B mode and Doppler ultrasonographic characteristics of the dominant follicle and corpus luteum in Criollo cows subjected to an oestrus synchronization protocol Característica ultrasonográficas B mode y Doppler del folículo dominante y cuerpo lúteo en vacas Criollas sometidas a un protocolo de sincronización de celo Perez Guerra Uri Harold1 , Luque Mamani Natalio2, Condori Apaza Rafael3 , Manrique Quispe Yan Pierr 4* , Escobedo Arizaca Ángel1 , Mamani Cato Rubén1 , Urviola Sánchez Jesús Martin1 , Pérez Durand Manuel Guido1 Article Data Abstract 1 National University of the Altiplano Puno. Faculty of Veterinary Medicine and Animal Hus- The objective was to determine the ultrasonographic B mode and Doppler characteristics of the dominant follicle bandry. Laboratory of Animal Reproduction. and corpus luteum in Criollo cows subjected to an oestrus synchronization protocol. The study was conducted at Av. Floral N° 1153. the Agricultural Experimental Station ILLPA during the months of May to July using 15 Criollo cows with regular Tel: + 051 599430. Puno - Peru. body condition and fed with natural pasture, the protocol consisted of placing estradiol benzoate and intravaginal 2 National University of the Altiplano. device on the first day, then on day 7 the device was removed and an analogue of Prostaglandin F2α was applied, Faculty of Veterinary Medicine and Animal Hus- bandry. On day 8 estradiol benzoate was applied again and on day 9 artificial insemination was performed with semen Chuquibambilla Experimental Centre. from a single Fleckvieh sire, ultrasonographic evaluation was performed on days 7 and 9 (synchronization started) Laboratory of Animal Health. Puno-Peru. to determine the diameter of the dominant follicle, growth rate and diameter of the uterine horn, the evaluation of 3 Ministry of Agrarian Development and Irrigation. the corpus luteum was performed on day 19 determining the diameter, volume and luteal vascular area (%), all Directorate of Agrarian Technological Develop- the analyses were performed with the Jamovi 1 Programme. 6.23.0. The results of the dominant follicle on day 7 ment. National Institute for Agrarian Innovation. was 8.69 mm and day 9 was 10.7 mm with a growth rate of 1.14 mm/day, the diameter of the right uterine horn Agricultural Experimental Station ILLPA. Puno - Peru. was 11.85 mm (day 7) which increased to 15.32 mm (day 9) while the left horn increased from 12.72 to 16.27 4 National Amazonian University of Madre de mm. 72 to 16.27 mm, the characteristics of the corpus luteum were 7.96 mm diameter, volume 0.23 mm3 and Dios. luteal vascular area was 20.96 %, finally, the pregnancy rate obtained was 6 cows out of 15 inseminated which Veterinary Medicine and Zootechnics. Laboratory of Animal Reproduction. represents 40 %. In conclusion, the diameters and volume of the dominant follicle and corpus luteum are lower Jorge Chávez Av. N° 1160. Telephone: +51 975842679. than those reported in other breeds in the same environmental conditions, the luteal vascular area was 20.96 %, Puerto Maldonado. Madre de Dios/Tambopata 17001. the proportion of blood irrigation of the CL in Criollo cows and finally the pregnancy rate was 40 %. However, it is necessary to point out that these are the first reports of Doppler characteristics in Criollo cows *Contact address: National Amazonian University of Madre de Dios. Veterinary Medicine and Zootechnics. Laboratory of Animal Reproduction Jorge Chávez Av. N° 1160. . Telephone: +51 975842679. Puerto Maldonado. Madre de Dios/Tambopata 17001. Yan Pierr Manrique Quispe E-mail address: yanpierrmvz@gmail.com Keywords: Corpus luteum, 2023. Journal of the Selva Andina Animal Science ®. Bolivia. All rights reserved. Creole, dominant follicle, pregnant, Resumen ultrasonography. In J. Selva Andina Anim. Sci. El objetivo fue determinar las características ultrasonográfica B mode y Doppler del folículo dominante y cuerpo 2023; 10(1):52-60. lúteo en vacas Criollas sometidas a un protocolo de sincronización de celo. El estudio fue realizado en la Estación Article ID: 121/JSAAS/2023 Experimental Agraria ILLPA durante los meses de mayo a julio utilizando 15 vacas de raza Criolla con condición Article history corporal regular y alimentadas con pasto natural, el protocolo consistió en colocar benzoato de estradiol y dispo- Received September, 2022. sitivo intravaginal el primer día, posteriormente el día 7 se retiró el dispositivo y se aplicó un análogo de Prosta- Returned November, 2022. glandina F2α, el día 8 se aplicó nuevamente benzoato de estradiol y el día 9 se realizó la inseminación artificial con Accepted January, 2022. Available online, April, 2023. 52 Perez Guerra et al. J. Selva Andina Anim. Sci. _______________________________________________________________________________________________________________ semen de un solo reproductor de raza Fleckvieh, la evaluación ultrasonográfica fue realizada los días 7 y 9 (ini- Edited by: Selva Andina ciado la sincronización) para determinar el diámetro del folículo dominante, tasa de crecimiento y diámetro de Research Society cuerno uterino, la evaluación del cuerpo lúteo fue realizada el día 19 determinando el diámetro, volumen y área vascular luteal (%), todos los análisis fueron realizados con el programa Jamovi 1.6.23.0. Los resultados del fo- lículo dominante el día 7 fue de 8.69 mm y día 9 de 10.7 mm con una tasa de crecimiento de 1.14 mm/día, el diámetro del cuerno uterino derecho fue 11.85 mm (día 7) mismo que aumento a 15.32 mm (día 9) mientras el cuerno izquierdo aumento de 12.72 a 16.27 mm, las características del cuerpo lúteo fueron diámetro 7.96 mm, Palabras clave: volumen 0.23 mm3 y área vascular luteal fue de 20.96 %, finalmente, la tasa de preñez obtenida fue 6 vacas de 15 Cuerpo lúteo, Criollo, inseminadas que representa el 40 %. En conclusión, los diámetros y volumen del folículo dominante y cuerpo folículo dominante, lúteo son inferiores a lo reportado en otras razas en las mismas condiciones ambientales, el área vascular luteal preñez, ultrasonografía. fue de 20.96 % proporción de irrigación sanguínea del CL en vacas Criollas finalmente la tasa de preñez fue del 40 %. Sin embargo, es necesario indicar que son los primeros reportes de características Doppler en vacas Criollas. 2023. Journal of the Selva Andina Animal Science®. Bolivia. Todos los derechos reservados. Introduction The cattle population in Peru is approximately 5 mil- cattle7, these technologies could be used in Criollo lion, 78 % is in the Sierra, more than half (70 %) is cattle, to schedule calving at times of the year with in the hands of small and medium producers, the pre- better environmental conditions4, currently being dominant breed, the Criolla, with crosses with the complemented with ultrasonography, in order to de- Brown Swiss breed1. This breed has an important termine the morphometry of ovarian structures dur- economic role, as it is a source of labour, animal pro- ing the CS process8, these findings are complemented tein food and family savings in altitudinal zones, with Doppler ultrasonography to obtain characteris- where other breeds do not produce efficiently2-4. tics related to the blood irrigation of different or- Criollo cattle, even though they are used for a triple gans9,10. The need to generate information on repro- purpose, meat, milk and work, are at a disadvantage ductive physiology in Criollo cattle, hence the objec- when compared to other breeds such as Holstein and tive of the study was to determine the ultraso- Brown Swiss. However, their strength lies in their ad- nographic B mode and Doppler characteristics of the aptation to the environment, lower feed require- dominant follicle (DF) and corpus luteum (CL) in ments, longevity, resistance to adverse conditions Criollo cows subjected to a CS protocol. and higher fertility1,5. This high fertility can be ex- ploited more efficiently through the use of reproduc- Materials and methods tive biotechnologies, generating greater genetic pro- gress by increasing the intensity of selection from the Study site and animals. The study was carried out at male through artificial insemination (AI) and from the Agricultural Experimental Station ILLPA be- the female through embryo transfer (ET), in both longing to the National Institute of Agrarian Innova- cases, the use of oestrus synchronization (OS) proto- tion (INIA) located in the district of Paucarcolla in cols with different synthetic hormones is necessary6. the province and region of Puno. Fifteen cows were The purpose of CS is to generate a new follicular evaluated cows Criollo breed The study was carried wave at the beginning, in order to synchronize ovu- out during the dry season, which is characteristic of lation, in most of the protocols used in beef and dairy 53 Vol. 10 No 1 2023 B mode and Doppler ultrasonographic features of the dominant follicle and corpus luteum ______________________________________________________________________________________________________________ the Peruvian Altiplano from May to July. The ani- All the images were stored in a USB which were later mals had a regular body condition between 2.5 and analyzed, finally, the diagnosis of gestation was 2.8 degrees with a feeding management based on nat- made on day 30 post IATF, to determine the presence ural pastures.Oestrus synchronization and artificial or not of the gestational sac and the embryo using the insemination. This process was preceded by an ob- same ultrasonographic equipment. stetric diagnosis by means of ultrasonography, se- Ultrasonographic evaluation of the corpus luteum lecting those apparently normal females (free of ap- (Colour Doppler). It was performed on day 19 post parent reproductive problems, evaluated by means of IATF using Draminski 4Vet® equipment, first, iden- a previous gynecological evaluation), those selected, tifying the CL only with B mode to determine the di- on the first day the CIDR® device was inserted (Pro- ameter (mm) and volume (mm3), then, the Colour gesterone in intravaginal device, active Progesterone Doppler mode was activated to determine the luteal 10 %: 1.9 g, Zoetis, Argentina) in addition to the ap- vascular area (AVL %) which was determined in per- plication of 2 mg intramuscularly (IM) of Estrovet® centage, once the cinestore (short video of the evalu- (Estradiol benzoate, Montana, Peru). After 7 days, ation of the CL) was stored it was analyzed with the the device was removed and 2 mg of Prostal® (D- Image J® programme on a computer, the methodol- Chlorprostenol, Over, Argentina) was applied IM. ogy was performed as recommended by Acosta et Finally, on day 8 Estrovet® 2 mg IM was applied al.11. again. Fixed-time artificial insemination (FTAI) was Statistical analysis. Statistical analysis was per- performed on day 9 with semen straws from a Fleck- formed using Jamovi 1.6.23.012 statistical software. vieh bull named INTI from the Ministry of Agricul- The data were analyzed with descriptive statistics, ture and Rural Affairs, the semen had a total motility determining the mean and standard deviation for the at unfreezing of approximately 50% and a concentra- characteristics of FD diameter, uterine horns and FD tion of 25x106. When the straws were thawed at 37° growth rate, in addition to a Student's test to compare C for 30 to 45 seconds, all females were inseminated the diameter of the FD and uterine horns during days with straws from the same bull. 7 and 9 of the SC protocol, while for the characteris- Ultrasonographic evaluation of the dominant follicle tics of the CL the mean, standard deviation and con- and uterine horns (B mode). It was preceded by fidence intervals at 95 % were evaluated. cleaning the perianal area of the females for the ex- amination, using Draminski 4Vet® equipment Results (Draminski ul. Owocowa 17, Poland) with a 6 MHz linear transducer was used to evaluate the morpho- Table 1 presents the B-mode morphometric charac- metric characteristics of the FD and uterine horns on teristics of the FDs of synchronized Criollo cows, as days 7 and 9 of CS to determine the following char- well as the uterine diameter of both horns on days 7 and 9 after the start of the protocol. acteristics: i) FD diameter on days 7 and 9, measured in mm, ii) Growth rate, measured in mm/day, iii) Uterine horn diameter on days 7 and 9, measured in mm. 54 Perez Guerra et al. J. Selva Andina Anim. Sci. _______________________________________________________________________________________________________________ Table 1 Ultrasonographic morphometric characteristics (Mode B) of the uterine follicle and uterine horns (n=15) Uterine diameter (mm) Dominant follicle (mm) Growth rate (mm/day) Right Left Day 7 8.69±1.57 a 11.85±2.66 a 12.72±1.43 a 1.14±0.58 Day 9 10.7±1.35 b 15.32±2.76 a 16.27±1.75 a (a, b) different letters in columns show statistical significance (p>0.05). The diameter of the follicle on day 7 after the begin- 11.85 to 15.32 mm for the right horn and from 12.72 ning of the synchronization protocol was 8.69 mm to 16.27 mm for the left horn. The diameter of uter- while on day 9 a diameter of 10.7 mm was observed, ine horns increased in size from day 7 to day 9 with allowing to observe that there was a development of the latter day for right horn being 15.32 mm and left the follicle, verified with the growth rate of 1.14 horn 16.27 mm. The growth rate was 1.14 mm/day. mm/day. As for the diameter of the right and left Table 2 shows the B-mode and Doppler morphomet- uterine horns, an increase in size was also observed ric characteristics of the CL of Criollo cows synchro- between day 7 and 9 respectively, ranging from nized with a SC protocol. Table 2 Ultrasonographic morphometric characteristics (B-mode and Doppler) of the corpus luteum (n=15) Diameter (mm) Volumen (mm3) Vascular Luteal Area (AVL %) Mean±SD 7.96±2.07 0.23±0.13 20.96 Confidence Interval (95 %) 6.82 - 9.10 0.16 - 0.31 13.16 - 28-76 Figure 1 Colour Doppler ultrasound evaluation of a corpus luteum of Criollo cows (day 19 post AI) The characteristics of the CL were 7.96 mm in diam- percentages being on average 20.96 % with intervals eter with sizes ranging from 6.82 to 9.10 mm, the vol- ranging from 13.16 to 28.76 %, all these characteris- ume of the CL was 0.23 mm3 with intervals ranging tics were determined with 95 % reliability. The col- from 0.16 to 0.31 mm3, the characteristic taken with our Doppler assessment, Figure 1. Doppler ultrasonography was the AVL evaluated in 55 Vol. 10 No 1 2023 B mode and Doppler ultrasonographic features of the dominant follicle and corpus luteum ______________________________________________________________________________________________________________ Discussion Brown Swiss breed due to its larger body size than Criollo cows17,19,20. The maximum diameter obtained on day 9 is similar The uterine diameter obtained was lower than those to that reported in crossbred animals with Criollo an- reported in Holstein cows of approximately 460 kg imals in the same conditions synchronised with Pro- live weight with diameters greater than 20 mm21, gesterone protocol reaching a size of 10.2 mm13, like- however, the increase in uterine diameter is related to wise, in Criollo cows evaluated during the entire es- the increase in estrogens also related to the follicular trous cycle in high altitude conditions, diameters in phase, in this phase estrogens increase blood irriga- the rainy season of 11.25 mm and in the dry season tion which generates oedema at the level of the uter- of 11.67 mm were reported14, the follicular develop- ine horns which are observed with an increase in di- ment from day 7 to 9 reflects the positive feedback ameter on ultrasonography22,23. The growth rate was after the extraction of the progesterone device that al- similar to that reported in cows crossed with Criollas lows the free development of the FD until the respec- in the same environmental conditions with a similar tive insemination, at this moment it is known that the synchronization protocol reporting a rate of 1.2 FD will increase the number of receptors for FSH and mm/day, although the diameter of the FD was later for LH to continue with the development and higher17 , the growth rate reported was similar being maturation of the FD15,16. Higher reports are obtained 1.05 mm/day in Criollo cows called BON, also re- in altitude conditions of 1500 masl in Black and ported rates similar to those reported in Criollo cows White Creole (BON) cows with a FD17 size of 14.3 in dry and rainy season which were 1.01 mm/day and mm. The difference could be due to the effect of the 1.0 mm/day respectively14. The growth rate obtained higher altitude where the present study was carried suggests the positive development of the FD from the out since it generates the highest production of reac- day the DIB (bovine intrauterine device) was re- tive oxygen species (ROS) which are involved in re- moved until the day before IATF, which indicates the productive functions such as follicular maturation, action of the gonadotropin hormones (FSH and LH) ovulation, steroidogenesis, CL functions and lu-teol- that produce the development of the FD24. ysis18, therefore, smaller follicular diameters could For the evaluation of the CL, its volume was evalu- be obtained compared to studies carried out at lower ated, observing differences that were referenced by altitudes. The diameter of the CL in Criollo cows is various authors, who reported smaller CL diameters related to the diameters of the FD (evaluated on day in Criollo cows compared to other studies carried out 9), these diameters are lower than those reported in in other breeds such as Holstein, with the same rea- Brown Swiss cows which report 17.92 mm in cows sons found after comparing the diameter of in production and 11.32 mm in heifers. 32 mm eval- CL13,14,17,25. In addition, Doppler Colour Doppler was uated on day 15 post AI, while in the present study it evaluated in altitude conditions and an average of was evaluated on day 19 post AI, this difference may 20.96 % AVL was reported, which is interpreted as be due to the fact that these structures, according to the percentage of blood irrigation in relation to the the physiology of the estrous cycle, are structures in total area of the CL, with no marked difference be- regression process, as well as to racial effects of the tween those cows that were pregnant and those that 56 Perez Guerra et al. J. Selva Andina Anim. Sci. _______________________________________________________________________________________________________________ were empty respectively therefore, this percentage is Funding Source descriptive, indicating that in Creole cows at 15 days This article is not financed by any source other than post AI or post estrus reported a CL with an irrigation the research group's own resources. of approximately 20.96 %, this method measures the speed and intensity of blood flow and the number of Conflicts of interest red blood cells moving through the blood vessels per min19,26, it is also necessary to indicate that the col- The undersigned authors declare that they have no ouring of the colour Doppler is based on the principle potential personal or financial conflicts of interest that the red colouring are those blood vessels that are with other persons or organizations that could unduly approaching the transducer, while the blue colouring influence this manuscript. are the blood vessels that are moving away, all this at the time of the ultrasound examination25,27, compared Acknowledgments to the results, no differences between pregnant and non-pregnant cows could be reported, because the To the technical and administrative staff of the Agri- day of evaluation (19 days post AI) coincides with cultural Experiment Station ILLPA. the CL regression of those cows that could not get pregnant and in this process it has been studied that before the secretion of Prostaglandin F2α occurs Ethical considerations there is a sudden increase in blood supply11,25, which The authors declare that the study presented has been could be taken as a false positive (diagnosing a preg- carried out in accordance with the Code of Ethics nant cow as non-pregnant), as well as mentioning conducted in accordance with the Code of Ethics for that the assessment of blood flow by Doppler ultra- Animal Experiments for animal experiments, as re- sound alone was insufficient for diagnosis and would flected in the regulations as reflected in the regula- have to be accompanied by assessment of progester- tions described in the web page: http://ec.eu- one concentrations28. Finally, the pregnancy rate ob- ropa.eu/environment/chemicals/lab_animals/legisl tained after ultrasonographic evaluation on day 30 ation_en.htm post AI was 6 cows out of 15 that were synchronised which would represent 40%. Authors' contribution to the article Colour Doppler ultrasonography in Criollo cows. The ultrasonographic characteristics B mode before Pérez Durand Manuel Guido, Perez Guerra Uri AI for FD diameter were lower, compared to other Harold, Luque Mamani Natalio, Condori Apaza Ra- breeds, similarly the diameter and volume of the CL fael, Escobedo Arizaca Ángel, preparation and exe- was lower while AVL of 20.96 % evaluated on day cution. Perez Guerra Uri Harold, Manrique Quispe Yan Pierr, Condori Apaza Rafael, Urviola Sánchez 19 post AI. However, the study aims to determine the Jesús Martin, methodology development. Pérez Du- morphometry of ovarian structures and uterine horns rand Manuel Guido, Urviola Sánchez Jesús Martin, in Criollo cows. Finally, the cows subjected to SC achieved a pregnancy rate of 40 %. 57 Vol. 10 No 1 2023 B mode and Doppler ultrasonographic features of the dominant follicle and corpus luteum ______________________________________________________________________________________________________________ Escobedo Arizaca Ángel, conception and design. Pé- versidad Nacional Agraria La Molina; 2016 [ci- rez Durand Manuel Guido, Perez Guerra Uri Ha- tado 26 de octubre de 2022]. Recuperado a partir rold, Mamani Cato Ruben, Manrique Quispe Yan de: https://repositorio.concytec.gob.pe/handle/20. Pierr, article editing. Pérez Durand Manuel Guido, 500.12390/2029 Luque Mamani Natalio, Mamani Cato Ruben, study 6. Gonella Diaza ÁM, Atuesta Bustos JE, Bernal supervision. Ulloa SM, Chacón Jaramillo L. Overview of the production of bovine embryos in vitro. Rev Inves- Research limitations tig Agrar Ambient 2013;4(1):65-80. 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Anim Reprod 2013;10(3):215-22. Editor's Note: Journal of the Selva Andina Animal Science (JSAAS). All statements expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated or- ganizations, or those of the publisher, editors and reviewers. Any product that may be eval- uated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. 60