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Equine body temperature and progesterone fluctuations during estrus and near parturition
THERIOGENOLOGY
EQUINE BODY TEMPERATURE AND PROGESTERONE FLUCTUATIONS DURING ESTRUS AND NEAR PARTURITION S.F. Ammons,l lDepartments
Received
W. R. Threlfalll
and R.C. Kline2
of Animal Science and Veterinary Clinical Sciences 2Department of Animal Science The Ohio State University Columbus, OH 43210
for publication: Accepted:
January Februaq
19, 1988 21, 1989
ABSTRACT
Body temperature and serum progesterone concentrations were measured in mares to determine if a change in either could be useful in predicting estrus, ovulation or parturition. There was no significant correlation (P > 0.1) between rectal temperature and the environmental temperature or progesterone concentration. Progesterone concentration did correlate with stage of estrous cycle and the stage of pregnancy. Significant differences (P < 0.05) in temperature were noted at different times throughout the day. No change in temperature occurred that could be utilized to predict estrus, ovulation or parturition. The changes in serum progesterone concentration were only useful in detecting estrus.
Key words:
temperature,
progesterone,
estrus, parturition,
equine
INTRODUCTION
The ability to accurately determine the time of ovulation and the time of parturition would greatly increase the conception rate and the birthrate of healthy foals. The reproductive cycle of the mare is subject to great variability. Mares usually demonstrate seasonal polyestrous behavior, yet 20 to 25% of them exhibit polyestrous behavior year round (1,2). Estrus usually lasts 5 to 6 d, however, when the mare is coming into or going out of winter anestrous, estrus may be much longer. Mares may also exhibit a split estrus or a silent heat. Some mares do not exhibit estrus while suckling their foals even though they may be ovulating regularly. The interval from the onset of estrus to ovulation is extremely variable. Since ovulation is related to the end of estrus, not the onset, predicting the time of ovulation is difficult (3). In the mare, the difficulty in determining when ovulation will occur is partially responsible for the poor reproductive performance observed in this species. An objective method of determining the time of ovulation is needed to overcome this problem. Equine parturition is also difficult to predict because of variable (3) and vast differences in the appearance and the intensity of the signs parturition (4-!I), which in mares is normally very rapid and strenuous. not provided immediately after the detection of a problem, the fetus placental separation. Therefore, it would be helpful to have a method capable of predicting when parturition will occur so that assistance could
MAY 1989 VOL. 31 NO. 5
gestation length of approaching If assistance is will die due to which would be be available.
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THERIOGENOLOGY
Body temperature and the level of circulating progesterone have been studied and suggested as possible predictors of estrus, ovulation, and parturition in several domestic species and in the human. For example, increases in the rectal and vaginal temperature of cattle have been related to estrous behavior (9-17). A decrease in body temperature has been noted on the day preceding estrus, with an increase in temperature the day of estrus (9,11,15,17). In the equine, progesterone concentrations in milk as well as in plasma have been found to be accurate methods of evaluating estrous cycle activity (l&19). Concentration of circulating progesterone in the plasma of mares reportedly fluctuates with the phases of the ovarian cycle, with a peak being exhibited during the luteal phase and a nadir during estrus or the follicular phase (20-30). Estrous behavior is not usually seen until progesterone concentration is less than or equal to 1 ng/ml (21,22,25,28,30). The lowest progesterone concentration is observed near ovulation. The average length of however, gestations as short normal foals. The ability to aid in the prevention of inadequate milk supply, foal
gestation in the mare ranges between 335 to 350 d (3); as 305 d (31) and as long as 400 d (32) have produced determine the time of parturition is of major importance to mare or foal death due to retained placenta, dystocia, suffocation, and the like.
In the other domestic species and in the human, much work has been done to investigate the correlation between body temperature and parturition. The body temperature of cows reportedly decreases prior to parturition (9,33-35). The highest temperature usually occurs between the second and fourth days before calving and averages 39.3”C (range 38.55 to 40.17”C). An average drop of 0.61”C (range 0.11 to 1.06”C) beginning an average of 54 h (range 74 to 33 h) before parturition has been noted. The temperature of sheep also decreases at parturition (36,37), while an increase in body temperature is associated with parturition in sows (38,39). Although the body temperature of the mare prior to parturition has been studied, the results have been Research in the mare does indicate that the progesterone inconclusive (40-42). concentration in the peripheral plasma drops prior to parturition (43,44). The purpose of this study was to determine if there is a change in body temperature that can be useful in predicting ovulation or parturition in the horse mare. The objectives were to 1) monitor the body temperature of nonpregnant cyclic mares from Day 1 of estrus through 3 d after the end of the following estrus, 2) monitor circulating progesterone levels of nonpregnant cyclic mares from Day 1 of estrus through 3 d after the end of the following estrus, 3) correlate the body temperature and progesterone level of nonpregnant cyclic mares with the time of ovulation, 4) monitor the body temperature of pregnant mares starting 2 wk prior to expected parturition through 3 d after the last day of foal heat, 5) monitor circulating progesterone levels of pregnant mares starting 2 wk prior to expected parturition through 3 d after the last day of foal heat, 6) correlate the body temperature and progesterone level of pregnant mares with the time of parturition and foal heat ovulation, 7) correlate the body temperature and progesterone level of all mares with the environmental temperature.
1008
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
MATERIALS
AND METHODS
Fourteen Registered Quarter Horse mares were used in this project. Mares were housed in 10 x 12 foot stalls at The Ohio State University Horse Barn. They had access Pregnant and nonpregnant mares were fed to free-choice water, salt and minerals. approximately 20 pounds of good quality alfalfa hay and nine pounds of 12% crude protein Countrymarka pellets daily, divided equally between morning and evening feedings. Mares with foals were fed approximately 20 pounds of good quality alfalfa hay and 16 pounds of 14% crude protein Countrymark pellets divided equally between Weather permitting, all mares and foals were allowed morning and afternoon feedings. outside for exercise, but were returned to their stalls at least 1 h before the next scheduled temperature reading. This study was conducted during the months of March, April and May 1987. Group 1 was comprised of four nonpregnant mares (one mare was 2 yr old, two mares were 3 yr old, and one mare was 7 yr old). The three oldest mares were treated orally with Altrenogest (10 cc Regu-mate)b daily for 12 consecutive days; On the thirteenth day, they were administered 10 mg of Prostaglandin F2 alpha (10 mg i.m. Lutalyse)c to induce cyclicity prior to the start of the study. Mares were monitored from the first day observed in estrus through 3 d after the end of their second estrus. Group 2 was comprised of ten pregnant mares, ranging in age from 5 to 17. The mares were monitored from 2 wk prior to the calculated due date (335 d following breeding) through 3 d after the last day of foal heat. Mares were teased daily to determine the beginning and end of estrus and palpated every other day during estrus to determine the day of ovulation. Ovulation was determined by the presence of an ovulation depression or a corpus hemorrhagicurn at the time of palpation. When an ovulation depression was detected, ovulation was said to have occurred at 6:00 a.m. that same day. When a corpus hemorragicum was detected, ovulation was said to have occurred at 600 a.m. the previous day. Rectal temperatures of all mares were taken four times daily (0000, 0600, 1200, 1800 h) with a high-speed digital thermometerd. The probe was inserted 14.5 cm into the rectum and held against the rectal wall for 30 sec. Jugular blood samples were collected daily (1200 h) from all mares for progesterone analysis. Following collection, blood was allowed to clot at room temperature for 30 min, then centrifuged at 6000 x g Serum was stored at -20°C until the time of assay. Levels of circulating for 15 min. progesterone were determined using a rapid Competitive Linked Immunoassaye developed for quantitative analysis of equine progesterone. The method for assay was followed as described by Cambridge Veterinary Sciences, except for a modification in a
Countrymark
b
American
c
The Upjohn
d
GLA Agricultural
e
Inc., PO Box 1206, Delaware,
Hoechst
Corporation,
Company,
Ovusure - Elanco
Products
MAY 1989 VOL. 31 NO. 5
43015.
Animal Health Division, Somerville,
Kalamazoo,
Electronics.
OH
MI
08876.
49001.
4743 Brooks Street, Montclair. Company,
NJ
Indianapolis,
IN
CA
91763.
46285
1009
THERIOGENOLOGY
the amount of stopping solution. The assays were run in duplicate, and a Socorexf micropipetter was used. The plates used had 96 wells precoated with sheep antiprogesterone serum, and filled with stabilizing buffer. First the plates were emptied and patted dry on paper towels. Ten microliters of standard (0.5, 1.0, 5.0, 10.0 and 30.0 ng/ml standards were used) or sample were added to each well. Then 200 ul of conjugate (progesterone-alkaline phosphatase) were added, the plates were covered and left to incubate at room temperature for 30 min. Plates were then emptied and rinsed three times with tap water. Two hundred microliters of substrate reagent (a solution of 1.0 M diethanolamine and 0.5 mM magnesium chloride at pH 9.8 to which three p-nitrophenyl phosphate tablets had been added) were added to each well. The plates were covered and left to incubate for 30 min at room temperature. Then 40 ul of stopping solution (0.5 M Di-potassium hydrogen orthophosphate and 0.5 mM EDTA) The plates were read on an EIA manual reader, model #EL 3078, at a were added. 405-nm wavelength. The reader was calibrated to zero before each plate was read. The data were analyzed using General and Student’s t-test, where appropriate.
Linear Models Procedure,
Mean Separation
RESULTS There was no significant correlation (P > 0.1) in the Group 1 nonpregnant mares between the rectal temperature and environmental temperature or the level of circulating progesterone. In the Group 1 nonpregnant mares (Figures 1 and 2) and in the Group 2 pregnant mares that were monitored during foal heat (Figure 3), the level of circulating progesterone correlated with the stage of the estrous cycle in that an increase 2 1 ng/ml Progesterone concentration continued to increase was noted the day after ovulation. until Day 5 after ovulation, and it ranged from 10 to 13 ng/ml on Day 5. Throughout the first estrus monitored, there was no significant difference (P > 0.05) in rectal During the second estrus temperatures of Group 1 at different times of the day. studied, there was a significant difference (P < 0.05) between the 0000 and 0600 rectal temperatures and the 1200 and 1800 h rectal temperatures. In Group 2, there was no significant correlation (P > 0.1) of rectal temperature with environmental temperature or with the level of circulating progesterone, but the level of circulating progesterone did correlate with the stage of late pregnancy (Figure 4). Progesterone was 2 12.5 ng/ml during the last 2 wk of gestation, dropped below 8 ng/ml within 1 d after parturition, and continued to decrease to below 3 ng/ml by 3 d after foaling. Pregnant mares monitored through parturition showed a significant difference (P < 0.05) between the 0000 and 0600 h rectal temperatures and the 1200 and 1800 h rectal temperatures. These same mares monitored during foal heat exhibited a significant difference (P < 0.05) in rectal temperature at 1800 versus the 0000, 0600, and 1200 h readings. The variables measured, environmental temperature, day, time of day, and level of circulating progesterone accounted for 20% of the variation in rectal temperature, as indicated by the general linear models procedure of statistical analysis.
f
Socorex ISBA SA, I020 Renens, Switzerland.
g
Bio-Tek
1010
Instruments,
Inc., I Mill Street, Burlington, VT
05401.
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
0l-P1
Figure 1.
MAY 1989 VOL. 31 NO. 5
Non-pregnant, First OvUlatlOn
Vertical
line
denotes
time of
ovulationa
1011
THERIOGENOLOGY
Group 1
Figure 2.
1012
Non-pregnant,
2nd Ovulation
Vertical line denotes time of ovulation.
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
Group 2
Foal Moat Oruhtlon
G 0’ 310. 25-
10
Figure 3.
11
12
11
14
1r
1m
20
Vertical line denotes time of ovulation.
MAY 1989 VOL. 31 NO. 5
1013
THERIOGENOLOGY
Group 2
20
P i! e 0 5
I J/
10
CA1
s
2
Figure
1014
P8rturltlon
r
4
3
4.
5
6
t
8
9
10
11
12
13
14
15
16
17
10
10
20
Vertical bar denotes day of parturition.
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
DISCUSSION There was no significant correlation (P > 0.05) between rectal temperature and environmental temperature in any of the mares. Our study was conducted in a heated barn during the months of March, April and May 1987, and the environmental temperature was maintained within a range of 5” to 27°C (mean 15°C). Since horses and ponies are homeothermic, they maintain a relatively constant body temperature that is independent of the environmental temperature (4546). This is important because if rectal temperature fluctuated as environmental temperature fluctuated, it would be extremely difficult to determine a significant change in rectal temperature in response to other variables. Any such response would be hidden within changes associated with the environmental temperature. There was no significant correlation (P > 0.05) between rectal temperature and level of circulating progesterone. Although contradictory results have been obtained in cattle (9) and rats (47) and in women (48-52), individual differences within species have been shown to affect the action of progesterone on temperature regulation (53). Progesterone has a short plasma half-life of several minutes (54). More frequent analysis of progesterone concentration may have revealed a higher correlation between level of progesterone and rectal temperature. Rectal temperatures were recorded four times daily, while blood was drawn only once a day for progesterone analysis. Rectal temperature was shown to be significantly different (P < 0.05) at different times of the day, and in a study by Niekerk (24), mean progesterone concentration was significantly higher (P < 0.025) in the morning than in the evening (24). Analysis of progesterone at the time of each temperature recording may have provided a more accurate assessment of the correlation between rectal temperature and progesterone. Circulating progesterone concentration correlated with stage of the estrous cycle as an increase > 1 ng/ml was noted the day after ovulation in both groups of mares (Figures 1, 2 and 3). Progesterone concentration continued to increase until Day 5 after ovulation and ranged from 10 to 13 ng/ml on Day 5. This is in agreement with the results obtained by Plotka (29), and is important as a means of varifying recent ovulation. The concentration of circulating progesterone correlated with the stage of late pregnancy in all Group 2 mares (Figure 4). Progesterone was z 12.5 ng/ml during the last 2 wk of gestation, dropped below 8 ng/ml within 1 d after parturition, and continued to decrease to below 3 ng/ml by 3 d after foaling. Progesterone concentration is high during the last 2 wk of gestation, apparently because of the placental production of progesterone. At parturition, the placenta is expelled and a decrease in progesterone occurs. In Group 1 mares, there was no significant difference (P > 0.05) in rectal temperature at different times of the day during the first estrus monitored. There was a significant difference (P < 0.05) between the 0000 and 0600 h rectal temperatures and the 1200 and 1800 h rectal temperatures during the second estrus of the nonpregnant The first estrus monitored was within the first cycle of the breeding season. mares. The first cycle during the transitional period from winter anestrus to the breeding season is often very different from later cycles in the breeding season. In addition, three of the mares were treated orally with Altrenogest (10 cc) daily for 12 consecutive days followed by prostaglandin F2 alpha administration (10 mg i.m.) 13 d prior to the first estrus. No hormonal treatments were administered between the first and second Perhaps the administration of the altrenogest or the prostaglandin F2 estrus studied. alpha or the two in combination suppressed the temperature difference that was
MAY 1989 VOL. 31 NO. 5
1015
THERIOGENOLOGY
exhibited during the second estrus. In support of this, researchers found that heifers that were treated with prostaglandin F2 alpha did not exhibit the usual temperature increase during the induced estrus (55). The Group 2 pregnant mares that were monitored through parturition also exhibited a significant difference (P < 0.05) between the 0000 and 0600 h rectal temperatures and the 1200 and 1800 h rectal temperatures. However, these same mares, when monitored through foal heat, exhibited a significant difference (P < 0.05) in rectal temperature at the 1800 h reading. It is clear that there are many variables that affect temperature regulation. Of the variables that were monitored in our study, there is a need to evaluate not only the length of time between blood collection for progesterone analysis, but also the length of time between temperature recordings. An increased body temperature of 0.5”C (P 5 0.05) has been reported in ponies within 6 min of the start of exercise (46). Additionally, acepromazine, azaperone and D-Ala2-Met-enkephalinamide have been reported to cause body temperature changes in horses of 0.9” to 3.O”C in periods ranging from 20 min to 3 h following treatment (56). From this, it is apparent that horses and ponies can experience temperature changes within a short period of time. Thus, 6-h temperature readings may be inadequate. This may have accounted for much of the 80% of the temperature variation which was not accounted for by the variables measured (environmental temperature, day of the cycle, time of day and circulating progesterone). In our study, no change in rectal temperature was apparent that could be used to predict estrus, the time of ovulation or the time of parturition in the horse mare. Additional studies are needed to determine if more frequent temperature recordings or the determination of other presently unknown variables affecting temperature would permit this technique to be utilized for ovulation and parturition prediction in the horse mare. REFERENCES
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G. H. and Kennedy, P. C. The estrous 2. Hughes, J. P., Stabenfeldt, selected functional and pathologic ovarian abnormalities in the mare. North Am. 2:225-239 (1980). 3. Evans, J. W. Horses: A Guide to Selection, and Co., San Francisco, 1981, pp. 486-500. 4.
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Wrenn, T. R., Bitman, J. and Sykes, J. F. Body temperature variations in dairy cattle during the estrous cycle and pregnancy. J. Dairy Sci. 41:1071-1076 (1958).
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in the oestrous 14. Valdivia, R. R. and Vallenas, P. A. Some physiological variations cycle of the cow. Rectal and cervical temperature, pH, and crystallization of the cervical secretion and milk yield. Anim. Breed. &I~51 abstr. (1966). and 15. Sharma, 0. P., Singh, B. P. and Tomar, N.S. Studies on body temperature leucocyte count in Hariana cows during oestrous cycle. Indian Vet. J. 28:233-237 (1968). L., Ibrishimov, N. and Kolev, Ya. Changes of vaginal and rectal 16. K’nchev, temperature during the oestrous cycle of cows. Anim. Breed. 42:553 abstr. (1974). 17. Lewis, G. S., Newman, S. K. Changes throughout estrous cycles of variables might indicate estrus in dairy cows. J. Dairy Sci. 67:146-152 (1984).
that
18. Hunt, B. Monitoring of plasma and milk progesterone for evaluation of postpartum estrous cycles and early pregnancy in mares. J. Am. Vet. Med. Assoc. 172:12981302 (1978). 19. Gunther, J. D., Foley, C. W., Gaverick, H. A., and Plotka, E. D. Comparison of milk and blood plasma progesterone concentrations in cycling and pregnant mares. J. Anim. Sci. 51:1131-1138 (1980). Progesterone concentrations in the 20. Smith, I. D., Bassett, J. M., Williams, T. peripheral plasma of the mare during the oestrous cycle. J. Encocrinol. 42523-524 (1970). 21. Plotka, E. D., Witherspoon, D. M., and Foley, C. W. Luteal function in the mare as reflected by progesterone concentrations in peripheral blood plasma. Am. J. Vet. Res. 12:917-920 (1972). 22. Stabenfeldt, G. H., Hughes, J. P., and Evans, J. W. Ovarian activity estrous cycle of the mare. Endocrinology @1379-1384 (1972).
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in pony 23. Allen, W. E. and Hadley, J. C. Peripheral blood levels of progesterone mares during the oestrous cycle and early pregnancy. Vet. Rec. 9277 (1973). 24. Niekerk, C. H., Morgenthal, J. C., Sanders, C. P., and Malan, J. E. Progesterone concentration in the peripheral plasma of the mare during the oestrous cycle and early pregnancy. J. South Afr. Vet. Assoc. a363-373 (1973). MAY 1999 VOL. 31 NO. 5
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THERIOGENOLOGY
Changes in peripheral plasma progesterone 25. Sharp, D.C. and Black, D. L. J. Reprod. Fertil. 52:535-538 throughout the oesteorus cycle of the pony mare. (1973). Serum concentrations of FSH, LH and 26. Evans, M. J. and Irvine, C.H.G. progesterone during the oestrous cycle and early pregnancy in the mare. J. Reprod. Fertil. a(supplement):l93-200 (1975). 27. Noden, P. A., Oxender, W. D., and Hafs, H. D. The cycle of oestrous, ovulation and plasma levels of hormones in the mare. J. Reprod. Fertil. a(supplement):l89192 (1975). 28. Palmer, E. and Jousset, B. Urinary oestrogen and plasma progesterone non-pregnant mares. J. Reprod. Fertil. ~(supplement):213-221 (1975).
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changes in 29. Plotka, E. D., Foley, C. W., and Witherspoon, D. M. Periovulatory peripheral plasma progesterone and estrogen concentrations in the mare. Am. J. Vet. Res. j&1359-1362 (1975). P. D., and Mantri, M. B. Levels of serum progesterone 30. Mantri, A., Sardeshpande, Indian J. Anim. Sci. and oestradiol-17R during the oestrous cycle in mares. a:524-526 (1985). 31. Hintz, H. F., Hintz, R. L., Lein, D. H., and VanVleck, L. D. Length of gestation periods in Thoroughbred mares. J. Equine Med. Surg. 1:289-292 (1979). 32. Law, J. Diseases of the generative organs. jp: Melvin, A. D. (ed). Diseases of the Horse. U. S. Government Printing Office, Washington, D.C., 1923, pp. 164-209. 33. Ewbank, R. Predicting the time of parturition in the normal cow: a study of the precalving drop in body temperature in relation to the external signs of imminent calving. Vet. Rec. 75:367-371 (1963). 34. Porterfield, I. D. and Olson, N. 0. Vaginal temperature of dairy cows before after calving. J. Am. Vet. Med. Assoc. &l1381-382 (1957). 35. Dufty, J. H. Determination of Australian Vet. J. 47:77-82 (1971).
the
onset
36. Ewbank, R. The fall in rectal temperature Reprod. Fertil. 19:569-571 (1969).
of
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seen before
in Hereford
parturition
37. Winfield, C. G., Makin, A. W., and Williams, A. H. Prediction parturition in sheep. Australian Vet. J. 49:549-553 (1973).
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39. Littledike, E. T., Witzel, D. A., and Riley, J. L. Body temperature changes sows during the periparturient period. Lab. Anim. Sci. 29:621-624 (1979).
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Cox, J. E. Rectal temperature as an indicator mare. Equine Vet. J. 1:174-176 (1969).
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38. King, G. J., Willoughby, R. A., and Hacker, R. R. Fluctuations temperature of swine at parturition. Can. Vet. J. u:72-74 (1972).
40. Wright, J. G. Parturition
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(1943). in the
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42. Jeffcott, L. B. Observations 4:209-213 (1972).
on parturition
Progesterone concentrations 43. Smith, I. D. during pregnancy. Res. Vet. Sci. ul14-116
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pony mares.
in the peripheral (1974).
plasma
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of the mare
44. Burns, S. J. and Fleeger, J. L. Plasma progestagens in the pregnant mare in the first and last 90 days of gestation. J. Reprod. Fertil. a(supplement):435-439 (1975). 45. Kaminski, R.P., Forster, H.V., Bisgard, G.E., Pan, L.G., and Dorsey, S.M. Effect of altered ambient temperature on breathing in ponies. J. Appl. Physiol. sS:l5851591 (1985). 46. Pan, G. L., Forster, H. V., and Kaminski, R. P. Arterial vs rectal temperature in and thermal stresses. ponies: rest, exercise CO2 inhalation, J. Appl. Physiol. 6_1:1577-1581 (1986). 47. Nieburgs, H. E., Kupperman, H. S., and Breenblatt, R. B. Studies on temperature variations in animals as influenced by the estrous cycle and the steroid hormones. Anat. Rec. p6:529 abstr. (1946). 48. Palmer, R. and Devillers, J. The ovarian cycle and utilization of the thermic curve for the diagnosis of the date of ovulation. Compt. rend Sot. franc de gynec. 9:60 (1939). 49. Mocquot, P. and Palmer, hormones and in menstrual Presse med. 48:305 (1940).
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51. Nieburgs, H. E. Body temperature - A diagnostic aid in menstrual sterility. J. Obstet, Gynaecol. Br. Emp. =435-462 (1945). 52. Israel, S. C. and Schneller, Steril. 1:53-64 (1950).
0.
The thermogenic
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disorders
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and
Fertil.
53. Czaja, J. A. and Butera, P. C. Body temperature and temperature gradients: changes during estrous cycle and in response to ovarian steroids. Physiol. Behavior 26:591-596 (1986). 54. McEnvoy, G. K. (ed.). American Hospital Formulary Service Drug Information. American Society of Hospital Pharmacists, Inc., USA, 1984, pp. 1304-1306. 55. Zartman, D. L., Hallford, D. M., Tierney, L. A., and Hussain, M. Y. Reproductive characteristics of Holstein heifers fitted with intravaginal temperature transmitters. Theriogenology 19:541-554 (1983). 56. Clark, W. G., Lipton, J. M. Changes in body temperature amino acids, peptides, dopamine, neuroleptics and related Biobehav. Rev. 3299-371 (1985).
MAY 1999 VOL. 31 NO. 5
after administration of agents: II. Neurosci.
1019
EQUINE BODY TEMPERATURE AND PROGESTERONE FLUCTUATIONS DURING ESTRUS AND NEAR PARTURITION S.F. Ammons,l lDepartments
Received
W. R. Threlfalll
and R.C. Kline2
of Animal Science and Veterinary Clinical Sciences 2Department of Animal Science The Ohio State University Columbus, OH 43210
for publication: Accepted:
January Februaq
19, 1988 21, 1989
ABSTRACT
Body temperature and serum progesterone concentrations were measured in mares to determine if a change in either could be useful in predicting estrus, ovulation or parturition. There was no significant correlation (P > 0.1) between rectal temperature and the environmental temperature or progesterone concentration. Progesterone concentration did correlate with stage of estrous cycle and the stage of pregnancy. Significant differences (P < 0.05) in temperature were noted at different times throughout the day. No change in temperature occurred that could be utilized to predict estrus, ovulation or parturition. The changes in serum progesterone concentration were only useful in detecting estrus.
Key words:
temperature,
progesterone,
estrus, parturition,
equine
INTRODUCTION
The ability to accurately determine the time of ovulation and the time of parturition would greatly increase the conception rate and the birthrate of healthy foals. The reproductive cycle of the mare is subject to great variability. Mares usually demonstrate seasonal polyestrous behavior, yet 20 to 25% of them exhibit polyestrous behavior year round (1,2). Estrus usually lasts 5 to 6 d, however, when the mare is coming into or going out of winter anestrous, estrus may be much longer. Mares may also exhibit a split estrus or a silent heat. Some mares do not exhibit estrus while suckling their foals even though they may be ovulating regularly. The interval from the onset of estrus to ovulation is extremely variable. Since ovulation is related to the end of estrus, not the onset, predicting the time of ovulation is difficult (3). In the mare, the difficulty in determining when ovulation will occur is partially responsible for the poor reproductive performance observed in this species. An objective method of determining the time of ovulation is needed to overcome this problem. Equine parturition is also difficult to predict because of variable (3) and vast differences in the appearance and the intensity of the signs parturition (4-!I), which in mares is normally very rapid and strenuous. not provided immediately after the detection of a problem, the fetus placental separation. Therefore, it would be helpful to have a method capable of predicting when parturition will occur so that assistance could
MAY 1989 VOL. 31 NO. 5
gestation length of approaching If assistance is will die due to which would be be available.
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THERIOGENOLOGY
Body temperature and the level of circulating progesterone have been studied and suggested as possible predictors of estrus, ovulation, and parturition in several domestic species and in the human. For example, increases in the rectal and vaginal temperature of cattle have been related to estrous behavior (9-17). A decrease in body temperature has been noted on the day preceding estrus, with an increase in temperature the day of estrus (9,11,15,17). In the equine, progesterone concentrations in milk as well as in plasma have been found to be accurate methods of evaluating estrous cycle activity (l&19). Concentration of circulating progesterone in the plasma of mares reportedly fluctuates with the phases of the ovarian cycle, with a peak being exhibited during the luteal phase and a nadir during estrus or the follicular phase (20-30). Estrous behavior is not usually seen until progesterone concentration is less than or equal to 1 ng/ml (21,22,25,28,30). The lowest progesterone concentration is observed near ovulation. The average length of however, gestations as short normal foals. The ability to aid in the prevention of inadequate milk supply, foal
gestation in the mare ranges between 335 to 350 d (3); as 305 d (31) and as long as 400 d (32) have produced determine the time of parturition is of major importance to mare or foal death due to retained placenta, dystocia, suffocation, and the like.
In the other domestic species and in the human, much work has been done to investigate the correlation between body temperature and parturition. The body temperature of cows reportedly decreases prior to parturition (9,33-35). The highest temperature usually occurs between the second and fourth days before calving and averages 39.3”C (range 38.55 to 40.17”C). An average drop of 0.61”C (range 0.11 to 1.06”C) beginning an average of 54 h (range 74 to 33 h) before parturition has been noted. The temperature of sheep also decreases at parturition (36,37), while an increase in body temperature is associated with parturition in sows (38,39). Although the body temperature of the mare prior to parturition has been studied, the results have been Research in the mare does indicate that the progesterone inconclusive (40-42). concentration in the peripheral plasma drops prior to parturition (43,44). The purpose of this study was to determine if there is a change in body temperature that can be useful in predicting ovulation or parturition in the horse mare. The objectives were to 1) monitor the body temperature of nonpregnant cyclic mares from Day 1 of estrus through 3 d after the end of the following estrus, 2) monitor circulating progesterone levels of nonpregnant cyclic mares from Day 1 of estrus through 3 d after the end of the following estrus, 3) correlate the body temperature and progesterone level of nonpregnant cyclic mares with the time of ovulation, 4) monitor the body temperature of pregnant mares starting 2 wk prior to expected parturition through 3 d after the last day of foal heat, 5) monitor circulating progesterone levels of pregnant mares starting 2 wk prior to expected parturition through 3 d after the last day of foal heat, 6) correlate the body temperature and progesterone level of pregnant mares with the time of parturition and foal heat ovulation, 7) correlate the body temperature and progesterone level of all mares with the environmental temperature.
1008
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
MATERIALS
AND METHODS
Fourteen Registered Quarter Horse mares were used in this project. Mares were housed in 10 x 12 foot stalls at The Ohio State University Horse Barn. They had access Pregnant and nonpregnant mares were fed to free-choice water, salt and minerals. approximately 20 pounds of good quality alfalfa hay and nine pounds of 12% crude protein Countrymarka pellets daily, divided equally between morning and evening feedings. Mares with foals were fed approximately 20 pounds of good quality alfalfa hay and 16 pounds of 14% crude protein Countrymark pellets divided equally between Weather permitting, all mares and foals were allowed morning and afternoon feedings. outside for exercise, but were returned to their stalls at least 1 h before the next scheduled temperature reading. This study was conducted during the months of March, April and May 1987. Group 1 was comprised of four nonpregnant mares (one mare was 2 yr old, two mares were 3 yr old, and one mare was 7 yr old). The three oldest mares were treated orally with Altrenogest (10 cc Regu-mate)b daily for 12 consecutive days; On the thirteenth day, they were administered 10 mg of Prostaglandin F2 alpha (10 mg i.m. Lutalyse)c to induce cyclicity prior to the start of the study. Mares were monitored from the first day observed in estrus through 3 d after the end of their second estrus. Group 2 was comprised of ten pregnant mares, ranging in age from 5 to 17. The mares were monitored from 2 wk prior to the calculated due date (335 d following breeding) through 3 d after the last day of foal heat. Mares were teased daily to determine the beginning and end of estrus and palpated every other day during estrus to determine the day of ovulation. Ovulation was determined by the presence of an ovulation depression or a corpus hemorrhagicurn at the time of palpation. When an ovulation depression was detected, ovulation was said to have occurred at 6:00 a.m. that same day. When a corpus hemorragicum was detected, ovulation was said to have occurred at 600 a.m. the previous day. Rectal temperatures of all mares were taken four times daily (0000, 0600, 1200, 1800 h) with a high-speed digital thermometerd. The probe was inserted 14.5 cm into the rectum and held against the rectal wall for 30 sec. Jugular blood samples were collected daily (1200 h) from all mares for progesterone analysis. Following collection, blood was allowed to clot at room temperature for 30 min, then centrifuged at 6000 x g Serum was stored at -20°C until the time of assay. Levels of circulating for 15 min. progesterone were determined using a rapid Competitive Linked Immunoassaye developed for quantitative analysis of equine progesterone. The method for assay was followed as described by Cambridge Veterinary Sciences, except for a modification in a
Countrymark
b
American
c
The Upjohn
d
GLA Agricultural
e
Inc., PO Box 1206, Delaware,
Hoechst
Corporation,
Company,
Ovusure - Elanco
Products
MAY 1989 VOL. 31 NO. 5
43015.
Animal Health Division, Somerville,
Kalamazoo,
Electronics.
OH
MI
08876.
49001.
4743 Brooks Street, Montclair. Company,
NJ
Indianapolis,
IN
CA
91763.
46285
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THERIOGENOLOGY
the amount of stopping solution. The assays were run in duplicate, and a Socorexf micropipetter was used. The plates used had 96 wells precoated with sheep antiprogesterone serum, and filled with stabilizing buffer. First the plates were emptied and patted dry on paper towels. Ten microliters of standard (0.5, 1.0, 5.0, 10.0 and 30.0 ng/ml standards were used) or sample were added to each well. Then 200 ul of conjugate (progesterone-alkaline phosphatase) were added, the plates were covered and left to incubate at room temperature for 30 min. Plates were then emptied and rinsed three times with tap water. Two hundred microliters of substrate reagent (a solution of 1.0 M diethanolamine and 0.5 mM magnesium chloride at pH 9.8 to which three p-nitrophenyl phosphate tablets had been added) were added to each well. The plates were covered and left to incubate for 30 min at room temperature. Then 40 ul of stopping solution (0.5 M Di-potassium hydrogen orthophosphate and 0.5 mM EDTA) The plates were read on an EIA manual reader, model #EL 3078, at a were added. 405-nm wavelength. The reader was calibrated to zero before each plate was read. The data were analyzed using General and Student’s t-test, where appropriate.
Linear Models Procedure,
Mean Separation
RESULTS There was no significant correlation (P > 0.1) in the Group 1 nonpregnant mares between the rectal temperature and environmental temperature or the level of circulating progesterone. In the Group 1 nonpregnant mares (Figures 1 and 2) and in the Group 2 pregnant mares that were monitored during foal heat (Figure 3), the level of circulating progesterone correlated with the stage of the estrous cycle in that an increase 2 1 ng/ml Progesterone concentration continued to increase was noted the day after ovulation. until Day 5 after ovulation, and it ranged from 10 to 13 ng/ml on Day 5. Throughout the first estrus monitored, there was no significant difference (P > 0.05) in rectal During the second estrus temperatures of Group 1 at different times of the day. studied, there was a significant difference (P < 0.05) between the 0000 and 0600 rectal temperatures and the 1200 and 1800 h rectal temperatures. In Group 2, there was no significant correlation (P > 0.1) of rectal temperature with environmental temperature or with the level of circulating progesterone, but the level of circulating progesterone did correlate with the stage of late pregnancy (Figure 4). Progesterone was 2 12.5 ng/ml during the last 2 wk of gestation, dropped below 8 ng/ml within 1 d after parturition, and continued to decrease to below 3 ng/ml by 3 d after foaling. Pregnant mares monitored through parturition showed a significant difference (P < 0.05) between the 0000 and 0600 h rectal temperatures and the 1200 and 1800 h rectal temperatures. These same mares monitored during foal heat exhibited a significant difference (P < 0.05) in rectal temperature at 1800 versus the 0000, 0600, and 1200 h readings. The variables measured, environmental temperature, day, time of day, and level of circulating progesterone accounted for 20% of the variation in rectal temperature, as indicated by the general linear models procedure of statistical analysis.
f
Socorex ISBA SA, I020 Renens, Switzerland.
g
Bio-Tek
1010
Instruments,
Inc., I Mill Street, Burlington, VT
05401.
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
0l-P1
Figure 1.
MAY 1989 VOL. 31 NO. 5
Non-pregnant, First OvUlatlOn
Vertical
line
denotes
time of
ovulationa
1011
THERIOGENOLOGY
Group 1
Figure 2.
1012
Non-pregnant,
2nd Ovulation
Vertical line denotes time of ovulation.
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
Group 2
Foal Moat Oruhtlon
G 0’ 310. 25-
10
Figure 3.
11
12
11
14
1r
1m
20
Vertical line denotes time of ovulation.
MAY 1989 VOL. 31 NO. 5
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THERIOGENOLOGY
Group 2
20
P i! e 0 5
I J/
10
CA1
s
2
Figure
1014
P8rturltlon
r
4
3
4.
5
6
t
8
9
10
11
12
13
14
15
16
17
10
10
20
Vertical bar denotes day of parturition.
MAY 1989 VOL. 31 NO. 5
THERIOGENOLOGY
DISCUSSION There was no significant correlation (P > 0.05) between rectal temperature and environmental temperature in any of the mares. Our study was conducted in a heated barn during the months of March, April and May 1987, and the environmental temperature was maintained within a range of 5” to 27°C (mean 15°C). Since horses and ponies are homeothermic, they maintain a relatively constant body temperature that is independent of the environmental temperature (4546). This is important because if rectal temperature fluctuated as environmental temperature fluctuated, it would be extremely difficult to determine a significant change in rectal temperature in response to other variables. Any such response would be hidden within changes associated with the environmental temperature. There was no significant correlation (P > 0.05) between rectal temperature and level of circulating progesterone. Although contradictory results have been obtained in cattle (9) and rats (47) and in women (48-52), individual differences within species have been shown to affect the action of progesterone on temperature regulation (53). Progesterone has a short plasma half-life of several minutes (54). More frequent analysis of progesterone concentration may have revealed a higher correlation between level of progesterone and rectal temperature. Rectal temperatures were recorded four times daily, while blood was drawn only once a day for progesterone analysis. Rectal temperature was shown to be significantly different (P < 0.05) at different times of the day, and in a study by Niekerk (24), mean progesterone concentration was significantly higher (P < 0.025) in the morning than in the evening (24). Analysis of progesterone at the time of each temperature recording may have provided a more accurate assessment of the correlation between rectal temperature and progesterone. Circulating progesterone concentration correlated with stage of the estrous cycle as an increase > 1 ng/ml was noted the day after ovulation in both groups of mares (Figures 1, 2 and 3). Progesterone concentration continued to increase until Day 5 after ovulation and ranged from 10 to 13 ng/ml on Day 5. This is in agreement with the results obtained by Plotka (29), and is important as a means of varifying recent ovulation. The concentration of circulating progesterone correlated with the stage of late pregnancy in all Group 2 mares (Figure 4). Progesterone was z 12.5 ng/ml during the last 2 wk of gestation, dropped below 8 ng/ml within 1 d after parturition, and continued to decrease to below 3 ng/ml by 3 d after foaling. Progesterone concentration is high during the last 2 wk of gestation, apparently because of the placental production of progesterone. At parturition, the placenta is expelled and a decrease in progesterone occurs. In Group 1 mares, there was no significant difference (P > 0.05) in rectal temperature at different times of the day during the first estrus monitored. There was a significant difference (P < 0.05) between the 0000 and 0600 h rectal temperatures and the 1200 and 1800 h rectal temperatures during the second estrus of the nonpregnant The first estrus monitored was within the first cycle of the breeding season. mares. The first cycle during the transitional period from winter anestrus to the breeding season is often very different from later cycles in the breeding season. In addition, three of the mares were treated orally with Altrenogest (10 cc) daily for 12 consecutive days followed by prostaglandin F2 alpha administration (10 mg i.m.) 13 d prior to the first estrus. No hormonal treatments were administered between the first and second Perhaps the administration of the altrenogest or the prostaglandin F2 estrus studied. alpha or the two in combination suppressed the temperature difference that was
MAY 1989 VOL. 31 NO. 5
1015
THERIOGENOLOGY
exhibited during the second estrus. In support of this, researchers found that heifers that were treated with prostaglandin F2 alpha did not exhibit the usual temperature increase during the induced estrus (55). The Group 2 pregnant mares that were monitored through parturition also exhibited a significant difference (P < 0.05) between the 0000 and 0600 h rectal temperatures and the 1200 and 1800 h rectal temperatures. However, these same mares, when monitored through foal heat, exhibited a significant difference (P < 0.05) in rectal temperature at the 1800 h reading. It is clear that there are many variables that affect temperature regulation. Of the variables that were monitored in our study, there is a need to evaluate not only the length of time between blood collection for progesterone analysis, but also the length of time between temperature recordings. An increased body temperature of 0.5”C (P 5 0.05) has been reported in ponies within 6 min of the start of exercise (46). Additionally, acepromazine, azaperone and D-Ala2-Met-enkephalinamide have been reported to cause body temperature changes in horses of 0.9” to 3.O”C in periods ranging from 20 min to 3 h following treatment (56). From this, it is apparent that horses and ponies can experience temperature changes within a short period of time. Thus, 6-h temperature readings may be inadequate. This may have accounted for much of the 80% of the temperature variation which was not accounted for by the variables measured (environmental temperature, day of the cycle, time of day and circulating progesterone). In our study, no change in rectal temperature was apparent that could be used to predict estrus, the time of ovulation or the time of parturition in the horse mare. Additional studies are needed to determine if more frequent temperature recordings or the determination of other presently unknown variables affecting temperature would permit this technique to be utilized for ovulation and parturition prediction in the horse mare. REFERENCES
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