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Obstetrics & Gynecology 2004;103:287-293
© 2004 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Maternal Temperature Monitoring During Labor: Concordance and Variability Among Monitoring Sites

Sujoy Banerjee, MD, DCH, Peter Cashman, BSc, PhD, Steve M. Yentis, BSc, MD and Philip J. Steer, BSc, MD

From the Academic Department of Obstetrics and Gynecology and Neonatology, the Bagrit Centre for Bioengineering, and the Magill Department of Anesthesia, Intensive Care and Pain Management, Faculty of Medicine, Imperial College London, Chelsea and Westminster Hospital, 369 Fulham Road, London, United Kingdom.

Address reprint requests to: Dr. S. Banerjee, 4 Bourne Court, New Wanstead, London, E11 2TG; e-mail: sujoybanerjee{at}doctors.org.uk.


   ABSTRACT
TOP
ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVE: Elevated maternal temperature in labor is associated with adverse immediate and long-term neonatal outcomes. Conventional methods of temperature measurement may not reflect the intrauterine temperature, which constitutes the fetal environment. The purpose of this study was to ascertain the most reliable noninvasive method of temperature monitoring in labor that would best reflect changes in intrauterine temperature.

METHODS: Women in labor receiving epidural analgesia had temperature readings taken every 10 seconds from the uterine cavity, ear canal, and skin surface of the leg and abdomen and hourly from the mouth.

RESULTS: Eighteen patients were studied for a mean of 228 minutes (range 56–464 minutes). The best indicator of intrauterine temperature was oral temperature, with a mean intraclass correlation coefficient of 0.6 (95% confidence interval 0.42, 0.77). On average, oral temperature underestimated intrauterine temperature by 0.8°C (95% confidence interval 0.7°C, 1°C). Allowing for this, oral temperature greater than 37.2°C detected an intrauterine temperature greater than 38°C with a sensitivity of 81% and a specificity of 96%. The intraclass correlation coefficients of all other sites with intrauterine temperature were poor (0.1 or less). As expected, the temperature at all sites increased as labor progressed.

CONCLUSION: Oral temperature, measured carefully, has an acceptable correlation with intrauterine temperature and is recommended for routine detection of maternal pyrexia in labor. Continuous skin and external auditory canal temperature measurements did not correlate well.

LEVEL OF EVIDENCE: II-3

Traditionally, maternal temperature in labor is assessed every 4 hours with an oral thermometer to detect infection, most commonly chorioamnionitis. However, in relation to the fetus, the intrauterine temperature is likely more relevant, because the uterus is the fetus’s immediate environment and, therefore, critically affects fetal temperature.1–3 Fetal temperature is important because animal studies have demonstrated that an increase in brain temperature of even 1°C worsens the degree of brain damage from hypoxia-ischemia.4–5 Intrapartum maternal fever has been reported to be associated with several adverse neonatal outcomes, including increased need for resuscitation, global hypotonia, encephalopathy, and seizures.6–10 Epidemiological data show a 9-fold increase in the incidence of cerebral palsy in infants weighing more than 2,500 g born to mothers with a fever exceeding 38°C in labor.11

Thus, it is important to detect accurately when fetal temperature is rising so that cooling measures can be taken or delivery expedited. However, the majority of studies of temperature in labor (including those on neonatal outcome) have relied on maternal oral and sometimes tympanic temperature measurements.12–14 Oral temperature measurement may be influenced by mouth breathing and oral intake of fluids and ice chips. Technique is also often poor, and this may result in pyrexia being missed.2 Tympanic temperature measurement requires substantial training of staff if it is to be used appropriately and is also difficult in the presence of wax in the ears.15,16 Moreover, Fusi et al17 and Macaulay et al2 suggested that oral temperature is usually substantially lower than intrauterine temperature and therefore underestimates the thermal stress on the fetus. However, the measurement of intrauterine temperature in all women is not done because it is usually perceived to be too invasive.

The purpose of this study was to ascertain the most reliable noninvasive method of temperature monitoring in labor that would reflect increases in the intrauterine temperature and thus allow cooling or delivery to be implemented before fetal temperature rose to dangerous levels.


   MATERIALS AND METHODS
TOP
ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The study was conducted at Chelsea and Westminster Hospital, London, between September 2002 and January 2003 and was approved by the Riverside Research Ethics Committee. Women were informed about the study in advance by information leaflets distributed in the antenatal clinics. Women were recruited into the study after informed consent once they had received epidural analgesia in labor and were pain free. We chose to study only women receiving epidural analgesia because 1) this made the insertion of intrauterine temperature probes more acceptable and 2) many reports have documented a higher incidence of pyrexia in women with epidurals.7,14,17–20

The inclusion criteria were the following:

  1. active labor with the use of low-dose epidural analgesia (intermittent boluses of 10–15 mL 0.1% bupivacaine with fentanyl 2 µg/mL after an initial dose of 15 mL)
  2. gestation of 37 weeks or more
  3. ruptured membranes
  4. clinical indication for the use of an intrauterine pressure catheter and/or informed consent by the women to allow insertion of the intrauterine temperature catheter for research purposes
    Exclusion criteria were the following:
  5. known hepatitis B or human immunodeficiency virus infection
  6. known placenta previa or uterine bleeding of undetermined origin
  7. febrile illness at the onset of labor

Simultaneous uterine, tympanic, and skin surface temperatures were recorded every 10 seconds throughout labor from recruitment to the beginning of active second stage. Oral temperature was recorded at least hourly.

The intrauterine temperature was measured with a disposable general purpose sensor (accuracy ± 0.1°C; Nellcor Inc, Pleasanton, CA). It incorporated a 400 series thermistor mounted in the tip of a sterile catheter, 48.5-cm long and 4-mm in diameter. The catheter was inserted by an obstetrician or an experienced midwife either along with an intrauterine pressure catheter or on its own at the time of a routine vaginal examination. The tip of the catheter was placed in the uterine cavity above the presenting part.

The skin temperatures were recorded with MLT 409 skin temperature thermistor probes (accuracy ± 0.1°C; ADInstruments Ltd, Oxfordshire, UK). The probes were placed on the medial aspect of the thigh and the surface of the abdomen under the fetal monitoring transducer belt, so as to be well insulated from room air. The skin probes were cold-sterilized after each use. We hypothesized that the skin sites might show a greater correlation with intrauterine temperature as a result of thermal equilibrium established due to peripheral vasodilation secondary to maternal pyrexia or sympathetic blockade in the lower part of the body (as a consequence of epidural analgesia).

We also took measurements from the tympanic membrane with a tympanic sensor (400 series thermistor; Nellcor Inc; accuracy ± 0.1°C). The sensor was placed in the external auditory meatus according to the manufacturer’s guidelines.

The thermistor signals from the above 4 channels were continuously acquired by separate ML309 Thermistor Pods (ADInstruments Ltd), two having been modified for use with the 400 series thermistors. The signals were then recorded with a Powerlab 4SP recorder with Windows-based Powerlab software (ADInstruments Ltd). The recordings were made after an initial stabilization period of 10 minutes.

Oral temperature was recorded at least hourly with the 3M Tempa.Dot single-use clinical thermometer (accuracy ± 0.1°C; 3M Corporation, St. Paul, MN) according to the manufacturer’s guidelines, except that the research fellow ensured that the thermometer was left in the mouth for at least 2 minutes (rather than the recommended 1 minute) before the temperature reading was recorded. Care was taken to ensure that the mother had not been drinking fluids in the 15 minutes before the recording was made. Ice chips were not used by any of the women.

The temperature sensors were calibrated with a mercury thermometer, and their linearity and tracking agreement was checked before and after the study with a waterbath, within the clinical range of 33–41°C. In all cases, full response to an abrupt change in temperature of 1°C occurred within 30 seconds. Ambient temperature was recorded during each study.

The clinical management of labor, including investigation for possible infection and the use of antibiotics and antipyretics such as paracetamol, was at the discretion of the clinical team and according to unit protocol. However, the timing and dosage of any such antipyretic administration was noted to ascertain any effect on maternal temperature.

Mean, standard deviation (SD), and 95% confidence intervals (CIs) were calculated by using SPSS 10 (SPSS Inc, Chicago, IL), which was also used to determine the intraclass correlation coefficient between the simultaneous measurements.


   RESULTS
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Sixty patients were approached in labor and 18 (30%) patients agreed to take part in the study. All received epidural analgesia in labor. Table 1Go illustrates the patients’ characteristics. The mean duration of the studies was 228 minutes (range 56–464 minutes). One patient refused tympanic temperature measurement. The ambient temperature was tightly controlled by the hospital central air conditioning system and was always between 22.2°C and 24°C, with a mean (SD) of 23.2 (0.56) °C.


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  		Table 1. Patients Recruited in the Study
 
The intrauterine site recorded the highest temperature at all times in all the studies; the maximum recorded was 39.3°C. The average temperature at each site was calculated for each patient. Figure 1Go shows the mean and SD of these averages. The intrauterine site showed the least fluctuation, whereas the tympanic and the skin surface sites showed wide fluctuations in temperature recordings (the mean of the within-patient standard deviations was 0.21°C for intrauterine, 0.23°C for oral, 0.48°C for skin abdomen, 0.68°C for tympanic, and 0.62°C for skin leg).



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  		Figure 1. Temperature recorded at different sites in °C (mean ± standard deviation). IUT = intrauterine temperature.

Banerjee. Monitoring Temperature in Labor. Obstet Gynecol 2004.

 
Of the 18 women who took part in the study, 14 (77. 8%) had an intrauterine temperature higher than 38°C at some point during the study. The mean difference between the intrauterine and the oral temperature was 0.8°C (95% CI 0.7°C, 1.0°C). Thus, to detect an intra-uterine temperature of 38°C, a threshold value of 37.2°C for oral temperature is appropriate. The differences between the mean intrauterine temperature and those at other sites are shown in Figure 1Go. On 63 occasions, when the intrauterine temperature was above 38°C and the oral temperature was also taken, it was above the threshold of 37.2°C in 51 occasions (a sensitivity of 81%). Only once in 25 occasions in which the intrauterine temperature was below 38°C was the oral temperature above 37.2°C (a specificity of 96%).

Because the sequential temperature measurements were not independent, we compared them using the measure of agreement given by the intraclass correlation coefficient (SPSS 10). Figure 2Go shows that the best indicator of intrauterine temperature was oral temperature, with a mean intraclass correlation coefficient of 0.6 (95% CI 0.42, 0.77). The intraclass correlation coefficients of all other sites with intrauterine temperature were poor (<= 0.1).



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  		Figure 2. Intraclass correlation coefficient of intrauterine temperature with temperature measured at different sites (mean ± 95% confidence interval).

Banerjee. Monitoring Temperature in Labor. Obstet Gynecol 2004.

 
All sites showed an increase in mean temperature as labor progressed. Because previous studies have shown the major factor in temperature rise to be the duration of epidural analgesia,9,14,17–20 the average temperature at each site for each 30 minutes from the institution of analgesia is shown in Figure 3Go. The number of patients contributing to each average varies according to how soon the recording was started after the institution of epidural analgesia and the duration of labor; the reliability of the sample is reflected in the standard error (points where only a single patient has contributed are identified by the absence of a standard error).



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  		Figure 3. Temperature measured (°C) at different sites against duration of epidural analgesia (mean ± standard error of the mean). IUT = intrauterine temperature.

Banerjee. Monitoring Temperature in Labor. Obstet Gynecol 2004.

 
The average rise in temperature for each patient was calculated as the temperature at the end of the study minus the temperature at the beginning, divided by the duration of the study. The average rate of rise was (mean and range): intrauterine 0.04°C/h (-0.36°C to 0.42°C), oral 0.03°C/h (-0.46°C to 0.22°C), tympanic 0.03°C/h (-0.38°C to 1.33°C). The greatest average rise of temperature of 0.35°C/h and 0.24°C/h was seen with the skin leg and skin abdomen sites, respectively.

A total of 8 women were given paracetamol during the study. The mean change in intrauterine temperature after paracetamol administration was -0.11°C/h (range -0.82°C to 0.14°C); temperature fell in 4, but increased in the other 4, despite paracetamol. The biggest falls in temperature were noted in women with an intrauterine temperature higher than 38.5°C (Figure 4Go).



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  		Figure 4. Effect of paracetamol on intrauterine temperature (°C) in 8 women who received it.

Banerjee. Monitoring Temperature in Labor. Obstet Gynecol 2004.

 
No adverse effects were noted in any of the women or newborns in the study despite the fact that 78% of the mothers had an intrauterine temperature higher than 38°C. All babies had Apgar scores of 6 or greater at 1 minute and 9 or greater at 5 minutes. None of them required any active resuscitation. Two mothers and three babies were treated with prophylactic antibiotics for 48 hours according to unit protocol based on high-risk criteria. None of the babies or mothers was clinically unwell, and antibiotics were stopped when microbiological investigations indicated an absence of infection. Those not investigated on clinical grounds remained well, with no signs of infection at discharge, which was usually between 24 and 48 hours after delivery.


   DISCUSSION
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The objectives of temperature monitoring in labor should be 1) to monitor maternal temperature to detect possible infection and 2) to monitor fetal temperature to avoid the potential harmful effects of hyperthermia. In this latter regard, the intrauterine temperature is likely the most important. We have shown that maternal oral temperature is a reasonable indicator of intrauterine temperature, provided that it is done according to the careful technique we have described. We had hoped that measurement of skin temperature at various sites would be a good indicator of a rising intrauterine temperature, potentially because of the peripheral vasodilatation that we anticipated would occur (as a response to pyrexia and the use of epidural analgesia). Although these sites showed the highest rate of rise in temperature consistent with vasodilatation, unfortunately they also showed a high degree of variability, which meant they were an unreliable indicator of increasing intrauterine temperature.

We carried out a systematic search of the literature, using MEDLINE (1966 to August 2003) and Pre-Medline and Embase (1980 to August 2003), for articles limited to the English language and restricted to humans (search terms: "labour," "labor," "obstetric," "body temperature," "temperature," "monitoring," "fetal monitoring," "monitoring physiologic," "uterine monitoring," "continuous monitoring," and "thermal stress"). Editorials, comments, letters, historic articles, and case reports were excluded from the analysis.

We were unable to find any other study that has investigated the relationship between continuous temperature measurements at multiple sites in the mother and relate these to the fetal environment. We have also defined an approach to oral temperature measurement that can be relied on to indicate intrauterine pyrexia with an acceptable sensitivity and specificity.

Unlike some previous studies from our group, we did not measure fetal temperature directly, but these and other studies have already demonstrated that intrauterine temperature is highly correlated with fetal surface and core temperature; fetal core temperature (rectal) is approximately 0.5°C warmer than intrauterine and 1°C from maternal rectal temperature.1–3,21 Thus, in one of our cases, the fetal core temperature would have reached close to 40°C. The tympanic sensor was poorly tolerated and subject to poor contact at times. As a result the temperatures recorded often reflected external auditory meatus temperature rather than tympanic. Intermittent tympanic measurement with an infrared tympanic thermometer might have been better tolerated, but we hoped that continuous measurement would give us an earlier warning of rising maternal temperature. In their study, Sciscione et al22 achieved good correlations with intra-uterine temperature using intermittent tympanic temperature measurement.

In this study, the values for intrauterine temperature were higher than those for oral temperature by an average of 0.8°C, which is similar to that obtained by Sciscione et al.22 Correlation between the intrauterine and oral temperature measurements was similar to that in the study by Sciscione et al,22 whereas it was slightly less in the study by Macaulay et al2. Despite major efforts to measure oral temperature accurately, the degree of correlation varied from one study to another as reflected in the confidence interval. This probably shows the inherent difficulty of measuring oral temperature accurately in the presence of so many confounding factors. Correlations are likely to be less in usual clinical circumstances when temperature recordings are taken by busy clinical staff, as was the case in the study by Macaulay et al.2 Because maternal temperature changed with duration of labor and with the administration of paracetamol, the mean values that we have reported would have been influenced by these factors.

Routine intrauterine temperature measurement in labor is probably the ideal. The risk of any adverse effect from the use of an intrauterine temperature measurement catheter is likely to be small and similar to that of intrauterine pressure catheters and fetal electrodes, which are widely used in many parts of the world.23–25 The risk of infection from internal monitoring has been estimated quantitatively to be similar to that caused by one vaginal examination (1.2%), and coordinating their insertion at the time of routine vaginal examination would minimize the risk.26 However, the risk is unlikely to be zero, and many women, midwives, and obstetricians dislike invasive monitoring of any kind. Rectal temperature could be an alternative to measuring intra-uterine temperature to assess core temperature in labor. However, in a preliminary survey of 65 women attending the antenatal clinic in our hospital, two thirds regarded this site of measurement as also unacceptable, for largely esthetic reasons. We have demonstrated that, carefully taken, oral temperature plus 0.8°C gives an acceptable indication of the intrauterine temperature and, hence, the fetal environment.

A small number of patients received paracetamol during our study. Paracetamol had a very small and inconsistent effect in lowering maternal intrauterine temperature. The effect was more marked in women who had temperatures exceeding 38.5°C. It is possible that paracetamol prevented a further rise in maternal temperature, and this may explain why the average rise in maternal temperature is less in our study than previously reported.17,19 However, larger studies are needed to confirm this finding. Of particular interest is a recent study that failed to show any effect of prophylactic paracetamol in preventing epidural induced maternal fever.27 If further studies confirm this finding, then alternative physical methods of lowering body temperature, eg, tepid sponging, fanning, and reducing ambient temperature in labor rooms, need to be explored.

Our study recorded a rise in both core and peripheral maternal body temperature as labor progressed. The mean intrauterine temperature in our study, in which all women received epidural analgesia, was 38.1°C. Previous work has shown that the normal range for rectal temperature in labors without epidural is 36–37°C.28 Sciscione et al22 reported that mean oral and intrauterine temperatures in labor before epidural analgesia (36.6°C and 37.2°C, respectively) were significantly elevated after epidural analgesia (37°C and 37.6°C, respectively) administration. It appears that pyrexia in labor has become more common with the widespread use of epidural analgesia, highlighting the need for convenient and accurate techniques for monitoring maternal temperature.20

Based on our study, we recommend that carefully taken oral temperature measurement be used for routine detection of maternal pyrexia in labor because it gives the best estimate of the fetal environmental temperature. Continuous measurements of skin temperature over the leg or abdomen, although convenient, are not sufficiently reliable for clinical use. The tympanic probe for continuous temperature measurement was poorly tolerated by women, thus limiting its usefulness. It is important to note our technique, which required leaving the oral thermometer in place for at least 2 minutes and not giving the women cold water, ice chips, or hot drinks for at least 15 minutes before the measurement. Provided that this technique is followed, oral temperature will give a reasonable estimate of the thermal stress to the fetus.


   Footnotes
 
The authors thank Ms Devika Vadher, AD Instruments, UK, for her technical help in setting up the instruments and Tyco Healthcare, UK, for providing the sensors for intrauterine temperature measurements.

doi: 10.1097/01.AOG.0000100155.85379.88

Received June 1, 2003. Received in revised form August 8, 2003. Accepted September 22, 2003.


   REFERENCES
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1. Wood C, Beard RW. Temperature of the human foetus. J Obstet Gynaecol Br Commonw 1964;71:768–9.[Medline]

2. Macaulay JH, Bond K, Steer PJ. Epidural analgesia in labor and fetal hyperthermia. Obstet Gynecol 1992;80: 665–9.[Abstract/Free Full Text]

3. Macaulay JH, Randall NR, Bond K, Steer PJ. Continuous monitoring of fetal temperature by noninvasive probe and its relationship to maternal temperature, fetal heart rate, and cord arterial oxygen and pH. Obstet Gynecol 1992; 79:469–74.[Medline]

4. Wass CT, Lanier WL, Hofer RE, Scheithauer BW, Andrews AG. Temperature changes of >=1 degree C alter functional neurologic outcome and histopathology in a canine model of complete cerebral ischemia. Anesthesiology 1995;83:325–35.[Medline]

5. Dietrich WD, Busto R, Valdes I, Loor Y. Effects of normothermic versus mild hyperthermic forebrain ischemia in rats. Stroke 1990;21:1318–25.[Abstract/Free Full Text]

6. Perlman JM. Maternal fever and neonatal depression: preliminary observations. Clin Pediatr (Phila) 1999;38: 287–91.[Abstract/Free Full Text]

7. Lieberman E, Lang J, Richardson DK, Frigoletto FD, Heffner LJ, Cohen A. Intrapartum maternal fever and neonatal outcome. Pediatrics 2000;105:8–13.[Abstract/Free Full Text]

8. Badawi N, Kurinczuk JJ, Keogh JM, Alessandri LM, O’Sullivan F, Burton PR, et al. Intrapartum risk factors for newborn encephalopathy: the Western Australian case-control study. BMJ 1998;317:1554–8.[Abstract/Free Full Text]

9. Impey L, Greenwood C, MacQuillan K, Reynolds M, Sheil O. Fever in labour and neonatal encephalopathy: a prospective cohort study. BJOG 2001;108:594–7.[Medline]

10. Lieberman E, Eichenwald E, Mathur G, Richardson D, Heffner L, Cohen A. Intrapartum fever and unexplained seizures in term infants. Pediatrics 2000;106:983–8.[Abstract/Free Full Text]

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12. Herbst A, Wolner-Hanssen P, Ingemarsson I. Maternal fever in term labour in relation to fetal tachycardia, cord artery acidaemia and neonatal infection. Br J Obstet Gynaecol 1997;104:363–6.[Medline]

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18. Camann WR, Hortvet LA, Hughes N, Bader AM, Datta S. Maternal temperature regulation during extradural analgesia for labour. Br J Anaesth 1991;67:565–8.[Abstract/Free Full Text]

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20. Yancey MK, Zhang J, Schwarz J, Dietrich CS III, Klebanoff M. Labor epidural analgesia and intrapartum maternal hyperthermia. Obstet Gynecol 2001;98:763–70.[Abstract/Free Full Text]

21. Walker DW, Wood C. Temperature relationship of the mother and fetus during labor. Am J Obstet Gynecol 1970;107:83–7.[Medline]

22. Sciscione AC, Zainia T, Leet T, Winn JN, Winn HN. A new device for measuring intrauterine temperature. Am J Obstet Gynecol 2001;184:1431–4.[Medline]

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