Journal of Equine Veterinary Science
Volume 28, Issue 11 , Pages 691-702 , November 2008

Early Embryonic Loss in the Mare

  • Dirk K. Vanderwall, DVM, PhD, Diplomate ACT

      Affiliations

    • Corresponding Author InformationReprint requests: Dirk K. Vanderwall, Northwest Equine Reproduction Laboratory, Department of Animal and Veterinary Science and Center for Reproductive Biology, University of Idaho, Moscow, ID 83844.

References 

  1. Woods GL, Baker CB, Baldwin JL, Ball BA, Bilinski J, Cooper WL, et al. Early pregnancy loss in brood mares. J Reprod Fertil. 1987;35(Suppl):455–459
  2. Vanderwall DK, Peyrot LM, Weber JA, Woods GL. Reproductive efficiency of the aged mare. Proceedings Annual Meeting Society of Theriogenology. 1989;153–156
  3. Carnevale EM, Ginther OJ. Relationships of age to uterine function and reproductive efficiency in mares. Theriogenology. 1992;37:1101–1115
  4. Hemberg E, Lundeheim N, Einarsson S. Reproductive performance of thoroughbred mares in Sweden. Reprod Dom Anim. 2004;39:81–85
  5. Carnevale EM, Coutinho da Silva MA, Panzani D, Stokes JE, Squires EL. Factors affecting the success of oocyte transfer in a clinical program for subfertile mares. Theriogenology. 2005;64:519–527
  6. Allen WR, Brown L, Wright M, Wilsher S. Reproductive efficiency of Flatrace and National Hunt Thoroughbred mares and stallions in England. Equine Vet J. 2007;39:438–445
  7. Ball BA, Little TV, Hillman RB, Woods GL. Pregnancy rates at days 2 and 14 and estimated embryonic loss rates prior to day 14 in normal and subfertile mares. Theriogenology. 1986;26:611–619
  8. Woods GL, Weber JA, Vanderwall DK, Freeman DA. Selective oviductal transport and fertilization rate of equine embryos. Proceedings AAEP. 1991;37:197–201
  9. Brinsko SP, Ball BA, Miller PG, Thomas PGA, Ellington JE. In vitro development of day 2 embryos obtained from young, fertile mares and aged, subfertile mares. J Reprod Fertil. 1994;102:371–378
  10. Carnevale EM, Griffin PG, Ginther OJ. Age-associated subfertility before entry of embryos into the uterus of mares. Equine Vet J. 1993;15(Suppl):31–35
  11. Woods GL, Hillman RB, Schlafer DH. Recovery and evaluation of embryos from normal and infertile mares. Cornell Vet. 1986;76:386–394
  12. Vogelsang SG, Vogelsang MM. Influence of donor parity and age on the success of commercial equine embryo transfer. Equine Vet J. 1989;8(Suppl):71–72
  13. Davies Morel MCG, Newcombe JR, Swindlehurst JC. The effect of age on multiple ovulation rates, multiple pregnancy rates and embryonic vesicle diameter in the mare. Theriogenology. 2005;63:2482–2493
  14. Ball BA, Little TV, Weber JA, Woods GL. Survival of day-4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares. J Reprod Fertil. 1989;85:187–194
  15. Ball BA, Woods GL. Embryonic loss and early pregnancy loss in the mare. Comp Cont Educ Pract Vet. 1987;9:459–470
  16. Ball BA. Embryonic loss in mares: Incidence, possible causes and diagnostic considerations. Vet Clin N Am: Equine Pract. 1988;4:263–290
  17. Squires EL, Barnes CK, Rowley HS, McKinnon AO, Pickett BW, Shideler RK. Effect of uterine fluid and volume of extender on fertility. Proceedings AAEP. 1989;35:25–30
  18. Troedsson MHT, Alghamdi A, Laschkewitsch T, Xue J-L. Sperm motility in altered in uterine secretions from mares with postbreeding endometritis. Proceedings AAEP. 1998;44:66–67
  19. Freeman DA, Weber JA, Geary RT, Woods GL. Time of embryo transport through the mare oviduct. Theriogenology. 1991;36:823–830
  20. Oxender WD, Noden PA, Bolenbaugh DL, Hafs HD. Control of estrus with prostaglandin F2a in mares: minimal effective dose and stage of estrous cycle. Am J Vet Res. 1975;36:1145–1147
  21. Adams GP, Kastelic JP, Bergfelt DR, Ginther OJ. Effect of uterine inflammation and ultrasonically detected uterine pathology on fertility in the mare. J Reprod Fertil. 1987;35(Suppl):445–454
  22. Newcombe JR. The effect of the incidence and depth of intra-uterine fluid in early dioestrus on pregnancy rate in mares. (abstr). Pferdeheilkunde. 1997;13:545
  23. Ball BA, Hillman RB, Woods GL. Survival of equine embryos transferred to normal and subfertile mares. Theriogenology. 1987;28:167–174
  24. Kenney RM. Cyclic and pathologic changes of the mare endometrium as detected by biopsy, with a note on early embryonic death. J Am Vet Med Assoc. 1978;172:241–262
  25. Gordon LR, Sartin EM. Endometrial biopsy as an aid to diagnosis and prognosis in equine infertility. J Equine Med Surg. 1978;2:328–336
  26. Doig PA, McKnight JD, Miller RB. The use of endometrial biopsy in the infertile mare. Can Vet J. 1981;22:72–76
  27. Stanton MB, Steiner JV, Pugh DG. Endometrial cysts in the mare. J Equine Vet Sci. 2004;24:14–19
  28. McKinnon AO, Squires EL, Voss JL. Ultrasonic evaluation of the mare's reproductive tract - part II. Comp Cont Educ Pract Vet. 1987;9:472–480
  29. McDowell KJ, Sharp DC, Grubaugh W, Thatcher WW, Wilcox CJ. Restricted conceptus mobility results in failure of pregnancy maintenance in mares. Biol Reprod. 1988;39:340–348
  30. Ginther OJ. The nature of embryo reduction in mares with twin conceptuses: Deprivation hypothesis. Am J Vet Res. 1989;50:45–53
  31. Chevalier-Clement F. Pregnancy loss in the mare. Anim Reprod Sci. 1989;20:231–244
  32. Tannus RJ, Thun R. Influence of endometrial cysts on conception rate of mares. Zentralbl Veterinarmed A. 1995;42:275–283
  33. Eilts BE, Scholl DT, Paccamonti DL, Causey R, Klimczak JC, Corley JR. Prevalence of endometrial cysts and their effect on fertility. Mono Biol Reprod. 1995;1:527–532
  34. Griffin RL, Bennett SD. Nd:YAG laser photoablation of endometrial cysts: a review of 55 cases (2000-2001). Proceedings AAEP. 2002;48:58–60
  35. Allen WR. Luteal deficiency and embryo mortality in the mare. Reprod Dom Anim. 2001;36:121–131
  36. Pycock JF, Newcombe JR. The effect of the gonadotrophin-releasing hormone analog, buserelin, administered in diestrus on pregnancy rates and pregnancy failure in mares. Theriogenology. 1996;46:1097–1101
  37. Newcombe JR, Martinez TA, Peters AR. The effect of the gonadotropin-releasing hormone analog, buserelin, on pregnancy rates in horse and pony mares. Theriogenology. 2001;55:1619–1631
  38. Ginther OJ. Embryonic loss in mares: incidence, time of occurrence, and hormonal involvement. Theriogenology. 1985;23:77–89
  39. Darenius K, Fredriksson G, Kindahl H. Allyl trenbolone and flunixin meglumine treatment of mares with repeated embryonic loss. Equine Vet J. 1989;8(Suppl):35–39
  40. Newcombe JR. Spontaneous oestrous behaviour during pregnancy associated with luteal regression, ovulation and birth of a live foal in a part Thoroughbred mare. Equine Vet Educ/AE. 2000;2:111–114
  41. Vanderwall DK, Squires EL, Brinsko SP, McCue PM. Diagnosis and management of abnormal embryonic development characterized by formation of an embryonic vesicle without an embryo in mares. J Am Vet Med Assoc. 2000;217:58–63
  42. Carnevale EM, Ginther OJ. Defective oocytes as a cause of subfertility in old mares. Mono Biol Reprod. 1995;1:209–214
  43. Carnevale EM, Uson M, Bozzola JJ, King SS, Schmitt SJ, Gates HD. Comparison of oocytes from young and old mares with light and electron microscopy. (abstr). Theriogenology. 1999;51:299
  44. Rambags BPB, van Boxtel DCJ, Tharasanit T, Lenstra JA, Colenbrander B, Stout TAE. Oocyte mitochondrial degeneration during reproductive ageing in the mare. Havemeyer Foundation Monograph Series. 2006;18:25–27
  45. van Niekerk FE, Van Niekerk CH. The effect of dietary protein on reproduction in the mare. VI. Serum progestagen concentrations during pregnancy. J S Afr Vet Assoc. 1998;69:143–149
  46. Woods GL, Baker CB, Bilinski J, Hillman RB, Mank EC, Sluijter F. A field study on early pregnancy loss in Standardbred and Thoroughbred mares. J Equine Vet Sci. 1985;5:264–267
  47. Newcombe JR, Wilson MC. Age, body weight, and pregnancy loss. J Equine Vet Sci. 2005;25:188–194
  48. Blanchard TL, Thompson JA, Brinsko SP, Stich KL, Varner DD, Rigby SL. Mating mares on foal heat: a five-year retrospective study. Proceedings AAEP. 2004;50:525–530
  49. Bell RJ, Bristol F. Fertility and pregnancy loss after delay of foal oestrus with progesterone and oestradiol-17β. J Reprod Fertil. 1987;35(Suppl):667–668
  50. Meyers PJ, Bonnett BN, Mckee SL. Quantifying the occurrence of early embryonic mortality on three equine breeding farms. Can Vet J. 1991;32:665–672
  51. Morris LH, Allen WR. Reproductive efficiency of intensively managed Thoroughbred mares in Newmarket. Equine Vet J. 2002;34:51–60
  52. Woods J, Bergfelt DR, Ginther OJ. Effects of time of insemination relative to ovulation on pregnancy rate and embryonic loss rate in mares. Equine Vet J. 1990;22:410–415
  53. Koskinen E, Lindeberg H, Kuntsi H, Ruotsalainen L, Katila T. Fertility of mares after postovulatory insemination. Zentralbl Veterinarmed A. 1990;37:77–80
  54. Barbacini S, Gulden P, Marchi V, Zavaglia G. Incidence of embryo loss in mares inseminated before or after ovulation. Equine Vet Educ. 1999;11:251–254
  55. Ginther OJ. Fixation and orientation of the early equine conceptus. Theriogenology. 1983;19:613–623
  56. Jobert ML, LeBlanc MM, Pierce SW. Pregnancy loss rate in equine uterine body pregnancies. Equine Vet Educ/AE. 2005;7:207–210
  57. Lear TL, Lundquist J, Zent WW, Fishback WD, Clark A. Three autosomal chromosome translocations associated with repeated early embryonic loss (REEL) in the domestic horse (Equus caballus). Cytogenet Genome Res. 2008;120:117–122
  58. Van Niekerk CH, Morgenthal JC. Fetal loss and the effect of stress on plasma progestagen levels in pregnant Thoroughbred mares. J Reprod Fertil. 1982;32(Suppl):453–457
  59. Baucus KL, Ralston SL, Nockels CF, McKinnon AO, Squires EL. Effects of transportation on early embryonic death in mares. J Anim Sci. 1990;68:345–351
  60. Daels PF, Starr M, Kindahl H, Fredriksson G, Hughes JP, Stabenfeldt GH. Effect of Salmonella typhimurium endotoxin on PGF-2α release and fetal death in the mare. J Reprod Fertil. 1987;35(Suppl):485–492
  61. Daels PF, Stabenfeldt GH, Hughes JP, Odensvik K, Kindahl H. Effects of flunixin meglumine on endotoxin-induced prostaglandin F2 alpha secretion during early pregnancy in mares. Am J Vet Res. 1991;52:276–281
  62. Daels PF, Stabenfeldt GH, Hughes JP, Odensvik K, Kindahl H. Evaluation of progesterone deficiency as a cause of fetal death in mares with experimentally induced endotoxemia. Am J Vet Res. 1991;52:282–288
  63. Henneke DR, Potter GD, Kreider JL. Body condition during pregnancy and lactation and reproductive efficiency of mares. Theriogenology. 1984;21:897–909
  64. van Niekerk FE, Van Niekerk CH. The effect of dietary protein on reproduction in the mare. VII. Embryonic development, early embryonic death, foetal losses and their relationship with serum progestagen. J S Afr Vet Assoc. 1998;69:150–155
  65. Christiansen DL, Hopper R, Hill NS, Ryan PL. Early embryonic death in mares grazing endophyte infected fescue. (abstr). Proceedings Annual Meeting Soc for Theriogenology. 2003;43
  66. Brendemuehl JP, Boosinger TR, Pugh DG, Shelby RA. Influence of endophyte-infected tall fescue on cyclicity, pregnancy rate and early embryonic loss in the mare. Theriogenology. 1994;42:489–500
  67. Youngblood RC, Filipov NM, Rude BJ, Christiansen DL, Hopper RM, Gerard PD, et al. Effects of short-term early gestational exposure to endophyte-infected tall fescue diets on plasma 3,4-dihydroxyphenyl acetic acid and fetal development in mares. J Anim Sci. 2004;82:2919–2929
  68. Arns MJ, Pruitt JA, Sharp C. Influence of endophyte-infected tall fescue seed consumption on the establishment and maintenance of pregnancy in mares. Prof Anim Sci. 1997;13:118–123
  69. Webb BA, Barney WE, Dahlman DL, DeBorde SN, Weer C, Williams NM, et al. Eastern tent caterpillars (Malacosoma americanum) cause mare reproductive loss syndrome. J Insect Physiol. 2004;50:185–193
  70. Hansen PJ. To be or not to be-Determinants of embryonic survival following heat shock. Theriogenology. 2007;68(Suppl 1):S40–S48
  71. Hearn P, Bonnet B, Samper J. Factors affecting pregnancy and pregnancy loss on one Thoroughbred farm. Proceedings AAEP. 1993;39:161–163
  72. Voss JL, Pickett BW, Back DG, Burwash LD. Effect of rectal palpation on pregnancy rate of nonlactating, normally cycling mares. J Anim Sci. 1975;41:829–834
  73. Irwin CFP. Early pregnancy testing and its relationship to abortion. J Reprod Fertil. 1975;23(Suppl):485–489
  74. Vogelsang MM, Vogelsang SG, Lindsey BR, Massey JM. Reproductive performance in mares subjected to examination by diagnostic ultrasound. Theriogenology. 1989;32:95–103
  75. Platt H. Aetiological aspects of abortion in the Thoroughbred mare. J Comp Pathol. 1973;83:199–205
  76. Blanchard TL, Varner DD, Fernandez M, Buoen L, Zhang TQ, Womack JE, et al. Stallion karyotype variability and lack of association with abortion: A case report. Theriogenology. 1994;41:777–784
  77. England GCW, Keane M. The effect of x-radiation upon the quality and fertility of stallion semen. Theriogenology. 1996;46:173–180
  78. Vanderwall DK, Woods GL, Roser JF, Schlafer DH, Sellon DC, Tester DF, et al. Equine cloning: applications and outcomes. Reprod Fertil Dev. 2006;18:91–98
  79. McKinnon AO, Lacham-Kaplan O, Trounson AO. Pregnancies produced from fertile and infertile stallions by intracytoplasmic sperm injection (ICSI) of single frozen-thawed spermatozoa into in vivo matured mare oocytes. J Reprod Fertil. 2000;56(Suppl):513–517
  80. Hinrichs K, Choi YH, Walckenaer BE, Varner DD, Hartman DL. In vitro−produced equine embryos: Production of foals after transfer, assessment by differential staining and effect of medium calcium concentrations during culture. Theriogenology. 2007;68:521–529
  81. Chevalier F, Palmer E. Ultrasonic echography in the mare. J Reprod Fertil. 1982;32(Suppl):423–430
  82. Ginther OJ, Bergfelt DR, Leith GS, Scraba ST. Embryonic loss in mares: incidence and ultrasonic morphology. Theriogenology. 1985;24:73–86
  83. Bergfelt DR, Woods JA, Ginther OJ. Role of the embryonic vesicle and progesterone in embryonic loss in mares. J Reprod Fertil. 1992;95:339–347
  84. Papa FO, Lopes MD, Alvarenga MA, Meira C, Luvizotto MCR, Langoni H, et al. Early embryonic death in mares: clinical and hormonal aspects. Braz J Vet Res Anim Sci. 1998;35:170–173
  85. Ginther OJ. Embryonic loss in mares: nature of loss after experimental induction by ovariectomy or prostaglandin F2a. Theriogenology. 1985;24:87–98
  86. Darenius K, Kindahl H, Madej A. Clinical and endocrine studies in mares with known history of repeated conceptus losses. Theriogenology. 1988;29:1215–1232
  87. McKinnon AO, Tarrida Del Marmol Figueroa S, Nobelius AM, Hyland JH, Vasey JR. Failure of hydroxyprogesterone caproate to maintain pregnancy in ovariectomized mares. Equine Vet J. 1993;25:158–160
  88. McKinnon AO, Lescun TB, Walker JH, Vasey JR, Allen WR. The inability of some synthetic progestagens to maintain pregnancy in the mare. Equine Vet J. 2000;32:83–85
  89. Vanderwall DK, Marquardt JL, Woods GL. Use of a compounded long-acting progesterone formulation for equine pregnancy maintenance. J Equine Vet Sci. 2007;27:62–66
  90. Simpson DJ, Greenwood RES, Ricketts SW, Rossdale PD, Sanderson M, Allen WR. Use of ultrasound echography for early diagnosis of single and twin pregnancy in the mare. J Reprod Fertil. 1982;32(Suppl):431–439
  91. Villahoz MD, Squires EL, Voss JL, Shideler RK. Some observations on early embryonic death in mares. Theriogenology. 1985;23:915–924
  92. Forde D, Keenan L, Wade J, O'Connor M, Roche JF. Reproductive wastage in the mare and its relationship to progesterone in early pregnancy. J Reprod Fertil. 1987;35(Suppl):493–495
  93. Villahoz MD. Increased pregnancy rates in post-partum mares and early embryonic death. Proceedings Annual Meeting Society of Theriogenology. 1989;210–221
  94. Irvine CHG, Sutton P, Turner JE, Mennick PE. Changes in plasma progesterone concentrations from Days 17 to 42 of gestation in mares maintaining or losing pregnancy. Equine Vet J. 1990;22:104–106
  95. Lowis TC, Hyland JH. Analysis of post-partum fertility in mares on a thoroughbred stud in southern Victoria. Aust Vet J. 1991;68:304–306
  96. Bruck I, Anderson GA, Hyland JH. Reproductive performance of thoroughbred mares on six commercial stud farms. Aust Vet J. 1993;70:299–303
  97. Newcombe JR. Observations on early pregnancy diagnosis and early embryonic loss in the mare. Irish Vet J. 1997;50:534–536
  98. Carnevale EM, Ramirez RJ, Squires EL, Alvarenga MA, Vanderwall DK, McCue PM. Factors affecting pregnancy rates and early embryonic death after equine embryo transfer. Theriogenology. 2000;54:965–979

 Refereed

PII: S0737-0806(08)00331-6

doi: 10.1016/j.jevs.2008.10.001

Journal of Equine Veterinary Science
Volume 28, Issue 11 , Pages 691-702 , November 2008

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