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Contents

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References

The objective of this study was to determine sensitivity and specificity of a body temperature decline in bitches to predict parturition. Temperature loggers were placed into the vaginal cavity of 16 pregnant bitches on day 56–61 after estimated ovulation or first mating. This measurement technique has been validated previously and enabled continuous sampling of body temperature. The temperature loggers were expelled from the vagina before delivery of the first pup. The computed values for specificity (77–92%) were higher than sensitivity (53–69%), indicating a more precise prognosis of parturition not occurring. In conclusion, our findings may assist interpreting vaginal temperature measurements in order to predict parturition in bitches.


Introduction

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References

Monitoring the body temperature in clinical and research settings is a fundamental element within veterinary science (Goodwin 1998). For research purposes, methods for continuous measurement of body temperature are beneficial for obtaining more comprehensive data and reducing potential bias due to the handling of animals. The interest in the use of alternative techniques has been increasing (Quimby et al. 2009). One method of continuous body temperature measurement in cows utilized temperature loggers inserted into the vagina (Vickers et al. 2010; Burdick et al. 2011; Burfeind et al. 2011). A previous study assessed this measurement method in female dogs and demonstrated that the temperature loggers used provided accurate and reliable continuous temperature data (Maeder et al. 2012).

One parameter indicating impending parturition in dogs is a marked drop in body temperature approximately 24 h before whelping (Long et al. 1978; Johnston et al. 2001; Verstegen-Onclin and Verstegen 2008; England 2010; Linde-Forsberg 2010). Practitioners and owners are advised to monitor body temperature in bitches in order to improve prediction of parturition and to enable an early detection of potential dystocia (Kim et al. 2007; Johnson 2008; England 2010). Studies describing a temperature drop around the time of parturition in bitches relied on rectal temperature measurement twice daily or more (Concannon et al. 1977; Long et al. 1978; Tsutsui and Murata 1982). Another study by Veronesi et al. (2002), however, did not detect a temperature decrease in bitches before whelping. Due to some bitches not demonstrating a detectable temperature drop (Johnston et al. 2001), the accuracy in predicting parturition is negatively affected as stated by Luvoni and Beccaglia (2006). Therefore, the predictive value of a temperature drop in bitches around the time of parturition remains controversial (Long et al. 1978; Tsutsui and Murata 1982; Johnston et al. 2001; Michel et al. 2011). However, this evidence was based on rectal measurements only taken two to three times daily (Concannon et al. 1977; Long et al. 1978; Veronesi et al. 2002). Concannon et al. (1977) hypothesized that the prepartum hypothermia in bitches is most likely a response to the rapid changes in circulating hormone levels. He speculated that the prepartum decline in rectal temperature before parturition appeared to follow the decrease in progesterone by approximately 12 h. This event may represent the inability of thermoregulatory mechanisms to compensate for the rapid removal of the thermogenic effects of progesterone. A study by Veronesi et al. (2002) found no correlation between body temperature, plasma progesterone, cortisol and prostaglandin F2α in the periparturient bitch. Another study that investigated the endogenous and exogenous progesterone influence on body temperature in dairy cows (Suthar et al. 2012) detected greater vaginal temperature in cows with elevated progesterone concentrations due to pregnancy or progesterone supplementation. However, this study also found no existing correlation between serum progesterone concentrations and body temperature. Furthermore, as stated by Baan et al. (2005), it is not clear what triggers the onset of whelping in the dog in comparison with ruminants. Until now, there is no sound scientific proof as to why the temperature decreases before parturition. The lack of correlation between plasma progesterone concentration and body temperature suggests that progesterone could play only a partial role in a very complex mechanism.

The objective of this study was to record and document continuous vaginal temperature measurement in bitches before parturition and to calculate sensitivity and specificity of this measurement method for the prediction of parturition in bitches. Furthermore, simulations of measuring only once or twice daily were analysed for sensitivity and specificity for the prediction of parturition.

Material and Methods

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References

In total, 18 pregnant, privately owned bitches of different breeds were enrolled. Two bitches (breed: Cavalier King Charles) were excluded from analyses, due to a vaginal tumour and insufficient owner compliance, respectively. The participation of the bitches in this study was declared by informed consent of each owner. The breeds were as follows (n = 16): Beagle, Pomeranian, Pyrenean Mountain Dog, Golden Retriever, two Old English Bulldogs, Boston Terrier, Labrador Retriever, Hovawart, four Cavalier King Charles, Landseer, Dachshund and Staffordshire Bullterrier. The body weight and age ranged from 3 to 64 kg and from 2 to 6 years, respectively. Primiparous (n = 9) as well as multiparous bitches (n = 7) were included in this study. Pregnancy of the bitches was confirmed by ultrasonography between days 20 and 28 after ovulation (n = 9) or when this information was not available after first mating date (n = 7). The estimated day of ovulation was defined as the day when peripheral plasma progesterone level reached 4 ng/ml (Hase et al. 2000). A previously validated temperature logger (DST micro-T®, Star Oddi, Gardabaer, Iceland; Maeder et al. 2012) was inserted into the vagina of each of the bitches on day 56–61 after estimated ovulation or first mating date. The temperature loggers weighed 3.3 g and had a diameter of 8.3 mm and a length of 25.4 mm. The housing material consisted of implantable, biocompatible ceramic material. To prevent movement in the vagina and potential displacement, temperature loggers were attached to a progesterone-free modified Controlled Internal Drug Release device (CIDR-blank, Pfizer, New York, NY, USA) for ewes. The Y-shaped dimensions of the CIDR-blank were 6.0 × 3.5 cm with a diameter of 1.0 cm. A transponder (Backhome Bio Tec-Transponder®, Virbac, Virbac Corporation, Fort Worth, TX, USA) was placed under the silicon lining of the CIDR-blank. The transponder had a length of 1.4 cm and a diameter of 0.2 cm. Using a reading device (Minimax®, Virbac, Virbac Corporation, Fort Worth, TX, USA), the presence and position of the logger could be confirmed. The temperature loggers were programmed (Mercury Application Software®, version 2.05, Star Oddi, Gardabaer, Iceland) to measure temperatures at 10-min intervals. The loggers were inserted via a vaginal speculum. For smaller breed dogs with a body weight below 20 kg, a smaller speculum (Model 63 956, length 11 cm, diameter 1.3 cm, Storz, Tuttlingen, Germany) was used. Larger breed dogs had a larger speculum (Model 63956, length 15 cm, diameter 2 cm, Storz, Tuttlingen, Germany) inserted. The temperature logger was pushed through the speculum using a sterile cotton swab and placed approximately 14–18 cm deep in the vaginal cavity depending on the size of dog. A reapplication of the logger was necessary in case of logger loss due to moistness and softening of the vaginal tissue. All procedures were performed at the dogs' home to reduce stress of transport and unfamiliar surroundings. The dogs were kept in their familiar environment with no restrictions to their individual daily exercise routine. The temperature logger was expelled spontaneously from the vagina before delivery of the first puppy. This logger expulsion was defined as time of onset of parturition. Temperature data were downloaded after parturition (DST communication box, Star Oddi, Gardabaer, Iceland). Rectal temperature measurements were recorded with a digital thermometer (VT 1831®, Microlife USA, Incl, Clearwater, FL, USA) by the owners at their convenience.

Statistical analysis

Data from the temperature loggers were entered and downloaded (Mercury Application Software®, version 2.05), respectively into Excel spreadsheets (ms office 2003, Microsoft Corporation, Redmond, WA, USA), analysed using spss® for Windows (Version 18.0, SPSS Inc., Munich, Germany) and MedCalc software (version 10.1.3.0, Medcalc, Mariakerke, Belgium).

For further analysis, hourly means were calculated for every bitch independently. The temperature recordings at 10-min intervals that were lower than 36.0°C were considered as artefacts due to logger loss and were not included in the calculation of the hourly mean. To describe temperature before parturition, vaginal temperature was averaged in 24-h intervals (i.e. 1–24, 24–48, 49–72, 73–96 and 97–120 h) and 12-h intervals (i.e. 1–12, 13–24, 25–36, 37–48, 49–60, 61–72 and 73–84 h) preceding the time the bitch lost the logger. The average temperature from these intervals was compared using repeated-measures anova. The post hoc test of Bonferroni was performed.

The difference between vaginal temperature at a particular time of day and vaginal temperature measured 24, 36 and 48 h before was calculated for each of the hourly averages during the last 120-h before delivery. The diagnostic value of a decrease in vaginal temperature to predict parturition within the next 24, 36 and 48 h was tested using receiver-operating characteristics (ROC) analysis as described previously for dairy cows (Burfeind et al. 2011). The continuous variable was the difference in vaginal temperature (24, 36 or 48 h), and the classification variable was the occurrence of delivery within 24, 36 or 48 h. Due to continuous vaginal temperature measurement, calculated differences were available for 24 h/day. Therefore, 24, 36 and 48 positive events, defined as the occurrence of delivery within 24, 36 and 48 h respectively, existed per bitch. Sensitivity was defined as the proportion of positive events (occurrence of delivery within 24, 36 and 48 h) correctly predicted by the test (decrease in vaginal temperature). Specificity was defined as the proportion of negative events (absence of delivery within 24, 36 or 48 h) correctly diagnosed as negative by the test (no decrease in vaginal temperature).

Results

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References

Mean duration of vaginal temperature measurement in 16 dogs was 88 ± 42 h. The mean whelping of the bitches occurred 62.1 ± 1.8 days after estimated ovulation date (n = 9) and 60.6 ± 1.9 days after first mating (n = 7). The mean litter size was 6.0 ± 2.4. The total puppy count was n = 96 of which five puppies were born dead. Dystocia was encountered in three bitches of the breeds Old English Bulldog, Hovawart and Dachshund after the first pup was born. In these cases, a caesarean section was performed of which all puppies were alive and vital. The mean time from logger expulsion to delivery of the first pup was 7.3 ± 8.5 h. In 12 bitches, the logger was retained in vaginal position until expulsion with no reinsertion necessary. In two bitches, logger loss occurred once, and in two other bitches, reinsertion was necessary on two occasions. The temperature recordings at 10-min intervals that were lower than 36.0°C (n = 545, 6.1%) were excluded from further analyses from a total of n = 8952 measurements. Two bitches received their logger application less than 36 h before parturition and therefore were excluded from of ROC analysis for the diagnostic value of a vaginal temperature decrease of 36 and 48 h to predict parturition within 24, 36 and 48 h. No visible signs of negative effects were observed by owners such as abnormal vaginal discharge when the logger was present in the vaginal cavity of the bitches. In the last 24 h before parturition, mean temperature was lower (37.3 ± 0.3°C) than 24–48 h (37.6 ± 0.2°C), 49–72 h (37.7 ± 0.1°C), 73–96 h (37.7 ± 0.1°C) and 97–120 h (37.8 ± 0.1°C, p < 0.05, Fig. 1) earlier. Considering mean temperature from 12 h intervals before parturition, the intervals 1–12 h (37.3 ± 0.4°C) and 13–24 h (37.3 ± 0.3°C) did not differ (p = 0.99). The mean temperatures from the intervals 37–48 h (37.7 ± 0.2°C), 49–60 h (37.7 ± 0.2°C), 61–72 h (37.7 ± 0.2°C) and 73–84 h (37.7 ± 0.2°C) were higher than the intervals from 1 to 12 h (37.3 ± 0.4°C) and 13–24 h (37.3 ± 0.3°C, p < 0.05). Within 25–36 h (37.5 ± 0.2°C), mean temperature did not differ from earlier [1–12 h (37.3 ± 0.4°C, p = 0.66) and 13–24 h (37.3 ± 0.3°C, p = 0.72)] or later [37–48 h (37.7 ± 0.2°C, p = 0.30), 49–60 h (37.7 ± 0.2°C, p = 0.37), 61–72 h (37.7 ± 0.2°C, p = 0.23) and 73–84 h (37.7 ± 0.2°C, p = 0.70, Fig. 1)]. A temperature decrease by ≥ 0.3°C within 24 and 36 h predicted the onset of parturition within a period of 24 h with a sensitivity of 58% and 69% and a specificity of 84% and 77%, respectively (Table 1a and b). A temperature decrease of ≥ 0.4°C within 24 h predicted parturition within 48 h with a sensitivity of 69% and a specificity of 88% (Table 1a). The onset of parturition within 48 h after a temperature decrease of ≥ 0.3°C within 36 h was predicted with a sensitivity of 66% and specificity of 87% (Table 1b). The areas under the curve (AUC) ranged from 0.72 to 0.80 (p < 0.01, Table 1a–c). In order to calculate a clinical more applicable approach, we used our measurements to simulate a measurement taken only once daily at specific times (1.00–24.00). The test characteristics are based on a decrease in vaginal temperature (0.3 and 0.4°C) to predict parturition within 24 h. In Fig. 2, we present results for sensitivity, specificity and AUC for a single measurement per day for the different times (1.00–24.00). The calculation of repeated-measures anova of 12 and 24-h intervals led to the development of four different models for measurements taken only once every 12 h to corresponding time intervals. Model 1 tested the performance of a vaginal temperature decrease ≥ 0.2°C occurring in the interval from 0 to 12 h and in the interval from 12 to 24 h or a total vaginal temperature decrease ≥ 0.4°C in the interval from 0 to 24 h to predict parturition within 24, 36 and 48 h. Model 2 tested the performance of a vaginal temperature decrease ≥ 0.2°C occurring in the interval from 0 to 12 h and in the interval from 12 to 24 h or a total vaginal temperature decrease ≥ 0.4°C either in the interval from 0 to 12 h or in the interval from 12 to 24 h to predict parturition within 24, 36 and 48 h. Model 3 tested the performance of a vaginal temperature decrease ≥ 0.2°C in the interval from 0 to 12 h and in the interval from 12 to 24 h or a total vaginal temperature decrease ≥ 0.3°C in the interval from 0 to 24 h to predict parturition within 24, 36 and 48 h. Model 4 tested the performance of a vaginal temperature decrease ≥ 0.2°C in the interval from 0 to 12 h and in the interval from 12 to 24 h or a total vaginal temperature decrease ≥ 0.3°C in the interval from 0 to 12 h or in the interval from 12 to 24 h to predict parturition within 24, 36 and 48 h. The results of the models 1–4 are presented in Table 2. These present comparable values of test characteristics to continuous measurements to be seen in Table 1a–c. This indicates that measurements taken twice every 12 h can achieve similar test characteristics than with continuous 24 h measurements with the prediction of parturition within 24, 36 and 48 h.

Table 1. Test performance in% (95% CI) of incremental decrease in vaginal temperature measured over a (a) 24-h (n = 16), (b) 36-h (n = 14) and (c) 48-h (n = 14) period as a predictor of parturition within 24, 36 and 48 h
 VTa ≥ 0.3°CVT ≥ 0.3°CVT ≥ 0.4°C
  1. a

    VT, vaginal temperature.

  2. b

    Sen, sensitivity: proportion of bitches that whelped within 24, 36 and 48 h and showed a decrease in VT.

  3. c

    Spec, specificity: proportion of bitches that did not whelp within 24, 36 or 48 h and did not show a decrease in VT.

  4. d

    +PV, positive predictive value: proportion of bitches that showed a decrease in VT and whelped within 24, 36 and 48 h.

  5. e

    −PV, negative predictive value: proportion of bitches that did not show a VT decrease and did not whelp within 24, 36 and 48 h.

  6. f

    AUC, Area under the curve.

  7. g

    p < 0.01.

(a)
Parturition within24 h36 h48 h
Senb58 (52–63)53 (49–58)69 (63–74)
Specc84 (81–86)90 (87–92)88 (84–91)
+PVd63 (57–68)81 (76–85)76 (70–81)
−PVe80 (77–83)70 (66–74)83 (79–86)
AUCf0.72g (0.69–0.75)0.74g (0.72–0.77)0.80g (0.77–0.83)
(b)
Parturition within24 h36 h48 h
Senb69 (63–74)64 (60–69)66 (61–71)
Specc77 (74–81)84 (81–88)87 (83–90)
+PVd63 (57–68)79 (74–84)84 (79–88)
−PVe82 (78–85)72 (68–76)71 (66–75)
AUCf0.78g (0.75–0.81)0.80g (0.76–0.82)0.80g (0.77–0.83)
(c)
Parturition within24 h36 h48 h
Senb69 (63–74)54 (50–59)59 (54–64)
Specc88 (84–91)85 (81–89)92 (88–95)
+PVd76 (70–81)85 (81–89)93 (89–96)
−PVe83 (79–86)55 (50–59)57 (52–62)
AUCf0.80g (0.77–0.83)0.74g (0.71–0.77)0.79g (0.76–0.82)
Table 2. Test characteristics of four different models (see 'Results') predicting parturition within 24, 36 and 48 h
 Model 1Model 2Model 3Model 4
  1. a

    Sen, sensitivity: proportion of bitches that whelped within 24, 36 and 48 h and were predicted by the model.

  2. b

    Spec, specificity: proportion of bitches that did not whelp within 24, 36 and 48 h and were not predicted by the model.

  3. c

    +PV, positive predictive value: proportion of bitches that were predicted by the model and whelped within 24, 36 and 48 h.

  4. d

    −PV, negative predictive value: proportion of bitches were not predicted by the model and did not whelp within 24, 36 and 48 h.

Parturition within24 h
Sena47475661
Specb90858374
+PVc74666758
−PVd74737676
Parturition within36 h
Sena42465361
Specb96949283
+PVc92908880
−PVd60616466
Parturition within48 h
Sena35395653
Specb96969386
+PVc95959488
−PVd44464749
image

Figure 1. Mean vaginal temperature of 16 bitches in the last 90 h before parturition

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image

Figure 2. Test characteristics (···Specificity, —Area under the curve (AUC) × 100, --- Sensitivity) of a 24-h decrease in vaginal temperature measured at specific times (once daily) to predict parturition within 24 h. Test characteristics are based on a decrease in vaginal temperature of 0.4°C at 4, 8, 9 and 21 h and 0.3°C at all other times (*AUC: p < 0.05)

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Discussion

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References

To our knowledge, this is the first report of continuous temperature measurement before parturition of the bitch. Data collection with this measuring method proved to have a close correlation (r = 0.79, p < 0.05) with rectal measurements (Maeder et al. 2012). Unfortunately, the intervals, timing and frequency of rectal temperature measurements varied extremely between breeders. Therefore, it was not possible to analyse this data. Monitoring the decrease in body temperature as an indicator for imminent parturition is often recommended by veterinarians to owners (Kim et al. 2007; Michel et al. 2011). Until now, sensitivity and specificity of a decrease in body temperature in bitches for the prediction of parturition have neither been published for rectal nor for vaginal temperature measurements. Decreases in vaginal temperature over 24, 36 and 48 h intervals were able to distinguish between bitches that did and did not whelp within 24, 36 or 48 h, as demonstrated by AUC ranging from 0.72 to 0.80 (p < 0.01). If the test could distinguish perfectly between the two events, the area under the curve would be 1, whereas an AUC of 0.5 demonstrates that the test cannot distinguish between the 2 groups. These results are in accordance with prepartum changes in vaginal temperature to predict calving in dairy cows (Burfeind et al. 2011). When measuring once daily at specific times, the values for sensitivity were lower in the times from 2.00 to 19.00 (33.33–69.2%) in comparison with measurements taken within the time range of evening and night (20.00–1.00, 69.2–84.6%). From 2.00 to 19.00, the specificity ranged from 66.7% to 95.7%, and from 20.00 to 1.00, it ranged from 88.0% to 95.8%. These results suggest that when measuring only once daily, the test is more reliable when measurement is conducted in the evening from 20.00 to 1.00. These results cautiously suggest the hypothesis that owners of pregnant bitches should be advised to measure rectal temperature once daily in the later evening hours in order to predict parturition due to the close correlation of vaginal and rectal measurements (Maeder et al. 2012). This phenomenon could possibly be attributed to by the dogs' consistent reduced activity pattern and outside influence during this time what might affect body temperature in dogs (Angle and Gillette 2011). To prove this hypothesis, another study with rectal measurements taken at exact specific corresponding times with a greater number of dogs is needed. Furthermore, owners have to be trained in measuring rectal temperature because the procedure itself might affect measured results as it has been demonstrated in dairy cows (Burfeind et al. 2010). The simulation of intermittent monitoring of temperature (12-h interval and 24-h interval) in bitches shows results comparable to continuous measurements as demonstrated in four different models using different decision trees. These findings correspond with the results of Burfeind et al. (2011) generated by continuous vaginal temperature measurement in cows and rectal measurements taken twice daily. Tsutsui and Murata (1982) examined the interval between the time when rectal temperature reached to the lowest level (36.9 ± 0.04°C) and the onset of parturition. Rectal measurements were taken every 1–4 h. This interval ranged from 3 to 25 h and therefore was not interpreted as an adequate criterion for the prediction of parturition. The interval of time when body temperature fell to 37.5°C and the onset of parturition were 21.5 ± 0.8 h. Individual differences were small. As a result, the authors suggested that this interval may be of great practical value. However, Long et al. (1978) found that a temperature drop was too variable between individuals and should not be used as a sole criterion for the onset of parturition.

Continuous vaginal temperature measurement has been proven to be a reliable method for sampling of body temperature. Furthermore, this method was characterized by calculation of sensitivity and specificity of a temperature decline for the prediction of parturition. The computed values for specificity were higher than for sensitivity, providing evidence that the prognosis of parturition not occurring is more precise when measuring temperature continuously or at specific corresponding times than the prognosis of parturition occurring within the next 24, 36 or 48 h.

Although bitches may exhibit a decrease in vaginal temperature around the time of parturition, detecting this decrease does not determine the onset of whelping precisely, as seen in the calculated low values for sensitivity. Individual temperature changes not corresponding with parturition were observed. New technologies will be available in future that will allow real-time temperature measurement via radiotelemetry. In this instance, this method may assist in providing additional information in cases of dystocia. Owners and veterinarians, however, must be aware that the temperature decrease may be only 0.3°C or does not occur at all.

Acknowledgements

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References

The authors thank the owners of the dogs for their fantastic cooperation and time commitment. They also thank Maria Grau for her great assistance in handling the bitches. We are also grateful to Berglind Helgadottir, Star Oddi, Gardabaer, Iceland, for scientific support.

Author contributions

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References

B Geiser designed the study, analysed the data, drafted the paper. O Burfeind analysed the data, drafted the paper. W Heuwieser designed the study, analysed the data, drafted the paper. S Arlt designed the study, analysed the data, drafted the paper.

References

  1. Top of page
  2. Contents
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of interest
  9. Author contributions
  10. References
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