Evaluation of the short and long estrus synchronization protocol in inseminated sheep with frozen semen Evaluación del protocolo corto y largo de sincronización de celo en borregas inseminadas con semen congelado Manrique Quispe Yan Pierr1* , Pérez Guerra Uri Harold1 , Málaga Apaza Julio2 , Ayma Flores Wilbur Ru- bén3 , Cardenas Minaya Oscar Efrain4 , Pérez Durand Manuel Guido1 Data of the Article Abstract 1 National University of the Altiplano Puno. Faculty of Veterinary Medicine and Zootechnics. The objective of the study was to evaluate the effect of short (5 days) and long (9 days) SC protocols in ewes Animal Reproduction Laboratory. Av. Panamá No 710, Puno, Peru. inseminated with frozen semen on the diameter of the uterine horn and pregnancy rate. The experiment was carried Tel: + 051-599430. 2 out at the Carolina Experimental Center, belonging to the National University of the Altiplano, and 40 ewes be-National University of the Altiplano Puno. Faculty of Veterinary Medicine and Zootechnics. tween Corriedale and Criollas were used; in groups of 20 for each treatment, which were synchronized with in- Postgraduate Direction. Av. Floral Nº 1153. Puno, Peru. travaginal sponges based on Medroxyprogesterone acetate, for 9 days (long protocol) and 5 days (short protocol) Tel: + 051-599430. 3 National University of the Altiplano Puno. and at the time of sponge removal, 350 IU of eCG were applied. To measure the diameter of the uterine horn, Faculty of Veterinary Medicine and Zootechnics. ultrasonography was performed at 36 h post sponge removal and at 56 h after cervical insemination with thawed Carolina Experimental Center. Av. Floral Nº 1153. Puno, Perú. semen and a subsequent ultrasonography at 35 days to confirm gestation. Quantitative data were analyzed using Tel: +051-599430. 4 National Institute of Agrarian Innovation. the statistical t-test for uterine horn diameter and Chi-square for gestation rate. The results for uterine horn diameter Reproductive Biotechnology Laboratory. were 11.11±1.52 and 12.12±2.12 mm for the short and long synchronization protocol, respectively. Regarding the La rinconada - Salcedo s/n. Puno, Peru. Tel: + 051-363812. pregnancy rate, 21.05 % and 25 % were obtained for the short and long synchronization protocol, respectively. *Contact address: Therefore, we can conclude that the long progesterone treatment had better results than the short treatment both in National University of the Altiplano Puno. Faculty of Veterinary Medicine and Zootechnics. uterine diameter and pregnancy rate, but this difference was not significant (p>0.05). Animal Reproduction Laboratory. Av. Panamá No 710, Puno, Peru. Tel: + 051-599430. Yan Pierr Manrique Quispe E-mail address: yanpierrmvz@gmail.com Keywords: Estrus, fertility, ovine, 2021. Journal of the Selva Andina Animal Science®. Bolivia. Todos los derechos reservados. pregnancy, thawed semen, uterine diameter. Resumen In J. Selva Andina Anim. Sci. El objetivo del trabajo fue evaluar el efecto de los protocolos corto (5 días) y largo (9 días) de SC en borregas 2021; 8(2):73-81. inseminadas con semen congelado sobre el diámetro del cuerno uterino y tasa de preñez. El experimento se realizó ID of the article: 092/JSAAS/2021 en el Centro Experimental Carolina, perteneciente a la Universidad Nacional del Altiplano, y se utilizó 40 ovejas Record from the article entre Corriedale y Criollas, en grupos de 20 para cada tratamiento, que fueron sincronizadas con esponjas intrava- Received April 2021. ginales a base de Acetato de Medroxiprogesterona, durante 9 días (protocolo largo) y 5 días (protocolo corto) y al Returned July 2021. momento del retiro de la esponja se aplicó 350 UI de eCG. Para medir el diámetro del cuerno uterino se realizó la Accepted August 2021. Available online, October 2021. ecografía a las 36 h post retiro de la esponja y a las 56 h la inseminación cervical con semen descongelado y una posterior ecografía a los 35 días para confirmar la gestación. Los datos cuantitativos fueron analizados mediante la prueba estadística de “t” para diámetro de cuerno uterino y Ji cuadro para tasa de gestación. Los resultados para el diámetro de cuerno uterino fueron de 11.11±1.52 y 12.12±2.12 mm para el protocolo de sincronización corto y Edited by: Selva Andina largo, respectivamente. Respecto a la tasa de preñez se obtuvo 21.05 % y 25 %, para el protocolo de sincronización Research Society corto y largo, respectivamente. Por lo que podemos concluir que el tratamiento largo de progesterona, tuvo mejores 73 Manrique Quispe et al. J. Selva Andina Anim. Sci. _______________________________________________________________________________________________________________ resultados al tratamiento corto tanto en el diámetro de cuerno uterino y tasa de gestación, pero no fue significativo Palabras clave: esta diferencia (p>0.05). Estro, diámetro uterino, fertilidad, ovino, preñez, semen descongelado. 2021. Journal of the Selva Andina Animal Science®. Bolivia. All rights reserved. Introduction 5 6 Peru sheep sector has great potential, as it has a large Martinez-Ros et al. , Amer & Hazzaa , Ungerfeld & 7 3 number of animals, but unfortunately there is a neg- Rubianes , Knights et al. , mention that short syn- ative growth rate (-3.5%) and therefore a decrease in chronization treatment has similar fertility to tradi- 25 4 production (1.17%)1 therefore, it is necessary to es- tional ES, while Almadaly et al. , Viñoles et al. , 9 14 tablish improvements in the productive and repro- Farfán et al. Özyurtlu et al. Vilariño et al. 13 Sare- 26 ductive indexes through livestock improvement pro- minejad et al. report higher fertility results than the grams in order to increase herd production, hence the traditional synchronization treatment (5 to 7 days) promotion of the dissemination of semen for the pro- could be an alternative to the traditional use of long duction of semen for the production of sheep, the dis- synchronization, this would help to be more flexible semination of semen of high genetic value in the in the field and thus avoid the problems described ovine species Artificial insemination (AI) is an ap- above. propriate reproductive biotechnology to achieve this In view of this dilemma, we intend to evaluate the goal2 short and long ES protocol in ewe lambs inseminated Estrus synchronization (ES) methods are a very use- with frozen semen to determine which protocol is ful tool in AI programs2. Several ES techniques have more efficient in terms of uterine diameter and preg- been developed to induce estrus in sheep3. Long-term nancy rate. progestogen treatments (12 to 14 days) are com- monly applied in sheep4-13, with a percentage of ani- Materials and methods mals showing acceptable estrus and fertility rates12, but with lower fertility than natural estrus14-16. This Location and animals of the experiment. The experi- low fertility rate is due to different causes such as, ment was carried out at the Experimental Center deficiencies in detection and ES, slow follicular turn- "Carolina", belonging to the Faculty of Veterinary over that generates a persistent follicle4,17,18 on the Medicine and Animal Husbandry of the National other hand the traditional synchronization system University of the Altiplano, located in the District of brings vaginal infections15,19, with bacterial prolifer- Puno and province of Puno - Peru, around the coor- ation20 has also been associated with accumulation of dinates 15 52 11 south latitude and 70 24 32 west offensive vaginal mucus, bad odor21, vaginal adhe- longitude, at an altitude of 3995 meters above sea sions, vaginitis22, which result in low fertility rates, level. A total of 40 sheep were used (20 adult Corrie- after AI with fresh semen. Short protocols (5 to 7 dale ewes and 20 adult Criollo ewes) (Table 1), mul- days) with progestogenic devices4,23 have been re- tipras taken at random from the flock of sheep, with ported to be as effective as traditional protocols (12- a body condition of 2.5 (scale 1 to 5) that were ultra- 14 days)24. sounded to rule out pregnancy, clinically healthy, 74 Vol. 8 No 2 2021 Short and long estrus synchronization protocol in inseminated sheep ______________________________________________________________________________________________________________ with an extensive breeding system, kept before and were inseminated at 56 h post application of eCG, us- during the experiment in grazing conditions in natu- ing frozen semen in 0.25 mL straws, which had a ral pastures without supplementation. The experi- sperm concentration of 300 x 106 after thawing at ment was carried out between April and May. 35°C for 30 sec. A subjective evaluation of seminal motility was made, which was 45% on average8, due Table 1 Distribution of sheep according to treatment to the fact that they belonged to the same breeder. Corriedale sheep Criollo sheep Statistical analysis. The data were subjected to de- 20 20 scriptive statistics (mean, standard deviation, and co- *TL P4 **TC P4 *TL P4 **TC P4 10 10 10 10 efficient of variability), comparing two groups (short *LT P4: Long treatment with progesterone. and long treatment) and evaluating their normality ** ST P4: Short Treatment with progesterone. and homoscedasticity, the UHD were subjected to t- Synchronization of estrus. Bighorn sheep were given test, while the pregnancy rate obtained in proportions intravaginal sponges impregnated with 60 mg of was subjected to the non-parametric chi-square test, medroxyprogesterone acetate (MAP, Progespon both tests were evaluated with a reliability of 95%, Syntex S.A., Argentina)27 on a random day of the es- all data were evaluated in the R 3.4.1. program with trous cycle (Day 0), for a total of 5 days for the short its RCmdr (R Core Team, 2020) extension. progesterone protocol5,28 and 9 days for the long pro- gesterone protocol17,29. On Day 5 and 9 of the treat- Results ments, the P4 sponges were removed and 350 IU of equine chorionic gonadotropin (eCG, Novormon Table 2 describes the statistics for the UHD in Cor- Syntex S.A., Argentina) was applied intramuscularly riedale and Criollo ewe lambs synchronized with the to each ewe7,15. short and long synchronization protocol, observing Ultrasonographic evaluation and artificial insemi- similar means in relation to the type of protocol and nation. Ultrasonographic examinations for the meas- breed (p=0.1206 and 0.6197 respectively), which in- urement of uterine horn diameter (UHD) were per- dicates that the synchronization period does not in- formed at 36 h post application of eCG and gestation fluence the variation of the UHD nor the breed of diagnosis at 35 days’ post AI, in both cases a real ewe. A total of 5 sponges were lost (4 for the long time B-mode ultrasound scanner (Esoate Pie Medi- protocol and 1 for the short protocol). cal, Tringa Linear VET) was used. The ewe lambs Table 2 Diameter of uterine horn in ewe lambs Factors Levels No Mean±D.S (mm) CV (%) Sign. Corto 19 11.11±1.52 13.68 Synchronization period 0.1206 Largo 16 12.12±2.12 17.49 Corriedale 19 11.11±1.63 14.36 Sheep breed 0.6197 Criollo 16 11.87±2.17 19.08 Table 3 shows the pregnancy rate in ewe lambs ac- was 21.05 % and in ewes synchronized for 9 days cording to synchronization period and breed, the was 25 % (p=0.7817), in this sense there would be proportion of pregnant ewes synchronized for 5 days no dependence between the duration period of the 75 Manrique Quispe et al. J. Selva Andina Anim. Sci. _______________________________________________________________________________________________________________ estrus synchronization protocol (short and long) in relation to the higher or lower pregnancy rate. Table 3 Pregnancy rate in ewe lambs Factors Levels No No of fertile % of fertile Corto 19 4 21.05 Synchronization period Largo 16 4 25 (P > 0.7817) Discussion The comparison of UHD in relation to breed there is no statistical difference being for Creole sheep The results indicate the presence of significant UHD (11.87±2.17 mm) in comparison to Corriedale sheep in both treatments, which may be due to the applica- (11.35±1. 63 mm) which would indicate that Creole tion of eCG that reduces the atresia of preovulatory and Corriedale ewes had similar responses to the syn- follicles, thus generating an increase in the estrogen chronization protocols of the present study so estro- concentration, manifesting estrus and ovulation in gens influenced uterine diameter even though there the ewe lambs6,30-32 since we applied a dose of 350 are genetic or racial factors30 that could have influ- IU, which influenced the estrogen concentration. enced since the Creole breed is more prolific than the However, a slight difference is observed between the Corriedale, which probably caused greater sensitivity UHD being slightly superior the long treatment in re- to the synchronization protocol and therefore a lation to the short one, this characteristic could be greater UHD. Studies of UHD diameter due to the measured because the uterine wall has a more heter- effect of the synchronization protocol are scarce, so ogeneous ecotexture (due to the increase of vascular- this study could lay the foundation for further studies ization and the edema of the horns) than in estrus and on the subject, and would also help to identify indic- during estrus, it is normally possible to differentiate ative parameters that are useful for discarding sheep the endometrial folds and the myometrium, as well or as an indicator of the presence of estrogen. as the small accumulations of fluid in the uterine lu- Gestation rates (Table 3) are similar to those reported men33, this difference is due to the fact that during the by Gibbons & Cueto10 and Muñoz et al.11 for AI with long treatment a greater follicular growth could be frozen semen via cervical with a single insemination, observed4, which is characterized by a greater estro- while Perez et al.8 had a gestation rate of 68% for gen production that leads to a slight increase in uter- their double insemination with thawed semen11. They ine diameter due to the increase in endometrial de- also agree with Knights et al.3, Ungerfeld & Rubia velopment and endometrial glands, in addition to nes7 and Martinez-Ros et al.5, in reporting slightly edema due to greater vascularization compared to the higher gestation rates for long (12 days) than short (5 short treatment3,6,9. In addition, Teixeira de Sousa et days) protocols; while Koyuncu et al24, Da Silva et al.34 reported in heifers that there is an increase in al.12 and Amer & Hazzaa6 had much higher gestation UHD due to the effect of estrogen, favoring preg- rates for the long protocol (14 or 12 days) with re- nancy. spect to the short protocol (6 or 7 days); but they do 76 Vol. 8 No 2 2021 Short and long estrus synchronization protocol in inseminated sheep ______________________________________________________________________________________________________________ not agree with Vilariño et al.13, Farfán et al.9, Funding source Özyurtlu et al.14, Sareminejad et al.26 nor with Verdol jak et al.23 who reported a higher pregnancy rate for This article does not have any funding other than the the short protocol (6 or 7 days) with respect to the research group's own resources. long protocol (14 or 12 days). Our gestation results for the short treatment of 21. 05 % and for the long Conflicts of interest treatment of 25 % were low in comparison with other The authors declare that this research was carried out authors due to several factors such as the use of nat- at the Universidad Nacional del Altiplano Puno and ural mating3,5-7,12,25, balanced feeding6,12, application that there is no conflict of interest between the au- of cloprostenol12, application of eCG at higher thors of this article. doses3,5,7,12, male effect12, difference between breeds; while in our work we used thawed semen and it is Acknowledgements known that semen freezing decreases the gestation rate35,36, to this is added the nutritional deficiency To the technical and administrative personnel of the typical of the time of year6. The difference in our re- Carolina Experimental Center of the National Uni- sults due to the effect of the type of protocol could be versity of the Altiplano for their support in carrying due to the fact that eCG (350 IU) was applied at the out the research. end of the two treatments, which could have caused the formation of follicular cysts in the short treat- Ethical considerations ment4, while in the long protocol it could have coun- teracted the fertility problems4,17,37,38. The study was approved by the Ethics Committee of In addition, the long protocol had this improvement the Faculty of Veterinary Medicine and Animal Hus- bandry of the Universidad Nacional del Altiplano possibly due to the lack of use of prostaglandin in the 19,39 and the guidelines established by this Committee short protocol to eliminate the functional corpus were followed. luteum since it could affect its effectiveness5 in the productive period; finally, it should be considered Authors' contribution to the article that our long treatment was only 9 days, so it did not exceed the half-life of the corpus luteum (11 to 12 Manrique Quispe Yan Pierr, wrote the manuscript days)17, favoring follicular exchange, which could and the experimental part of the research. Perez generate oocytes in good conditions40,41. Therefore, Guerra Uri Harold Uri, carried out the experimental we can conclude that the long synchronization proto- design and writing of the manuscript. Malaga Apaza col had a higher UHD and gestation rate than the Julio, revised and wrote the manuscript. Ayma Flores short synchronization protocol, but not significantly. Wilbur Ruben, performed the experimental part of Nevertheless, from an economic and management the research and writing of the manuscript. Cardenas point of view, it is possible to replace the traditional Oscar, performed the experimental design and statis- P4 regimen (12-14 days) with a short synchroniza- tical analysis. Perez Durand Manuel Guido, did the writing and final revision of the manuscript. tion protocol (5-7 days). 77 Manrique Quispe et al. J. Selva Andina Anim. Sci. _______________________________________________________________________________________________________________ Limitations in the research efficiency of ewes during the non-breeding season. Vet Arh 2009;79(1):19-30. There were no limitations for the development of the 7. Ungerfeld R, Rubianes E. 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