M Ganjkhanlou 5
PMCID: PMC11327640  PMID: 39156798

Abstract

Background:

It is desirable in estrus synchronization in sheep to avoid intravaginal devices and to shorten the program from 14 to 6 days. Moreover, replacement of eCG with safe, cheap, and efficient gonadotropin is in worldwide demand.

Aims:

This study investigates the possibility of replacing eCG with human recombinant FSH (hrFSH) and CIDR with progesterone injections for estrous synchronization in ewes.

Methods:

Assaf and Lacaune ewes (n=170) were divided into two groups and synchronized with either progesterone injections for 6 days or CIDR for 14 days. Ewes assigned in the injection group, received progesterone (37.5 mg; SC) and GnRH analogue (7.5 µg Alarelin acetate; IM) on day 0 of the experiment. On days 3 and 6, ewes received 25 and 12.5 mg progesterone (SC), respectively. On day 6, ewes in both groups received prostaglandin F2α (250 µg Cloprostenol; IM), and were divided into two subgroups to receive either hrFSH (75 IU Follitropin alfa; SC) or eCG (400 IU; IM). On day 7, fertile rams were introduced to ewes for 21 days. Data were analyzed using GLM and Glimmix.

Results:

There was no difference in the respective lambing rates, prolificacy, and fecundity between CIDR (71.1, 1.63, and 1.16%) and injections (66.7, 1.55, and 1.03%); between eCG (71.4, 1.60, and 1.14%), and hrFSH (66.3, 1.58, and 1.05%, P>0.05).

Conclusion:

In conclusion, 6-day progesterone injection-based protocol produced similar results to 14-day CIDR program and hrFSH could be an effective alternative for eCG during estrus synchronization in ewes.

Key Words: CIDR, eCG, Human recombinant FSH, Progesterone injections, Sheep

Introduction

Synchronization of estrus during the non-breeding season in ewes plays an essential role in optimizing breeding programs, ensuring reproductive efficiency, and maximizing genetic gains (Hogue, 1987 ▶; Raoul and Elsen, 2020 ▶). Currently, the estrus synchronization programs mostly rely on progesterone-releasing intravaginal devices (controlled intravaginal drug release also known as CIDR and sponge) for 12 to 14 days (Robinson and Smith, 1967 ▶; Gomez et al., 2006 ▶; Swelum et al., 2015 ▶). Apart from the costs, there are several health issues and ethical concerns about using intravaginal devices, including vaginitis, purulent secretion, foul-smelling fluids, and subsequent impacts on ewe health and welfare (Godfrey et al., 1997 ▶; Martinez-Ros et al., 2018 ▶). Additionally, there is a risk of environmental contamination due to residual progesterone and the necessity of antibiotic use to prevent vaginitis (Viñoles et al., 2011 ▶). To overcome these limitations, we have developed a progesterone injection-based protocol consisting of three injections of progesterone on days 0, 3, and 6 in association with GnRH and prostaglandin F2α on days 0 and 6, respectively (Payan et al., 2022; Seidi Samani et al., 2023a, b).

To enhance prolificacy and fecundity, equine chorionic gonadotropin (eCG), Robinson and Smith, 1967; Langford et al., 1983; Pearce and Robinson, 1985; Ferdowsi et al., 2020), hMG (Seidi Samani et al., 2023b), and follicle stimulating hormone (FSH; Knights et al., 2001b) were used toward the end of estrus synchronization programs. Several concerns regarding eCG could restrict the widespread use of this gonadotropin including high cost, ethical controversies surrounding pregnant mare blood, and potential immune responses, which could diminish its efficacy with repeated use, resulting in a decline in fertility (Bodin et al., 1997; Roy et al., 1999; Animal Welfare Foundation, 2022). Alternatively, hMG provided promising outcomes to substitute eCG in combination with progesterone injection-based estrus synchronization programs (Seidi Samani et al., 2023b). However, hMG high cost causes a limitation to use in large sheep flocks.

FSH produces by the pituitary gland. Bovine FSH (Graff et al., 2000; Boscos et al., 2002) and porcine FSH (Knights et al., 2001a, b, 2003) have been used to enhance the ovulation rate in ewes. Tissue-derived gonadotropins, due to the variations in purity and potency, could be associated with variable ovarian responses (Murphy et al., 1984; Kanitz et al., 2002). Besides, gonadotropins derived from animal tissues may also be vectors for infectious diseases (Murphy et al., 1984; Manning et al., 1987; Phillips et al., 1993; Ludwig et al., 2002; Galli et al., 2003; Wrathall et al., 2008).

Recombinant FSH could remove many concerns regarding tissue-derived FSH (Daya, 2004; Lunenfeld, 2004). Recombinant FSH has been used for superovulation in ewes (Kendall et al., 2004; Rutigliano et al., 2014); however, there are limited and inconsistent studies about using recombinant FSH to enhance reproductive performance of ewes (Yavuzer et al., 2010 ▶; Zeitoun et al., 2020a, b ▶). To the best of our knowledge, there is no study using human recombinant FSH in combination with progesterone injection-based estrus synchronization program in ewes.

Cinnal-f® is a new recombinant human FSH (Follitropin alfa), synthetized in genetically modified Chinese hamster ovary cells, which received an approval from Iranian Food and Drug Administration in June 2013 (IRC: 3125387962296341). It is significantly more cost-effective compared to Folltropin-V and has been used successfully in cattle for superovulation (Khodadadi et al., 2022 ▶).

The objective of this study was to investigate the effectiveness of human recombinant FSH (Cinnal-f) compared to eCG for enhancing reproductive performance of Shal ewes using progesterone injection-based or CIDR protocols for estrus synchronization in ewes.

Materials and Methods

Ethics statement

The present study was approved by the Animal Ethics Committee of the Faculty of the Veterinary Medicine, University of Tehran, Tehran, Iran (SRT45/08.02.2022).

Experimental location and animals

This study was performed at the sheep flock of Avingen Company, Firuzkuh, Iran (latitude: 35°76’93” N; longitude: 52°93’17” E; altitude: 2180 m; Max temp: 38°C; Min temp: -21°C; breeding season: between August and November) between January and February, 2023. Healthy, non-pregnant and non-lactating Assaf and Lacaune ewes (n=170) were selected for this experiment. Thirty-two adult rams, with a previous history of sound fertility, were used for this study.

Experimental design

Healthy, non-pregnant and non-lactating Assaf and Lacune ewes (n=170) were assigned randomly into four experimental groups, considering their breed, weight, and parity, using 2 (injection; n=87, or CIDR; n=83) by 2 (FSH; n=86, or eCG; n=84) factorial design (Fig. 1).

Fig. 1.

Fig. 1

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Comparing CIDR vs progesterone injections and hrFSH vs eCG for estrus synchronization in ewes. Ewes received CIDR for 14 days (CIDR group; n=83) or three injections of progesterone on days 0, 3, and 6 in association with GnRH on day 0 and prostaglandin F2α on day 6 of the experiment (injection group; n=87). Ewes in each group were then divided and received either eCG (n=84) or FSH (n=86) at the end of progestogen treatment

Ewes were divided into two groups and were synchronized by inserting CIDR for 14 days or using the progesterone injection-based protocol, according to our previous study (Payan et al., 2022). In brief, on day 0 of the experiment, ewes received progesterone (37.5 mg; SC; Aburaihan Pharmaceutical Company, Iran) and GnRH analogue (7.5 µg Alarelin acetate; IM; Aburaihan Pharmaceutical Company, Iran). On days 3 and 6 of the experiment, ewes received subcutaneous injections of 25 and 12.5 mg progesterone, respectively. All ewes received prostaglandin F2α analogue (250 µg Cloprostenol; im; Nasr Pharmaceutical Company, Iran) on day 6 (Fig. 1). Concurrent with the final days of progestogen treatment, each group of ewes were divided into two subgroups and received either 75 IU hrFSH (sc; Cinnal-f®; Cinnagen, Iran) or 400 IU eCG (im; Gonaser®, Hipra, Spain). The day after progestogen treatments, fertile rams (1:5) were introduced to ewes and remained for 21 days (Fig. 1).

Semen analysis

Prior to introducing the rams, semen was collected by electro-ejaculator and the quality of semen was evaluated according to the methods described by Evans and Maxwell (1987). Rams with the mass motility of ≥3.5 and the individual motility of ≥70% were used in this study.

Reproductive parameters and statistical analysis

Data with discrete nature including lambing rate (ewes lambed per total number of ewes ×100), prolificacy (lambs born per ewes lambing) and fecundity (lambs born per total number of ewes) were analyzed using the Glimmix procedure including logistic regression (log) as Link Function and Binomial (for lambing rate) or Poisson (for prolificacy and fecundity) statements as type of distribution in the model. Treatments were considered as fixed effects and breed as random effects. The percentage of events was calculated using the Frequency procedure. Data with continuous nature including the time intervals to particular events were analyzed using GLM procedure after testing for normality (Shapiro-Wilk) using univariate normal plot procedure. Tukey Studentized Range (HSD) test was used for pair-wise comparisons. Data were presented as mean±SEM and percentage. Data were analyzed using SAS, 2016.

Results

There was no interaction between the main factors: progestogen treatments and gonadotropin treatments (P>0.05). Therefore, the results of the main effects were evaluated and presented (Tables 1 and 2). There was no difference in lambing rates, prolificacy, and fecundity between CIDR and progesterone injections (Table 1; P>0.05) and eCG and hrFSH (Table 2; P>0.05).

Table 1.

Reproductive performance in two groups of synchronized ewes that received CIDR for 14 days (n=83) or three injections of progesterone on day 0, 3, and 6 of the experiment, in association with GnRH on day 0 and prostaglandin F2α on day 6 of the experiment (injection group; n=87)

Group Lambing rates (%) No. of lambs Total lamb Prolificacy (%) Fecundity (%)
Single Twin Triple
CIDR 59/83 (71.1) 25 31 3 96 1.63 1.16
Injection 58/87 (66.7) 27 30 1 90 1.55 1.03
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Table 2.

Reproductive performance in two groups of synchronized ewes that received eCG (n=84) or FSH (n=86) at the end of progestogen treatment

Group Lambing rates (%) No. of lambs Total lamb Prolificacy (%) Fecundity (%)
Single Twin Triple
eCG 60/84 (71.4) 26 32 2 96 1.60 1.14
FSH 57/86 (66.3) 26 29 2 90 1.58 1.05
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Discussion

The main objective of this study was to investigate the effectiveness of hrFSH to enhance the reproductive performance of ewes. In the current study, hrFSH treated Lacaune and Assaf ewes had similar results in the respective prolificacy and fecundity (1.58 and 1.05) compared to eCG treated ewes (1.60 and 1.14). Yavuzer et al. (2010) reported that the administration of hrFSH (10 IU, Puregon, Organon, Turkey), 24 h prior to prostaglandin F2α injection, was associated with greater twin pregnant Awassi ewes (FSH treated: 57.1% vs control: 4.5%; Yavuzer et al., 2010). There was no information on the prolificacy and fecundity of experimental groups in the latter study. Recently, the effect of hrFSH (Gonal-F) on twinning rates of ewes was investigated in two similar studies (Zeitoun et al., 2020a, b). Due to the high doses of FSH used in the latter studies (133.33 Folltropin-V and 180 IU rh-FSH), close to the dose recommended for superovulation in ewes (176 to 256 mg Folltropin-V; Bartlewski et al., 2016), the rate of mortality in lambs was high. Accordingly, the recommended dose of FSH is not suitable to induce twin ovulation in ewes. Varying doses of Folltropin-V (48, 55, 64 mg) prescribed at different times (12, 24, and 36 h) before intravaginal progestogen removal could affect follicle growth and ovulation; however, it was unable to enhance the prolificacy of ewes during the non-breeding season (Knights et al., 2001a, b and 2003). The respective optimal prolificacy and fecundity were reported to be 1.3 to 1.6 and 1.2 to 1.5 during the breeding season (Youngquist and Threlfall, 2007). During the non-breeding season, fertility and fecundity might be 20% to 30% lower than during the breeding season (Davies, 2019). Therefore, the reproductive indices of the current study could be within the normal range.

In the present study, hrFSH was administered at the time of the last progesterone injection. Our previous results showed that hMG and eCG have to be administered at 24 or 48 h after the last progesterone injection (Payan et al., 2022; Seidi Samani et al., 2023b). This is because, increasing FSH concentrations during the preovulatory period, when the progesterone concentration is approaching its basal concentration, can be associated with an increase in ovulation rates (Henderson et al., 1988; Knights et al., 2003). Due to our previous study, it took a maximum of 72 h for plasma progesterone to reach to the basal concentration after the progesterone injection (Seidi Samani et al., 2023b). However, after removal of CIDR, it takes only 4 h for the plasma progesterone to reach to the basal concentration (Ainsworth and Downey, 1986). Therefore, the time of eCG administration is recommended before or concurrent with the intravaginal progesterone device removal (Evans and Maxwell, 1987; Ali, 2007) or prostaglandin F2α administration (Ferdowsi et al., 2020); whereas, the time of gonadotropin administration for the progesterone injection protocol should be concurrent, 24 and 48 h after the last progesterone injection (Payan et al., 2022; Seidi Samani et al., 2023b). In our recent study, the time of estrous expression, lambing rates, and prolificacy were similar when eCG was administered concurrently with and 24 h after the last progesterone injection (Payan et al., 2022). Therefore, in order to reduce the labor intensity, hrFSH was injected concurrently with the last progesterone injection.

In the current study, the lambing rates were similar between CIDR (71.1%) and progesterone injection (66.7%) groups, FSH (66.3%), and eCG (71.4%). Similar result following 26 to 30 days mating period was achieved in synchronized ewes using 42 (76%), and 68 (79%) mg Folltropin-V during the non-breeding season (Knights et al., 2003). The recommended lambing rate goal during the non-breeding season after one and two cycles was around 50% and 70%, respectively (Youngquist and Threlfall, 2007), which is close to the results obtained in the current experiment.

In conclusion, hrFSH (Cinnal-f) could replace eCG, and progesterone injection-based protocol could replace CIDR for estrus synchronization program in ewe. This in turn, not only eliminates the negative impacts and concerns following eCG administration but also reduces the overall cost of the estrus synchronization protocol in ewes.

Acknowledgements

This research was funded by the Deputy for Research, University of Tehran. The authors wish to express their great appreciation to CinnaGen Pharmaceutical Company for providing Cinnal-f (recombinant human FSH) and the staff of the sheep unit at Avingen Company for their kind assistance in performing this study.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Ainsworth L, Downey BR. A controlled internal drug-release dispenser containing progesterone for control of the estrous cycle of ewes. Theriogenology. 1986;26:847–856. [Google Scholar]
  2. Ali A. Effect of time of eCG administration on follicular response and reproductive performance of FGA-treated Ossimi ewes. Small Rum. Res. 2007;72:33–37. [Google Scholar]
  3. Animal Welfare Foundation. PMSG investigation in Argentina: Blood farm Syntex. 2022. URL: https://www.animal-welfare-foundation.org/en/blog/pmsg-investigation-in-argentina-blood-farm-syntex.
  4. Bartlewski PM, Seaton P, Oliveira MEF, Kridli RT, Murawski M, Schwarz T. Intrinsic determinants and predictors of superovulatory yields in sheep: Circulating concentrations of reproductive hormones, ovarian status, and antral follicular blood flow. Theriogenology. 2016;86:130–143. doi: 10.1016/j.theriogenology.2016.04.024. [DOI] [PubMed] [Google Scholar]
  5. Bodin L, Drion PV, Remy B, Brice G, Cognié Y, Beckers JF. Anti-PMSG antibody levels in sheep subjected annually to oestrus synchronisation. Reprod. Nutr. Dev. 1997;37:651–660. doi: 10.1051/rnd:19970604. [DOI] [PubMed] [Google Scholar]
  6. Boscos CM, Samartzi FC, Dellis S, Rogge A, Stefanakis A, Krambovitis E. Use of progestagen-gonadotrophin treatments in estrus synchronization of sheep. Theriogenology. 2002;58:1261–1272. doi: 10.1016/s0093-691x(02)01040-3. [DOI] [PubMed] [Google Scholar]
  7. Davies P. Infertility and abortion in sheep and goats. In: Noakes DE, Parkinson TJ, England GC, editors. Veterinary reproduction and obstetrics. 0th Edn. London, United Kingdom: W. B. Saunders ; 2019. pp. 510–525. [Google Scholar]
  8. Daya S. Follicle-stimulating hormone in clinical practice: an update. Treatments Endocrinol. 2004;3:161–171. doi: 10.2165/00024677-200403030-00004. [DOI] [PubMed] [Google Scholar]
  9. Evans G, Maxwell WC. Salamons’ artificial insemination of sheep and goats. 2nd Edn. Butterworths, Sydney, Australia: 1987. [Google Scholar]
  10. Ferdowsi HR, Vodjgani M, Gharagozloo F, Garoussi MT, Niasari-Naslaji A, Akbarinejad V. The effects of eCG injection time on the reproductive performance in Shal ewes treated with short-term synchronization program during the breeding season. J. Vet. Res. 2020;75:109–117. [Google Scholar]
  11. Galli C, Duchi R, Crotti G, Turini P, Ponderato N, Colleoni S, Lagutina I, Lazzari G. Bovine embryo technologies. Theriogenology. 2003;59:599–616. doi: 10.1016/s0093-691x(02)01243-8. [DOI] [PubMed] [Google Scholar]
  12. Godfrey RW, Gray ML, Collins JR. A comparison of two methods of oestrous synchronisation of hair sheep in the tropics. Anim. Reprod. Sci. 1997;47:99–106. doi: 10.1016/s0378-4320(97)00007-9. [DOI] [PubMed] [Google Scholar]
  13. Gomez JD, Balasch S, Gomez LD, Martino A, Fernandez N. A comparison between intravaginal progestagen and melatonin implant treatments on the reproductive efficiency of ewes. Small Rumin. Res. 2006;66:156–163. [Google Scholar]
  14. Graff KJ, Meintjes M, Han Y, Reggio BC, Denniston RS, Gavin WG, Ziomek C, Godke RA. Comparing follicle stimulating hormone from two commercial sources for oocyte production from out-of-season dairy goats. J. Dairy Sci. 2000;83:484–487. doi: 10.3168/jds.S0022-0302(00)74907-1. [DOI] [PubMed] [Google Scholar]
  15. Henderson KM, Savage LC, Ellen RL, Ball K, McNatty KP. Consequences of increasing or decreasing plasma FSH concentrations during the preovulatory period in Romney ewes. J. Reprod. Fertil. 1988;84:187–196. doi: 10.1530/jrf.0.0840187. [DOI] [PubMed] [Google Scholar]
  16. Hogue DE. Frequent lambing systems. In: Marai IFM, Owen JB, editors. New techniques in sheep production. 1st Edn. London, United Kingdom, Butterworth-Heinemann. PP: 1987. pp. 57–63. [Google Scholar]
  17. Kanitz W, Becker F, Schneider F, Kanitz E, Leiding C, Nohner HP, Pöhland R. Superovulation in cattle: practical aspects of gonadotropin treatment and insemination. Reprod. Nutr. Dev. 2002;42:587–599. doi: 10.1051/rnd:2002045. [DOI] [PubMed] [Google Scholar]
  18. Kendall NR, Gonzalez-Bulnes A, Campbell BK. proceedings of the British society of animal science. Cambridge University Press; 2004. The use of urinary and recombinant human FSH preparations to induce superovulation in sheep and the effect on FSH and LH concentrations; p. 59. [Google Scholar]
  19. Khodadadi A, Niasari-Naslaji A, Nikjou D, Mohammadi B. Superovulation of high-producing Holstein lactating dairy cows with human recombinant FSH and hMG. Theriogenology. 2022;191:239–244. doi: 10.1016/j.theriogenology.2022.08.010. [DOI] [PubMed] [Google Scholar]
  20. Knights M, Baptiste QS, Dixon AB, Pate JL, Marsh DJ, Inskeep EK, Lewis PE. Effects of dosage of FSH, vehicle and time of treatment on ovulation rate and prolificacy in ewes during the anestrous season. Small Rumin. Res. 2003;50:1–9. [Google Scholar]
  21. Knights M, Hoehn T, Lewis PE, Inskeep EK. Effectiveness of intravaginal progesterone inserts and FSH for inducing synchronized estrus and increasing lambing rate in anestrous ewes. J. Anim. Sci. 2001a;79:1120–1131. doi: 10.2527/2001.7951120x. [DOI] [PubMed] [Google Scholar]
  22. Knights M, Maze TD, Bridges PJ, Lewis PE, Inskeep EK. Short-term treatment with a controlled internal drug releasing (CIDR) device and FSH to induce fertile estrus and increase prolificacy in anestrous ewes. Theriogenology. 2001b;55:1181–1191. doi: 10.1016/s0093-691x(01)00476-9. [DOI] [PubMed] [Google Scholar]
  23. Langford GA, Marcus GJ, Batra TR. Seasonal effects of PMSG and number of inseminations on fertility of progestogen-treated sheep. J. Anim. Sci. 1983;57:307–312. doi: 10.2527/jas1983.572307x. [DOI] [PubMed] [Google Scholar]
  24. Ludwig M, Felberbaum RE, Diedrich K, Lunenfeld B. Ovarian stimulation: from basic science to clinical application. Reprod. BioMed. Online. 2002;5:73–86. doi: 10.1016/s1472-6483(11)60221-6. [DOI] [PubMed] [Google Scholar]
  25. Lunenfeld B. Historical perspectives in gonadotrophin therapy. Hum. Reprod. Update. 2004;10:453–467. doi: 10.1093/humupd/dmh044. [DOI] [PubMed] [Google Scholar]
  26. Manning AW, Rajkumar K, Bristol F, Flood PF, Murphy BD. Genetic and temporal variation in serum concentrations and biological activity of horse chorionic gonadotrophin. J. Reprod. Fert. 1987;35:389–397. [PubMed] [Google Scholar]
  27. Martinez-Ros P, Lozano M, Hernandez F, Tirado A, Rios-Abellan A, López-Mendoza MC, Gonzalez-Bulnes A. Intravaginal device-type and treatment-length for ovine estrus synchronization modify vaginal mucus and microbiota and affect fertility. Animals. 2018;8:226. doi: 10.3390/ani8120226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Murphy BD, Mapletoft RJ, Manns J, Humphrey WD. Variability in gonadotrophin preparations as a factor in the superovulatory response. Theriogenology. 1984;21:117–125. [Google Scholar]
  29. Payan M, Niasari-Naslaji A, Seidi Samani H, Darbandsari M, Alijani A, Baninajar M, Ganjkhanlou M. The time of eCG administration in progesterone injection-based estrus synchronization protocol could affect the time of estrus expression in ewes during non-breeding season. Small Rumin. Res. 2022;216:106814. [Google Scholar]
  30. Pearce DT, Robinson TJ. Plasma progesterone concentrations, ovarian and endocrinological responses and sperm transport in ewes with synchronized oestrus. J. Reprod. Fertil. 1985;75:49–62. doi: 10.1530/jrf.0.0750049. [DOI] [PubMed] [Google Scholar]
  31. Phillips DJ, Hudson NL, Lun S, Condell LA, McNatty KP. Biopotency in vitro and metabolic clearance rates of five pituitary preparations of follicle stimulating hormone. Reprod. Fertil. Dev. 1993;5:181–190. doi: 10.1071/rd9930181. [DOI] [PubMed] [Google Scholar]
  32. Raoul J, Elsen JM. Effect of the rate of artificial insemination and paternity knowledge on the genetic gain for French meat sheep breeding programs. Livest. Sci. 2020;232:103932. [Google Scholar]
  33. Robinson TJ, Smith JF. The evaluation of S G-9880-impregnated intravaginal sponges used with or without PMS for the advancement of the breeding season of British breed ewes. In: Robinson TJ The control of the ovarian cycle in sheep (1st Edn., editor. Sydney, Australia: Sydney Univ. Press; 1967. pp. 144– 157. [Google Scholar]
  34. Roy F, Combes B, Vaiman D, Cribiu EP, Pobel T, Delétang F, Combarnous Y, Guillou F, Maurel MC. Humoral immune response to equine chorionic gonadotropin in ewes: association with major histocompatibility complex and interference with subsequent fertility. Biol. Reprod. 1999;61:209–218. doi: 10.1095/biolreprod61.1.209. [DOI] [PubMed] [Google Scholar]
  35. Rutigliano HM, Adams BM, Jablonka-Shariff A, Boime I, Adams TE. Effect of time and dose of recombinant follicle stimulating hormone agonist on the superovulatory response of sheep. Theriogenology. 2014;82:455–460. doi: 10.1016/j.theriogenology.2014.05.010. [DOI] [PubMed] [Google Scholar]
  36. SAS. User’s Guide. Ver. 9.4. SAS Institute, Cary, NC, USA; 2016. [Google Scholar]
  37. Seidi Samani H, Niasari-Naslaji A, Shojaei A, Ganjkhanlou M, Baninajar M. Induction of estrus and fertility of Shal ewes using progesterone injections or intravaginal sponge followed by laparoscopic AI during non-breeding season. Iran. Vet. J. 2023a;19:117–126. [Google Scholar]
  38. Seidi Samani H, Niasari-Naslaji A, Vojgani M, Ganjkhanlou M, Baninajjar M, Alijani A. Synchronization of estrus using progesterone injections followed by human menopausal gonadotropin in ewes. Vet. Res. Forum. 2023b;14:145–151. doi: 10.30466/vrf.2022.542734.3311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Swelum AAA, Alowaimer AN, Abouheif MA. Use of fluorogestone acetate sponges or controlled internal drug release for estrus synchronization in ewes: Effects of hormonal profiles and reproductive performance. Theriogenology. 2015;84:498–503. doi: 10.1016/j.theriogenology.2015.03.018. [DOI] [PubMed] [Google Scholar]
  40. Viñoles C, Paganoni B, Milton JTB, Driancourt MA, Martin GB. Pregnancy rate and prolificacy after artificial insemination in ewes following synchronization with prostaglandin, sponges, or sponges with bactericide. Anim. Prod. Sci. 2011;51:565–569. [Google Scholar]
  41. Wrathall AE, Holyoak GR, Parsonson IM, Simmons HA. Risks of transmitting ruminant spongiform encephalopathies (prion diseases) by semen and embryo transfer techniques. Theriogenology. 2008;70:725–745. doi: 10.1016/j.theriogenology.2008.05.049. [DOI] [PubMed] [Google Scholar]
  42. Yavuzer Ü, Zonturlu AK, Faruk ARAL. Effect of recombinant follicle stimulating hormone (rFSH) on some fertility parameters in Awassi ewes synchronized with PGF2α in the breeding season. Ankara Üniv. Vet. Fakült. Dergisi. 2010;57:241–245. [Google Scholar]
  43. Youngquist RS, Threlfall WR. Current therapy in large animal theriogenology. 2nd Edn. Philadelphia, USA: Elsevier Health Sciences; 2007. pp. 701–714. [Google Scholar]
  44. Zeitoun MM, Ali MA, El-Dawas AO. Induction of twinning in ewes using two protocols of a recombinant human follicle stimulating hormone porcine pituitary-derived FSH and their subsequent impacts on maternal hormones. Maced. Vet. Rev. 2020a;43:111–123. [Google Scholar]
  45. Zeitoun MM, El-Dawas AO, Ateah MA, El-Deen MAS. Consequences of twinning induction to Noemi ewes by a recombinant human follicle-stimulating hormone compared with pituitary-derived porcine follicle-stimulating hormone on follicular dynamics, maternal biochemical attributes, and neonatal traits. Vet. World. 2020b;13:633–641. doi: 10.14202/vetworld.2020.633-641. [DOI] [PMC free article] [PubMed] [Google Scholar]

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