Ultrasound and endocrine findings that help to assess the risk of late embryo/early foetal loss by non-infectious cause in dairy cattle

Reproduction in Domestic Animals

Volumn 45, Issue SUPPL. 3, 2010, Pages 15-24

  Lopez Gatius F ^a   Garcia Ispierto I ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE;

ANIMAL; ANIMAL DISEASE; CATTLE; CATTLE DISEASE; COLOR ULTRASOUND FLOWMETRY; CORPUS LUTEUM; ECHOGRAPHY; EMBRYO DEATH; FEMALE; FETUS DEATH; FETUS ECHOGRAPHY; GESTATIONAL AGE; HUMAN; IMMUNE SYSTEM; MULTIPLE PREGNANCY; NIDATION; OVARY; PHYSIOLOGY; PREGNANCY; REPRODUCTION; REVIEW; VETERINARY ABORTION;

ABORTION, VETERINARY; ANIMALS; CATTLE; CATTLE DISEASES; CORPUS LUTEUM; EMBRYO IMPLANTATION; EMBRYO LOSS; FEMALE; FETAL DEATH; GESTATIONAL AGE; HORMONES; HUMANS; IMMUNE SYSTEM; OVARY; PLACENTATION; PREGNANCY; PREGNANCY, MULTIPLE; ULTRASONOGRAPHY, DOPPLER, COLOR; ULTRASONOGRAPHY, PRENATAL;

BOS;

EID: 77955235043     PISSN: 09366768     EISSN: 14390531     Source Type: Journal    
DOI: 10.1111/j.1439-0531.2010.01620.x     Document Type: Review

References (108)

1. Alnimer MA, Lubbadeh WF. Effect of progesterone (P4) intravaginal device (CIDR) to reduce embryonic loss and to synchronize return to oestrus of previously timed inseminated lactating dairy cows. Anim Reprod Sci 2008, 107:36-47.
2. Anderson GB. Methods for producing twins in cattle. Theriogenology 1978, 9:3-16.
3. Ayad A, Sousa NM, Sulon J, Hornick JL, Watts J, López-Gatius F, Iguer-Ouada M, Beckers JF. Influence of progesterone concentrations on secretory functions of trophoblast and pituitary during the first trimester of pregnancy in dairy cattle. Theriogenology 2007, 67:1503-1511.
4. Ball PJH. Later embryo and early fetal mortality in the cow. Anim Breed Abs 1997, 65:167-175.
5. Bartolome JA, Silvestre FT, Kamimura S, Arteche ACM, Melendez P, Kelbert D, McHale J, Swift K, Archbald LF, Thatcher WW. Resynchronization of ovulation and timed insemination in lactating dairy cows I: use of the Ovsynch and Heatsynch protocols after non-pregnancy diagnosis by ultrasonography. Theriogenology 2005a, 63:1617-1627.
6. Bartolome JA, Sozzi A, McHale J, Melendez P, Arteche ACM, Silvestre FT, Kelbert D, Swift K, Archbald LF, Thatcher WW. Resynchronization of ovulation and timed insemination in lactating dairy cows, II: assigning protocols according to stages of the estrous cycle, or presence of ovarian cysts or anestrus. Theriogenology 2005b, 63:1628-1642.
7. Bartolomé JA, Sozzi A, McHale J, Swift K, Kelbert D, Archbald LF, Thatcher WW. Resynchronization of ovulation and timed insemination in lactating dairy cows III. Administration of GnRH 23 days post AI and ultrasonography for nonpregnancy diagnosis on day. Theriogenology 2005c, 63:1643-1658.
8. Bech-Sàbat G, López-Gatius F, Santolaria P, García-Ispierto I, Pabón M, Nogareda C, Yániz JL, Almería S. Progesterone supplementation during mid-gestation increases the risk of abortion in Neospora-infected dairy cows with high antibody titres. Vet Parasitol 2007, 145:164-167.
9. Bech-Sàbat G, López-Gatius F, Yániz JL, García-Ispierto I, Santolaria P, Serrano B, Sulon J, De Sousa NM, Beckers JF. Factors affecting plasma progesterone in the early fetal period in high producing dairy cows. Theriogenology 2008, 69:426-432.
10. Bech-Sàbat G, López-Gatius F, García-Ispierto I, Santolaria P, Serrano B, Nogareda C, De Sousa NM, Beckers JF, Yániz J. Pregnancy patterns during the early fetal period in high producing dairy cows treated with GnRH or progesterone. Theriogenology 2009a, 71:920-929.
11. Bech-Sàbat G, García-Ispierto I, Yániz J, López-Gatius F. Therapeutic approaches to pregnancy loss of non-infectious cause during the late embryonic/early foetal period in dairy cattle. A review. Reprod Domest Anim 2009b, 10.1111/j.1439-0531.2009.01562.x, doi
12. Beckers JF, Drion PV, Garbayo JM, Perényi Z, Zarrouk A, Sulon J, Remy B, Szenci O. Pregnancy associated glycoproteins in ruminants: inactive members of the aspartic proteinase family. Acta Vet Hung 1999, 47:461-469.
13. Bollwein H, Baumgartner U, Stolla R. Transrectal Doppler sonography of uterine blood flow in cows during pregnancy. Theriogenology 2002, 57:2053-2061.
14. Boyd JD, Hamilton WJ, Hammond J. Transuterine ("internal") migration of the ovum in sheep and other mammals. J Anat 1944, 78:5-14.
15. Brand JM, Frohn C, Cziupka K, Brockmann C, Kirchner H, Luhm J. Prolactin triggers pro-inflammatory immune responses in peripheral immune cells. Eur Cytokine Netw 2004, 15:99-104.
16. Cartmill JA, El-Zarkouny SZ, Hensley BA, Lamb GC, Stevenson JS. Stage of cycle, incidence and timing of ovulation, and pregnancy rates in dairy cattle after three timed breeding protocols. J Dairy Sci 2001a, 80:3386-3398.
17. Cartmill JA, El-Zarkouny SZ, Hensley BA, Rozell TG, Smith JF, Stevenson JS. An alternative AI breeding protocol for dairy cows exposed to elevated ambient temperatures before of after calving or both. J Dairy Sci 2001b, 84:799-806.
18. Cerbito WA, Quero FV, Balagapo CR, Miyazawa K, Sato K. Spatial distribution of progesterone in bovine uterus in relation to corpus luteum location and function. Theriogenology 1994, 41:1663-1671.
19. Recommendations for standardizing bovine reproductive terms. Cornell Vet 1972, 62:216-237.
20. Csapo AI, Pulkinnen M. Indispensability of the human corpus luteum in the maintenance of early pregnancy. Lutectomy evidence. Obstet Gynecol Surv 1978, 33:69-81.
21. Curran S, Pierson RA, Ginther OJ. Ultrasonographic appearance of the bovine conceptus from days 20 through 60. J Am Vet Med Assoc 1986, 189:1295-1302.
22. Druckmann R, Druckmann MA. Progesterone and the immunology of pregnancy. J Steroid Biochem Mol Biol 2005, 97:389-396.
23. Fricke PM, Wiltbank MC. Effect of milk production on the incidence of double ovulation in dairy cows. Theriogenology 1999, 52:1133-1143.
24. Gábor G, Tóth F, Ózsvári L, Abonyi-Tóth Zs, Sasser RG. Early detection of pregnancy and embryonic loss in dairy cattle by ELISA tests. Reprod Domest Anim 2007, 42:633-636.
25. Gábor G, Tóth F, Ózsvári L, Abonyi-Tóth Zs, Sasser RG. Factors influencing pregnancy rate and late embryonic loss in dairy cattle. Reprod Domest Anim 2008, 43:53-58.
26. Garbayo JM, Serrano B, López-Gatius F. Identification of novel pregnancy-associated glycoproteins (PAG) expressed by the peri-implantation conceptus of domestic ruminants. Anim Reprod Sci 2008, 103:120-134.
27. García-Ispierto I, López-Gatius F, Santolaria P, Yániz JL, Nogareda C, López-Béjar M, De Rensis F. Relationship between heat stress during the peri-implantation period and early fetal loss in dairy cattle. Theriogenology 2006, 65:799-807.
28. García-Ispierto I, López-Gatius F, Santolaria P, Yániz JL, Nogareda C, López-Béjar M. Factors affecting the fertility of high producing dairy herds in northeastern Spain. Theriogenology 2007a, 67:632-638.
29. García-Ispierto I, López-Gatius F, Bech-Sabat G, Santolaria P, Yániz JL, Nogareda C, De Rensis F, López-Béjar M. Climate factors affecting the fertility of high producing dairy cows in northeastern Spain. Theriogenology 2007b, 67:1379-1385.
30. García-Ispierto I, López-Gatius F, Almería S, Yániz J, Santolaria P, Serrano B, Bech-Sàbat G, Nogareda C, Sulon J, De Sousa NM, Beckers JF. Factors affecting plasma prolactin concentrations throughout gestation in high producing dairy cows. Domest Anim Endocrinol 2009, 36:57-66.
31. Gestel L, Jland MMI, Hoogland HJ, Evers JLH. Endometrial wave-like activity in non-pregnant uterus. Hum Reprod Update 2003, 9:131-138.
32. Ginther OJ. Ultrasonic Imaging and Animal Reproduction: Book 1. Fundamentals 1995, Equiservices Publishing, Cross Plains, Wisconsin
33. Ginther OJ. Ultrasonic Imaging and Animal Reproduction: Book 3. Cattle 1998, Equiservices Publishing, Cross Plains, Wisconsin
34. Ginther OJ. Ultrasonic Imaging and Animal Reproduction: Book 4. Color-Doppler ultrasonography 2007, Equiservices Publishing, Cross Plains, Wisconsin
35. Ginther OJ, Knopf L, Kastelic JP. Ovarian follicular dynamics in heifers during early pregnancy. Biol Reprod 1989, 41:247-254.
36. Ginther OJ, Kot K, Kulick LJ, Martin S, Wiltbank MC. Relationship between FSH and ovarian follicular waves during the last six months of pregnancy in cattle. J Reprod Fertil 1996, 108:271-279.
37. Graham TW, Giri SN, Daels PF, Cullor JS, Keen CL, Thurmond MC, Dellinger JD, Stabenfeldt GH, Osburn BI. Associations among prostaglandin F2Alpha, plasma zinc, copper and iron concentrations and fetal loss in cows and mares. Theriogenology 1995, 44:379-390.
38. Grimard B, Freret S, Chevallier A, Pinto A, Ponsart C, Humblot P. Genetic and environmental factors influencing first service conception rate and late embryonic/foetal mortality in low fertility dairy herds. Anim Reprod Sci 2006, 91:31-44.
39. Hanrahan JP. The inter-ovarian distribution of twin ovulations and embryo survival in bovine. Theriogenology 1983, 20:3-11.
40. Hansen PJ, Soto P, Natzke RP. Mastitis and fertility in cattle - possible involvement of inflammation or immune activation in embryonic mortality. Am J Reprod Immunol 2004, 51:294-301.
41. Hanzen CH, Drion PV, Loutrie O, Depierreux C, Christians E. Embryonic mortality. Part 1. Clinical aspects and etiological factors in the bovine species. Ann Med Vet 1999, 143:91-118.
42. Henderson J, Willson K, Jago JR, Whittingham TA. A survey of the acoustic output of diagnostic ultrasound equipment in current clinical use. Ultrasound Med Biol 1997, 21:699-705.
43. Herzog K, Bollwein H. Application of Doppler ultrasonography in cattle reproduction. Reprod Domest Anim 2007, 42(Suppl. 2):51-58.
44. Herzog K, Brockhnan-Lüdemann M, Kaske M, Beindorff N, Paul V, Niemann H, Bollwein H. Luteal blood flow is a more appropriate indicator for luteal function during the bovine estrous cycle than luteal size. Theriogenology 2010, 73:691-697.
45. Honnens A, Voss C, Herzog K, Niemann H, Rath D, Bollwein H. Uterine blood flow during the first 3 weeks of pregnancy in dairy cows. Theriogenology 2008, 70:1048-1056.
46. Horder MM, Barnett SB, Vella GJ, Edwards MJ, Wood AK. Ultrasound-induced temperature increase in guinea-pig fetal brain in utero: third trimester gestation. Ultrasound Med Biol 1998, 24:1501-1510.
47. Hughes EA, Davies DAR. Practical uses of ultrasound in early pregnancy in cattle. Vet Rec 1989, 124:456-458.
48. Humblot P. Use of pregnancy specific proteins and progesterone assays to monitor pregnancy and determine the timing, frequencies and sources of embryonic mortality in ruminants. Theriogenology 2001, 56:1417-1433.
49. Inskeep EK, Dailey RA. Embryonic death in cattle. Vet Clin N Am-Food A 2005, 21:437-461.
50. Jirasek TE, Uher J, Uhrova M. Water and nitrogen content of body of young human embryos. American Journal of Obstetrics and Gynecology 1966, 96:868-71.
51. Johanson JM, Berger PJ, Kirkpatrick BW, Dentines MR. Twinning rates for North American Holstein sires. J Dairy Sci 2001, 84:2081-2088.
52. Kähn W. Veterinary Reproductive Ultrasonography 1994, 83-129. Schlüterse, Hannover and Mosby-Wolfe, London, pp
53. Kidder HE, Black WG, Wiltbank JN, Ulberg LC, Casida LE. Fertilization rates and embryonic death rates in cows bred to bulls of different levels of fertility. J Dairy Sci 1954, 37:691-697.
54. King GJ, Atkinson BA, Robertson HA. Development of the bovine placentome from days 20 to 29 of gestation. J Reprod Fertil 1980, 59:95-100.
55. Labèrnia J, López-Gatius F, Santolaria P, López-Béjar M, Rutllant J. Influence of management factors on pregnancy attrition in dairy cattle. Theriogenology 1996, 45:1247-1253.
56. López-Gatius F. Site of semen deposition in cattle: a review. Theriogenology 2000, 53:1407-1414.
57. López-Gatius F. Is fertility declining in dairy cattle? A retrospective study in northeastern Spain. Theriogenology 2003, 60:89-99.
58. López-Gatius F. The effect on pregnancy rate of progesterone administration after manual reduction of twin embryos in dairy cattle. J Vet Med A Physiol Pathol Clin Med 2005, 52:199-201.
59. López-Gatius F, Camón-Urgel J. Confirmation of estrus rates by palpation per rectum of genital organs in normal repeat dairy cows. Zentralbl Veterinarmed A 1991, 38:553-556.
60. López-Gatius F, Garcia-Ispierto I. Return to heat after positive diagnosis in the first trimester of gestation: therapeutic approach. Large Animal Review 2009, 15:81-84.
61. López-Gatius F, Hunter RHF. Spontaneous reduction of advanced twin embryos: its occurrence and clinical relevance in dairy cattle. Theriogenology 2005, 63:118-125.
62. Lopez-Gatius F, Almeria S, Donofrio G, Nogareda C, Garcia-Ispierto I, Bech-Sabat G, Santolaria P, Yaniz JL, Pabon M, De Sousa NM, Beckers JF. Protection against abortion linked to gamma interferon production in pregnant dairy cows naturally infected with Neospora caninum. Theriogenology 2007c, 68:1067-1073.
63. López-Gatius F, Labèrnia J, Santolaria P, López-Bejar M, Rutllant J. Effect of reproductive disorders previous to conception on pregnancy attrition in dairy cows. Theriogenology 1996, 46:643-648.
64. López-Gatius F, Santolaria P, Yaniz J, Rutllant J, López-Béjar M. Factors affecting pregnancy loss from gestation day 38 to 90 in lactating dairy cows from a single herd. Theriogenology 2002, 57:1251-1261.
65. López-Gatius F, Yániz J, Madriles-Helm D. Effects of body condition score and score change on the reproductive performance of dairy cows. Theriogenology 2003, 59:801-812.
66. López-Gatius F, Santolaria P, Yániz JL, Garbayo JM, Hunter RHF. Timing of early foetal loss for single and twin pregnancies in dairy cattle. Reprod Domest Anim 2004a, 39:429-433.
67. López-Gatius F, Pabon M, Almería S. Neospora caninum infection does not affect early pregnancy in dairy cattle. Theriogenology 2004b, 62:606-613.
68. López-Gatius F, Santolaria P, Yániz JL, Hunter RHF. Progesterone supplementation during the early fetal period reduces pregnancy loss in high-yielding dairy cattle. Theriogenology 2004c, 62:1529-1535.
69. López-Gatius F, López-Béjar M, Fenech M, Hunter RHF. Ovulation failure and double ovulation in dairy cattle: risk factors and effects. Theriogenology 2005, 63:1298-1307.
70. López-Gatius F, Santolaria P, Martino A, Delétang F, De Rensis F. The effects of GnRH treatment at the time of AI and 12 days later on reproductive performance of high producing dairy cows during the warm season in northeastern Spain. Theriogenology 2006a, 65:820-830.
71. López-Gatius F, García-Ispierto I, Santolaria P, Yániz J, Nogareda C, López-Béjar M. Screening for high fertility in high-producing dairy cows. Theriogenology 2006b, 65:1678-1689.
72. López-Gatius F, Garbayo JM, Santolaria P, Yániz JL, Almería S, Ayad A, De Sousa NM, Beckers JF. Plasma pregnancy-associated glycoprotein-1 (PAG-1) concentrations during gestation in Neospora-infected dairy cows. Theriogenology 2007a, 67:502-508.
73. López-Gatius F, Hunter RH, Garbayo JM, Santolaria P, Yaniz J, Serrano B, Ayad A, De Sousa NM, Beckers JF. Plasma concentrations of pregnancy-associated glycoprotein-1 (PAG-1) in high producing dairy cows suffering early fetal loss during the warm season. Theriogenology 2007b, 67:1324-1330.
74. López-Gatius F, Garbayo JM, Santolaria P, Yániz J, Ayad A, De Sousa NM, Beckers JF. Milk production correlates negatively with plasma levels of pregnancy-associated glycoprotein (PAG) during the early fetal period in high producing dairy cows with live fetuses. Domest Anim Endocrinol 2007c, 32:29-42.
75. López-Gatius F, Mirzaei A, Santolaria P, Bech-Sàbat G, Nogareda C, García-Ispierto I, Hanzen Ch, Yániz JL. Factors affecting the response to the specific treatment of several forms of clinical anestrus in high producing dairy cows. Theriogenology 2008, 69:1095-1103.
76. López-Gatius F, Szenci O, Bech-Sàbat G, García-Ispierto I, Serrano B, Santolaria P, Yániz J. Factors of non-infectious nature affecting late embryonic and early foetal loss in high producing dairy herds in north-eastern Spain. Magy Allatorvosok Lapja 2009, 131:515-531.
77. López-Gatius F, García-Ispierto I, Hunter RHF. Factors affecting spontaneous reduction of corpora lutea and twin embryos during the late embryonic/early fetal period in multiple-ovulating dairy cows. Theriogenology 2010, 73:293-299.
78. Matsui M, Miyamoto A. Evaluation of ovarian blood flow by colour Doppler ultrasound: practical use for reproductive management in the cow. Vet J 2009, 181:232-240.
79. Nielen M, Schukken YH, Scholl DT, Wilbrink HJ, Brand A. Twinning in dairy cattle: a study of risk factors and effects. Theriogenology 1989, 32:845-862.
80. Niswender GD. Getting cows pregnant and keeping them pregnant requires progesterone. 2004, 73-77. Proceed Thirty-seventh Ann Conf, Am Assoc Bov Pract, Texas, USA, pp
81. Niswender GD, Juengel JL, Silva PJ, Rollyso MK, McIntush EW. Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev 2000, 80:1-29.
82. Perkins JR, Olds D, Seath DM. A study of 1,000 bovine genitalia. J Dairy Sci 1954, 37:1158-1163.
83. Peters AR. Embryo mortality in the cow. Anim Breed Abs 1996, 64:587-598.
84. Raghupathy R. Th-1 immunity is incompatible with successful pregnancy. Immunol Today 1997, 18:478-482.
85. Reynolds LP, Redmer DA. Growth and microvascular development of the uterus during early pregnancy in ewes. Biol Reprod 1992, 47:698-708.
86. Rhinehart JD, Starbuck-Clemmer MJ, Flores JA, Milvae RA, Yao J, Poole DH, Inskeep EK. Low peripheral progesterone and late embryonic/early fetal loss in suckled beef and lactating dairy cows. Theriogenology 2009, 71:480-490.
87. Riding GA, Lehnert SA, French AJ, Hill JR. Conceptus-related measurements during the first trimester of bovine pregnancy. Vet J 2008, 175:266-272.
88. Romano JE, Thompson JA, Forrest DW, Westhusin ME, Tomaszweski MA, Kraemer DC. Early pregnancy diagnosis by transrectal ultrasonography in dairy cattle. Theriogenology 2006, 66:1034-1041.
89. Sangsritavong S, Combs DK, Sartori R, Armentano LE, Wiltbank MC. High feed intake increases liver blood flow and metabolism of progesterone and estradiol-17β in dairy cattle. J Dairy Sci 2002, 85:2831-2842.
90. Santolaria P, López-Gatius F, García-Ispierto I, Bech-Sàbat G, Angulo E, Carretero T, Sánchez-Nadal JA, Yániz J. Effects of cumulative stressful and acute variation episodes of farm climate conditions on late embryo/early fetal loss in high producing dairy cows. Int J Biometeorol 2010, 54:93-98.
91. Santos JEP, Thatcher WW, Chebel RC, Cerri RLA, Galvão KN. The effect of embryonic death rates in cattle on the efficacy of estrus synchronization programs. Anim Reprod Sci 2004, 82-83:513-535.
92. Scanlon PF. Frequency of transuterine migration of embryos in ewes and cows. J Anim Sci 1972, 34:791-794.
93. Serrano B, López-Gatius F, Hunter RHF, Santolaria P, García-Ispierto I, Bech-Sabat G, De Sousa NM, Beckers JF, Yániz JL. Anomalous pregnancies during late embryonic/early foetal period in high producing dairy cows. Reprod Domest Anim 2009, 44:672-676.
94. Silva-del-Río N, Kirkpatrick BW, Fricke PM. Observed frequency of monozygotic twinning in Holstein dairy cattle. Theriogenology 2006, 66:1292-1299.
95. Silva-del-Río N, Colloton JD, Fricke PM. Factors affecting pregnancy loss for single and twin pregnancies in a high-producing dairy herd. Theriogenology 2009, 71:1462-1471.
96. Spencer TE, Burghardt RC, Johonson GA, Bazer FW. Conceptus signals for establishment and maintenance of pregnancy. Anim Reprod Sci 2004, 82-83:537-550.
97. Starbuck MJ, Dailey RA, Inskeep EK. Factors affecting retention of early pregnancy in dairy cattle. Anim Reprod Sci 2004, 84:27-39.
98. Svennersten-Sjaunja K, Olsson K. Endocrinology of milk production. Domest Anim Endocrinol 2005, 29:241-258.
99. Szenci O, Beckers JF, Humblot P, Sulon J, Sasser G, Taverne MAM, Varga J, Baltusen R, Schekk G. Comparison of ultrasonography, bovine pregnancy-specific protein B, and bovine pregnancy-associated glycoprotein 1 tests for pregnancy detection in dairy cows. Theriogenology 1998a, 50:77-88.
100. Szenci O, Taverne MAM, Beckers JF, Sulon J, Varga J, Börzsönyi L, Hanzen CH, Schekk G. Evaluation of false ultrasonographic diagnoses in cows by measuring plasma levels of bovine pregnancy-associated glycoprotein 1. Vet Rec 1998b, 142:304-306.
101. Szenci O, Humblot P, Beckers JF, Sasser G, Sulon J, Baltusen R, Varga J, Bajcsy CSA, Taverne MAM. Plasma profiles of progesterone and conceptus proteins in cows with spontaneous embryonic/fetal mortality as diagnosed by ultrasonography. Vet J 2000, 159:287-290.
102. Thatcher WW, Guzeloglu A, Mattos R, Binelli M, Hansen TR, Pru JK. Uterine-conceptus interactions and reproductive failure in cattle. Theriogenology 2001, 56:1435-1450.
103. Thomas I, Dobson I. Oestrus during pregnancy in the cow. Vet Rec 1989, 124:387-390.
104. Biological effects due to heat and the most thermally sensitive sites with particular reference to the embryo and fetus. Ultrasound Med Biol 1992, 18:739-750.
105. Whitlock BK, Maxwell HS. Pregnancy-associated glycoproteins and pregnancy wastage in cattle. Theriogenology 2008, 70:550-559.
106. Wilczyński JR. Th1/Th2 cytokines balance -yin and yang of reproductive immunology. Eur J Obstet GYN R B 2005, 122:136-143.
107. Wiltbank WC, Dysko RC, Gallagher KP, Keyes PL. Relationship between blood flow and steroidogenesis in the rabbit corpus luteum. J Reprod Fertil 1988, 84:513-520.
108. Wiltbank M, Lopez H, Sartori R, Sangsritavong S, Gümen A. Changes in reproductive physiology of lactating dairy cows due to elevated steroid metabolism. Theriogenology 2006, 65:17-29.