Study of CIDR for the reproduction control of Rembi ewes during low sexual activity period in Western Algeria highlands

A R Benia^1,3, N Benamor² and K Zidane^1,3

¹ Department of Biomedicine. Institute of Veterinary Sciences, University of Tiaret, BP 78, 14000, Tiaret, Algeria
vetoarb@gmail.com
² Department of Natural Sciences and Life. University of Tiaret, BP 78, 14000, Tiaret, Algeria
³ Farm animal reproduction laboratory. Institute of Veterinary Sciences, University of Tiaret, BP 78, 14000, Tiaret, Algeria

Abstract

This study is a contribution to the evaluation of the reproductive potential of Rembi sheeps subjected to two different oestrus synchronization protocols in February-March (low sexual activity) in Algeria highlands. A first group of 120 ewes divided into two batches (60 CIDR5: 5 days of treatment and 60 CIDR12: 12 days) were synchronized with CIDRs impregnated with natural progesterone (0.35 g) associated on the day of withdrawal with 500 IU of PMSG and for the CIDR5 lot 5 mg of prostaglandin. The second group of 60 ewes was left without hormonal program (witness). All the animals were subjected to the feeding programs of Flushing and Steaming.

The hormone therapy resulted in short intervals "CIDR withdrawal – oestrus onset" of 39.8 ± 1.9h and 32.0 ± 1.0h respectively for CIDR5 and CIDR12 lots with very significant differences (p< 0.0001). The impact of CIDR on the reproductive parameters of Rembi ewes during the period of low sexual activity led to very significant increases, especially for long-term treatments (12 days). Lots CIDR5 and CIDR12 respectively achieved high fertility rates (76.7 ± 4.3% and 88.3 ± 3.2%, respectively), high fecundity rates (108 ± 8% and 137 ± 7%, respectively) and high prolificacy (141 ± 5% and 155 ± 5%) compared to those of the witness group which were only 66.7 ± 4.8%, 76.7 ± 6.2% and 115 ± 4%. Therefore, PMSG appeared to significantly improve fertility, fecundity and prolificacy in Rembi ewes.

No significant differences in perinatal mortalities were observed between the different lots, knowing that the highest rates were recorded in the witness ewes group (7.5 ± 0.2%). A good mastery of the reproductive parameters allows a better productivity.

Keywords: fecundity, fertility, mortality, oestrus, prolificacy, synchronization

Introduction

Algeria by its strategic geographical position in Africa and the heterogeneity of the bioclimatic stages, represents a natural capital of biodiversity of genetic resources animals. The practice of animal husbandry is present almost throughout the Algerian territory but its concentration is greater in the highlands of the country, with however a higher concentration in the steppe (Mamine 2010).

The national sheep herd represents the largest animal resource, it is estimated at more than 29 million heads including 14 million breeding ewes (MADR 2020).

This sheep farming, despite its economic and social importance, is poorly conducted, both in technical organization and in the operation of its production systems. Its mode is characterized by insufficient food resources, uncontrolled natural reproduction whether for ram/ewe load, selection, age of breeding or age at reform. Not to mention the poor breeding practices resulting from the low level of technicality of breeders (Mamine 2010).

Mastering the reproduction of females in a herd is one of the keys to the durability of any breeding. The evaluation of a rearing system is done through certain zootechnical parameters including reproductive parameters (numerical productivity: fertility, fecundity, prolificacy and mortality of lambs) (Soltner 1989).

CIDR (Controlled Internal Drug Release) is an intravaginal device used mainly in the off-season to induce estrus and ovulation. But it can also be used in the sexual season to synchronize the estrus of the ewes, which makes it possible to make the most of the fodder availability, to adapt the supply to the demand, to limit the unproductive periods (by reducing the periods of anestrus), to increase the prolificacy of the females and to accelerate the genetic progress by allowing a wider use of artificial insemination (Fatet et Tuauden 2013).

Despite a good number of studies evaluating the effectiveness of CIDR for estrus induction in ewes, the conditions under which this product is used differ greatly. There is also a wide variability in the protocols used which is accompanied by results on equally variable reproduction parameters. No standard protocol, unlike the vaginal sponge, seems to be established.

In Algeria, no scientific research studied the particular conditions under which CIDR is used confirming its effectiveness and proving its properties on local sheep breeds, due to multiple factors including its recent launch on the national market.

The main objective of our study is to value the reproductive parameters of Rembi Ewes during the season of low sexual activity by reducing unproductive periods (advance/synchronization of puberty, off-season reproduction, decrease in the duration of postpartum anœstrus) which can increase and improve the productivity and profitability of sheep farms whilst determining the real effectiveness of the CIDR by optimizing its performance and by testing its main synchronization protocols.

Materials and methods

Choice of the study location

The present study took place in the region of Ksar Chellala (Highlands of Western Algeria), located 116 km southeast of the Wilaya of Tiaret and 260 km south of the capital Algiers. It is a steppe region with a purely pastoral vocation, whose geographical coordinates are: degree of longitude 2°19' East, degree of latitude 35°10' North and at 839 meters above sea level. It is characterized by its semi-arid pre-continental climate with a cold and wet winter and a hot and dry summer. The temperature varies between a minimum of -1.1°C and a maximum of 16.4°C in winter and between 21.9°C and 39.5°C in summer. The daily photoperiod ranges from 9.3 hours during the winter solstice to 14.2 hours during the summer solstice (Aster satellite data).

Choice of the breed

The Rembi breed is one of the main Algerian sheep breeds with a total number of around 3,390,000 according to the National Commission AnGR (2019), and located in the northwest of the country. The ewe has an average morphology (height at withers: 72 cm; body length: 73 cm; chest depth: 32 cm; ear length: 15 cm), a fawn head, very strong limbs and carcass of red fawn color (bright weight between 60 and 70 kg). It is an interesting breed by its physical, productive and reproductive abilities (sexual precocity: late breed (12 months); age at first lambing: 17 to 18 months; fertility: 90%; fecundity: 95%; prolificacy: between 105 and 115%; estrus seasonality: April to July and September to December) (Laoun 2015).

Framework of the study

We carried out our work in a farm specialized in sheep farming with the collaboration of the Technical Institute of Livestock (ITELV) of Ksar Chellala during the period from February to September 2021.

The experiment was carried out on a herd of 180 multiparous ewes of the Rembi breed identified by earrings and which had a "last lambing-mating" interval of more than 80 days. For the rams, 18 sexually experienced males (aged between 05 and 07 years) all from the farm were selected and removed from the contact of the ewes before the start of mating. All animals were in an acclimatization period for about one month before the start of the experimental phase.

The mode of feeding of the herd is semi-intensive, with in addition to pasture and crop residues, a feed ration consisting of a supplement of complete commercial concentrate (700 grams / head / day) based on crushed barley (40%), bran (15%), corn (20%) and soybeans (20%) as well as minerals and vitamins (5%). A supplementation of 230 grams of a barley feed in grains per head per day was given from 4 weeks before until 3 weeks after natural mating (Flushing). A Steaming at the end of gestation, one month before the scheduled date of lambing, at the rate of 200 grams of the same feed per ewe per day was added. Water and barley straw were distributed at will.

Ewes with adult ages ranging from 04 to 06 years with body conditions fluctuating between 3.0 and 3.5 (body condition scores) were randomly assigned to two uniform groups:

a) The first group consists of 120 females, has been lead in controlled reproduction (estrus synchronization) with hand mating.

b) The second group (witness), lead in natural mating without synchronization, including 60 females.

All the sheep used for our study underwent the following examinations: stoutness, clinical examination and in particular of the genital and locomotor systems. Prophylactic treatments were recommended (deworming, antibiotic therapy and vitamin therapy), and only healthy subjects were retained.

Each ewe is represented by an individual numerical productivity sheet (fertility, fecundity, prolificacy and perinatal mortality of lambs).

Products and instruments for estrus induction and synchronization

Intravaginal CIDR (CIDR® Ovis, Zoetis, France: T-shaped device consisting of an inert nylon support on which is moulded a silicone elastomer impregnated with natural progesterone 0.35 g) stored at room temperature not exceeding 30 ° C, away from light and moisture; injectable PMSG (Pregnant Mare Serum Gonadotropin; Folligan 1000 IU: injectable lyophilisate + solvent stored in the refrigerator between 2 and 6°C); Prostaglandin F_2α (Dinolytic® 5 mg, Zoetis, Spain); latex gloves; 02 CIDR applicators; gynaecological lubricant; warm water; disinfectant (iodine 4%); clean paper (paper towel); chisel.

Experimental protocol

For the first group treated by the CIDR, the ewes were randomly divided into 02 lots (Table 1):

- Batch CIDR12 (60 ewes): the device was introduced into the anterior part of each ewe's vagina for 12 days after insertion, followed by an intramuscular injection of 500 IU of PMSG at the time of removal of the device.

- Batch CIDR5 (60 ewes): short-term protocol where CIDRs were applied for 05 days for each ewe with simultaneous injection of 500 IU of PMSG and 5 mg of prostaglandin intramuscularly on the day of withdrawal.

After distribution, the ewes were housed in two mating pens, isolated from one another.

24 hours after the withdrawal of the CIDR for lots CIDR5 and CIDR12, the detection of ewes in heat was done by the introduction of rams equipped with marking harnesses. This detection lasted 02 days until all ewes came to estrus (Ferdowsi et al 2018). The matings were carried out the same day of estrus and the ratio ram to ewe used was 1/5.

For the second (witness) group of 60 ewes (without synchronization treatment), 04 rams were introduced with the group (ram/ewe ratio of about 1/15) for a total mating time of 50 days. Lambing dates and number of lambs born were noted for each ewe.

Evaluation of reproductive parameters

The reproductive performance data of the ewes in our study were estimated. The calculations mainly concerned the fertility, fecundity, prolificacy and mortality rates at the first week of age of new-borns, calculated by the following formulas respectively.

Overall Fertility rate = (Number of ewes that have lambing / Number of ewes put to breed)*100.

Overall Fecundity rate = (Number of lambs born "dead and alive" / Number of ewes put to breed) *100.

Overall Prolificacy rate = (Number of lambs born "dead and alive" / Number of ewes that have lambing) *100.

The Mortality rate at the first week of age (0 - 7 days) = (Number of lambs dead in the first week of age / Number of lambs born "dead and alive") * 100.

CIDR withdrawal-oestrus interval = time interval (hours) elapsed between the time of removal of the CIDR and the first behavioural signs of oestrus of the ewe.

Statistical analysis

In this study, using PAST 4.08 software (Hammer et al 2001), we used descriptive statistics, such as mean, standard deviation, and coefficient of variation to describe the data. The results were subjected to the Shapiro-Wilk normality test with a 5% probability. We applied the parametric test (student t-test) to compare quantitative variables. When the distribution of data was not normal, the Mann Whitney test was adopted with a significance level of 5%. A principal component analysis (PCA) was used to highlight the effectiveness of the CIDR for estrus induction and synchronization in Rembi ewes that exhibit variations in reproductive parameters during the low season of sexual activity.

Results

On the day of withdrawal of the CIDRs, we noted no loss of this intravaginal device for ewes in each batch in the first group (n=120) (Table 1).

The mean intervals "CIDR withdrawal -onset of estrus" obtained in lot CIDR12 were 32.0 ± 1.0h and were shorter compared to those obtained in lot CIDR5 (39.8 ± 1.9h) (Table 2). The degree of signification calculated in the comparison of these intervals shows the existence of a very highly significant difference between the two hormonal treatments (p< 0.0001) (Table 3).

The percentages of the highest fertility, fecundity and prolificacy rates were observed in the CIDR12 lot (intravaginal device for 12 days with intramuscular injection of 500 IU of PMSG at the time of withdrawal) and the lowest in the witness group (without hormonal treatment). On the other hand, the highest lamb mortality rates (at the first week of age) were recorded in the second witness group (7.50 ± 0.24%) compared to the first group (CIDR5 batch : 2.89 ± 0.11% and CIDR12 batch : 2.20 ± 0.12%) (Table 2).

Based on the results obtained by the statistical analysis (Table 3), we can say that the oestrus induction and synchronization protocols of the CIDR12 batch significantly influenced the fertility of the females compared to that of the witness group (p=0.005).

These analyses indicated that the percentage of fecundity was higher in the first group compared to the witness group with a very highly significant difference observed especially in batch CIDR12 (p< 0.0001). Fecundity associated with CIDR12 treatment showed a tendency to be higher with a significant difference than that obtained with CIDR5 treatment (137% vs. 108%; P = 0.0354; Tables 2 and 3).

In terms of prolificacy rates, no significant differences were observed between oestrus induction and synchronization programs between long and short-term protocols (Table 3). Comparatively to the unsynchronized female group (witness), hormonal treatments significantly influenced the prolificacy of ewes (p=0.0125) in lot CIDR5 and very highly significantly (p< 0.0001) in lot CIDR12.

Regarding the mortality rates of lambs at the first week of age, no significant differences were observed between the different groups and batches of our study (Table 3). Knowing that the highest percentages were recorded in lambs from ewes of the second group (7.5 ± 0.24%, Table 2).

The statistical study (Table 4, Figure 1) shows that the variables (fertility, fecundity and prolificacy) are positively correlated with each other, knowing that no significant correlation was recorded between these variables and that of mortality.

Figure 1. Principal Component Analysis (PCA) of CIDRs with the different parameters studied

Figure 1 illustrates the interpretation of all the results of our study by a CPA (Principal Component Analysis). The ascending hierarchical classification is represented by:

- The first class: represented mainly by the first group of ewes treated by the CIDR. This class was correlated positively with the factors of reproduction (fertility, fecundity and prolificacy) in particular the CIDR12 batch of which we noted the highest rates.

- The second class: consisting of the witness ewes group, with a fairly high perinatal mortality rate of lambs compared to the first group.

Discussion

In the present study, the 0% CIDR loss rate recorded during treatment was comparable to those reported in some studies, which put it between 0 and 4% (Ghalsasi et Nimbkar 1996, Hashemi et al 2006). This can be explained by the technique of its instructions for use (the free CIDR fins are perfectly folded which will retain the device well inserted in the anterior portion of the vagina). However, Omontese et al (2010) reported in their study much higher CIDR loss rates of between 10 and 16%.

The essential purpose of estrus induction and synchronization for a group of females is to achieve a regular onset of estrus after the end of treatments. In our experiment, a 100% estrial response was observed in all synchronized ewes of the first group with fairly short CIDR withdrawal - onset oestrus intervals (CIDR5: 39.8 ± 1.9h; CIDR12: 32.0 ± 1.0h). Similar results of estrial responses have been reported in several studies with short and regular intervals between device removal and rutting onset (Martemucci and D'Alessandro 2010, Sirjani et al 2011, Moradi Kor 2012). However, other authors have reported lower heat induction rates ranging from 46% to 96% following CIDR treatments (Naderipour et al 2012) with longer intervals between device removals and estrus induction (Knights et al 2003). The short duration in the manifestation of ruts after 12 days of CIDR treatment is mainly due to the action of PMSG (500 IU) injected at the time of withdrawal. This allows ewes in the off-season to obtain more precise and predictable synchronizations of ovulatory heat thanks to the effect of this hormone on follicular growth by the faster stimulation of pituitary-ovarian responses which positively promote the secretion of estrogen (Barrett et al 2004, Simonetti et al 2008). Our results are consistent with Abdalla et al (2014), who reported that administration of eCG (equine chorionic gonadotropin) reduced the interval between removal of the progestin device and induction of estrus and improved the efficiency of ovulatory heat synchronization during and outside the breeding season. In our work, the five-day CIDR program does not have the same effect on the duration of the onset of heat as the twelve-day program (p< 0.0001), which is in contradiction with the findings of some authors (Blais et al 2014, Thériault et al 2014, Almadaly et al 2016) who reported in their trials of different CIDR protocols in the off-season, that a synchronization of only 5 days in combination with prostaglandins was just as effective as a treatment of 12 to 14 days and even, by being shorter, this protocol has two main advantages, namely the decreased risk of loss of CIDR and the reduction of the unproductive period of females.

As shown in Tables 2 and 3, the 5- and 12-day CIDR programs improved fertility on induced heat compared to the control ewes group, knowing that no significant differences were noted between the two hormonal protocols (p=0.0948). This can be explained by the elevation of progesteronemia from CIDR which is the cause of a negative feedback on the pituitary secretions of FSH and LH (Noakes et al 2019), which leads to follicular atresia which will be followed by a generation of a new estrous cycle with new waves of good quality follicles and consequently an adequate increase in the plasma level of 17β-estradiol (Martinez and Gonzalez 2019). Some researchers have shown that 5- to 14-day CIDR programs generate regular follicular waves because progesterone levels (in addition to PMSG injection during different treatments) are adequate to ensure follicular growth and production of good quality eggs (Martinez and Gonzalez 2019, Nowicki et al 2017). Short-term hormonal patterns (5-9 days), which maintain a high concentration of progesterone throughout the duration of treatment, have generally been shown to be beneficial for fertility outcomes in ewes treated off-season (Knights et al 2003, Pinna et al 2012). Our fertility results are consistent with those obtained in other studies (Ozyurtlu et al 2010, Nowicki et al 2017).

Compared to the witness group of the 60 ewes in our research, the fecundity rate was found to be higher with significant differences in the group of ewes that underwent CIDR treatment and in particular in the CIDR12 lot (Tables 2 and 3). Karaca et al (2009) reported that for CIDR treatments performed at the beginning of the breeding season, the fecundity rate was significantly higher in ewes that underwent a short-term protocol (7 days: 87.3%) than in the long term (12 days: 71.6%). Conversely, Ataman et al (2006) reported that for fertility, fecundity and prolificacy parameters in Akkaraman cross-ewes, no significant difference was observed between short-term (7 days) and long-term (12 days) CIDR treatments performed during the sexual season. Similarly, Ustuner et al (2007) described that short-term (6 days) and long-term (12 days) progestin protocols resulted in similar fecundity rates in Awassi ewes during the high breeding season. Our results are distinctly higher compared to those cited in several previous studies (Zonturlu et al 2011, Taher 2014, Almadaly et al 2016) in which the maximum fecundity rate of synchronized subjects was 100% while Titi et al (2010) reported a rate below 67%. The fecundity rate recorded in our ewes of the two lots of the first group (CIDR5: 108 ± 8% and CIDR12: 137 ± 7%) reflects very high ovulation rates. Koyuncu et al (2010) reported that eCG administration (PMSG) stimulated follicular development and increased ovulation rate in ewes. Similarly, Barrett et al (2004) revealed that intramuscular injection of 500 IU of eCG after 12 days of intravaginal progestin treatment had tonic effects on ovarian follicular wave dynamics in ewes in seasonal anestrus.

The prolificacy rates obtained in the two groups of our experiment were very considerable (CIDR5: 141 ± 5%; CIDR12: 155 ± 5%; Control: 115 ± 4%). Our statistical results shows that no significant difference was observed between the two treatments of the first group (p=0,193). On the other hand and compared to the witness group of untreated ewes, CIDR, and in particular used in the long term (12 days), had a very highly significant influence on prolificacy (p=0.0002). This increase in prolificacy rates and consequently multiple births can be attributed to the use of PMSG at the dose of 500 IU in the synchronization protocol. Akoz et al (2006) determined that the use of 500 IU of PMSG per ewe increased the rate of ovulation, twin pregnancies and the number of lambs born. Boscos et al (2002) concluded that the use of eCG after treatment with a progestogen device increases ovarian response, fecundity rate and the percentage of multiple births from induced ovulations. Both Gulyuz & Kozat (1995) pointed out that the administration of eCG improved the number and quality of follicles and consequently the increase in twinness and tripling rates. However, there is great variability in responses to eCG that may be associated with breed, individuals of a breed, category of females, time of year and general condition of the animal (Boscos et al 2002) and dose and timing of administration of eCG (Timurkan and Yildiz 2005). Comparing our results with other works, the prolificacy rates we recorded were higher than those reported by Moradikor et al (2012) and Almadaly et al (2016), and slightly lower than those described by Koyuncu et al (2010). We recall that the ewes we experimented received a supplementation of 230 grams of a barley feed in grains per head per day for 4 weeks before coitus and 3 weeks after coitus, hence as an advantage the elimination of all factors that can have an influence on the smooth running of this preparatory stage. According to Faleh (2000) the application of a good Flushing three weeks before and three weeks after the mating period greatly improves reproductive parameters in sheep.

According to Table 2, the perinatal mortality rates of lambs recorded during the first week of age in the two groups of our study are very low compared to those of 15 to 20% reported by Fragkou et al (2010) and Lepeltier (2010). These authors indicated that its percentages were related to breeding factors, such as environmental conditions related to the atmosphere and maintenance of the herd and not to the synchronization treatment combining a progestagen with a dose of PMSG with or without prostaglandin. Allouche et al (2011) highlighted the influence of multiple factors on mortality rates (breed and age of mothers, weight of lambs at birth, mode of birth, sex of lambs and environmental conditions). Our data showed that the highest perinatal mortality rates were recorded in lambs from unsynchronized ewes compared to those from ewes treated by the IDFR without any significant difference (Tables 2 and 3). This can be explained by the fact that for the farmer synchronization will be a good choice to create a balance between productivity, market adaptation and family life. Thus, the concentration of lambings over a few days limits intervention and monitoring times, which reduces perinatal mortality and consequently breeding costs. Madani et al (2009) specified that heat synchronization also facilitates dietary adjustments by the constitution of homogeneous batches of animals: grouping of lactating females and lambs (in weaning and growing periods). Taherti and Kaidi (2017) reported that the concentration of births over a very limited time interval allows a better control, which reduces prenatal mortalities, shortens the duration of postpartum anestrus in ewes, and makes possible the goal of 2 lambings per year very achievable.

Conclusion

• Progestin treatment (CIDR: 35 mg progesterone) combined with a dose of 500 IU of PMSG over a long and short-term period (with 5 mg prostaglandin) induced and synchronized the appearance of heat in Rembi ewes during the season of low reproductive activity. The early onset of estrus is based on the duration of CIDR placement and was more advanced with a 12-day therapeutic protocol.
  
  
• Ovarian stimulation with a dose of 500 IU of PMSG following 12 days of intravaginal CIDR placement (with a Flushing and a Steaming) allowed better rates of fertility, fecundity and prolificacy in Rembi ewes. Thus, for more practicability in field conditions a short-term CIDR protocol can be a good alternative to a long-term treatment (12 days).
  
  
• The perinatal mortality rates of lambs recorded during the first week of age were very low and without significant difference between the different groups and batches of this work; the highest percentages were recorded in the witness ewe group. Knowing that these mortalities depend more on multiple environmental factors, farms and individuals than on CIDR treatments.

Acknowledgments

We thank the officials and workers of the Ksar Chellala Technical Institute for Livestock for their invaluable help in carrying out this work. Our thanks also go to Dr KHALDI Mohamed for his wise advice in writing this article.

References

Abdalla E B, Farrag B, Hashem A L S, Khalil F A F, Fattah 2014 Effect of progesterone, PGF2α, PMSG and GnRH on estrus synchronization and some reproductive traits in Barki ewes. Journal of Agroalimentary Processes and Technologies, 20: 93-101.

Akoz M, Bulbul B, Ataman M B, Dere S 2006 Induction of multiple birth in Akkaraman cross-bred sheep synchronized with short duration and different doses of progesterone treatment combined with ECG outside the breeding season. Bulletin of the Veterinary Institute in Pulawy, 50: 97-100.

Allouche L, Belkasmi F, Madani T, Semara L, Mouffok C 2011 Effet du comportement maternel de la brebis Ouled Djellal en présence du berger sur la croissance, la mortalité et le comportement néonatal des agneaux. Renc. Rech. Ruminants, 18.

Almadaly E, Ashour M, El-kon I, Heleil B, Fattouh E 2016 Efficacy of various synchronization protocols on estrus behavior, lambing rate and prolificacy in Rahmani Egyptian ewes during the non-breeding season. Asian Journal of Animal and Veterinary Advances, 11: 34-43.

Ataman M B, Akoz M, Akman O 2006 Induction of synchronized oestrus in Akkaraman cross-bred ewes during breeding and anestrus seasons: the use of short-term and long-term progesterone treatments. Revue de médecine vétérinaire, 157: 257-260.

Barrett D M W, Bartlewski P M, Batista-Arteaga M, Symington A & Rawlings N C 2004 Ultra-sound and endocrine evaluation of the ovarian response to a single dose of 500 IU of eCG following a 12-day treatment with progestagen releasing intra-vaginal sponges in the breeding and nonbreeding seasons in ewes. Theriogenology, 61: 311-327.

Blais É, Castonguay F, Demers‐Caron V, Thériault M 2014 Utilisation du CIDR pour le contrôle de la reproduction des brebis en contre‐saison sexuelle. Rapport de recherche remis au conseil pour le développement de l’agriculture du Québec (projet No 6606), 111 p.

Boscos C M, Samartzi F C, Dellis S, Rogge A, Stefanakis A, Krambovitis E 2002 Use of progestagen-gonadotrophin treatments in estrus synchronization of sheep. Theriogenology, 58: 1261-1272.

Commission Nationale An G R 2019 Rapport National sur les Ressources Génétiques Animales: Algérie. 45 p.

Faleh H A 2000 Alimentation des troupeaux ovins tout au long de l’année". Bovins & ovins, 24: 4-5.

Fatet A et Tuauden M 2013 Reproduction des chèvres en toute saison: FLOCK-REPROD, une solution durable. Guide pratique FLOCK-REPROD, version française. Projet de recherche européen Flock-Reprod, INRA, France. 22p.

Ferdowsi H R, Vodjgani M, Gharagozloo F, Talebkhan Garoussi M, Niasari Naslaji A, Akbarinejad V 2018 The effects of eCG injection time on the reproductive performance in Shal ewes treated with short-term synchronization program during the breeding season. Journal of veterinary Research, 75 (1): 109-117.

Fragkou I A, Mavrogianni V S, Fthenakis G C 2010 Small Ruminant Research, 92: 41-44.

Ghalsasi P M et Nimbkar C 1996 Evaluation of laparoscopic intrauterine insemination in ewes. Small Ruminant Research, 23: 69-73.

Gulyuz F et Kozat S 1995 Synchronization of oestrous in sheep and the effect of PMSG dose on lambs number. The Journal of the Faculty of Veterinary Medicine (University of Yuzuncu Yil), 6: 64-66.

Hammer Ø, Harper DAT, Ryan P D 2001 PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 9pp. http://palaeo-electronica.org/2001_1/past/issue1_01.html.

Hashemi M, Safdarian M et Kafi M 2006 Estrous response to synchronization of estrus using different progesterone treatments outside the natural breeding season in ewes. Small Ruminant Research, 65: 279-283.

Karaca F, Ataman M, Coyan A 2009 Synchronization of estrus with short-and long-term progestagen treatments and the use of GnRH prior to short-term progestagen treatment in ewes. Small Ruminant Research, 81: 185-188.

Knights M, Baptiste Q S, Dixon A B, Pate J L, Marsh D J, Inskeep E K, Lewis P E 2003 Effects of dosage of FSH, vehicle and time of treatment on ovulation rate and prolificacy in ewes during the anestrous season. Small Ruminant Research, 50: 1-9.

Koyuncu M et Altiçekiç O 2010 Effects of progestagen and PMSG on estrous synchronization and fertility in Kivircik ewes during natural breeding season. Asian-Australasian Journal of Animal Science, 23: 308-311.

Laoun A, Harkat S, Benali R, Yabrir B, Hakem A, Ranebi D, Maftah A, Madani T, Da Silva A et Lafri M 2015 Caractérisation phénotypique de la race ovine Rembi d’Algérie. Revue d’Elevage et de Médecine vétérinaire des Pays tropicaux, 68(1): 19–26. doi: 10.19182/remvt.20572.

Lepeltier G 2010 Enquête sur la mortalité des agneaux en élevage ovin allaitant de la région Limousin : incidence des pertes et facteurs zootechniques. Thèse vétérinaire, Ecole nationale vétérinaire de Nantes, 139 p.

Madani T, Chouia F, Abbas K 2009 Effect of oestrus synchronisation and body condition on reproduction of anoestrous Ouled Djellal ewes. Asian Journal of Animal and Veterinary Advances, 4:34-40.

MADR 2020 Ministère de l’agriculture et du développement rural. Direction des Systèmes d’Information, des Statistiques et de la Prospective : sous-directrice chargée du développement des filières animales. Bétail : en 2020, le cheptel ovin a grossi. Reporters Algérie (quotidien national d’information). https://www.reporters.dz/betail-en-2020-le-cheptel-ovin-a-grossi/

Mamine F 2010 Effet de la suralimentation et de la durée de traitement sur la synchronisation des chaleurs en contre-saison des brebis Ouled Djellal en élevage semi-intensif. Editions Publibook, p. 11-13.

Martemucci G et D’Alessandro D 2010 Estrous and fertility responses of dairy ewes synchronized with combined short-term GnRH, PGF2α and estradiol benzoate treatments. Small Ruminant Research, 93: 41-47.

Martinez P R, Gonzalez A B 2019 Efficiency of CIDR-Based Protocols Including GnRH Instead of eCG for Estrus Synchronization in Sheep. Animals (Basel), 9: 146.

Moradikor N, Sadeghi S, Ziaei N 2012 Comparison reproductive performance in Kermani ewes Treated with two synchronization methods and subsequent eCG treatment out of the breeding season. International Journal of Biological and Medical Research, 3: 1485-1489.

Naderipour H, Yadi J, Ghazikhani Shad A, Sirjani M A 2012 The effects of three methods of synchronization on estrous induction and hormonal profile in Kalkuhi ewes: A comparison study. African Journal of Biotechnology, 11: 530-533.

Noakes D E, Parkinson T J, England G C W 2019 Pharmacological Agents in the Control of Reproduction. In: Veterinary reproduction and obstetrics. (10th ed). Saunders Elsevier Philadelphia, USA, p. 240-241.

Nowicki A, Baranski W, Baryczka A, Janowski T 2017 OvSynch protocol and its modifications in the reproduction management of dairy cattle herds an update. Journal of Veterinary Research, 61: 329-336.

Omontese B O, Rekwot P I, Makun H J, Obidi J A, Ruwaan J S et Chiezey N P 2010 Synchronization of estrus using EAZI-Breed™ CIDR® and FGA-30® intravaginal sponge in pre-partum Yankasa ewes. Research Journal of Animal Sciences. 4: 53-57.

Ozyurtlu N, Kucukaslan I, Cetin Y 2010 Characterization of oestrous induction response, oestrous duration, fecundity, and fertility in Awassi ewes during the non-breeding season utilizing both CIDR and intravaginal sponge treatments. Reproduction in Domistic Animals. 45: 464-467.

Pinna A E, Brandão F Z, Cavalcanti A S, Borges A M, Souza J M G, Fonseca J F 2012 Reproductive parameters of Santa Inês ewes submitted to short-term treatment with re-used progesterone devices. Arquivo Brasileiro de Medicina Veterinãria. Zootecnica, 64: 333-340.

Simonetti L, Forcada F, Rivera OE, Carou N, Alberio R H, Abecia J A, Palacin I 2008 Simplified superovulatory treatments in Corriedale ewes. Animal Reproduction Science, 104: 227–237.

Sirjani M A, Shahir M H, Kohram H, Shahneh A Z 2011 Effect of gonadotropin-releasing hormone (GnRH) treatment on multiple births in Afshari ewes. African Journal of Biotechnology, 10: 1358-1362.

Soltner D 1989 La reproduction des animaux d’élevage. Zootechnie générale. Tome I Bovins-chevaux-ovins-caprins-porcins-volailles-poissons. Collection Sciences et Techniques Agricoles. 147 p.

Taher J K 2014 Different estrus induction methods in Awassi ewes during the out of breeding season. Basrah Journal of Veterinary Research, 1: 66-74.

Taherti M et Kaidi R 2017 Variations de l'état corporel d'ovins et systèmes d'élevage dans la région de Chlef, Algérie. Revue d'Elevage et de Médecine vétérinaire des Pays tropicaux, 69 (3): 105. http://dx.doi.org/10.19182/remvt.31193.

Thériault M, Demers‐Caron V, Castonguay F 2014 Le CIDR: un moyen efficace, mais pas infaillible, pour la reproduction des brebis en contre‐saison. Ovin Québec, 14(1): 27‐32.

Timurkan H et Yildiz H 2005 Synchronization of estrus in Hamdani ewes: The use of different PMSG doses. Bulletin of the Veterinary Institute in Pulawy, 49: 311-314.

Titi H H, Kridli R T, Alnimer M A 2010 Estrus synchronization in sheep and goats using combination of GnRH, progestagen and prostaglandin F2a. Reproduction in Domestic Animals, 45: 594-599.

Ustuner B, Gunay U, Nur Z, Ustuner H 2007 Effect of long and short-term progestagen treatments combined with PMSG on oestrus synchronization and fertility in Awassi ewes during the breeding season. Acta Veterinaria Brno, 76: 391-397.

Zonturlu A K, Ozyurtlu N, Kacar C 2011 Effect of different doses ECG on estrous synchronization and fertility in Awassi ewes synchronized with progesterone during the transition period. Kafkas Universitesi Veteriner Fakultesi Dergisi, 17: 125-129.