Changes in Rectal Temperature During the Normal Oestrous Cycle in the Beagle Bitch

Changes in Rectal Temperature During the Normal Oestrous Cycle in the Beagle Bitch

Br. vet. ]. ( 1970), 127, 93 CHANGES IN RECTAL TEMPERATURE DURING THE NORMAL OESTROUS CYCLE IN THE BEAGLE BITCH BY D. w. CHRISTIE AND E. T. BELL...

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Br. vet. ]. ( 1970), 127, 93

CHANGES IN RECTAL TEMPERATURE DURING THE NORMAL OESTROUS CYCLE IN THE BEAGLE BITCH BY

D.

w.

CHRISTIE AND

E. T.

BELL

Endocrine Unit, Petfoods Limited, Melton Mowbray, Leicestershire

SUMMARY

Changes in the body temperature of nine beagle bitches were recorded during the oestrous cycle commencing early in proestrus and continuing into metoestrus. Vaginal smears were collected and plasma progesterone determinations made during the study. Most animals showed a thermal nadir during oestrus followed by a rise and a period of higher temperature values; there was no close correlation between the timing of changes in vaginal cytology and progesterone levels and that of the nadir. The bitch does not show a typical hi phasic temperature pattern as seen in women and it seems unlikely that the parameter will prove useful in predicting the stage of the canine oestrous cycle. INTRODUCTION

A good deal of attention has been paid to the changes that occur in the basal body temperature of the normal menstruating woman (see Marshall, Ig6s; Brown, I g6s ). It is well established that during the follicular phase the basal temperature remains low until at approximately mid-cycle the temperature rises sharply over a period of normally two days often by as much as I °F; this higher level is generally maintained until the onset of the next menstrual loss. The temperature rise, when it is greater than 0·4 °F, is considered to be indicative of the occurrence of ovulation. This biphasic pattern is the one most commonly seen though on occasions the temperature rise may extend over a number of days or may even show a step-wise upward progression. No information is available on the nature of temperature changes occurring during the normal oestrous cycle in the bitch. The aim of this investigation is to examine temperature changes occurring in the beagle bitch from early in proestrus until during metoestrus. MATERIAL AND METHODS

The study to be reported was conducted on nine beagle bitches during the period of a normal oestrous cycle. Seven of the animals-I66, I67, 202, 204, 237, 240 and 242-were parous and from three to five years of age; two animals, I20 and I28, were approximately one year old and were studied during their first oestrous cycle. All animals were housed in a controlled environment kennel at a temperature of 55 o to 6o °F and with ten to twelve air changes per hour. The animals were provided with an electrically heated concrete sleeping area which was set at a temperature of 80 °F throughout the period of the test.

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All body temperatures were taken with a thermometer manufactured by Brannan Ltd., London. The temperature scale extended from 95 o to I 03 °F with divisions ofo·I all readings were made to the nearest o·I °F. The thermometer was smeared with petroleum jelly and introduced up to 2 inches into the rectum and readings were made after an insertion time of at least one minute. In a preliminary study the rectal temperature in four animals in anoestrus was recorded. The recordings were made hourly between o8·45 and I6·45 h, each day for four days. All animals were fed at 09.00 h and exercised at 09.I5 and I6.oo h. It was found that most animals showed the highest temperature of the day at the 9·45 or 10.45 recording; generally the temperature then fell, reaching lowest levels at I 4·45 or I 5·45 h. At I 5·45 the range of temperature variation over the four days was for the four anoestrus animals 0.2, 0.2, 0.2 and 0.4 °F. All temperature readings in the study presently reported were taken between I5.30 and I5·45 h. Vaginal smears were taken from all animals in the study on a weekly basis, until they showed first signs of vulval bleeding, when smears were taken three times each week for three weeks and then two times per week for a further three weeks. The method of collection and staining was as described by Christie, Bailey & Bell ( I 970). Blood samples were also taken from six animals in the experimental group twice per week and assays for plasma progesterone were conducted (Horth, Bell, Christie & Palmer I970). 0

;

RESULTS

The results of temperature recordings are shown in Fig. I. The fixed point for the presentation of these data (day o) is the first day of female standing (B) as determined in behavioural tests and this may be defined as the day on which the female stands in a receptive manner and continues to stand for at least a further two days. Each horizontal line represents the mean temperature value for the individual animal. During the period of study all subjects showed a marked variation in temperature. The mean range for the group during the study was I·52 °F with the highest figure for range being 2·I °F (bitch 240) and the lowest I·0 °F (bitch 202). Bitches 242, 202, I67, 204 and I28 exhibited a thermal nadir during the period of oestrus from day +I to +8, which was followed by a phase of temperature rise extending over a period of from 4 to 6 days. The mean temperature rise during this phase for the five bitches was I ·02 °F with a range of from o·8 ° to I ·2 °F. Following the termination of the rise the temperature in bitches 202, I67 and 204 was maintained at a level at least 0·4 °F above the thermal nadir reading in oestrus for a mean of I4·6 days. Animals 242 and I 28 did not show a temperature recording below a level of I ·o and o·6 °F respectively above the nadir after termination of the phase of temperature rise. The phase of elevated temperature was seen in each of the five bitches mentioned above in late oestrus and early metoestrus. Bitch I66 showed two distinct low temperature readings during oestrus, the second being followed by a period of temperature elevation in late oestrus

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and early metoestrus. Bitch 240 showed a fluctuating temperature pattern in oestrus with a temperature nadir at day +Io. This was followed by an irregular rise extending over seven days; the level of o·4 °F above the nadir was maintained for ten days. Bitch I 2o: showed no thermal nadir in oestrus which was followed by a subsequent period of temperature rise. Bitch 237 showed a generally declining temperature pattern throughout oestrus with only short phases of temperature rise in metoestrus which were not maintained.

204

101•8 101 ·4 10/0 10 06 100·2 /030

~ 102·6 102·2 /0/•8 /01 ·4 10/0 1006 /0 2·2 101 ·8

t

/0 /•4 I 0 l oQ

Day of study

Fig. 1. Changes in daily rectal temperature in the beagle bitch during the oestrous cycle. A = first day of bleeding, B = first day of female standing, C = last day of female standing.

Results of the vaginal cytology determinations and the assay of plasma progesterone are shown in Table I. With respect to vaginal cytology the timing of the peak eosinophilic index (E.I) values are only recorded where such a peak was clearly visible. The progesterone results indicate the day on which plasma levels first exceeded IO ngfml. In all cases the progesterone rise represented at least a two-fold increase over basal levels and formed the initial part of the major rise to high progesterone levels ranging from 20-40 ngfml.

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TABLE I DATA ON VA G INAL C YTOLO G Y AND PLA S MA PROGE S TERONE LEVEL S IN NI N E BEA G L E BITCHE S D AY 0 = TH E FIRST DAY OF FEMAL E STANDIN G

Bitch No.

Day qf eosinophilic index peak

+7

N.A.

+s +8 +g

-3

N.A. N .A. N.A. = no t

+3

+8

N.A.

.A.

Day progesterone level first exceeds 1 o ngfml

+7

N.A. N.A. 0

+g +3

available DISCUSSIO N

The results presented in this paper suggest that the bitch does not, as does the human female, show a clearly established biphasic pattern in body temperature during the reproductive cycle. The data are not entirely comparable with the basal body temperature results normally obtained in women by oral measurement immediately after awakening, since in the bitch the recordings were made by rectal measurement during the afternoon. The decision to take temperature recordings at between I5.30 and I5·45 h was based on the results of the preliminary experiment which suggested that it was at this stage of the day when values were most settled. In women the pre-ovulatory and post-ovulatory temperature plateaux can be demonstrated irrespective of the choice of recording time (Southam & Gonzaga, I965 ) ; it is therefore clear that oral basal body temperature recordings are not a prerequisite for the demonstration of the biphasic temperature pattern. The variation in temperature during the oestrous cycle study was greater than that seen in the four animals studied in anoestrus, the mean ranges being I·62 °F and o·25 °F respectively. Since in both groups the temperatures were taken at the same period during the day, that is, from I5.30 to I5·45 h, it suggests that the onset of the oestrous cycle heralds a period of wider temperature fluctuation on a day-to-day basis when compared to the situation in the reproductively inactive bitch. Five of the bitches showed a single temperature nadir during oestrus which was followed by a rise and a subsequent plateau for at least I4 days. Two other animals showed a similar rising temperature pattern but exhibited two separate low levels during the period of oestrus. The phase during which the temperature rose after the nadir, which extended for at least four days, is probably somewhat longer than that observed in women. However, in a small proportion of women the temperature rise may extend over a number of days and occasionally show a step-wise upward progression (Brown, I965 ). It is possible that this extended rise is associated with the retarded growth of the corpus luteum due to the unduly prolonged period of escape of follicular fluid after rupture (D ecker, I 95 I) . The results

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in the bitch do not show a phase of lowered pre-ovulatory temperature values which may be compared to that seen in the follicular phase in women. The low temperatures during the follicular phase are considered to be due to the temperature depressing activity of oestrogens and the thermogenic action of progesterone has been considered to be the cause of the luteal phase elevation (see Pincus, I 965). Of the eight bitches in which sufficient results in proestrus were available for evaluation, seven had some relatively high values compared with the subsequent oestrus values and those in early metoestrus, while four of them showed the highest readings of the total study during proestrus. In the human female the relationship between the exact time of ovulation and the changes in basal body temperature are controversial. However, it is generally accepted that there is a close relationship. Griffiths & Amoroso (I 939) have suggested that ovulaton in the bitch occurs during days I and 2 of oestrus. The results presented suggest that there is some degree of correlation between the temperature nadir and the phase of oestrus. Bitches I 28, 204 and I 67 showed the nadir on days I or 2 of oestrus, while bitch 242 showed a significant fall in this period. On the other hand, the results presented for the rise in progesterone values do not confirm that a close correlation exists between the increased secretion of this hormone and the time of change in body temperature. It may be that in a species where multiple ovulation is the norm the time relationship between increased progesterone production and temperature changes is modified. The E.I. peak value which bears some relation to the release of endogenous oestrogen is also not correlated with temperature rise. This is not surprising since it is well established that in the human female the relationship between the peak values of oestrogen production during the normal menstrual cycle are not closely related temporally to the occurrence of ovulation (see Bell & Christie, I 97 I). In some women an ovulatory cycle is not accompanied by any evidence of temperature change (Brown, Klepper & Loraine, I958) while conversely a typical biphasic pattern may be observed where ovulation is shown not to have occurred by assay of hormone levels (Brown, Fotherby & Loraine, I962). Such findings suggest that the relationship between temperature change and ovulation is not absolute. It is, however, certainly a parameter with a wellestablished use in man but the results presented here suggest that it is not likely to be useful in predicting the stage of the oestrous cycle in the bitch.

REFERENCES

BELL, E. T. & CHRISTIE, D. W. ( I97I). Steroidologia., in press. BROWN, J. B., FoTHERBY, K. & LoRAINE, J. A. (I962). ]. Endocr., 25, 331. BRowN,]. B., KLOPPER, A. & LoRAINE,]. A. (I958) . ]. Endocr., 17,401. BROWN, P. F. E. ( I965 ) . Practitioner 194, 525. CHRISTIE, D. W., BAILEY,]. B. & BELL, E. T. (I970) . Vet. Rec., 87, 265. DECKER, A. (I95I). Fert. Steril., 2, 253. GRIFFITHS, W. F. B. & AMoRoso, E. C. (I939). Vet. R ec., 51, I279· HORTH, C., BELL, E. T., CHRISTIE, D. W. & PALMER, R . F. (I970). Proc. Third Int. Gong. on Horm. Steroids, p. I03. Amsterdam: Excerpta Medica Foundation. MARSHALL, J. ( I965 ). Planning for a Family. London: Faber.

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PINcus, G. (1965). The Control of Fertility. New York: Academic Press. SouTHAM, A. L. & GoNZAGA, F. P. (1965) . Am.]. Obstet. Gynec., 91 , 142.

Acceptedfor publication 22 September 1970 Changements de Ia temperature rectale pendant le cycle normal de I' oestrus chez Ia chienne Bigle (Christie et Bell) Reswne. On a enregistre les changements de temperature du corps de neuf chiennes bigles pendant le cycle de !'oestrus en commenc;ant tot au cours du proestrus et en continuantjusque dans le metoestrus. On a preleve des frottis vaginaux et fait des determinations de la progesterone dans le plasma au cours de cette etude. La plupart des animaux presentaient un nadir thermal pendant !'oestrus suivi d'une augmentation et d'une periode ou les temperatures avaient des valeurs plus elevees; il n'y avait aucune correlation etroite entre le moment des changements cytologiques du vagin et des taux de progesterone et celui du nadir. La chienne ne presente pas un diagramme de temperature biphasique typique comme on !'observe chez les femmes et il semble peu probable que ce parametre puisse servir a prevoir le moment du cycle de !'oestrus de la chienne. Veranderungen der rektalen Temperatur wiihrend des nonnalen Menstruationzyklus bei Spiirhunden (Beagles) (Christie und Bell) ZusaDllnenfassung: Veranderungen der Korpertemperaturwurden bei neun Beagle-Hundinnen wahrend des Menstruationszyklus fest-gestellt. Die Beobachtung begann im Beginn des Praemenstruums und wurde bis Mitte des Zyklus fortgesetzt. Vaginalabstriche und Progesterongehalt des Plasmas wurden untersucht. Die meisten Tiere hatten einen Temperaturabfall wahrend des Oestrus, dem ein Ansteigen und eine Periode hoherer Temperatur folgte. Eine definitive Beziehung zwischen dem Eintreten von zytologischen Veranderungen in den Abstrichen sowie den Progestronkonzentrationen und dem Sinken der Temperatur konnte nicht festgestellt werden. Die Hiindin hat nicht den biphasischen menschlichen Temperaturtypus und es ist unwahrscheinlich, class der Parameter von Nutzen sein kann, urn das Stadium des Menstruationszyklus beim Hunde vorauszusagen. Cambios en Ia temperatura del recto durante el ciclo normal de celo de Ia perra sabuesa (Christie y Bell) Reswnen. Se registraron cam bios en la temperatura corporal de nueve perras sabuesas durante el ciclo estroso, empezando temprano en el proestroso y continuando hasta el metoestroso. Se recogieron frotis vaginales y se efectuaron determinaciones de la progesterona del plasma durante el estudio. La mayoria de los animales mostraron un nadir termico durante el celo, que fue seguido por una subida y un periodo de valores de temperatura mas elevados; no existi6 una exacta correlaci6n entre el tiempo de los cambios en la citologia vaginal y los niveles de progesterona y el del nadir. La perra no muestra un patr6n tipico de temperatura bifasica como sucede con la mujer, y no parece probable que el parametro sera uti! para predecir la etapa del ciclo de celo canino.