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1 Peripheral Temperature Monitoring during Cardiopulmonary Bypass Operation Stanley Muravchick, M.D., Ph.D., Daniel P. Conrad, M.D., and Abelardo Vargas, M.D. ABSTRACT Almost one-third of 24 adult patients undergoing hypothermic cardiopulmonary bypass (CPB) for elective cardiac operation were found to have upper extremity skin and muscle temperatures of 30.0"C or less at termination of CPB despite the return of nasopharyngeal temperature to normal values. Within 45 minutes, the mean nasopharyngeal temperature of these patients fell spontaneously from 37.1" f 0.3"C (f standard deviation) to 35.1" 0.4"C, a significantly greater fall (p C 0.005) than was observed for patients with extremity temperatures greater than 30.0"C. Persistent hypothermia of the upper extremities correlated statistically with large body mass; it appears that these patients incur disproportionately large caloric debts during hypothermic CPB. Inadvertent hypothermia after CPB can be minimized if both core and extremity temperatures are utilized to provide an assessment of the adequacy of warming prior to return to spontaneous circulation. In 1961, Bernhard and co-workers [21 reported the existence of large gradients between peripheral body temperatures and the temperatures of the core organs during hypothermic extracorporeal perfusion. The spontaneous development of large but unpredictable core/ periphery temperature gradients was reported in anesthetized patients shortly thereafter [221 and has been confirmed subsequently [15]. These gradients have been attributed to persistence of hypothalamic thermoregulatory From the Departments of Anesthesiology and Surgery, Division of Thoracic and Cardiovascular Surgery, University of Miami School of Medicine, and the Anesthesia and Surgical Services, Miami Veterans Administration Medical Center, Miami, FL. Presented in part at the 52nd Congress of the International Anesthesia Research Society, Mar 20, 1978, San Francisco, CA. Accepted for publication Mar 9, Address reprint requests to Dr. Muravchick, Miami Veterans Administration Medical Center, 1201 NW 16th St, Miami, FL mechanisms as well as to abnormal muscle tone, metabolic activity, and regional perfusion patterns [14, 15, 18, 21, 221. Considering the substantial contribution of the weight of the extremities to total body mass, the normalization of esophageal or nasopharyngeal "core" temperature alone would appear to be an inadequate criterion of full reversal of induced hypothermia, although it remains an accepted clinical practice following hypothermic cardiopulmonary bypass [lo, 251. The purpose of this study was to measure the gradients between core and upper extremity skin and muscle temperatures at the termination of cardiopulmonary bypass (CPB) in patients undergoing heart operation with contemporary perfusion techniques and anesthetic agents, and to relate these gradients to the core temperatures obtained after CPB. Methods Twenty-four informed and consenting adult male patients undergoing CPB for elective cardiac operation were studied. Anesthetics included morphine, halothane, and enflurane, all with nitrous oxide in oxygen. After induction of anesthesia and tracheal intubation, ventilation was mechanically controlled through a semiclosed circle-type anesthesia system with 3 to 5 liters per minute of unwarmed, dry, fresh gas inflow. Muscle relaxation was maintained with pancuronium or d-tubocurarine and was monitored by electrical stimulation of the ulnar nerve. Calibrated thermistor temperature probes (Yellow Springs Instruments [YSII 401) were placed in the nasopharynx approximately 5 cm from the external nares, and a thermistor needle (YSI KM7106) was placed intramuscularly 0.5 cm beneath the skin of the forearm or thumb. The flat thermistor probe (YSI 7009) used to measure forearm or thumb skin temperature was fixed in place by transparent tape and cov by Stanley Muravchick

2 37 Muravchick, Conrad, and Vargas: Peripheral Temperature Monitoring during CPB ered with one layer of Webril cotton wool. Temperatures were measured at 5-minute intervals (YSI temperature monitor 43TA, calibrated by mercury thermometer to 0.1"C) throughout operation. Ambient dry-bulb temperature in the operating room ranged from 20.5" to 21.5"C, with sixteen complete changes of air per hour. A Sarns roller pump maintained circulation during CPB by means of vena cava and aortic arch cannulae using a Bentley oxygenator with built-in heat exchanger. Perfusion was maintained at 1.8 to 2.4 liters per square meter of body surface per minute and a mean arterial pressure of 55 to 90 torr. During warming, the oxygenator water bath temperature was maintained no more than 10 C higher than nasopharyngeal temperature (maximum bath temperature, 41 C). A water-type warming blanket (Aquamatic K-thermia RK 600) was placed under the patient and set at 41 C during warming, and all intravenous fluids were warmed to 37 C. Pressor agents were used only when clinically indicated in the period after CPB. Data were evaluated using Student's t test or a chi-square calculation for contingency tables with Yates' correction for continuity as indicated. A p value of less than 0.05 was the criterion of statistical significance. Results Initial nasopharyngeal temperature recorded within 30 minutes of anesthetic induction averaged 35.1" & 0.1"C (mean f standard deviation) for all patients studied. Patients were cooled to 27.4" f 0.3"C (nasopharyngeal temperature) in 23.0 & 2.5 minutes; mean duration of hypothermia was 53.6 k 4.4 minutes. The time from initiation of warming to termination of CPB averaged 47.6 f 2.8 minutes, and mean total duration of CPB was f 25.4 minutes. The mean nasopharyngeal temperature for all 24 patients at termination of CPB was 37.2" f 0.1"C. The mean extremity skin temperature for all patients at the end of CPB was 31.7" f 0.6"C, not significantly different from the mean extremity muscle temperature of 31.6" f 0.6"C. Plotting skin temperature versus muscle temperature for all patients during CPB produced a -6- L W a a t I /... a. * *.... *...-- '...: *...- :. */ 25.0 /.' POV' " " I '" " " ' 231) ) 311) INTRAMUSCULAR TEMPERATURE ("C.) Fig I. Correlation between skin and muscle temperatures of the upper extremity during rapid rewarming on cardiopulmonary bypass. linear regression equation of slope 0.99 (Fig 1) with a highly significant correlation coefficient (p < 0.01). Nasopharyngeal temperature data after CPB were grouped according to extremity temperatures above or below 29.0" to 32.0"C. Compartmentalization of data into two groups with boundaries of 29.0", 30.0", or 31.0"C resulted in statistically significant differences between groups, but a 30.0" boundary gave the highest level of statistical significance for comparably sized groups. Seven patients had upper extremity muscle temperatures less than or equal to 30.0"C at termination of CPB, and their core temperature decreased significantly (p < 0.005) from a mean value of 37.1" f 0.3"C to 35.1" f 0.4"C during the first 45 minutes of spontaneous circulation. In the 17 patients with muscle temperatures greater than 30.0"C at termination of CPB, nasopharyngeal temperature drifted from 37.3" k 0.7"C to 35.9" k 0.6"C (p < 0.005) over the same time period. The difference between the mean nasopharyngeal temperatures of these two patient groups was significant at both 30 and 45 minutes after CPB (Fig 2). Mean rectal temperature measured on arrival in the intensive care unit after operation was 35.4" f 0.2"C in patients with muscle temperature less than or equal to 30.0"C at termination of CPB, significantly less (p C 0.05) than the mean of

3 38 The Annals of Thoracic Surgery Vol 29 No 1 January 1980 Fig 2. Nusopharyngeal temperature after cardiopulmonary bypass (CPB) in patients with initial upper extremity muscle temperature greater than or less than or equal to 30.0"C. (SD = standard deviation; NS = not statistically significant.) 36.0" f 0.1"C for patients who had muscle temperatures greater than 30.0"C at termination of CPB. Patients with a large difference between nasopharyngeal and upper extremity skin temperature demonstrated a temperature course after CPB similar to that just described for patients with large gradients between core and peripheral muscle temperature. In the group of 7 patients with skin temperatures less than or equal to 30.0"C at termination of CPB, mean nasopharyngeal temperature drifted from 37.3" f 0.5"C to 35.0" f 0.3"C (p < 0.005) during the subsequent 45 minutes. This decrease was significantly greater (p < 0.005) than the mean decrease seen in the group of patients with skin temperatures above 30.0"C at the termination of CPB (Fig 3), although the differences in mean nasopharyngeal temperature between the two groups at the end of CPB or 15 minutes after CPB were not significant. There were no significant differences between patient groups in duration of CPB, warming time, room temperature, or patient age. Chi-square analysis revealed no significant relationship between anesthetic technique and the temperature course after CPB. However, those patients with skin or muscle temperatures less than or equal to 30.0"C at termination of CPB had a mean body weight of 93.6 f 3.5 kg, significantly greater (p < 0.025) than the 79.6 k 4.6 kg mean body weight of patients with extremity temperatures greater than 30.0"C. Comment Generalized moderate hypothermia is widely used to produce rapid, reversible depression of the metabolic rates of vital organs and protect against ischemic injury during extracorporeal perfusion. An early experimental study with animals, however, demonstrated a direct relationship between the duration of hypothermia (greater than two hours) and mortality [9]. More recent investigations in humans during induced and inadvertent generalized hypothermia describe many major adverse effects: cardiac irritability and dysrhythmias [13, 23, 261, peripheral vasoconstriction and lactic acidosis 12, 21, 261, opening of arteriovenous shunts 1211, depression of metabolic and hepatic function [2, 5, 261, depression of renal function [4, 13, 161, and increased blood viscosity and affinity of hemoglobin for oxygen [21, 261. Because of corelperiphery temperature gradients, rectal, nasopharyngeal, and esophageal temperatures do not reflect a so-called general body temperature reliably during hypothermic

4 39 Muravchick, Conrad, and Vargas: Peripheral Temperature Monitoring during CPB Fig 3. Nasopharyngeal temperature after cardiopulmonary bypass (CPB) in patients with initial upper extremity skin temperature greater than or less than or equal to 30.0"C. (SD = standard deviation; NS = not statistically significant.) cardiopulmonary bypass or inadvertent hypothermia during general anesthesia. Rectal temperature is acknowledged to be of little use in monitoring rapid heat loss or gain [22-24, 261, and probe tip placement is imprecise. Esophageal thermistors follow central blood or heart temperatures closely if they are accurately positioned in the lower third of the esophagus [12, 18, 241 but may bear little relationship to extremity temperatures [221 or the heat content of any other part of the body. In addition, controlled mechanical ventilation of the patient with unwarmed anesthetic gases may introduce a source of error to esophageal temperature measurements because of evaporative cooling of the lower trachea and mediastinum [241. Hercus and associates [121 demonstrated that nasopharyngeal temperature correlates well with the temperature of the cerebral cortex but lags slightly behind it during rapid cooling or warming. We think nasopharyngeal temperature reflects accurately the heat content of the head and neck, a consistently well-perfused part of the body, and have chosen this temperature as the "core" or vital organ temperature to be used as a basis for comparison with the temperature of extremities. In the present study, nasopharyngeal temperature was less well maintained after CPB in patients who had extremities less than or equal to 30.0"C at termination of CPB than it was in those with warmer extremity skin or muscle temperatures. There are several possible explanations. 1. The inability of patients with cold extremities to increase heat production or cardiac output adequately to repay heat debts incurred prior to termination of CPB 2. Marked differences in the magnitude of the heat debt present 3. Continued heat loss at a rate greater than the available heat production In all patients, heat production by skeletal muscle activity was suppressed to the same extent (80 to 90% evoked twitch depression) by pharmacologically induced neuromuscular blockade. All patients, regardless of extremity temperature, survived the immediate period after CPB without major therapeutic intervention (e.g., intraaortic balloon assist) and demonstrated adequate cardiac output as judged by clinically acceptable perfusion of major organs, although cardiac output was not measured in most patients. No correlation was established between nasopharyngeal temperature after CPB

5 40 The Annals of Thoracic Surgery Vol 29 No 1 January 1980 and the use of vasopressors, vasodilators, or anesthetics known to accelerate heat loss by altering cutaneous blood flow [131. Other major sources of heat loss, such as proportion of body surface exposed, ambient temperature, anesthetic apparatus and the use of unwarmed gases [61, and intravenous fluid therapy, were comparable for all patients. Intense peripheral vasoconstriction can produce delayed warming of the extremities [201, but in our study, no patients received a vasopressor infusion prior to or at termination of CPB. We attribute the range or corelperiphery temperature gradients observed at the end of CPB to individual differences in the total caloric requirements for complete warming. Although all patients underwent a similar duration of warming time, mean body mass was found to be significantly less in patients with extremity temperatures greater than 30.0"C than it was in patients with colder extremities at the end of CPB. As is common practice, total body perfusion with warmed blood during CPB was regulated according to estimated body surface area, which varies as the square of the scale factor of patient size. Although heat production and heat loss are proportional to body surface area [3], body mass and heat content vary as the cube of the scale factor. We suggest that in larger patients a heat debt develops that is out of proportion to the usual adjustment of perfusion flow rate. Consequently, the larger patients would be most likely to undergo incomplete reversal of generalized hypothermia despite normalization of core temperature. The direct correlation between metabolic rate and corelperiphery temperature gradients in unanesthetized humans is well established [171 and has been described in detail [lll. Under the conditions of minimal anesthetic depth and incomplete muscle paralysis [71 common just prior to termination of CPB, the temperature gradients observed in the present study are of sufficient magnitude to stimulate shivering or nonshivering thermogenesis and increase a patient's metabolic rate to two to three times the basal value. This estimate is supported by the study of Dyde and Lunn 181 who observed patients undergoing thoracotomy and found a heat debt proportional to the degree of spon- taneously occurring peripheral hypothermia. They estimated that the caloric deficit associated with extremity temperatures of 32 C required a 200% increase in total body oxygen consumption during emergence from anesthesia. The associated demands for increased cardiac output and myocardial oxygen delivery would be of particular concern in patients with coronary artery disease. The cardiovascular implications of the massive increases in total body oxygen usage noted in fully awake, grossly shivering patients in the immediate postoperative period are obvious [l, 191. We have demonstrated significant temperature gradients between core and peripheral sites at termination of CPB in 29% of the patients studied. The presence of these gradients was not predictable from observations of core temperature alone, and we conclude that monitoring of both core and upper extremity temperatures during CPB provides a more accurate index of the adequacy of warming following hypothermic perfusion. Skin temperature measurement as described here is a noninvasive technique, which, under the conditions of this and a previous study utilizing subcutaneous placement of thermistors [221, appears to provide information equivalent to that obtained from intramuscular monitoring. Although the relationship between mild central or peripheral hypothermia and patient morbidity and mortality remains, to be evaluated, confirmation of full reversal of induced generalized hypothermia would avoid the unnecessary increases in oxygen consumption and cardiac output that can accompany unsuspected hypothermia following CPB. References 1. Bay J, Nunn JF: Oxygen consumption during recovery from anaesthesia. Br J Anaesth 39:518, Bernhard WF, Carroll SE, Schwartz HF, et al: Metabolic alterations associated with profound hypothermia and extracorporeal circulation in the dog and man. J Thorac Cardiovasc Surg 42:793, Bernstein LM, Johnston LC, Ryan R, et al: Body composition as related to heat regulation in women. J Appl Physiol 9:241, Boylan JW, Hong SK: Regulation of renal function in hypothermia. Am J Physiol211:1371,1966

6 41 Muravchick, Conrad, and Vargas: Peripheral Temperature Monitoring during CPB 5. Brauer RW, Holloway RJ, Krebs JS, et al: The liver in hypothermia. Ann NY Acad Sci 80:395, Brock L, Skinner JM, Manders JT: The importance of peripheral vasoconstriction in influencing body temperatures and the part played by certain environmental factors: the effect of inhaled gases. Br J Anaesth 49:755, Conrad DP, Muravchick S: Hypothermia and neuromuscular blockade by pancuronium in man. Presented at the annual meeting of the American Society of Anesthesiologists, New Orleans, LA, Oct, 1977, Abstracts of Scientific Papers, p Dyde JA, Lunn HF: Heat loss during thoracotomy. Thorax 25:355, Fedor EJ, Fisher B, Lee SH: Rewarming following hypothermia of two to twelve hours: I. Cardiovascular effects. Ann Surg 174:515, Feldman S: Anaesthesia for cardiac surgery. Int Anesthesiol Clin 5:132, Hayward JS, Eckerson JD, Collis ML: Thermoregulatory heat production in man: prediction equation based on skin and core temperatures. J Appl Physiol 42:377, Hercus V, Cohen D, Bowring AC: Temperature gradients during hypothermia. Br Med J 2:1439, Little DM Jr: Hypothermia. Anesthesiology 20: 842, Matthews HR, Meade JB, Evans CC: Peripheral vasoconstriction after open heart surgery. Thorax 29:338, Morris RH, Wilkey BR: The effects of ambient temperature on patient temperature during sur- gery not involving body cavities. Anesthesiology 32:102, Moyer JH: The effect of hypothermia on renal function and renal damage from ischemia. Ann NY Acad Sci 80:424, Nadel ER, Horvath SM, Dawson CA, et al: Sensitivity to central and peripheral thermal stimulation in man. J Appl Physiol 29:603, Newman BJ: Control of accidental hypothermia. Anaesthesia 26:177, Roe CF, Goldberg MJ, Blair CS, et al: The influence of body temperature on early postoperative oxygen consumption. Surgery 60:85, Ross BA, Brock L, Anysley-Green A: Observations on central and peripheral temperatures in the understanding and management of shock. Br J Surg , Sellick BA: Induced hypothermia. Int Anesthesiol Clin 5:118, Smith NT: Subcutaneous, muscle, and body temperatures in anesthetized man. J Appl Physiol 17:306, Stephen CR, Dent SJ, Hall KD, et al: Physiologic reactions during profound hypothermia with cardioplegia. Anesthesiology 22:873, Stupfel M, Severinghaus JW: Internal body temperature gradients during anesthesia and hypothermia and effect of vagotomy. J Appl Physiol 9:380, Tarhan S, White RD, Moffitt EA: Anesthesia and postoperative care for cardiac operations (collective review). Ann Thorac Surg 23:173, Vandam LD, Bumap TK: Hypothermia. N Engl J Med 26196, 1959

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