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.
Use of Temperature to Evaluate Ovulation in Mares                                                  271

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