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Anesth Analg 2002;94:409-414
© 2002 International Anesthesia Research Society

OBSTETRIC ANESTHESIA

Active Warming During Cesarean Delivery

Ernst-Peter Horn, MD*, Frank Schroeder, MD*, Andrè Gottschalk, MD*, Daniel I. Sessler, MD{dagger}, Natascha Hiltmeyer, MD*, Thomas Standl, MD*, and Jochen Schulte am Esch, MD*

*Department of Anesthesiology, University Hospital Hamburg-Eppendorf, Hamburg, Germany; and the {dagger}Outcomes ResearchTM Institute and Department of Anesthesiology, University of Louisville, Louisville, Kentucky

Address correspondence and reprint requests to E-P Horn, MD, Department of Anesthesiology, University Hospital Eppendorf, Martinistreet 52, 20246 Hamburg, Germany. Address e-mail to ephorn{at}12move.de


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
We tested the hypothesis that 15 min of forced-air prewarming, combined with intraoperative warming, prevents hypothermia and shivering in patients undergoing elective cesarean delivery. We simultaneously tested the hypothesis that maintaining maternal normothermia increases newborn temperature, umbilical vein pH, and Apgar scores. Thirty patients undergoing elective cesarean delivery were randomly assigned to forced-air warming or to passive insulation. Warming started 15 min before the induction of epidural anesthesia. Core temperature was measured at the tympanic membrane, and shivering was graded by visual inspection. Patients evaluated their thermal sensation with visual analog scales. Rectal temperature and umbilical pH were measured in the infants after birth. Results were compared with unpaired, two-tailed Student’s t-tests and {chi}2 tests. Core temperatures after 2 h of anesthesia were greater in the actively warmed (37.1°C ± 0.4°C) than in the unwarmed (36.0°C ± 0.5°C; P < 0.01) patients. Shivering was observed in 2 of 15 warmed and 9 of 15 unwarmed mothers (P < 0.05). Babies of warmed mothers had significantly greater core temperatures (37.1°C ± 0.5°C vs 36.2°C ± 0.6°C) and umbilical vein pH (7.32 ± 0.07 vs 7.24 ± 0.07).

IMPLICATIONS: Perioperative forced-air warming of women undergoing cesarean delivery with epidural anesthesia prevents maternal and fetal hypothermia, reduces maternal shivering, and improves umbilical vein pH.


   Introduction
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 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Neuraxial anesthesia reduces the threshold (triggering core temperature) for vasoconstriction and shivering (1); it often also produces a lower-body sympathectomy that provokes a core-to-peripheral redistribution of body heat (2). The clinical situation is further complicated because core temperature is rarely measured during neuraxial anesthesia and because reductions in core temperature are poorly perceived by patients (3). The result is that surgical patients given epidural or spinal anesthesia frequently become hypothermic—hypothermia that is rarely detected by either the patient or the anesthesiologist (4).

Mild hypothermia causes numerous complications, including morbid myocardial outcomes (5), coagulopathy (6), and reduced resistance to surgical wound infections (7). There are several etiologies for perioperative shivering-like tremor (8), but hypothermia is undoubtedly among them (9). Shivering during cesarean deliveries is common and is disturbing to mothers and anesthesiologists alike. Maintaining normothermia is likely to prevent the thermoregulatory component of shivering.

It is difficult to treat the core-to-peripheral redistribution of body heat (10) that follows the induction of general (11) or epidural (2) anesthesia. However, redistribution can be prevented by preanesthetic cutaneous warming (12). Prewarming hardly changes core temperature that remains well regulated, but it markedly increases peripheral tissue heat content (12). As a result, prewarming reduces the core-to-peripheral tissue temperature gradient and the propensity for redistribution after the induction of anesthesia.

Previous studies have shown that 1–2 h of prewarming prevents intraoperative hypothermia, even in unwarmed patients undergoing prolonged abdominal surgery (13). Furthermore, laboratory studies suggest that as little as 30 min should provide clinical benefit (14). The difficulty, of course, is that an hour or more of prewarming will not fit the clinical routine of most hospitals. However, a brief period of prewarming, such as 15 min, would be easy to accommodate and could be combined with intraoperative warming, which is undoubtedly effective (10) once the redistribution period has passed.

A fetus generates considerable heat that must be dissipated to its mother. Because heat flows only down a temperature gradient, the temperature of the fetus is usually slightly greater than that of the mother. Fetal temperature is thus directly related to maternal temperature, and therefore maternal hypothermia is likely to be associated with hypothermia in newborn infants.

We therefore tested the hypothesis that 15 min of forced-air prewarming, combined with intraoperative warming, prevents hypothermia and shivering during cesarean delivery. We simultaneously tested the hypothesis that maintaining maternal normothermia increases newborn temperature, umbilical vein pH, and Apgar scores.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
With approval of the local ethics committee and written informed consent, we studied 30 healthy pregnant women undergoing elective cesarean delivery with epidural anesthesia. Indications for cesarean delivery included previous cesarean delivery and breech presentation. None of the parturients was in labor.

Patients were excluded when they were younger than 18 yr, had a diagnosis of preeclampsia or eclampsia, or had a history or clinical evidence of a clotting disorder. Patients taking any chronic medications other than perinatal vitamins were excluded as well.

The sample size for this study was based on an expected treatment effect of 1°C. Thirty participants, evenly divided, were estimated to provide 80% power for detecting a statistically significant difference at an {alpha} level of 0.05.

All patients were premedicated with 150 mg of oral ranitidine 2 h before surgery. All women had fasted for at least 6 h. A venous cannula was inserted into the forearm, and an infusion of lactated Ringer’s solution was started. In accordance with our routine practice, all fluids were warmed to 37°C. Patients were randomly assigned, on a 1:1 basis, to be covered with a single cotton blanket (passive insulation) or to forced-air heating (active warming). Randomization was based on computer-generated codes that were maintained in sequentially numbered opaque envelopes. The forced-air cover (Bair Hugger; Augustine Medical, Eden Prairie, MN) was positioned over the upper body 15 min before insertion of the epidural catheter; a Model 501 warmer was set to "high" (43°C). The intraoperative ambient temperature was maintained near 24°C.

An 18-gauge Tuohy needle was inserted between the second and third (L2-3) or the third and fourth (L3-4) interspace with the patient in the sitting position. The loss-of-resistance technique was used to identify the epidural space. A catheter was inserted 4–5 cm, and 3 mL of ropivacaine 0.75% was injected as a test dose. Additional doses of ropivacaine, each 4 mL without epinephrine, were injected into the catheter until a bilateral T4 block (pinprick) was established. The patients were not given opioids during the study period. The cesarean delivery began soon after an adequate epidural block was established. The designated warming method was continued during catheter placement and throughout surgery.

During the observation period we recorded heart rate and arterial blood pressures (Dinamap; Critikon, Tampa, FL). Core temperature was measured at the tympanic membrane by using Mon-a-Therm thermocouples (Mallinckrodt Anesthesiology Product, Inc., St. Louis, MO). The aural probes were inserted by the volunteers until they felt the thermocouple touch the tympanic membrane; appropriate placement was confirmed when volunteers easily detected a gentle rubbing of the attached wire. The aural canal was occluded with cotton and taped in place.

Mean skin temperature was calculated from measurements at the chest, arm, thigh, and calf (Mallinckrodt Anesthesiology Products, Inc.) (15). Forearm-minus-fingertip skin-surface temperature gradients were used to indicate postoperative vasoconstriction (16); gradients <0°C were considered evidence of vasodilatation.

Shivering was graded by an investigator blinded to core and skin temperatures, by using a four-point scale (0 = no shivering; 1 = intermittent, low-intensity shivering; 2 = moderate shivering; 3 = continuous, intense shivering). Participating patients used a visual analog scale (VAS) to quantify pain: 0 mm indicated no pain, and 100 mm identified maximal pain. Thermal comfort was evaluated with another 100-mm VAS on which 0 mm was defined as worst imaginable cold, 50 mm as thermally neutral, and 100 mm as insufferably hot. A new, unmarked scale was used for each evaluation. The parturients were instructed on the use of both VASs just before beginning the study. Measurements were recorded at 15-min intervals during the preoperative period and throughout surgery.

Umbilical vein blood from the infants was sampled for pH (ABL 330; Radiometer, Inc., Copenhagen, routinely calibrated every 4 h) directly after birth. The rectal temperature of the infants was recorded immediately after birth with a digital thermometer (Hartmann Digital Thermometer; Paul Hartmann, Heidenheim, Germany). A pediatrician determined Apgar scores of the infants 1, 5, and 10 min after birth.

Mean arterial pressure and heart rate were first averaged over time within each patient. These values were subsequently averaged among the patients in each group. Continuous, normally distributed variables were analyzed with one-way analysis of variance and the Scheffé test. Changes during time within each group were evaluated with repeated-measures analysis of variance and the Scheffé test. Differences between the groups were compared by use of unpaired, two-tailed Student’s t-tests. Categorical variables were analyzed with Fisher’s exact tests. Data are expressed as mean ± SD; P < 0.05 was considered significant.


   Results
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 Abstract
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 Methods
 Results
Discussion
 References
 
Morphometric characteristics and the duration of surgery were similar among the groups (Table 1). The lumbar segments at which the epidural catheter was inserted (L2-3 or L3-4) and the total volume of epidurally injected ropivacaine also did not differ between the groups. Finally, there were no statistically significant or clinically important hemodynamic differences between the treatment groups (Table 1). Surgery started 89 ± 25 min after the induction of epidural anesthesia in the Passive Insulation group and after 81 ± 31 min in the Actively Warmed patients.


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  		Table 1. Morphometric and Demographic Characteristics and Surgical and Epidural Anesthesia Data
 
Preinduction tympanic membrane temperatures were comparable in the two groups. Core temperatures decreased comparably in each group for the first 30 min of warming. Subsequently, core temperatures in the Passive Insulation group continued to decrease, whereas temperatures in the Actively Warmed patients increased linearly for the remainder of the study. Consequently, core temperatures differed significantly and by more than 1°C at the end of surgery: 37.1°C ± 0.4°C vs 36.0°C ± 0.5°C (Fig. 1). Preoperative and intraoperative mean skin-surface temperatures were approximately 1.5°C greater in the Actively Warmed patients (Fig. 2).



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  		Figure 1. Core temperature in patients assigned to passive insulation or active warming. Data are expressed as means ± SD. All values after 60 elapsed minutes differed significantly in the two treatment groups (*). Core temperatures at the end of surgery were significantly greater in the actively warmed patients (37.1°C ± 0.4°C) than in those assigned to passive insulation (36.0°C ± 0.5°C; P < 0.05).

 


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  		Figure 2. Skin temperature in patients assigned to passive insulation or active warming. Data are expressed as means ± SD. All values after 30 elapsed minutes differed significantly in the two treatment groups (*).

 
During epidural anesthesia, 8 (53%) of 15 Actively Heated patients and 9 (60%) of 15 Passively Warmed parturients were vasoconstricted (skin-temperature gradients <0°C). Shivering was observed in 9 (60%) of 15 of the Passively Warmed mothers, an incidence that was significantly reduced to only 2 (13%) of 15 in the Actively Heated mothers (P < 0.05; Table 2).


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  		Table 2. Skin Temperature Gradients and Shivering
 
Pain scores were low in all patients throughout the observation period and did not differ significantly between the groups. After 15 min of treatment, patients who were actively heated felt warmer (63 ± 11 mm) than those who were passively warmed (52 ± 9 mm). However, thermal comfort did not differ significantly between the groups at any other time.

Immediately after birth, umbilical vein pH was higher in babies of Actively Heated mothers (Fig. 3). Furthermore, rectal temperatures of the newborns were higher in babies of the Actively Heated mothers. Apgar scores at each measurement time were similar in the two groups (Table 3).



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  		Figure 3. Umbilical vein pH in the newborns immediately after delivery. Squares identify individual values. The arrows identify mean values in the patients assigned to passive insulation (7.24 ± 0.07) and active warming (7.32 ± 0.07; P < 0.05).

 

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  		Table 3. Babies’ Data
 

   Discussion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
Skin temperature in the unwarmed patients was approximately 33°C, which is typical. Forced-air warming increased mean skin temperature by approximately 2°C, which is also typical. Skin temperature in the Actively Warmed patients thus remained well below core temperature. Nonetheless, heat transferred by the warmer combined with endogenous metabolic heat production was sufficient to increase core temperature in the heated patients; in contrast, core temperature consistently decreased in the others.

Core temperature is the best single representation of body temperature, but the thermal core represents only approximately half the body mass (11). It is both protected and isolated from the skin surface by intervening peripheral tissues (17). The benefits of core isolation are apparent during sudden exposure to a cold environment: the decrease in core temperature is delayed by the time required to cool peripheral tissues. Conversely, peripheral tissues slow core rewarming when heat is applied to the skin surface. The half-hour delay before core temperature began to increase in our Actively Warmed patients is an intrinsic feature of cutaneous warming and has been noted in other studies (10). Delayed transfer of heat applied to the skin surface is the major reason that core-to-peripheral redistribution of body heat dominates core temperature changes during the initial hour after the induction of anesthesia—with or without surface heating (11). For the same reason, postoperative rewarming is faster in patients with residual spinal anesthesia than in those recovering from general anesthesia (18).

To prevent redistribution hypothermia, peripheral tissues must be warmed to nearly core temperature before the induction of anesthesia. This reduces the core-to-peripheral tissue temperature gradient and therefore the ability of heat to move within the body. (Heat can flow only down a temperature gradient.) Prewarming is effective in preventing redistribution hypothermia after both epidural (19) and general (12) anesthesia.

Internal core-to-peripheral redistribution of body heat is usually the primary cause of core hypothermia during the first hour of general (11) or epidural (2) anesthesia. Nonetheless, redistribution seemed to contribute little to core hypothermia in our patients (as seen by the gradual, rather than precipitous, decrease in core temperature after the induction of anesthesia in the unwarmed patients). Although atypical, little redistribution is consistent with the fact that labor wards are kept relatively warm compared with preoperative areas. A sufficiently warm preoperative environment eventually produces vasodilatation that is similar to active prewarming in that it reduces the normal core-to-peripheral tissue temperature gradient and reduces the amount of redistribution (20). Although a lack of redistribution hypothermia suggests that peripheral tissues were relatively warm in our patients, only approximately half were vasodilated. However, is possible that they vasoconstricted after arriving in the operating room but still retained a relatively high body heat content. It is also possible that vasoconstriction resulted in part from anxiety rather than thermoregulation per se.

Core temperature in the unwarmed patients averaged approximately 36°C after two hours of anesthesia. Because even mild hypothermia may cause adverse outcomes (5–7), there is more or less a consensus among anesthesiologists that efforts should be made to maintain intraoperative core temperature greater than 36°C (21). Consistent with this theory, blood loss is larger in patients at 36°C than those at 36.5°C (22). Core temperature in humans normally ranges from 36.5°C to 37°C, depending on the time within the circadian cycle (23). Our unwarmed patients were thus actually somewhat hypothermic.

Shivering-like activity was significantly less common in actively heated patients than in those who were passively warmed. This difference is consistent with the fact that both core and mean skin temperatures were significantly greater in the actively heated patients. Most shivering was accompanied by vasoconstriction and was thus consistent with thermoregulatory shivering (24). The remainder was presumably nonthermoregulatory muscular activity (8).

The unwarmed patients did not feel cold, a finding that is consistent with previous studies (3). Thermal comfort in the face of mild hypothermia presumably results in part because epidural anesthesia inhibits central thermoregulatory control (25). But equally important, thermal comfort is largely determined by mean skin temperature (26), which was near normal in our patients. In contrast, the heated patients felt slightly warm. We did not evaluate patient satisfaction in this study. However, previous work indicates that active warming improves it (27).

Fetal temperature is typically approximately 1°C higher than maternal temperature. This is the reason that maternal hyperthermia is potentially dangerous. However, newborn infants lose heat rapidly via evaporation from wet skin and because their surface area is large compared to their metabolic rates. As a result, the core temperature in the babies equaled maternal temperature within minutes after birth. Babies born to mothers who were actively warmed nonetheless remained a full degree centigrade warmer than those born to unwarmed mothers. The clinical importance of this difference remains unclear. However, it is intriguing that umbilical vein pH was significantly greater in the warmed babies. This observation suggests that even very mild maternal hypothermia is not entirely benign. Apgar scores, however, were similar in the two groups. Apgar scores are an insensitive indicator of fetal health and might easily miss subtle, but still clinically relevant, effects of subtle maternal hypothermia.

A limitation of our study is that investigators who were aware of group assignment evaluated shivering. Similarly, patients were well aware of the warming system. The reason, simply, is that it would be difficult to hide the forced-air warming system from either the investigators or patients. Bias may thus have confounded our evaluation of shivering and thermal comfort. All our other findings, though, were objective and thus intrinsically resistant to bias. It is therefore unlikely that full blinding, even if technically possible, would much alter our conclusions.

In summary, perioperative forced-air warming of women having cesarean deliveries with epidural anesthesia prevented maternal and fetal hypothermia, reduced maternal shivering, and improved umbilical vein pH. The clinical implication of this study is that women undergoing cesarean delivery with epidural anesthesia benefit from active warming. Thus, we recommend active warming in all women undergoing cesarean delivery with high risk of bleeding, difficulty with wound healing, and cardiac problems and especially in cases of emergency cesarean delivery. We favor a period of 15 min of prewarming because vasodilatation follows directly after the onset of the epidural block that triggers hypothermia. Additionally, active warming of mothers during cesarean delivery seems to improve the outcome of newborns.


   Acknowledgments
 
Supported by Augustine Medical, Inc. (Eden Prairie, MN), NIH Grant GM 58273 (Bethesda, MD), the Joseph Drown Foundation (Los Angeles, CA), and the Commonwealth of Kentucky Research Challenge Trust Fund (Louisville, KY). Mallinckrodt Anesthesiology Products, Inc. (St. Louis, MO) donated the thermocouples used. Dr. Sessler is a consultant for ThermaMed, GmbH.


   Footnotes
 
Presented in part at the German Congress of Anesthesiology, Wiesbaden, Germany, May 5–8, 1999, and the annual meeting of the American Society of Anesthesiologists, Dallas, TX, October 9–13, 1999.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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  20. Kurz A, Kurz M, Poeschl G, et al. Forced-air warming maintains intraoperative normothermia better than circulating-water mattresses. Anesth Analg 1993; 77: 89–95.[Abstract/Free Full Text]
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Accepted for publication October 19, 2001.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins and Stanford University Libraries' HighWire Press®. Copyright 2002 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press