Utilizing Body Temperature to - Evaluate Ovulation in Mares
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The Professional Animal Scientist 23 (2007):267–271 Utilizing Body Temperature to Evaluate Ovulation in Mares M. C. Bowman,*1 M. M. Vogelsang,* P. G. Gibbs,* B. D. Scott,* E. M. Eller,* C. Honnas,† and K. Owen‡ Departments of *Animal Science and †Veterinary Large Animal Clinical Science, Texas A&M University, College Station 77843 and ‡Electronic ID, Inc., Cleburne, Texas 76033 lation. No difference was found in rectal thy and Rockette, 1986). Palmer ABSTRACT temperature in relation to the presence or (1950) found that the diurnal fluctua- absence of a follicle. Under specific cir- tions of body temperature were much Although reproductive technology has cumstances, temperatures obtained using greater on the day of ovulation in added many dimensions to the horse the microchip were higher (P < 0.05) women, even in those sleeping con- breeding industry, less invasive and more prior to ovulation compared with those tinuously. This was presumed due to efficient methods of evaluating follicular temperatures collected immediately fol- the onset of the formation of the cor- development and ovulation would be ben- lowing ovulation. pus luteum and subsequent progester- eficial to both the commercial breeder one excretion. A similar phenome- and private horse owner. Because of the Key words: follicle, mare, ovulation, non is also apparent in cattle as inves- highly variable estrous cycle of the mare, body temperature tigated by Wrenn et al. (1958), who it is difficult for breeders to coordinate in- concluded that body temperature is semination with ovulation, and much time is invested in evaluation via palpa- INTRODUCTION lowest prior to estrus, high on the day of estrus, and then low again at tion, ultrasound, and teasing. In both The extended and variable estrus of the time of presumed ovulation. The dairy cattle and women, a significant the mare makes it difficult to predict body temperature then returned to a change in body temperature has been ovulation accurately for timed insemi- higher state during the luteal phase, measured during the hours immediately nation. Breeders rely on teasing, pal- which was apparently related to in- prior to ovulation. Research exploring the pation, and ultrasonography to evalu- creased progesterone secretion. relationship of body temperature and ovu- ate follicular development. However, In cattle and humans, temperature lation in horses has been limited to one these methods can be time consum- fluctuations have been established as study in which no relationship between ing and, at times, dangerous. Al- a useful tool in predicting ovulation; temperature and ovulation was identi- though alternatives to predict ovula- however, research conducted to inves- fied. The current study utilized 38 ma- tion such as the use of serum oes- tigate this phenomenon in horses has ture mares and was conducted during trone sulfate and progesterone levels been limited. If this inexpensive, sim- the physiologic breeding season. Each have been investigated, Koskinen et ple, and safe technique was also appli- mare was implanted in the nuchal liga- al. (1989) ultimately reported the cable to horses, the breeder’s time, en- ment with a microchip capable of re- most accurate method was the size, ergy, and other resources could be uti- porting body temperature, and rectal tem- shape, and consistency of the follicle lized more efficiently. peratures were obtained using a digital and the degree of relaxation of the Ammons et al. (1989) investigated thermometer. Once an ovulatory follicle cervix. the utilization of temperature fluctua- was detected using ultrasonography and As reported by McCarthy and Rock- tions and progesterone concentra- the mare was exhibiting signs of estrus, ette (1986), Van de Velde (1904) re- tions to predict ovulation in the the follicle size and temperature were re- ported the relationship between body mare. They found no significant corre- corded approximately every 6 h until ovu- temperature and the menstrual cycle lation between the rectal tempera- in women, and the utilization of tures and the circulating progesterone tracking fluctuations in body tempera- level. Further, although significantly 1 Corresponding author: CoralSB123@ ture to predict ovulation has been im- different rectal temperatures were aol.com plemented since the 1940s (McCar- noted throughout different times of
268 Bowman et al. the day, Ammons et al. (1989) con- times daily using both the microchip ovary, and 2.6% ovulated from both cluded that under these experimental and digital thermometer. Addition- ovaries during the same cycle. These circumstances, there was no change ally, ovarian activity was evaluated results are consistent with the data re- in temperature that could be used to via ultrasound approximately every 6 ported by Andrews and McKenzie predict estrus or ovulation. h (approximately 0900, 1200, 1800, (1941), Osborne (1966), Arthur and 2400 h) to track the develop- (1969), Ginther et al. (1972), Belling MATERIALS AND METHODS ment of the Graafian follicle and (1984), Koskinen et al. (1989), and eventual ovulation. Detection of ovu- Shirazi et al. (2004). lation was the termination point for Furthermore, ovulation seemed to The current study utilized 38 ma- observations. occur more frequently during the ture cycling American Quarter Horse The data were interpreted using AN- night periods than during the day. mares and was conducted during the OVA in the STATA (Version 8) statisti- Ovulation occurred in 72.2% of cy- physiologic breeding season (March cal program (StataCorp, 2005). In cles at night, with 38.9% occurring to August) for the Northern Hemi- those cases where a significant differ- between 1800 and 2400 h and 33.3% sphere. All mares were from the ence (P < 0.05) was indicated, further occurring between 2400 and 0900 h. breeding herd at Horse Center and analysis was conducted using the Of the ovulations that occurred dur- were managed consistently regarding modified Fishers test, Fisher-Hayter ing the day, 2.8% occurred between routine vaccinations, deworming, and pairwise comparison, or 2-sample t- 0900 and 1200 h and 25% occurred hoof care. During the study, all test. between 1200 and 1800 h. This is horses were maintained at the Horse supported by Witherspoon and Tal- Center in accordance with the Institu- RESULTS AND DISCUSSION bot (1970) who reported that the ma- tional Agricultural Animal Care and jority of ovulations occur between Use Committee (AUP #2004-32). 2300 and 0700 h. However, several The mares were fed a commercially Ovulation Data studies (Ginther et al., 1972; Koski- formulated concentrate of 13% CP The mares utilized in this study nen et al., 1989) reported ovulations twice daily at an amount to fulfill or ovulated more frequently from the occurring equally throughout the exceed nutritional requirements for re- left ovary than from the right ovary. day. productive function as outlined by Of the 38 cycles observed, 63.2% of Pronounced changes in follicular ge- the NRC (1989). To provide adequate the mares ovulated from the left ometry were also noted prior to ovula- roughage, the mares were housed on ovary, 34.2% ovulated from the right tion. Most follicles were symmetrical pasture with free-choice grass or hay of similar qualities. All mares also had ad libitum access to water. Before the onset of data collection, each mare was implanted in the nu- chal ligament with a microchip con- taining a unique alpha-numeric iden- tification code and temperature sens- ing capabilities (Electronic ID, Inc., Cleburne, TX). Microchip informa- tion was collected using a specialized scanner (Digital Angel Corporation, South St. Paul, MN). Rectal tempera- tures were obtained using a conven- tional digital thermometer. The mares were evaluated for signs of estrus every Monday, Wednesday, and Friday in conjunction with the regular breeding activities at the Horse Center. Once signs of behav- ioral estrus (increased interest in a stallion, frequent urination in the presence of a stallion, winking of the vulvar lips, squatting, and tail raising) were observed and the presence of a preovulatory follicle (> 35 mm) was Figure 1. Temperature (°C) change of cycling mares throughout 4 time-of-day periods (1 = 0001 detected, temperature was recorded 4 to 0900 h; 2 = 0901 to 1200 h; 3 = 1201 to 1800 h; 4 = 1801 to 2400 h).
Use of Temperature to Evaluate Ovulation in Mares 269 ples have differing results, they sug- Table 1. Rectal and microchip temperatures of cycling mares during 4 gest that any exogenous hormone times of day ± SEM treatment can potentially affect body temperature. Therefore, the results re- Time-of-day period Rectal temperature (°C) Microchip temperature (°C) garding the presence of a significant 1 (0001 to 0900 h) 36.7 ± 0.89a 38.0 ± 0.14a diurnal effect are supported by the 2 (0901 to 1200 h) 37.6 ± 0.04a,b 38.3 ± 0.09b findings of Ammons et al. (1989). 3 (1201 to 1800 h) 37.8 ± 0.02b 38.5 ± 0.05b This diurnal variation may prove to 4 (1801 to 2400 h) 37.7 ± 0.03b 37.6 ± 0.12c have a confounding effect on at- tempts to utilize temperature data as a–c Values in same column with different superscripts are different (P < 0.05). a tool to predict ovulation, as it could mask the slight changes that may be exhibited prior to ovulation. during growth but became more non- than period 4 temperature. Also, Temperature Changes Pre- spherical immediately prior to rup- mean temperatures in periods 2 and ture. This change in geometry was and Postovulation 3 were higher than period 4 mean most notable in the 3 d prior to ovu- temperature (P < 0.01). There was no difference in rectal lation, which was also seen by Gastal In a similar study, Ammons et al. temperature related to the presence et al. (1998), and has been attributed (1989) saw no diurnal effect during or absence of a preovulatory follicle. to a decrease in the fluid pressure the first estrous cycle but found a sig- However, with the values obtained us- within the antrum of the follicle nificant effect in the second cycle. ing the implanted microchip, temper- (Townson and Ginther, 1989; Pierson They speculated that the first cycle’s atures were higher (P < 0.05) when a and Ginther, 1990). effect was possibly masked by a previ- follicle of greater than 35mm was ous altrenogest and prostaglandin F2α present (Table 2) when compared Diurnal Temperature Fluctuations treatment used to induce cyclicity as with the temperatures collected fol- no treatment was administered be- lowing ovulation. This may indicate Rectal temperature was very tween the first and second cycle. This that temperature drops slightly follow- strongly correlated with temperature theory is supported by additional re- ing ovulation and is only reflected reported by the microchip (r = search conducted in the human, rat, with the microchip because of the ex- 0.9962, P < 0.0001). It was important and cow. Not only is body tempera- treme sensitivity of the implant (lo- to establish whether a significant diur- ture higher during pregnancy in the cated in a more static environment) nal temperature fluctuation was pres- human (Palmer, 1950) when natural and its ability to more closely reflect ent in the equine body as this could progesterone levels are increased, but minute changes in body temperature. influence the significance of tempera- exogenous progesterone causes an in- This may be helpful to breeders by ture data collected relative to ovula- crease in body temperature in both in- confirming that ovulation success- tion. To accomplish this, both the rec- tact and ovariectomized women (Fi- fully occurred, therefore reducing the tal and microchip temperatures were scher, 1954; Gianavoli and Moggian, need for unnecessary palpation or ul- recorded approximately every 6 h 1954; Cohen et al., 1956) and in trasonography following breeding or throughout estrus. For ease of analy- ovariectomized rats (Nieburgs et al., insemination. However, the differ- sis, each day was divided into 4 peri- 1946). Zartman and DeAlba (1981) ence (P < 0.05) between pre- and post- ods: period 1 = 0001 to 0900 h, pe- demonstrated that heifers treated ovulatory temperatures obtained us- riod 2 = 0901 to 1200 h, period 3 = with prostaglandin F2α did not ex- ing the microchip was only seen in 1201 to 1800 h, and period 4 = 1801 hibit the normal temperature increase period 1 (0001 to 0900 h). Many of to 2400 h. A significant difference during estrus. Although these 2 exam- the ovulations were first discovered was found between several of the daily periods in both the rectal and microchip temperatures. As illustrated in Figure 1 and Table 1, the mean rec- Table 2. Rectal and microchip temperatures in mares pre- and tal temperature in period 1 was lower postovulation ± SEM (P < 0.05) than in periods 3 and 4. A diurnal effect was also observed when Follicular status Rectal temperature (°C) Microchip temperature (°C) comparing the mean microchip tem- Preovulation 37.8 ± 0.07a 38.2 ± 0.05a peratures. Period 1 mean microchip Postovulation 37.8 ± 0.10a 37.9 ± 0.20b temperature was approximately one- half degree lower than periods 2 and Values in same column with different superscripts are different (P < 0.05). a,b 3 microchip temperatures, but higher
270 Bowman et al. the varying times of ovulation, fur- Table 3. Microchip temperature (°C) ± SEM by presence of follicle ther analysis was performed compar- separated by time-of-day period ing the temperature at the time ovula- tion was discovered and approxi- Time-of-day period mately 24 h prior, for “night” and 1 2 3 4 “day” ovulations separately. The Preovulation 38.13 ± 0.13 a 38.35 ± 0.10 a 38.51 ± 0.06a 37.67 ± 0.11a mares that ovulated at “night” did so Postovulation 37.59 ± 0.43b 38.11 ± 0.44a 38.34 ± 0 .13a 37.42 ± 0 .63a between 1800 and 0900 h, and those that ovulated during the “day” ovu- Values in the same column with different superscripts are different (P < 0.05) a,b lated between 0901 and 1759 h. No significant difference (P > 0.05) was found in the rectal or microchip tem- peratures, or in the “day” or “night” during this period because the major- tion were also analyzed for change in ovulations. Therefore, these data do ity of the mares ovulated between temperature corresponding with the not suggest any useful temperature 1800 and 0900 h the following morn- ovulation. Data were first analyzed change in the period 24 h prior to ing. Therefore, this observation was hour by hour from 48 h prior to the ovulation that could be used to pre- made immediately following ovula- discovered ovulation until 30 h post- dict ovulation. tion in many cases. If a temperature ovulation. When analyzed in these change does occur relative to ovula- hourly increments, no difference (P > tion, this would be the time period in 0.05) was found in either the rectal IMPLICATIONS which to expect to see the difference or the microchip temperatures. (Table 3). Because of the established Because of the variation among the Although the utility of temperature diurnal effect, it is possible that this times for data collection of each indi- fluctuations to predict ovulation is change in body temperature is related vidual, data were regrouped for evalu- questionable, this tool may be useful to diurnal fluctuation. There are tem- ation into 10 periods of 5 h each be- to confirm that ovulation has oc- perature fluctuations that can be used ginning 48 h prior to and extending curred. However, historical data on to predict or detect ovulation in postovulation (Table 4). After evalua- each individual must be collected to other species such as the human tion, no difference (P > 0.10) was correct for any temporary changes in (Greulich and Morris, 1941; Palmer, seen among any of the periods pre- temperature (possibly associated with 1950; McCarthy and Rockette, 1986) ceding ovulation in either the rectal weather, stress, exercise, feeding, diet, and the cow (Wrenn et al., 1958; Ku- or the microchip temperature. There- or hormonal patterns), resulting in maran et al., 1966; Clapper et al., fore, according to these analyses, frequent handling of mares at consis- 1990). there was no change in body tempera- tent intervals throughout a 24- to 48- ture in relation to these time incre- h period. At large commercial facili- ments prior to ovulation that could ties, breeders may find this less effi- Temperature Changes cient than palpation or ultrasound, es- be utilized to help predict ovulation Immediately Prior to Ovulation pecially if they already have the nec- (Table 4). Data related to the time immedi- To compensate for the previously essary resources for those procedures ately preceding and following ovula- established diurnal fluctuation and at their disposal. Additionally, having microchips capable of radiotelemetric transmission with the data readily in- terpreted by computer algorithms for Table 4. Microchip and rectal temperature (°C) ± SEM by 5-h the breeder to evaluate would in- incremental ovulation periods crease efficiency for the industry. As available temperature-capable mi- Ovulation period Microchip temperature Rectal temperature crochip technology improves, utiliza- 48 to 43 h preovulation 38.18 ± 0.27 37.78 ± 0.04 tion of body temperature changes to 42 to 37 h 38.24 ± 0.29 37.78 ± 0.06 predict or confirm ovulation in the 36 to 31 h 38.20 ± 0.22 35.41 ± 2.31 mare may become an efficient man- 30 to 25 h 38.57 ± 0.18 37.97 ± 0.05 agement tool. 24 to 19 h 38.36 ± 0.09 37.71 ± 0.06 18 to 13 h 38.16 ± 0.20 37.72 ± 0.07 12 to 7 h 38.05 ± 0.18 37.65 ± 0.05 ACKNOWLEDGMENTS 6 to 1 h 38.51 ± 0.12 37.78 ± 0.08 0h 37.92 ± 0.29 37.74 ± 0.08 We would like to acknowledge Elec- Postovulation 37.81 ± 0.36 37.78 ± 0.05 tronic ID, Inc., Cleburne, Texas, and Digital Angel Corporation, South St.
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