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LH and FSH profiles at superovulation and embryo production in the cow
THERIOGENOLOGY
LH AND FSH PROFILES AT SUPEROVULATIONAND EMBRYO PRODUCTION
IN THE COW
Rio
Received
E. Donaldsona International, Inc. Rt. 9 Box 242 San Antonio, Texas 78227 Lloyd Vista
for
publication: Accepted
:
April 11, 1984 October 31, 1984
ABSTRACT The variability of the superovulation response in cattle is an important problem to the commercial embryo transfer Plasma LH and FSH concentrations around the time industry. of estrus and ovulation were studied in relation to embryo Sixteen cows to try and elucidate this problem. production, were superovulated with 38 mg FSH-P and estrus synchronized with prostaglandin F2 alpha, On the third and fourth day of superovulation increases in plasma LH but not FSH were The LH and FSH profiles appeared to be normal in detected. the size of the surge but in many cases they were were Transferable embryo production appeared abnormal in timing. to be lower in cows in which the LH and FSH surges were not and in cows where the surges were early OS late coincident, FSH appeared to be primarily with reference to estrus. responsible for the number of embryos produced and LH for the number transferable. their quality, i.e. Key words: embryo superovulation.
production,
LH , FSH, cattle,
INTRODUCTION Saumonde (1) showed that the basic levels of LH in the donor cow were not altered by the superovulation treatment, and the preovulatory surge appeared about 44 hours after the prostaglandin injection. The duration of the surge and the value of the maximum LH concentration and the area under the curve were not related to the number of ovulations (1). Plasma LH and progesterone levels have been related to embryo quality in PMSG-prostaglandin treated cows. At the onset of estrus the progesterone concentration in superovulated cows with optimal embryo quality was significantly lower than in cows which yielded unfertilized ova. The LH surge in the cows with optimal embryo a Present
MARCH
address:
Rt.1
1985VOL.23 NO.3
Box 32,
Wilsonville,
Alabama,
35186
441
THERIOGENOLOGY
production occurred within a narrower time interval and reached a higher level than in the cows that yielded unfertilized ova (2). Greve et al. (3) reported that a high proportion of superovulated cows developed abnormal LH profiles which had a detrimental effect on both ovulation and fertilization rates. The abnormalities of the LH profiles included no surge, moderate, premature or delayed This study attempted to relate LH and FSH profiles surge. to embryo production. MATERIALS AND METHODS Sixteen commercial Brahman crossbred cows were superovulated with 38 mg FSH-P (Burns Biotec, Omaha, NE.) injected twice a day in doses of 5/5, 5/5, 4/4, 3/3 and 2/2 mg per injection. Estrus was synchronized with 30 mg prostaglandin F2 alpha Kalamazoo, MI.) injected in (PGF, Lutalyse, The Upjohn Co., three doses of 10 mg morning noon and evening on the fourth Estrus was detected by direct observation continuously day. from 6AM to 1lPM for 3 days commencing the day after PGF The and between 2AM and 3AM on the second night. treatment; cows were bred three times with one unit of semen at about Eleven 3, 12 and 24 hours after the detection of estrus. venous blood samples were drawn from each cow into vacuum tubes containing EDTA. The first sample was drawn at 5.30PM on the third day of FSH treatment, and the second on the next morning at 7.15AM before FSH-P and PGF treatments. Nine samples were taken at four hourly intervals commencing at 6.30AM on the last day of FSH-P treatment. The timing of this interval was within 15 minutes before or after. The plasma LH and FSH levels were determined by radio immunoassay (4,5). These assays were validated and performed in the laboratories of Dr. William Hansel at Cornell University. RESULTS AND DISCUSSION Fourteen of the 16 cows were detected in estrus an average of 42.3 hours after the first PGF injection (Table 1). The cows produced an average 2.2 transferable embryos from a total collection of 8.2 embryos and ova. The percent The LH levels on days 3 and 4 of transferable was 37.9%. the FSH-P treatment were 1.7 and 1.9 ng/ml. These are higher than normal levels of 1.0 ng/ml determined by the same assay procedure using the same antibody (6). The FSH The levels were not detectably elevated being 0.6 ug/ml. data from the blood samples collected at 4 hourly intervals were normalized to the LH surge (Figure 1). There was a highly significant rise in LH levels to the surge level of This surge was, when considering height and 24 ng/ml.
442
MARCH
1985 VOL. 23 NO. 3
THERIOGENOLOGY
TABLE 1. ONSET OF ESTRUS, EMBRYO PRODUCTION THE PLASMA LH AND FSH SURGE COW NO.TIME 1ST PGF TO ONSET OF ESTRUS (HRS)
HOURS FROM EMBRYOS FSH NO. TRANS- % TRANSLH FERABLE SURGE SURGE FERABLE
TOTAL
1 2 3 4 5 6 7 8 9 10 11 12 13 14
48 33 50 32 37 46 37 28 47 52 37 50 51 46
4 6 13 15 13 16 19 4 4 4 3 14
MEAN S E
42.3 2.16
8.2 1.72
AND TIMING OF
0 4 0 1 3 7 ;
100 0 8 20 54 6 0 0 50 100 67 50
0 2 4 2 7 2.2
37.9
0.66
10.9
-: t4 0 -8 t4 0 -4 t8 t8 -4 -4 -8 0
;: -4 0 8 -4 t4 0 -4 -16 t4 t4 t8 0
TABLE 2. THE TIMING OF THE LH AND FSH SURGE AND EMBRYO PRODUCTION PLASMA HORMONE
SURGE
NO. COWS TOTAL
EMBRYOS NO. TRANS- % TRANSFERABLE FERABLE
FSH/LH at same time
2
10.0
3.5
35
LH within 4 hours of onset of estrus
4
5.5
3.5
64
LH before onset of estrus
6
6.7
2.7
40
LH > 4 hours after the onset of estrus
5
9.8
1.6
16
FSH within 4 hours of onset of estrus
3
12.0
2.7
23
FSH before onset of estrus
5
8.4
1.4
17
FSH > 4 hours after the onset of estrus
6
6.3
2.7
43
MARCH
1985 VOL. 23 NO. 3
443
THERIOGENOLOGY duration, comparable to that seen in nonsuperovulated cows The timing of the LH surges was normal in four (1,7,8). cows which produced 3.5/5.5 transferable/total embryos (64% transferable, Table 2). when the LH sur.Je was early (6 cows, 2.7/6.7, 40%) or late (5 cows, 1.6/9.8, 16%), total embryo production increased, and the number and percent transferable declined. There was no LH surge in the two cows that did not show estrus. These results agree with Greve et al. (3) who associated early, late or the absence of an LH surge with poor embryo production. The correlation between the percent transferable and LH levels were significant at the time of the LH surge (r= 0.68, P = 0.0151, while the correlation with the number of transferable embryos was significant four hours later (I: = 0.60, P = 0.024). The higher the LH surge the higher the percent transferable, and the longer the LH surge remained high, the more transferable embryos. Jensen et al. (2) found that the higher the LH surge the better was embryo The rise in LH at estrus stimulates the OOCyte to quality. mature (9) so that the quantity of LH conceivably could be limiting on the number of oocytes that can be stimulated to mature normally, affecting both the number of oocytes that mature into normal embryos and the percent of embryos that are transferable. There was an FSH surge which on the average was coincident Plasma levels rose from 0.52 to 0.95 with the LH surge. ug/ml (P = 0.001). In three cows where the FSH surge was within the first four hours of estrus, transferable embryo production (2.7/12, 23%) was similar to six cows with a 43%), whereas five cows with earlier later surge (2.7/6.3, FSH levels on day 4 of FSH surges produced 1.4/8.4 (17%). FSH treatment were significantly correlated with total On the third day embryo production (I: = 0.56, P = 0.034). of FSH treatment and at four and eight hours before the LH surge, FSH levels were correlated with total embryo It seemed as if the higher production (I: = 0.51, P = 0.06). the FSH levels before estrus, the better the total embryo which might be expected since FSH stimulates production, the procedures did not folliculogenesis (10). However, detect an elevation in plasma FSH levels from exogenous FSH at the time of sampling approximately 10 and 24 hours after Embryo production was higher in two cows FSH treatment. where the FSH and LH surges were coincident (3.5/10, 35%), than in seven cows with earlier FSH surges (2.4/7.6, 32%) and four cows with later FSH surges (1.8/10.5, 17%, Table 2). It seems that a normal LH surge was important for a high number and percent of transferable embryos while the timing of the FSH surge had a more important effect on the These results have some support total embryos recovered. The surge-like release of FSH and LH from current theory. LH is induces a series of biochemical events in the ovary.
444
MARCH 1985 VOL. 23 NO. 3
THERIOGENOLOGY
2422201816-
- 0.8
14-
-0.7
f \
12-
-0.6
E
I -J IO-
-0.5
5k
8-
- 0.4
6-
-0.3
4-
-0.2
2-
-0.i
f \ Y:
OI
3_4
(8
0
l8
Day of FSH Treatment Figure 1
MARCH
3 4
-8
/Hours
0
l0
from LH Peak
\
LH and FSH profiles in superovulated cows (Bars indicate S E of mean)
1985VOL.23NO. 3
445
THERIOGENOLOGY responsible for the resumption of meiosis in the preovulatory oocyte (91, and causes ovulation, luteinization and progesterone production from the granulosa cells (10). When the LH surge is delayed, the oocyte may not have reached nuclear and cytoplasmic maturation before ovulation resulting in a high level of nontransferable embryos. On the other hand, when the LH surge occurs prematurely, luteinization may occur leading to abnormal levels of progesterone during estrus , which have been shown to decrease transferable embryo production (11). On the other hand, the FSH surge is mainly associated with promoting growth (mitotic activity, protein synthesis) of small antral follicles to ensure another wave of follicles The loss of capacity of for the next ovulatory cycle (12). growing follicles to produce estradiol and the onset of regression, coincides with a decrease in serum FSH levels FSH is essential for ovarian estradiol production and (13). plays a supportive role in the physical events surrounding ovulation (10). Although the number of cows in this study is small it appears as if a normal LH and FSH profile is The results suggest helpful for optimum embryo production. that FSH is involved in the number of follicles (and thus embryos and ova) produced and LH with the subsequent quality of the embryos. REFERENCES 1.
Saumonde, J. Concentrations of luteinizing hormone, oestradiol-17 beta and progesterone in the plasma of heifers treated to induce superovulation. J. Endocrfno (1980). -84: 425-437
2.
Jensen, A.M., Greve, T., Madej, A. and Edquist, Endocrine profiles and embryo quality in the PMSG-PGF alpha treated cow. Theriogenology -18: 33-44 (13821.
3.
P. H. and Hythel, T., Calleson, of plasma LH-profiles in superovulated (abstr.). Theriogenology -21: 237 (1984)
4.
Hobson, W.C. ovariectomy, administration (1972).
5.
and application Bolt, D.J. and Rollins, K. Development of a radioimmunoassay for bovine follicle stimulating hormone. J. Anim. Sci. (1983). -56: 146-154
Greve,
1,
L.E.
Characterization dairy cows.
w. Plasma LH levels after and Hansel, corpus luteum removal and oestradiol in cattle. Endocrinology -91: 185-190
MARCH 1985 VOL. 23 NO. 3
THERIOGENOLOGY
6.
Butler, W.R., Katz, L.S., Arriola, J., MilVae, R.A. and Foote, R.H. On negative feedback regulation of gonadotropins in castrate and intact cattle with comparison of two radioimmunoassays. J. Anim. Sci. -56: 919-929 (1983).
I.
Akbar,A.M., Reichert, L.E., Jr., and Dunn, T.G. Serum levels of follicle-stimulating hormone during the bovine estrous cycle. J. Anim. Sci. -39: 360-365 (1974).
8.
Rahe, C.H., Owens, R.E., Fleeger, J.L., Newton, H.J. and Harms, P.G. Pattern of plasma luteinizing hormone in the cyclic cow: Dependance upon the period of the cycle. Endocrin. 107: 498-503 (1980).
9.
Moor, R.M., Kruip, Th.A.M. and Green D. IntraOVarian control of folliculogenesis: limits to superovulation? Theriogenology -21: 103-116 (1984).
10.
Chappel, S.C., Ulloa-Aguirre, A. and Coutifaris, C. Biosynthesis and secretion of follicle-stimulating hormone. Endocrine Rev. ff: 179-211 (1983).
11.
Greve, T., Calleson, H. and Hytel, P. Plasma progesterone profiles and embryo quality in superovulated dairy cows. Theriogenology -21: 238 (1984) (abstr.).
12.
Richards, J.S. Maturation of ovarian follicles: Actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol. Rev. -60: 51-88 (1980).
13.
Ireland, T.J. and Roche, J.F. Development of nonovulatory antral follicles in heifers: changes in steroids in follicular fluid and receptors for gonadotropins. Endocrinology 112: 150-156 (1983).
MARCH
1985 VOL. 23 NO. 3
447
LH AND FSH PROFILES AT SUPEROVULATIONAND EMBRYO PRODUCTION
IN THE COW
Rio
Received
E. Donaldsona International, Inc. Rt. 9 Box 242 San Antonio, Texas 78227 Lloyd Vista
for
publication: Accepted
:
April 11, 1984 October 31, 1984
ABSTRACT The variability of the superovulation response in cattle is an important problem to the commercial embryo transfer Plasma LH and FSH concentrations around the time industry. of estrus and ovulation were studied in relation to embryo Sixteen cows to try and elucidate this problem. production, were superovulated with 38 mg FSH-P and estrus synchronized with prostaglandin F2 alpha, On the third and fourth day of superovulation increases in plasma LH but not FSH were The LH and FSH profiles appeared to be normal in detected. the size of the surge but in many cases they were were Transferable embryo production appeared abnormal in timing. to be lower in cows in which the LH and FSH surges were not and in cows where the surges were early OS late coincident, FSH appeared to be primarily with reference to estrus. responsible for the number of embryos produced and LH for the number transferable. their quality, i.e. Key words: embryo superovulation.
production,
LH , FSH, cattle,
INTRODUCTION Saumonde (1) showed that the basic levels of LH in the donor cow were not altered by the superovulation treatment, and the preovulatory surge appeared about 44 hours after the prostaglandin injection. The duration of the surge and the value of the maximum LH concentration and the area under the curve were not related to the number of ovulations (1). Plasma LH and progesterone levels have been related to embryo quality in PMSG-prostaglandin treated cows. At the onset of estrus the progesterone concentration in superovulated cows with optimal embryo quality was significantly lower than in cows which yielded unfertilized ova. The LH surge in the cows with optimal embryo a Present
MARCH
address:
Rt.1
1985VOL.23 NO.3
Box 32,
Wilsonville,
Alabama,
35186
441
THERIOGENOLOGY
production occurred within a narrower time interval and reached a higher level than in the cows that yielded unfertilized ova (2). Greve et al. (3) reported that a high proportion of superovulated cows developed abnormal LH profiles which had a detrimental effect on both ovulation and fertilization rates. The abnormalities of the LH profiles included no surge, moderate, premature or delayed This study attempted to relate LH and FSH profiles surge. to embryo production. MATERIALS AND METHODS Sixteen commercial Brahman crossbred cows were superovulated with 38 mg FSH-P (Burns Biotec, Omaha, NE.) injected twice a day in doses of 5/5, 5/5, 4/4, 3/3 and 2/2 mg per injection. Estrus was synchronized with 30 mg prostaglandin F2 alpha Kalamazoo, MI.) injected in (PGF, Lutalyse, The Upjohn Co., three doses of 10 mg morning noon and evening on the fourth Estrus was detected by direct observation continuously day. from 6AM to 1lPM for 3 days commencing the day after PGF The and between 2AM and 3AM on the second night. treatment; cows were bred three times with one unit of semen at about Eleven 3, 12 and 24 hours after the detection of estrus. venous blood samples were drawn from each cow into vacuum tubes containing EDTA. The first sample was drawn at 5.30PM on the third day of FSH treatment, and the second on the next morning at 7.15AM before FSH-P and PGF treatments. Nine samples were taken at four hourly intervals commencing at 6.30AM on the last day of FSH-P treatment. The timing of this interval was within 15 minutes before or after. The plasma LH and FSH levels were determined by radio immunoassay (4,5). These assays were validated and performed in the laboratories of Dr. William Hansel at Cornell University. RESULTS AND DISCUSSION Fourteen of the 16 cows were detected in estrus an average of 42.3 hours after the first PGF injection (Table 1). The cows produced an average 2.2 transferable embryos from a total collection of 8.2 embryos and ova. The percent The LH levels on days 3 and 4 of transferable was 37.9%. the FSH-P treatment were 1.7 and 1.9 ng/ml. These are higher than normal levels of 1.0 ng/ml determined by the same assay procedure using the same antibody (6). The FSH The levels were not detectably elevated being 0.6 ug/ml. data from the blood samples collected at 4 hourly intervals were normalized to the LH surge (Figure 1). There was a highly significant rise in LH levels to the surge level of This surge was, when considering height and 24 ng/ml.
442
MARCH
1985 VOL. 23 NO. 3
THERIOGENOLOGY
TABLE 1. ONSET OF ESTRUS, EMBRYO PRODUCTION THE PLASMA LH AND FSH SURGE COW NO.TIME 1ST PGF TO ONSET OF ESTRUS (HRS)
HOURS FROM EMBRYOS FSH NO. TRANS- % TRANSLH FERABLE SURGE SURGE FERABLE
TOTAL
1 2 3 4 5 6 7 8 9 10 11 12 13 14
48 33 50 32 37 46 37 28 47 52 37 50 51 46
4 6 13 15 13 16 19 4 4 4 3 14
MEAN S E
42.3 2.16
8.2 1.72
AND TIMING OF
0 4 0 1 3 7 ;
100 0 8 20 54 6 0 0 50 100 67 50
0 2 4 2 7 2.2
37.9
0.66
10.9
-: t4 0 -8 t4 0 -4 t8 t8 -4 -4 -8 0
;: -4 0 8 -4 t4 0 -4 -16 t4 t4 t8 0
TABLE 2. THE TIMING OF THE LH AND FSH SURGE AND EMBRYO PRODUCTION PLASMA HORMONE
SURGE
NO. COWS TOTAL
EMBRYOS NO. TRANS- % TRANSFERABLE FERABLE
FSH/LH at same time
2
10.0
3.5
35
LH within 4 hours of onset of estrus
4
5.5
3.5
64
LH before onset of estrus
6
6.7
2.7
40
LH > 4 hours after the onset of estrus
5
9.8
1.6
16
FSH within 4 hours of onset of estrus
3
12.0
2.7
23
FSH before onset of estrus
5
8.4
1.4
17
FSH > 4 hours after the onset of estrus
6
6.3
2.7
43
MARCH
1985 VOL. 23 NO. 3
443
THERIOGENOLOGY duration, comparable to that seen in nonsuperovulated cows The timing of the LH surges was normal in four (1,7,8). cows which produced 3.5/5.5 transferable/total embryos (64% transferable, Table 2). when the LH sur.Je was early (6 cows, 2.7/6.7, 40%) or late (5 cows, 1.6/9.8, 16%), total embryo production increased, and the number and percent transferable declined. There was no LH surge in the two cows that did not show estrus. These results agree with Greve et al. (3) who associated early, late or the absence of an LH surge with poor embryo production. The correlation between the percent transferable and LH levels were significant at the time of the LH surge (r= 0.68, P = 0.0151, while the correlation with the number of transferable embryos was significant four hours later (I: = 0.60, P = 0.024). The higher the LH surge the higher the percent transferable, and the longer the LH surge remained high, the more transferable embryos. Jensen et al. (2) found that the higher the LH surge the better was embryo The rise in LH at estrus stimulates the OOCyte to quality. mature (9) so that the quantity of LH conceivably could be limiting on the number of oocytes that can be stimulated to mature normally, affecting both the number of oocytes that mature into normal embryos and the percent of embryos that are transferable. There was an FSH surge which on the average was coincident Plasma levels rose from 0.52 to 0.95 with the LH surge. ug/ml (P = 0.001). In three cows where the FSH surge was within the first four hours of estrus, transferable embryo production (2.7/12, 23%) was similar to six cows with a 43%), whereas five cows with earlier later surge (2.7/6.3, FSH levels on day 4 of FSH surges produced 1.4/8.4 (17%). FSH treatment were significantly correlated with total On the third day embryo production (I: = 0.56, P = 0.034). of FSH treatment and at four and eight hours before the LH surge, FSH levels were correlated with total embryo It seemed as if the higher production (I: = 0.51, P = 0.06). the FSH levels before estrus, the better the total embryo which might be expected since FSH stimulates production, the procedures did not folliculogenesis (10). However, detect an elevation in plasma FSH levels from exogenous FSH at the time of sampling approximately 10 and 24 hours after Embryo production was higher in two cows FSH treatment. where the FSH and LH surges were coincident (3.5/10, 35%), than in seven cows with earlier FSH surges (2.4/7.6, 32%) and four cows with later FSH surges (1.8/10.5, 17%, Table 2). It seems that a normal LH surge was important for a high number and percent of transferable embryos while the timing of the FSH surge had a more important effect on the These results have some support total embryos recovered. The surge-like release of FSH and LH from current theory. LH is induces a series of biochemical events in the ovary.
444
MARCH 1985 VOL. 23 NO. 3
THERIOGENOLOGY
2422201816-
- 0.8
14-
-0.7
f \
12-
-0.6
E
I -J IO-
-0.5
5k
8-
- 0.4
6-
-0.3
4-
-0.2
2-
-0.i
f \ Y:
OI
3_4
(8
0
l8
Day of FSH Treatment Figure 1
MARCH
3 4
-8
/Hours
0
l0
from LH Peak
\
LH and FSH profiles in superovulated cows (Bars indicate S E of mean)
1985VOL.23NO. 3
445
THERIOGENOLOGY responsible for the resumption of meiosis in the preovulatory oocyte (91, and causes ovulation, luteinization and progesterone production from the granulosa cells (10). When the LH surge is delayed, the oocyte may not have reached nuclear and cytoplasmic maturation before ovulation resulting in a high level of nontransferable embryos. On the other hand, when the LH surge occurs prematurely, luteinization may occur leading to abnormal levels of progesterone during estrus , which have been shown to decrease transferable embryo production (11). On the other hand, the FSH surge is mainly associated with promoting growth (mitotic activity, protein synthesis) of small antral follicles to ensure another wave of follicles The loss of capacity of for the next ovulatory cycle (12). growing follicles to produce estradiol and the onset of regression, coincides with a decrease in serum FSH levels FSH is essential for ovarian estradiol production and (13). plays a supportive role in the physical events surrounding ovulation (10). Although the number of cows in this study is small it appears as if a normal LH and FSH profile is The results suggest helpful for optimum embryo production. that FSH is involved in the number of follicles (and thus embryos and ova) produced and LH with the subsequent quality of the embryos. REFERENCES 1.
Saumonde, J. Concentrations of luteinizing hormone, oestradiol-17 beta and progesterone in the plasma of heifers treated to induce superovulation. J. Endocrfno (1980). -84: 425-437
2.
Jensen, A.M., Greve, T., Madej, A. and Edquist, Endocrine profiles and embryo quality in the PMSG-PGF alpha treated cow. Theriogenology -18: 33-44 (13821.
3.
P. H. and Hythel, T., Calleson, of plasma LH-profiles in superovulated (abstr.). Theriogenology -21: 237 (1984)
4.
Hobson, W.C. ovariectomy, administration (1972).
5.
and application Bolt, D.J. and Rollins, K. Development of a radioimmunoassay for bovine follicle stimulating hormone. J. Anim. Sci. (1983). -56: 146-154
Greve,
1,
L.E.
Characterization dairy cows.
w. Plasma LH levels after and Hansel, corpus luteum removal and oestradiol in cattle. Endocrinology -91: 185-190
MARCH 1985 VOL. 23 NO. 3
THERIOGENOLOGY
6.
Butler, W.R., Katz, L.S., Arriola, J., MilVae, R.A. and Foote, R.H. On negative feedback regulation of gonadotropins in castrate and intact cattle with comparison of two radioimmunoassays. J. Anim. Sci. -56: 919-929 (1983).
I.
Akbar,A.M., Reichert, L.E., Jr., and Dunn, T.G. Serum levels of follicle-stimulating hormone during the bovine estrous cycle. J. Anim. Sci. -39: 360-365 (1974).
8.
Rahe, C.H., Owens, R.E., Fleeger, J.L., Newton, H.J. and Harms, P.G. Pattern of plasma luteinizing hormone in the cyclic cow: Dependance upon the period of the cycle. Endocrin. 107: 498-503 (1980).
9.
Moor, R.M., Kruip, Th.A.M. and Green D. IntraOVarian control of folliculogenesis: limits to superovulation? Theriogenology -21: 103-116 (1984).
10.
Chappel, S.C., Ulloa-Aguirre, A. and Coutifaris, C. Biosynthesis and secretion of follicle-stimulating hormone. Endocrine Rev. ff: 179-211 (1983).
11.
Greve, T., Calleson, H. and Hytel, P. Plasma progesterone profiles and embryo quality in superovulated dairy cows. Theriogenology -21: 238 (1984) (abstr.).
12.
Richards, J.S. Maturation of ovarian follicles: Actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol. Rev. -60: 51-88 (1980).
13.
Ireland, T.J. and Roche, J.F. Development of nonovulatory antral follicles in heifers: changes in steroids in follicular fluid and receptors for gonadotropins. Endocrinology 112: 150-156 (1983).
MARCH
1985 VOL. 23 NO. 3
447