Embryonic mortality in sheep: a review
Embryonic mortality in sheep: a review
Despite extensive research on the reproductive health of domestic animals, embryonic mortality continues to be a problemthat brings about significant losses for both commercial breeding and scientific research. This review paper discusses the genetic andenvironmental factors that affect embryo mortality rates in sheep along with the different techniques developed to overcome this issue.Additionally, one of the objectives of this study is to emphasize the importance of the use of time-lapse cinematography and colorDoppler ultrasonography as quick and reliable methods for early detection of pregnancy and embryonic death.
___
- 1. de Kretser DM, Loveland KL, Meinhardt A, Simorangkir D,
Wreford N. Spermatogenesis. Human Reproduction 1998; 13
(1): 1-8. doi: 10.1093/humrep/13.suppl_1.1
- 2. Schuetz WA. Local control mechanisms during oogenesis and
folliculogenesis. In: Browder LW (editor). Developmental
Biology. A Comprehensive Synthesis. Volume 1, 1st Ed. New
York, NY, USA: Plenum Press; 1985. pp. 3-73. doi: 10.1007/978-
1-4615-6814-8
- 3. Dai K, Gillies CB, Dollin AE. Synaptonemal complex analysis of
domestic sheep (Ovis aries) with Robertsonian translocations.
II. Trivalent and pairing abnormalities in Massey I and Massey
II heterozygotes. Genome 1994; 37 (4): 679-689. doi: 10.1139/
g94-096
- 4. Long SE, Williams CV. Frequency of chromosomal
abnormalities in early embryos of the domestic sheep (Ovis
aries). Reproduction 1980; 58 (1): 197-201. doi: 10.1530/
jrf.0.0580197
- 5. Murray JD, Boland MP, Moran C, Sutton R, Nancarrow CD et
al. Occurrence of haploid and haploid/ diploid mosaic embryos
in untreated and androstenedione-immune Australian Merino
sheep. Journal of Reproduction and Fertility 1985; 74 (2): 551-
555. doi: 10.1530/jrf.0.0740551
- 6. Perkel KJ, Tscherner A, Merrill C, Lamarre J, Madan P. The
ART of selecting the best embryo: a review of early embryonic
mortality and bovine embryo viability assessment methods.
Molecular Reproduction & Development 2015; 82 (11): 822-
838. doi: 10.1002/mrd.22525
- 7. Bolet G. Timing and extent of embryonic mortality in pigs,
sheep and goats: genetic variability. In: Sreenan JM, Diskin
MG (editors). Embryonic Mortality in Farm Animals. Current
Topics in Veterinary Medicine and Animal Science, Vol 34.
Dordrecht, the Netherlands: Springer; 1986. pp. 12-43. doi:
10.1007/978-94-009-5038-2
- 8. Dupont C, Segars J, DeCherney A, Bavister BD, Armant DR et
al. Incidence of chromosomal mosaicism in morphologically
normal non-human primate preimplantation embryos.
Fertility and Sterility 2010; 93 (8): 2545-2550. doi: 10.1016/j.
fertnstert.2009.06.040
- 9. Coppola G, Alexander B, Di Berardino D, St John E, Basrur
PK et al. Use of cross-species in-situ hybridization (ZOOFISH)
to assess chromosome abnormalities in day-6 in-vivoor
in-vitro-produced sheep embryos. Chromosome Research
2007; 15 (3): 399-408. doi: 10.1007/s10577-007-1125-2
- 10. Abdel-Mageed II, Abd El-Gawad MH. Does parity and
nutrition in early pregnancy affect viability of embryos in both
Rahmani and Barki Egyptian sheep? Asian Journal of Animal
and Veterinary Advances 2015; 10 (1): 25-34. doi: 10.3923/
ajava.2015.25.34
- 11. Grazul-Bilska AT, Borowczyk E, Bilski JJ, Reynolds LP, Redmer
DA et al. Overfeeding and underfeeding have detrimental
effects on oocyte quality measured by in vitro fertilization
and early embryonic development in sheep. Domestic
Animal Endocrinology 2012; 43 (4): 289-298. doi: 10.1016/j.
domaniend.2012.05.001
- 12. Viñoles C, Glover KMM, Paganoni BL, Milton JTB, Martin
GB. Embryo losses in sheep during short-term nutritional
supplementation. Reproduction, Fertility and Development
2012; 24 (8): 1040-1047. doi: 10.1071/RD11281
- 13. Small E. 38. Lupins – benefit and harm potentials. Biodiversity
2012; 13 (1): 54-64. doi: 10.1080/14888386.2012.658327
- 14. Santolaria P, Yániz J, Fantova E, Vicente-Fiel S, Palacín I. Climate
factors affecting fertility after cervical insemination during the
first months of the breeding season in Rasa Aragonesa ewes.
International Journal of Biometeorology 2014; 58 (7): 1651-
1655. doi: 10.1007/s00484-013-0770-8
- 15. Goff AK. Embryonic signals and survival. Reproduction in
Domestic Animals 2002; 37 (3): 133-139. doi: 10.1046/j.1439-
0531.2002.00344.x
- 16. Diskin MG, Morris DG. Embryonic and early foetal losses in
cattle and other ruminants. Reproduction in Domestic Animals
2008; 43 (2): 260-267. doi: 10.1111/j.1439-0531.2008.01171.x
- 17. Ziebe S, Petersen K, Lindenberg S, Andersen AG, Gabrielsen
A et al. Embryo morphology or cleavage stage: how to select
the best embryos for transfer after in-vitro fertilization.
Human Reproduction 1997; 12 (7): 1545-1549. doi: 10.1093/
humrep/12.7.1545
- 18. Sugimura S, Akai T, Hashiyada Y, Somfai T, Inaba Y et al.
Promising system for selecting healthy in vitro–fertilized
embryos in cattle. PLoS One 2012; 7 (5): e36627. doi: 10.1371/
journal.pone.0036627
- 19. Fenwick J, Platteau P, Murdoch AP, Herbert M. Time from
insemination to first cleavage predicts developmental
competence of human preimplantation embryos in vitro.
Human Reproduction 2002; 17 (2): 407-412. doi: 10.1093/
humrep/17.2.407
- 20. Magli CM, Gianaroli L, Ferraretti AP, Lappi M, Ruberti A et al.
Embryo morphology and development are dependent on the
chromosomal complement. Fertility and Sterility 2007; 87 (3):
534-541. doi: 10.1016/j.fertnstert.2006.07.1512
- 21. Gardner DK, Leese HJ. Assessment of embryo viability prior
to transfer by the noninvasive measurement of glucose uptake.
Journal of Experimental Zoology 1987; 242 (1): 103-105. doi:
10.1002/jez.1402420115
- 22. Thompson JG, Simpson AC, Pugh PA, Tervit HR. Requirement
for glucose during in vitro culture of sheep preimplantation
embryos. Molecular Reproduction and Development 1992; 31
(4): 253-257. doi: 10.1002/mrd.1080310405
- 23. Sharkey S, Callan RJ, Mortimer R, Kimberling C. Reproductive
techniques in sheep. Veterinary Clinics of North America:
Food Animal Practice 2001; 17 (2): 435-455. doi: 10.1016/
S0749-0720(15)30037-2
- 24. Green WW, Winters LM. Prenatal development of the sheep.
Minnesota Technical Bulletin 1945; 169: 3-36.
- 25. Barbagianni MS, Ionnidi KI, Vasileiou NGC, Mavrogianni VS,
Orfanou DC et al. Ultrasonographic examination of pregnant
ewes: from early diagnosis of pregnancy to early prediction
of dystocia. Small Ruminant Research 2017; 152: 41-55. doi:
10.1016/j.smallrumres.2016.12.008
- 26. Moraes EPBX, Freitas Neto LM, Aguiar Filho CR, Bezerra
FQG, Santos MHB et al. Mortality determination and gender
identification of conceptuses in pregnancies of Santa Ines ovine
by ultrasound. South African Society for Animal Science 2009;
39 (4): 307-312.
- 27. Yotov SA. Ultrasound diagnostics of late embryonic and foetal
death in three sheep breeds. Journal of Veterinary Advances
2012; 2 (3): 120-125.
- 28. Schrick FN, Inskeep EK. Determination of early pregnancy
in ewes utilizing transrectal ultrasonography. Theriogenology
1993; 40 (2): 295-306. doi: 10.1016/0093-691X(93)90267-9
- 29. Dixon AB, Knights M, Winkler JL, Marsh DJ, Pate JL et al.
Patterns of late embryonic and fetal mortality and association
with several factors in sheep. Journal of Animal Science 2007;
85 (5): 1274-1284. doi: 10.2527/jas.2006-129
- 30. Petridis IG, Barbagianni MS, Ionnidi KS, Samaras E, Fthenakis
GC et al. Doppler ultrasonographic examination in sheep.
Small Ruminant Research 2017; 152: 22-32. doi: 10.1016/j.
smallrumres.2016.12.015
- 31. Arashiro EKN, Ungerfeld R, Clariget RP, Pinto PHN, Balaro
MFA et al. Early pregnancy diagnosis in ewes by subjective
assessment of luteal vascularisation using colour Doppler
ultrasonography. Theriogenology 2018; 106: 247-252. doi:
10.1016/j.theriogenology.2017.10.029
- 32. McCracken JA, Custer EE, Lamsa JC. Luteolysis: A
neuroendocrine-mediated event. Physiological Reviews 1999;
79 (2): 263-323. doi: 10.1152/physrev.1999.79.2.263
- 33. Cosentino IO, Balaro MFA, Arashiro EKN, Santos JDR,
da Silva Carvalho AB et al. Hormonal protocols for early
resynchronization of ovulation in ewes: The use of progestagens,
eCG, and inclusion of early pregnancy diagnosis with color
Doppler ultrasound. Theriogenology 2019; 133: 113-118. doi:
10.1016/j.theriogenology.2019.04.033
- 34. Otsuka F, McTavish K, Shimasaki S. Integral role of GDF-9
and BMP-15 in ovarian function. Molecular Reproduction and
Development 2011; 78 (1): 9-21. doi: 10.1002/mrd.21265.
- 35. McNatty KP, Galloway SM, Wilson T, Smith P, Hudson NL et
al. Physiological effects of major genes affecting ovulation rate
in sheep. Genetics Selection Evolution 2005; 37 (1): 25-38. doi:
10.1051/gse:2004029
- 36. Ptak GE, D’Agostino A, Toschi P, Fidanza A, Zacchini F et al.
Post-implantation mortality of in vitro produced embryos is
associated with DNA methyltransferase 1 dysfunction in sheep
placenta. Human Reproduction 2013; 28 (2): 298-305. doi:
10.1093/humrep/des397
- 37. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA
methyltransferase gene results in embryonic lethality. Cell
1992; 69 (6): 915-926. doi: 10.1016/0092-8674(92)90611-F
- 38. Mishra A, Reddy IJ, Gupta PSP, Mondal S. Developmental
regulation and modulation of apoptotic genes expression in
sheep oocytes and embryos cultured in vitro with L-carnitine.
Reproduction in Domestic Animals 2016; 51 (6): 1020-
1029. doi: 10.1111/rda.12789
- 39. Bogliolo L, Ariu F, Leoni G, Uccheddu S, Bebbere D. High
hydrostatic pressure treatment improves the quality of in
vitro-produced ovine blastocysts. Reproduction, Fertility and
Development 2011; 23 (6): 809-817. doi: 10.1071/RD11023
- 40. Waldenström U, Engström A, Hellberg D, Nilsson S. Lowoxygen
compared with high-oxygen atmosphere in blastocyst
culture, a prospective randomized study. Fertility and Sterility
2009; 91 (6): 2461-2465. doi: 10.1016/j.fertnstert.2008.03.051
- 41. Abecia J, Forcada F, Vázquez M, Muiño-Blanco T, Cebrián-
Pérez JA et al. Role of melatonin on embryo viability in sheep.
Reproduction, Fertility and Development 2018; 31 (1): 82-92.
doi: 10.1071/RD18308
- 42. Mezza-Herrera CA, Ross TT, Hallford DM, Hawkins DE,
Gonzales-Bulnes A. High periconceptional protein intake
modifies uterine and embryonic relationships increasing early
pregnancy losses and embryo growth retardation in sheep.
Reproduction in Domestic Animals 2010; 45 (4): 723-728. doi:
10.1111/j.1439-0531.2009.01341.x
- 43. Abecia JA, Forcada F, Palacín I, Sánchez-Prieto L, Sosa C et al.
Undernutrition affects embryo quality of superovulated ewes.
Zygote 2015; 23 (1): 116-124. doi: 10.1017/S096719941300035X