Core Temperature—The Intraoperative Difference Between Esophageal Versus Nasopharyngeal Temperatures and the Impact of Prewarming, Age, and Weight: A Randomized Clinical Trial Anne Erdling, CRNA, MSc Anders Johansson, CRNA, PhD Unplanned perioperative hypothermia is a well-known complication to anesthesia. This study compares esophageal and nasopharyngeal temperature measured in the same patient for a period of 210 minutes of anesthesia. Forty-three patients undergoing colorectal surgery were randomly assigned in 2 groups, with or without a prewarming period (group A = prewarming [n = 21] or group B = no prewarming [n = 22]). Demographics were similar in both groups. Mean temperatures at 210 minutes were statistically different between the groups at both sites of measurement. Esophageal temperature in group A was 36.5 ± 0.6 vs 35.8 ± 0.7 in group B (P = .001), and nasopharyngeal D espite recommendations and several clinical guidelines, prevention of unplanned perioperative hypothermia (UPH) is still missing in many anesthetized patients and the incidence of inadvertent hypothermia remains high.1-4 Considering the high incidence of UPH and the accompanied complication rates in hemostatic function, cardiac morbidity, healing problems, enhanced incidence levels of pressure ulcers, surgical site infection, and patient discomfort, core body temperature should be recorded continually.5-9 Implementation of guidelines for the prevention of UPH imposes technical concerns, since thermometry carries inadequacies, and warming strategies diverge.10,11 Unplanned perioperative hypothermia is defined as body core temperature <36°C, at any moment in the perioperative period.12 UPH is related to the environmental temperature in the operating room and altered thermoregulation in the body. General anesthesia (volatile gas, hypnotics, and analgesics) and neuroaxial anesthesia (spinal, epidural) act both in the central nervous system and peripheral tissues.13-15 Vasodilatation properties of general anesthetics cause a core-to-peripheral redistribution of body heat during the first hour of anesthesia (phase I) followed by several hours of heat loss exceeding heat production, leading to a linear reduction in core tem- www.aana.com/aanajournalonline temperature was 36.7 ± 0.6 and 36.0 ± 0.6 in group A and group B, respectively (P = .002). A negative correlation was found between esophageal temperature and age (r 2 = –.381, P < .012). Esophageal temperature was different with respect to BMI below or above 25. The temperatures were 35.81 ± 0.66 in the lower BMI group vs 36.46 ± 0.59 (P < .001). These results demonstrate a difference between the 2 measurement techniques and that prewarming, age and BMI have an impact on measured temperatures. Keywords: Anesthesia, core temperature, esophageal, nasopharyngeal, prewarming. perature (phase II). In the final plateau phase (phase III), hypothermia stabilizes due to vasoconstriction induced by the low temperature. Internal heat redistribution depends on heat storage in peripheral tissues and changes, such as heat lost over the skin (radiation and convection), alter the core temperature.14 Neuroaxial anesthesia decreases the thresholds for shivering and vasoconstriction and impairs central control of thermoregulatory responses resulting in a similar redistribution of body heat.14 Temperature Measurements Efficiency in preventing UPH depends on valid temperature measurement and effective warming routines.1,2 Body temperature is regulated in the hypothalamus in a narrow thermodynamic range and maintained to optimize synaptic transmission of biochemical reactions. During anesthesia, the brain temperature is the most clinically relevant site for normothermia. Brain and core temperatures (in internal organ tissues) correlate to each other during normothermia but may decouple during anesthesia.10 Since the temperature of blood perfusing the hypothalamus is not readily measured, invasive temperature measurement in the pulmonary artery is the gold standard. When noninvasive core temperature measurements are wanted during surgery, the tympanic, AANA Journal April 2015 Vol. 83, No. 2 99 esophageal, and nasopharyngeal temperatures are regarded as reliable alternatives.10,16,17 These methods enable a continuously monitored temperature measurement during surgery. The esophageal temperature permits a placement fairly close to the aorta and the surgical site, particularly for abdominal surgery. This method is considered to be low risk and provides the most accurate measurement of changes in core temperature, especially during rapid temperature alterations, and may be preferred whenever possible.18-21 Positioning of the esophageal probe may involve considerations at insertion, such as placement verification and esophageal anomalies.21-24 The nasopharyngeal temperature, known as an easy and reliable method, well accepted by the awake patient, permits a method for continuous measurement useful pre- and postanesthesia. Positioned above the palate, the probe will be placed close to the brain. However, bleeding and tissue injury may complicate insertion of the nasopharyngeal probe, and alterations in nasopharyngeal perfusion may have an impact on measurement reliability.20 Several studies evaluating esophageal and nasopharyngeal temperatures are conducted,17-20 but to our knowledge there have been no reports directly comparing these 2 measuring techniques in the same patient. Concept of Prewarming and Intraoperative Warming Prewarming, defined as both actively warming the skin before anesthesia starts12 and active intraoperative warming, is an effective way to prevent UPH during surgery.18,25-27 Warming prior to anesthesia induction reduces the core-to-peripheral temperature gradient, increases the total body heat content and is thus essential to the prevention of intraoperative hypothermia.28 One reason why UPH prevention still fails may be the lack of consensus in prewarming time, warming devices, and warming methods. Intraoperative warming prevents intraoperative heat loss from exceeding the heat production.29 Circulating water, resistive heating, and forced-air are effective warming techniques for the prevention of UPH. Recommendations in prewarming times differ from 10–120 minutes.11,16,25,30,31 However, without prewarming, these techniques often fail to prevent the temperature drop during the first hour of anesthesia.32 Prewarming may be perceived as disturbing to the surgical preparation process and may raise concerns as a source of contamination, enhancing the risk of surgical site infections (SSIs).23,30 However, since most warming equipment has bacterial filters, this risk has been considered negligible.33 In a recent study, it was concluded that there is a need for improved intake filtration in order to reduce contamination and emission risks.34 A later study found no evidence of increased risk when using forcedair warming intraoperative.35 Patients undergoing abdominal surgery are at specific 100 AANA Journal April 2015 Vol. 83, No. 2 risk of developing intraoperative hypothermia due to massive heat loss from tissues. Age and BMI are factors known to affect core body temperature, partly explained by a more severe thermoregulatory impairment in the elderly and by increased insulation by excessive fat in the obese.36,37 Awareness of the risks of perioperative hypothermia is the key to prevention and an important component in the prevention of UPH-related adverse effects is to maintain a normothermic condition constantly during surgery. This requires the use of a temperature monitoring method that provides accurate and consistent measurements. This study was conducted to determine the intraoperative temperatures with 2 different measurement techniques (esophagus vs nasopharynx). This issue was evaluated in 2 groups with and without an extended warming period. Materials and Methods •Participants. All patients were recruited from a waiting list for colorectal surgery at a general hospital in southern Sweden. Patients included were adult and of both genders with ASA physical status 1 and 2, who were to undergo elective open colorectal surgery under general anesthesia, combined with regional analgesia for an anticipated anesthesia time of at least 210 minutes. Patients who did not give their informed consent or understand the information were not eligible for the study, as were patients with known nasal or esophageal anomalies. Patients with thyroid dysfunction and known ischemic peripheral vessel disease were also excluded. •Study Design. In this explorative parallel-group study, patients were randomly assigned to 1 of 2 groups. The study was approved by the Ethics Committee of the Medical Faculty, Lund University (VEN 15-11) and was performed in accordance with the Helsinki declaration.38 The study was further accepted by the heads of the anesthesia and surgical departments. In order to reduce performing bias, all the measurements were carried out by the author of this study. Consent to participate in the study was obtained from each patient. The patients signed a consent form a week prior to surgery and a second session with information was given the day before surgery. The study was designed to perform repeated core temperature measurements in two groups: A (pre- and intraoperative warmed) and B (intraoperative warmed), from probes in the esophagus and nasopharynx. In the OR, patients were randomly assigned by a sealed envelope technique to group A (n = 26) or group B (n = 26). To minimize diurnal variation in body temperature as a confounding factor, all studies started at 7:30 AM. •Temperature Measures. In all patients, both esophageal and nasopharyngeal thermometers were used to collect core temperatures. The Level 1 disposable general purpose temperature probes (Smiths Medical ASD Inc.) www.aana.com/aanajournalonline www.aana.com/aanajournalonline AANA Journal X X X XX XXXX X X Warming Outflow Table 1. Time Schedule for Documentation of Temperatures X X X X X XX XXXX Air (OR) X Esophagus April 2015 X X X X X XX XXXX X X Nasopharynx X X X X XX XXXX X X X XX XXXX Skin (thorax) X X X X X XX XXXX X X X X X Skin (calf) 450 510 390 330 270 210 150 120 90 Post 30 min Surgery start Anesthesia start After EA test dose Before epidural Reading sites were used to measure core temperature via placement in the lower esophagus and nasopharynx. Prior to insertion of the epidural catheter, a nasopharyngeal probe was placed 6–8 cm beyond one of the nostrils using the individual nose-to-ear distance, and confirming that the probe was not visible in the mouth. Thus a baseline temperature was achieved. Following intubation, a temperature probe was immediately placed in the distal esophagus at an individually adjusted distance of 40 ± 4 cm from the nostrils using the Mekjavić–Rempel formula (calculated from patient height in cm x 0.228, resulting in placement at level T8/T9 corresponding to the aorta).39 Documentation of temperatures was according to schedule (Table 1) with the intention to reflect the 3 phases (peripheral redistribution, heat loss exceeding heat production, and the plateau phase) of hypothermia.17 Skin temperatures were obtained from probes positioned on the right calf and upper thorax to detect any overheating from the warming device (Siemens Temperature Probe 5204644E530U Adult). Ambient room temperature was read at a site not affected by the warming device and recorded at the same time as body temperatures. A temperature probe was also placed in the warming equipment. All probes were connected to the KION vital signs monitor (Maquet Critical Care, Solna, Sweden) and values were displayed continuously on the monitor screen, but recorded according to the study protocol. The probes were all calibrated prior to use and the monitors were calibrated yearly by the engineering department according to manufacturer’s recommendations. •Warming Procedure. The warming procedure started in the operating room, where all the anesthesia and surgical preparations took place. Pre- and intraoperative warming in this study was defined as warming the patients’ skin using a forced-air device (Warm Touch, Nellcor, or Gaymar, Smiths Medical), set to 43°C, covering both arms, head, and thorax. Prewarming (extended warming) in group A started after epidural catheter insertion but before epidural anesthesia test dose was given and this warming was continued during 210 minutes of surgery. Warming intraoperatively in group B started after surgical preparation was completed using the same warming equipment and continued similarly. All fluids given intravenously were warmed to 39°C in both groups and passive insulation was applied to a layer of quilted cotton on the legs only and covered with the surgical drape. •Anesthesia Procedure. The epidural anesthesia was initiated with a 3–6 mL test dose of mepivacaine (20 mg/ mL) and epinephrine (5 µg/mL) just before anesthesia start and the dermatome level of sensory blockade was verified to T9–10 by loss of cutaneous cold sensation. General anesthesia was induced with propofol (1.5–3 mg/ kg) and remifentanil (0.3–0.5 µg/kg) and orotracheal intubation was facilitated with suxamethonuim (1 mg/kg). Anesthesia was maintained with remifentanil (0.15–0.3 Vol. 83, No. 2 101 Characteristics All, N=52 Group A, Group B, n=26 n=26 Assessed for eligibility (N=52) Excluded (n=0) Gender Female, n (%) 29 (55.8%) 14 (48.3%) 15 (51.7%) Male, n (%) 23 (44.2%) 12 (52.2%) 11 (47.8%) 24 (46%) 12 (23%) 12 (23%) 70±13 (32–92) 70 ±15 (32–92) 72 ±11 (41–90) Beta blocking medication Age (y); mean SD (range) Body mass index (kg/m²); mean (SD: range) 2626 (5: 16–34) (4: 19–37) Table 2. Demographic Data of the Patients Presented in Absolute and Relative Numbers µg/kg/min) and sevoflurane at an end-tidal concentration of 0.7%–1.0% due to age. The lungs were mechanically ventilated with a KION anesthesia machine (Maquet Critical Care, Solna, Sweden) using a low-flow recirculation system, with Fio2 0.4 and rate and volume sufficient to maintain normocapnia. Neuromuscular blockade was maintained with rocuronium 10 mg/mL guided by appropriate monitoring. According to the surgical care plan, the patients were given Ringer’s solution 3 mL/kg/h. In case of hypotension, the patient was given vasopressive drugs (norepinephrine or ephedrine) in order to keep MAP between 70–100 mm Hg. A continuous epidural infusion of fentanyl (2 μg/mL) and ropivacaine hydrochloride (1 mg/mL) 10 mL/h was started just before surgical incision. Vital signs (arterial blood pressure, HR, etco2, Spo2, airway pressure) were recorded every 5 minutes and the patient data sheet was completed with demographic characteristics as well as vital signs, temperature readings, and length of surgery, and the use of vasopressive drugs was recorded (Tables 1-2). •Data Analysis. Data were analyzed using SPSS for Windows version 20 Chicago, IL, USA. A power calculation revealed that a clinically relevant temperature difference of 0.2°C40 would reach a power of 0.80 at P < 0.05 with 16 patients per group. The distribution of data collected in the different groups was tested for normality using the one-sample Kolmogorov–Smirnov test. A paired two tailed t-test was used to compare groups A and B with respect to temperatures at 210 minutes. Spearman’s rank correlation was used for testing correlation between age and esophageal temperature. A postpower calculation was done to ensure the power included a population of 21 patients in each group. Our results demonstrate an intergroup difference of approximately 0.6°C with an average standard deviation of at least 0.6°C and the result reached a power of 0.90. Results Fifty-two adults aged 32–92 years were enrolled in the 102 AANA Journal April 2015 Vol. 83, No. 2 Allocated to Group A (n=26) Analyzed (n=21) • Excluded due to loss of final analysis (n=5) Allocated to Group B (n=26) Analyzed (n=22) • Excluded due to loss of final analysis (n=4) Figure 1. Flow Diagram for Enrolled Patients (Group A Pre- and Intraoperative Warmed, Group B Intraoperative Warmed) study. Forty-three patients (21 in group A and 22 in group B) were analyzed at 210 minutes since 9 patients were excluded due to shorter surgery (Figure 1). Three patients (1 in group A and 2 in group B) did not receive epidural anesthesia due to anticoagulant treatment or spine anomalies. There were no problems or complications due to temperature probe insertion. Groups A and B were not different with respect to demographic variables (Table 2) and the warming period in group A was 42 ± 10 minutes longer than in group B. Overall, preoperative use of beta blockers was 46% and was similar in both groups (Table 2). All patients were given norepinephrine 0.02–0.20 μg/kg/ min to keep MAP between 70 and 100 mm Hg. BMI was ≥25 in 2/3 (67.3%) of the patients and they were evenly distributed between the groups. Ambient air temperature at anesthesia induction was similar in both groups (21.9 ± 0.8°C) and differed slightly at 210 minutes, group A 22.1 ± 0.6°C and group B 22.4 ± 0.7°C. Just after test dose the skin temperature had increased in both groups, and was 0.2°C higher in group B. The baseline of the nasopharyngeal temperature was also higher in group B (Figure 2). In all patients (group A and B), the temperatures in the esophagus and the nasopharynx showed a significant mean difference of 0.2 °C throughout the procedure (Figure 3). The esophageal temperature in group B declined at 30 minutes post-surgical start. A similar decrease was observed in the esophageal temperature in group A at 60 minutes. This was not seen in the nasopharyngeal temperatures (Figure 2). At 210 minutes, there were statistically significant differences between the groups A and B in both measuring techniques, ES 36.5 ± 0.6 vs 35.8 ± 0.7, (P = 0.001), and NF 36.7 ± 0.6 versus 36.0 ± 0.6, (P = 0.002) (Table 3). From anesthesia start to the 210-minute mark, the esophageal temperature in A had increased a mean 0.65 ± 0.63°C (P = 0.001). In B, this difference was smaller (0.27 ± 0.62°C) and not statistically significant (P = 0.052). A negative correlation was found between the esophageal temperature and age (r2 = –0.381, P < 0.012). Statistical differences could also be seen between 2 BMI www.aana.com/aanajournalonline Figure 2. Nasopharyngeal and Esophageal Temperatures During Surgery in Group A and B Figure 3. Mean Values for Nasopharyngeal and Esophageal Temperatures in All Patients Group Temperature site nMean SD P value A prewarmed Esophageal 21 36.46 0.59 B not prewarned Esophageal 22 35.81 0.66 A prewarmed Nasopharyngeal 21 36.65 0.63 B not prewarned Nasopharyngeal 22 36.02 0.60 0.001 0.002 Table 3. Esophageal and Nasopharyngeal Temperatures and Differences Between the Groups of Prewarmed (A) and Not Prewarmed (B) Patients at 210 Minutes of Surgery Note: The values were significantly lower in the B group (Paired t-test; P < 0.05). groups (BMI <25 and ≥25, respectively) measured with the esophageal temperature at 210 minutes (35.81 ± 0.66 vs 36.46 ± 0.59, P < 0.001). Discussion This study compared 2 different core temperature measurements in the same patient; one from a probe placed in the lower esophagus and the other placed in the nasopharynx. A statistical significant difference was found between the esophageal and nasopharyngeal temperatures during the scheduled measurement (Figure 3). The higher temperature values in the nasopharyngeal www.aana.com/aanajournalonline readings were continued during surgery and exceeded the temperatures measured in the esophagus on average by 0.2°C. Consistent to other studies we found that the trend for both techniques was similar, although the esophageal temperatures seemed to react stronger than the nasopharyngeal to temperature alterations.18-21 This may be of importance in how to maintain a normothermic condition constantly during surgery, and requires the use of a temperature monitoring method giving accurate and consistent measurements. As the nasopharyngeal probe was placed before induction of general and epidural anesthesia, it provided measurement both before and AANA Journal April 2015 Vol. 83, No. 2 103 during anesthesia. Owing to probable patient discomfort, the esophageal probe was placed post induction and no esophageal baseline temperature was therefore obtained. All patients were hypothermic before start of anesthesia (Figure 2) but no further decrease in core temperature was noted during the first hour of anesthesia. Several studies have shown the positive effect of prewarming,11 while in a recent study it was demonstrated to have no benefit.41 The duration of prewarming has been explored and the effects on daily routines and prewarming–related delays in anesthesia start have been discussed.27,32 Horn et al25 concluded that only 10 or 20 minutes of prewarming might reduce the incidence of UPH. In this study, we evaluated the temperature difference in a shortened prewarming routine that did not affect the anesthesia start. Group A was prewarmed for 42 minutes during anesthesia and surgical preparations while group B was warmed according to daily routines, when all these preparations were done. The positive influence of prewarming seen in group A was probably an effect of the early cutaneous warming, but may also be referred to impacts of the preoperative beta blockade and vasopressors used during anesthesia.16,42 Patients in group A were more likely to be normothermic at end of surgery than patients in group B (Table 3). When compared to core temperature at the start of anesthesia, esophageal temperature at 210 minutes had increased twice as much in group A as in group B. In this study, prewarming started immediately after epidural catheter insertion and patients had an intraoperative benefit of a longer warming time as demonstrated by Horn et al.25 Since there was only a small temperature drop before surgical start (in esophagus, group B, warmed only 15 minutes during the first hour of anesthesia), we conclude that warming for a short period seems to be valuable. In this study, an upper body forced-air warming device was used and in agreement with other studies we find it a sufficient method to prevent UPH.11,18,25,27 Similarly to other findings, the outflow temperature in the warming device varied considerably during warming, by –1°C to +5°C, and differed from the preset of 43°C.42 The skin temperature on the upper thorax was measured continuously and no skin reaction from warming device was observed. A smaller increase in ambient air temperature of 0.2–0.5°C was seen during surgery and the warming device may have contributed to this. There were no complaints from OR personnel or the surgeon. Results of the current study confirm that age and BMI is of importance to core temperature. The elderly are more likely to get hypothermic and the risk of hypothermia is reduced in the obese. This is consistent with findings during both general and regional anesthesia, and may partly be explained by a more severe thermoregulatory impairment in elderly and by increased insulation by excessive fat in obese patients.36,37 Because anesthesia most often is multimodal, it is 104 AANA Journal April 2015 Vol. 83, No. 2 difficult to evaluate the effect on thermoregulation of each drug during surgery. Twelve patients in each group were using beta blockers preoperatively. Beta blockers have been shown to reduce hypothermia by decreasing cardiac output.43 The impact this may have had on the core temperature was not evaluated; neither was possibly augmented precapillary vasoconstriction induced by vasopressors given during the procedures. The effect of these drugs on tissue at the measurement sites is unclear and further studies on this subject are warranted. •Limitations. Blinding was not possible in this study. Because of limitations in population size, types of surgery, and anesthesia techniques, results from this study may not be generalized to all populations and institutions. It is possible that different placement of the temperature probes occurred and affected our results; however, we used the Mekjavić–Rempel formula for the length of esophageal insertion in order to minimize differences in placement. Another limitation could be referred to patient conditions, such as perfusion and tissue disorders; however, the preoperative use of beta blockade was similar in both groups and all patients were preoperatively given a low dose of vasopressive drugs. Conclusion We conclude small but statistical significant difference between the esophageal and the nasopharyngeal temperatures. Though the temperature differences were statistically significant, the mean difference of 0.2°C may be of clinical significance only when patients are at extreme risk of hypothermia. In this study, core temperature was recorded continuously and this enabled the detection of hypothermic periods during surgery. Within the first hour of surgery, there were decreasing temperatures registered at the esophagus in both groups and this was not noted at the nasopharyngeal site. This may indicate a higher accuracy in the esophageal measurement. Results in this study also confirm that prewarming has a positive effect on core temperature even in patients only warmed intraoperatively. We suggest that even a shorter prewarming time may be of benefit for the prevention of unplanned hypothermia. REFERENCES 1. Wagner VD. Patient safety chiller: unplanned perioperative hypothermia. AORN J. 2010;92(5):567-571. 2. Lynch S, Dixon J, Leary D. Reducing the risk of unplanned perioperative hypothermia. AORN J. 2010;92(5):553-562. 3. AORN Recommended Practices Committee. Recommended practices for the prevention of unplanned perioperative hypothermia. AORN J. 2007;85(5):972-974.. 4. 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Anaesthesia. 2012;67(12):1364-1369. 38. WMA Declaration of Helsinki - Ethical Principles for Medical Research Involving Human Subjects. http://www.wma.net/en/30publications/10 policies/b3/index.html. Accessed January 30, 2015. 39. Mekjavić IB, Rempel ME. Determination of esophageal probe insertion length based on standing and sitting height. J Appl Physiol. 1990;69(1):376-379. 40.Clinical Practice Guideline. The management of inadvertent perioperative hypothermia in adults. National Collaborating Centre for Nursing and Supportive Care commissioned by National Institute for Health and Clinical Excellence (NICE). April 2008. http://www.ncbi. nlm.nih.gov/books/NBK53797/. Accessed January 30, 2015. 41. Adriani MB, Moriber N. Preoperative forced-air warming combined with intraoperative warming versus intraoperative warming alone in the prevention of hypothermia during gynecologic surgery. AANA J. 2013;81(6):446-451. 42. Janicki P, Higgins MS, Jansen J, Johnson RF, Beattie C. Comparison of two different temperature maintenance strategies during open abdominal surgery: upper body forced-air warming versus whole body water garment. Anesthesiology. 2001;95(4):868-874. 43. Inoue S, Abe R, Kawaguchi M, Kobayashi H, Furuya H. Beta blocker infusion decreases the magnitude of core hypothermia after anesthesia induction. Minerva Anestesiol. 2010;76(12):1002-1009. AUTHORS Anne Erdling, CRNA, MSc, is a nurse anesthetist and student manager at Kristianstad General Hospital, Sweden. At the time this paper was written, she was a student in the master’s program in Medical Science at Lund University, Sweden. Email: anne.erdling@skane.se. Anders Johansson, CRNA, PhD, is an associate professor in the faculty of medicine at Lund University and Lund University Hospital, Sweden. Email: anders.johansson@med.lu.se. DISCLOSURES The authors have declared they have no financial relationships with any commercial interest related to the content of this activity. The authors did not discuss off-label use within the article. AANA Journal April 2015 Vol. 83, No. 2 105