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Small Ruminant Research 113 (2013) 365–370

Contents lists available at SciVerse ScienceDirect

Small Ruminant Research

journa l homepage: www.e lsev ier .com/ locate /smal l rumres

he effectiveness of supplemental administration ofrogesterone with GnRH, hCG and PGF2� on the fertility ofuj sheep during the non-breeding season�

emra Kayaa,∗, Cihan Kacara, Duygu Kayaa, Selim Aslanb

Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, 36300 Kars, TurkeyDepartment of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ankara University, 06110 Ankara, Turkey

a r t i c l e i n f o

rticle history:eceived 9 November 2012eceived in revised form 13 March 2013ccepted 22 March 2013vailable online 20 April 2013

eywords:uj ewenRHCGGF2�

aginal spongestrus synchronization

a b s t r a c t

This study investigated the effects on fertility parameters of combined administration offlugestone acetate, GnRH, hCG and PGF2� to Tuj ewes during the non-breeding season. Inthe study, 60 Tuj ewes were separated into four groups. Seven days before administeringan intravaginal gestagen (20 mg Flugestone acetate, sponge) to the ewes in Group I (GI,n = 15), they were given an injection of GnRH (8.4 �g Buserelin acetate). Seven days after thesponge was administered, the ewes were given a second intramuscular injection of GnRH.The sponge was left in the vagina for 14 days. Immediately after removing the sponge, anintramuscular injection of PGF2� (15 mg) was administered. The ewes in Group II (GII, n = 15)were administered hCG injections at a dose of 1000 IU/ewe instead of the GnRH injectionthat was given to the first group. The ewes in Group III (GIII, n = 15) were only administeredintravaginal sponge. The ewes in Group IV (n = 15) were kept as a control group and were notgiven any treatment. Immediately after the sponges were removed, rams were introducedin all groups, ensuring that ewes exhibiting estrus were mated. The percentage of ewesexhibiting estrus was found to be significantly higher in all the study groups (GI, GII andGIII) than in the control group (GIV) (P < 0.05). It was determined that the pregnancy ratiofor ewe mating at the first estrus was higher in group GII than in all the other groups(46.6%) (P < 0.05). The overall pregnancy rate and lambing rate was found to be significantlyhigher in GII (100%) than the other study groups (GI: 66.6% and 66.6%; GIII: 66.6% and46.6%, respectively, P < 0.05) as well as the control group (GIV: 6.6% and 0%, respectively,

P < 0.01). On day 7 after the sponge was administered, the mean plasma progesterone level(3.64 ng/ml) was found to be higher in the ewes in GII, and this difference was found tobe statistically significant (P < 0.01). We concluded in this study that administering hCGand vaginal sponges to Tuj ewes during the non-breeding season had a positive effect on

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pregnancy and lam

� This study was presented on a poster at the “15th Annual Conferencef the European Society Domestic Animals Reproduction”, Antalya, Turkey5–18 September 2011, and the abstract was published in Reproduction

n Domestic Animals, 46 (Suppl. 3), 117, 2011.∗ Corresponding author. Tel.: +90 474 2426807; fax: +90 474 2426853.

E-mail addresses: semra-kafkas@hotmail.com (S. Kaya),ihan3000@hotmail.com (C. Kacar), dykaya@gmail.com (D. Kaya),elim.aslan@gmail.com (S. Aslan).

921-4488/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.smallrumres.2013.03.018

tes.© 2013 Elsevier B.V. All rights reserved.

1. Introduction

Lambs are the most important source of revenue whenraising sheep. However, due to a rather long anestrousperiod after lambing, it is usually only possible for an ewe togive birth once per year. For this reason, various hormones

are administered in order to increase the fertility of ewesand to obtain lambs twice in one year or three times in twoyears (Ainsworth et al., 1982; Bazer et al., 2007; Gordon,1997; Goulet and Castonguay, 2002).

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366 S. Kaya et al. / Small Rumin

The hypothalamus is quite sensitive to the negativefeedback effect of estradiol in ewes during the seasonalanestrous period. During this period, LH is secreted lessfrequently, resulting in a lack of estrus and ovulation. Forthis reason, gonadotropin is needed for small and medium-sized follicles to continue developing (Leyva et al., 1998).

Administration of GnRH can stimulate ovulation in ane-strous ewes, but premature luteal regression can occurin these animals. In order to prevent this, progesteroneis administered prior to ovulation to inhibit oxytocinreceptors in the endometrium, thus reducing the uterineresponse to oxytocin for the secretion of PGF2� (Leyva et al.,1998).

Intravaginal sponges are usually preferred for the pur-pose of estrus synchronization in animals that are cyclicand in seasonal anestrus (Wildeus, 2000). It has been deter-mined that progesterone treatment followed by GnRHinjections in ewes during the anestrous period results infollicular development, ovulation and luteal function thatare similar to ewes in the breeding season (Mcleod et al.,1982; Wright et al., 1983, 1984). Administration of hCGin ewes during the anestrous period is usually performedafter mating or insemination. This aids CL developmentand helps to increase the secretion of progesterone. Thiseffect prevents early embryonic losses during the anestrousperiod (Fukui et al., 2001). Administering a PGF2� injectionone day before the vaginal sponges are removed or on theday the sponges are removed prevents the occurrence ofluteolysis at different times and prevents the delay of theestrus (Ataman et al., 2006; Dogan and Nur, 2006; Wildeus,2000).

The goal of this study was to research how fertilityparameters are affected by the combined use of GnRH, hCGand PGF2� administered together with a vaginal spongefor the purpose of estrus synchronization during the non-breeding season in the Tuj breed of ewes raised in theprovince of Kars and the surrounding area.

2. Materials and methods

2.1. Location

The study was performed between the months of May and July of2010 on Tuj ewes at the Kafkas University Veterinary Faculty Researchand Application Farm in Kars province, which is located at 40.5◦ northlatitude and 43◦ east longitude.

Fig. 1. Study design in experimenta

arch 113 (2013) 365–370

2.2. Animals

Sixty multiparous Tuj ewes aged three to six years old with a bodycondition score (Thompson and Meyer, 1994) of between 2 and 3 and 6Tuj rams aged four to five years old were used in the study. The animalswere grazed freely in a pasture during the day. The animals were givenapproximately 300 gr of concentrate feed per day and water ad libitum.The groups were selected such that the condition scores and age distri-bution were even. The ewes in each group were marked with differentcolors.

This study was approved by Kafkas University, Animal Local EthicsCommittee (KAÜ-HADYEK; 2010/12).

2.3. Experimental groups

2.3.1. Group I (n = 15)Seven days before the animals in this group were administered a vagi-

nal sponge (20 mg Flugestone acetate, Chronogest® CR, MSD, Turkey) (day−7), they were given intramuscular (IM) an injection of GnRH (0.0084 mgBuserelin acetate, Receptal® , MSD, Turkey). The sponge was administeredintravaginally (on day 0) and left in the vagina for 14 days. Seven days afterthe sponge was administered, the ewes were given a second injection ofGnRH. The sponge was removed on the 14th day and immediately after-ward an IM injection of PGF2� (7.5 mg/per animal, Dinoprost, Dinolytic® ,Pfizer, Turkey) was administered. On the same day, rams were joined tothis group, enabling them to mate with ewes in estrus.

2.3.2. Group II (n = 15)Seven days before a vaginal sponge was administered to the animals

in this group, they were given an IM injection of 1000 IU hCG (Chorulon® ,MSD, Turkey). Seven days after the injection, a sponge containing FGAwas placed in the vagina. Seven days after the sponge was administered,a second IM injection of hCG was given. Other applications were same asin GI.

2.3.3. Group III (n = 15)The ewes in this group were administered an intravaginal sponge for

a period of 14 days. On day 14, the sponge vas removed and the otherapplications were same as in the other treatment groups.

2.3.4. Group IV (n = 15)The ewes in this group were set aside as a control group and no hor-

mones were administered to them. On the same days as the other threegroups (21 days after the first hormone treatment), teaser rams werejoined to ensure that the ewes in estrus mated. Study design in groupsis shown in Fig. 1.

In order to determine progesterone levels, blood was taken from thejugular vein of all animals using EDTA 10 ml tubes on days −7, 0, 7 and 14and during the first, second and third estrus periods.

2.4. Diagnosis of pregnancy

To determine pregnancy status of ewes that mated with fertile rams,transrectal ultrasonography was performed using a Pie Medikal 100 Falko

l groups. B: blood samples.

S. Kaya et al. / Small Ruminant Research 113 (2013) 365–370 367

Table 1Fertility parameters for the groups.

Parameters Groups

Group I Group II Group III Group IV

Number of ewes (n) 15 15 15 15First estrus response (%) 66.6a (10/15) 60a (9/15) 73.3a (11/15) 20b (3/15)Pregnancy rate at first estrus (%) 6.6a (1/15) 46.6b (7/15) 0a (0/15) 6.6a (1/15)Ram joining-start of estrus (h) 54.8a,b 50.3a,b 59.6a 16.7b

Total pregnancy rate (%) 66.6a (10/15) 100b (15/15) 66.6a (10/15) 6.6c (1/15)Lambing rate (%) 66.6a (10/15) 100b (15/15) 46.6a* (7/15) 0c (0/15)Percentage of twins 0a 1a (1/15) 0a 0a

V tly significant. First estrus response: a,bP < 0.05; Pregnancy rate at first estrus:a bP < 0.05; a,b,cP < 0.01; Lambing rate: a,bP < 0.05; a*,bP < 0.01; a,a*,b,cP < 0.01.

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between the groups with regard to average lamb weights(P > 0.05).

Table 2Average lamb weights (kg) and standard deviations in the groups.

Groups Average lambweight

Male lambweight

Female lambweight

alues with different superscripts (a, b) in the same row are significan,bP < 0.01; Ram joining-start of estrus: a,bP < 0.05; Total pregnancy rate: a,

et. Equipment with a linear (6.0– 8.0 MHz) probe on days 29–31 afterating.

.5. Progesterone analysis

Progesterone in the blood samples was tested with the radioim-unoassay (RIA) method using commercial kits (Immunotech® , France).

he intra-assay and inter-assay coefficients for the kits were 6.5% and 7.2%espectively.

.6. Evaluation of fertility parameters

The ewes were observed for symptoms of estrus for the 7 days afteroining the rams. The ear number and the date and time that estrusbserved were recorded for each ewe. Ewes that did not exhibit symptomsf estrus were monitored for two cycles. The fertility parameters, calcu-ated following treatment, were estrus occurrence rate (number of ewesxhibiting estrus/total number of ewes in the group × 100), first estrusregnancy rate (number of pregnant ewes/number of ewes mated in eachroup × 100), total pregnancy rate (pregnancy ratios were calculated sepa-ately for three cycles and then the total pregnancy ratio was determinedor each group), lambing rate (number of ewes that lambed/number ofregnant ewes × 100) and lamb weight (the lamb was weighed on the day

t was born – within the first 24 h) (Karaca et al., 2009; Zarkawi et al., 1999,999b; Zonturlu et al., 2011).

.7. Statistical analysis

Statistical analysis of the data obtained in the study was performedsing the SPSS 16.0 statistical program. Differences between the groupsere calculated with the ANOVA test. Pregnancy and lambing rates in the

roups were statistically evaluated using the chi-squared test.

. Results

Estrus symptoms following ram joining began the ear-iest in the control group. Ewes in this group were foundo begin exhibiting estrus symptoms in an average of6.7 ± 3.2 h. The average estrus start time was found to be4.8, 50.3 and 59.6 h in treatment Group I, Group II androup III, respectively. The statistical evaluation revealed aignificant difference between Group III and Group IV withegard to the start time of estrus symptoms (P < 0.05). Notatistically significant difference was identified betweenroup I, Group II and Group IV (P > 0.05).

The estrus occurrence rates, pregnancy rates and lamb-ng rates for the study and control groups have been shownn Table 1. No statistically significant difference was iden-

ified between the study groups (Groups I, II and III) in anvaluation of the estrus rates, but all of the study groupsere found to be statistically higher than the control group

P < 0.05). We determined that the pregnancy rate at first

Fig. 2. The mean concentration of plasma progesterone (P4) in the groups.

estrus was higher in the group that was administered hCG(Group GII) than in the other three groups (P < 0.05).

The total pregnancy rates were found to be statisti-cally higher in GII than in all the other groups (P < 0.01;P < 0.05). A statistically significant difference was alsofound between the other study groups and the controlgroup with regard to total pregnancy rates (P < 0.01). Sim-ilarly, when all the ewes were evaluated, the lambing ratewas found to be statistically higher in GII than both theother study groups and the control group (P < 0.01) Table 1.

Progesterone levels increased in the study groups untilday 7. Furthermore, it was determined that the proges-terone levels in the ewes in Group II were significantlyhigher than the control group (P < 0.01) (Fig. 2).

Lamb weights were determined by weighting the lambsin the first 24 h following birth. The results revealed thatthere was no statistically significant difference betweenthe male and female lambs with regard to weight (P > 0.05;Table 2). There was also no significant difference found

Group I 4.2 ± 0.5 4.4 ± 0.6 3.9 ± 0.1Group II 3.9 ± 0.5 4.0 ± 0.5 4.0 ± 0.5Group III 4.3 ± 0.5 4.4 ± 1.1 4.4 ± 0.3Group IV – – –

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4. Discussion

It has been reported that the pregnancy rate in ewesadministered progestagen treatment during the anestrousperiod is 22–70% (Karagiannidis et al., 2001). This differ-ence depends on breed, diet, whether the ewe is lactating,which period of the anestrus the animal is in when thetreatment starts, the treatment protocol and the fertility ofthe ram (Echternkamp et al., 1976; Hulet and Stormshak,1972; Karagiannidis et al., 2001; Moeini et al., 2007).

In a study carried out by Bekyurek (1993), on Tuj ewes inthe anestrous period, vaginal sponges containing MAP wereadministered to one group. Vaginal sponges were admin-istered to the first and second groups for 14 days. On theday the sponges were removed, an intramuscular injectionof 500 IU PMSG was administered to in the second grouponly. No treatment was given to the ewes in the third group,which was kept as a control group. The estrus occurrencerates were 60% in the first group and 80% in the secondgroup, but no sexual activity was identified in the controlgroup (0%). The duration of estrus was determined to be61 ± 19 and 42 ± 13 h in Group I and Group II. The studyidentified pregnancy rates of 30% and 70%, respectively,in the groups that received treatment, but no pregnancieswere observed in the control group.

The results obtained in this study were similar to thoseof the aforementioned study. In our study, first estrusoccurrence rates varied from 60% to 73.3% in the studygroups, while pregnancy rates varied from 66.6% to 100%after combination therapies. These results indicate thatestrus occurrence and pregnancy rates will vary dependingon the method that is used.

Similarly, it was observed that the estrus start time aftertreatment varied depending on the treatment that wasperformed for estrus synchronization during the anestrusperiod. It has been reported that for Tuj ewes during thenon-breeding season, the time from the conclusion of treat-ment in ewes which are given CIDR alone or CIDR and PMSGon the day the CIDR is removed until the time that estrussymptoms begin varies from 34.5 h to 74 h (Gungor et al.,2007, 2009; Kacar et al., 2008). In our study, we determinedthat the time until the onset of estrus symptoms variedfrom 50.3 h to 59 h in the different study groups. In thepresent study exhibited signs of estrus at 54.8 (G1), 50.3(GII) and 59.6 (GIII) h, while it was observed in the con-trol group at 16.7 h. We must note that the fact that thefirst estrus occurrence rate in the control group was 20%,in other words that we could only evaluate the results for3 out of 15 ewes, is what caused this result.

In our study, although the estrus rate in Tuj ewes thatreceived GnRH was close to the rate of the group thatreceived hCG, the pregnancy rate after first estrus obtainedin ewes in this group was 6.6% less than in the groupthat was administered hCG (46.6%) (P < 0.01). It has beenreported that administration of hCG and GnRH has differ-ent effects on the vitality of the embryo, and that betterresults are obtained with hCG (Cam and Kuran, 2004).

Because secretion of gonadotropin is insufficient duringthe periovulatory phase during the non-breeding season,fully functional CL does not occur and progesterone secre-tion is insufficient (Spencer et al., 2004). For this reason,

arch 113 (2013) 365–370

alternative treatment methods have been developed inwhich treatment with hCG is administered in order toincrease the pregnancy rate (G’omez-Brunet et al., 2007).Human chorionic gonadotropin injection has a similareffect to the luteinizing hormone, helps the oocyte tomature and stimulates ovulation (Schmitt et al., 1996),causes the conceptus to grow and leads to significantincreases in placentation and the number of lambs born(Khan et al., 2003). In our study, the administration of hCGand sponges in Tuj ewes increased the total pregnancy andlambing rate to 100%, which supports the aforementionedfindings. The result was determined to be statistically dif-ferent from both sponge combined with GnRH and thecontrol group (P < 0.01 and P < 0.05). We think that theadministration of hCG supported the luteal structure, thuscausing an increase in the pregnancy rate. We base thison reports that the increase in pregnancy rates is relatedto the fact that hCG enhances progesterone productionand increases uterine secretions that are embryotrophic(Nephew et al., 1994; Cam and Kuran, 2004). This view issupported by the fact that the P4 levels increased signifi-cantly more on day 7 in Group II than in the other studygroups, even though the increase was not statistically sig-nificant, and that the levels were significantly higher inGroup II than in the control group (P < 0.01).

Other studies have shown that progesterone levels aresignificantly higher than the control group in groups thatare administered hCG on days 11, 12 and 13 after matingsubsequent to administer progesterone (Kittok et al., 1983).

These results lead to the conclusion that human chori-onic gonadotropin stimulates ovulation in this process,thus causing an increase in progesterone levels.

We identified fetal deaths in three of pregnant ewes inGroup III and one ewe in the control group. It has beenfound that GnRH has a positive effect on the vitality of theembryo by increasing and regulating LH stimulation (Camet al., 2002) and that in a similar fashion, administrationof hCG causes the same effect by increasing progesteronelevels because it causes the accessory corpus lutea to form(Beck et al., 1998; Nephew et al., 1994). Furthermore,studies performed with color Doppler have found thatadministering hCG increases the blood flow in the corpusluteum significantly more than GnRH (Aslan et al., 2011),which is an indication of the reason that the group receiv-ing hCG had much higher rates of continued pregnancy andlambing than all the other ewes.

It is thought that hCG treatment results in the devel-opment of a stronger conceptus, more regular and highersecretion of IFN-tau, and suppression of the luteolyticmechanism, which increases the lambing rate because thelamb develops better (Nephew et al., 1994; Spencer et al.,1996). The increase in the number of placentomes formingafter hCG treatment proves this fact (Khan et al., 2003).

It was determined that total pregnancy rates afteradministering gonadotropin releasing hormone togetherwith vaginal sponges were the same as in the group thatwas administered only a vaginal sponge. No statistically

significant difference was found with regard to lamb-ing rates either (Fukui et al., 1985, 1991; Kridli et al.,2003). Certain publications have reported no increase inP4 serum/plasma levels after administering GnRH and even

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hat drops have been observed (Lucy and Stevenson, 1986;yan et al., 1991; Naohisa et al., 1999). In this study, weid not observe any increase in P4 serum levels due todministering GnRH either.

Similar to what was found by Saharrea et al. (1998), ourtudy also shows that the GnRH has a lower effect on fer-ility in ewes than hCG. It has been reported that hCG helpshe blastocyst to develop and down regulates estradiol andxytocin, thus strongly suppressing the secretion of PGF2�

nd causing the blastocyst to secrete more IFN-� (Nephewt al., 1994). This may explain why the administration ofvaginal sponge and hCG provided better fertility results

han other groups during the non-breeding season.Lashari and Tasawar (2010), gave PGF2� injections to

wes during the breeding season at 11 day intervals andhen mated the ewes that showed signs of estrus; on theay they were mated, half of these ewes were given an

njection of GnRH in an attempt to identify the effect onamb weight. It was determined that the birth weights ofambs in the group that were given GnRH injections wereigher than the control group. In contrast, Cam et al. (2002),eported that the GnRH injection (4 �g) they gave 12 daysfter ewes were mated during the breeding season did notffect the weight of the newborn lambs. In our study, theact that no difference was identified between the groupsith regard to birth weights supports the view that the

reatments that were administered had no effect on theamb weights.

. Conclusions

We concluded in this study that administering hCGogether with vaginal sponges to Tuj ewes during theon-breeding season increased the pregnancy and lambingates.

cknowledgements

The study was financially supported by Kafkas Univer-ity, Scientific Research Projects Coordination Unit (BAProject number: 2010-VF-13).

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