Afterdrop following cardiopulmonary bypass results from redistribution of body heat to inadequately warmed peripheral tissues. However, the distribution of heat between the thermal compartments and the extent to which core-to-peripheral redistribution contributes to post-bypass hypothermia remains unknown.
Patients were cooled during cardiopulmonary bypass to nasopharyngeal temperatures near 31 degrees C (n=8) or 27 degrees C (n=8) and subsequently rewarmed by the bypass heat exchanger to approximately 37.5 degrees C. A nasopharyngeal probe evaluated core (trunk and head) temperature and heat content. Peripheral compartment (arm and leg) temperature and heat content were estimated using fourth-order regressions and integration over volume from 19 intramuscular needle thermocouples, 10 skin temperatures, and "deep" foot temperature.
In the 31 degrees C group, the average peripheral tissue temperature decreased to 31.9+/-1.4 degrees C (means+/-SD) and subsequently increased to 34+/-1.4 degrees C at the end of bypass. The core-to-peripheral tissue temperature gradient was 3.5+/-1.8 degrees C at the end of rewarming, and the afterdrop was 1.5+/-0.4 degrees C. Total body heat content decreased 231+/-93 kcal. During pump rewarming, the peripheral heat content increased to 7+/-27 kcal below precooling values, whereas the core heat content increased to 94+/-33 kcal above precooling values. Body heat content at the end of rewarming was thus 87+/-42 kcal more than at the onset of cooling. In the 27 degrees C group, the average peripheral tissue temperature decreased to a minimum of 29.8 +/-1.7 degrees C and subsequently increased to 32.8+/-2.1 degrees C at the end of bypass. The core-to-peripheral tissue temperature gradient was 4.6+/-1.9 degrees C at the end of rewarming, and the afterdrop was 2.3+/-0.9 degrees C. Total body heat content decreased 419+/-49 kcal. During pump rewarming, core heat content increased to 66+/-23 kcal above precooling values, whereas peripheral heat content remained 70+/-42 kcal below precooling values. Body heat content at the end of rewarming was thus 4+/-52 kcal less than at the onset of cooling.
Peripheral tissues failed to fully rewarm by the end of bypass in the patients in the 27 degrees C group, and the afterdrop was 2.3+/-0.9 degrees C. Peripheral tissues rewarmed better in the patients in the 31 degrees C group, and the afterdrop was only 1.5+/-0.4 degrees C.
CORE temperature is often deliberately reduced in patients undergoing cardiac surgery because even mild hypothermia provides substantial protection against cerebral ischemia. [1,2]Target core temperatures vary considerably among centers, but values between 28 and 32 [degree sign]C are typical. On completion of surgery, patients are rewarmed using the bypass pump. This procedure rapidly increases core temperature to normal or even hyperthermic values. Discontinuation of bypass warming, however, is frequently associated with a rapid decrease in core temperature. [3–5]The resulting hypothermia may trigger shivering, [dagger, dagger] inhibit coagulation, increase myocardial stress, and reduce resistance to surgical wound infections. 
Precipitous core hypothermia after cardiopulmonary bypass is reminiscent of the decrease after induction of general or epidural anesthesia and to the afterdrop observed when aggressive warming is initiated in persons with accidental hypothermia. [12,13]Indeed, core hypothermia in all three cases is believed to arise similarly from the core-to-peripheral redistribution of body heat. Consistent with this theory, postbypass hypothermia can be ameliorated by vasodilation with nitroprusside or prolonged rewarming. 
Cardiopulmonary bypass is thus associated with large thermal perturbations, both deliberate and unintentional, that have significant clinical consequences. Interestingly, however, body heat balance and regional heat distribution have yet to be evaluated during and after cardiac surgery. The extent to which body heat content decreases during cooling therefore remains unknown, as does the adequacy of body heat replenishment during rewarming. Also unknown is how heat is distributed between the thermal compartments, and the extent to which core-to-peripheral redistribution contributes to postbypass hypothermia. Therefore we measured body heat content and regional heat distribution in patients undergoing cardiopulmonary bypass. Because all these factors are likely to depend on the target bypass temperature, we evaluated patients maintained at nasopharyngeal temperatures near 31 [degree sign]C and 27 [degree sign]C.
Materials and Methods
With approval from the Committee on Human Research at the University of Vienna and written informed patient consent, we studied 16 patients undergoing elective cardiac surgery. All patients had left-ventricular ejection fractions >40%. We enrolled only patients ages 20 - 80 yr in whom we did not anticipate the need for intra- or postoperative vasoactive medications. Patients with a body mass index >30 or classified as American Society of Anesthesiologists physical status IV were excluded.
Patients were premedicated with 10 mg oral diazepam. Anesthesia was induced by intravenous administration of 0.25 mg/kg etomidate, 0.1 mg/kg midazolam, 5 [micro sign]g/kg fentanyl, and 0.1 mg/kg pancuronium. The patients' tracheas were intubated and mechanical ventilation adjusted to maintain end-tidal carbon dioxide tension near 35 mmHg. Anesthesia was maintained with 0.3 mg/h fentanyl and 4 mg/h midazolam in oxygen and air. After induction of anesthesia, a central-venous catheter was inserted into the superior vena cava and another into a radial artery.
Eight patients were cooled during cardiopulmonary bypass to a nasopharyngeal temperature of 30.8 +/- 1 [degree sign]C, and eight were cooled to 27.2 +/- 1.3 [degree sign]C. Bypass temperature was not randomly assigned; instead, they were assigned by the surgeons based on anticipated difficulty of the procedure. Five of the patients in the warmer (31 [degree sign]C) group had coronary bypass grafting and three had valve replacements. All took vasoactive medications before surgery (i.e., nitroglycerin, beta-blocking drugs, inhibitors of angiotensin converting enzyme, or all three). Two of the patients in the cooler (27 [degree sign]C) group had coronary bypass grafting, one had a valve replacement, and five underwent a Ross procedure (pulmonary-to-aortic valve switch). Only three of these patients took vasoactive medications before surgery.
The arterial cannulation site was the ascending aorta, and topical cardiac cooling was not used. The bypass pump was primed with 2,000 ml lactated Ringer's solution, and bypass flow was maintained at 2.5 l/m2. A membrane oxygenator was used in all cases. Patients were then rewarmed to a nasopharyngeal temperature near 37.5 [degree sign]C in both groups. Rewarming was accomplished using the heat exchanger on the cardiopulmonary bypass machine. The initial fluid - blood gradient was near 8 [degree sign]C, and arterial inflow temperature never exceeded 37.5 [degree sign]C. Cardiopulmonary bypass was subsequently discontinued and patients were transferred intubated and sedated to the intensive care unit or postoperative recovery unit. Patients in each group were covered by standard surgical draping; no active surface warming was used during the study.
Blood pressures and heart rates were recorded at 5-min intervals (Hellige, Inc., Freiburg, Germany), along with arterial saturation and end-tidal carbon dioxide tension (Drager, Lubeck, Germany). Vasomotor status was evaluated using forearm minus fingertip and calf minus fingertip skin-temperature gradients. Gradients exceeding 0 [degree sign]C were considered evidence of significant vasoconstriction because this value correlates with clinically important isolation of the core and peripheral thermal compartments. Core temperatures were recorded from the nasopharynx. Mean skin-surface temperatures were determined from 15 area-weighted sites. 
Arm and leg tissue temperatures were determined as previously described. Briefly, the length of the thigh (groin to mid-patella) and lower leg (mid-patella to ankle) were measured in centimeters. Circumference was measured at the mid-upper thigh, mid-lower thigh, mid-upper calf, and mid-lower calf. At each circumference, right leg muscle temperatures were recorded using, 8-, 18-, and 38-mm-long, 21-gauge needle thermocouples (Mallinckrodt Anesthesiology Products, St. Louis, MO) inserted perpendicular to the skin surface. Skin surface temperatures were recorded immediately adjacent and directly posterior to each set of needles. Subcutaneous temperature was measured at the ball of the foot using a Coretemp (Terumo Medical Corp., Tokyo, Japan)“deep tissue” thermometer. This device estimates tissue temperature [almost equal to] 1 cm below the skin surface and was used instead of inserting needles into the foot.
The lengths of the right arm (axilla to elbow) and forearm (elbow to wrist) were measured in centimeters. The circumference was measured at the mid-point of each segment. As in the right leg, 8-, 18-, and 38-mm-long needle thermocouples were inserted into each segment. Skin surface temperatures were recorded immediately adjacent to each set of needles. In addition, an 8-mm-long needle thermocouple was inserted directly into the adductor pollicis. Core, skin surface, and muscle temperatures were recorded from thermocouples connected to two calibrated Iso-Thermex 16-channel electronic thermometers (Columbus Instruments International, Columbus, OH) and Mon-a-Therm 6510 two-channel thermometers (Mallinckrodt Anesthesiology Products).
All temperatures were recorded using Mon-a-Therm thermocouples. Temperatures were recorded from thermocouples connected to calibrated Iso-Thermex 16-channel electronic thermometers having an accuracy of 0.1 [degree sign]C and a precision of 0.01 [degree sign]C (Columbus Instruments International). Temperatures were measured at 5-min intervals, starting [almost equal to] 30 min after induction of anesthesia.
The leg was divided into five segments: upper thigh, lower thigh, upper calf, lower calf, and foot. Each thigh and calf segment was further divided into an anterior and posterior section, with one third of the estimated mass considered to be posterior.
Anterior segment tissue temperatures, as a function of radial distance from the center of the leg segment, were calculated using skin surface and muscle temperatures using fourth-order regressions. Temperature at the center of the thigh was set to core temperature. In contrast, temperature at the center of the lower leg segments was estimated from the regression Equation withno similar assumption. Anterior limb heat content was estimated from these temperatures, as previously described, using the formula:Equation 1where Q sub (O [arrow right] r)(cal) is heat content of the leg segment from the center to the radius r, L (cm) is the length of the leg segment (i.e., groin to mid-thigh, mid-calf to ankle), [Greek small letter rho](g/cm3) is tissue density, s (cal [middle dot][degree sign]C-1[middle dot] g-1) is the specific heat of leg tissues, a0([degree sign]C) is the temperature at the center of the leg segment, and a2([degree sign]C/cm2) and a4([degree sign]C/cm (4)) are the fourth-order regression constants. The specific heat of muscle was taken as 0.89 cal [middle dot][degree sign]C-1[middle dot] g-1and density as 1.06 g/cm3. 
Rather than assume full radial symmetry, we assumed only that radial temperature distribution in the posterior leg segments would also be parabolic. Accordingly, we calculated the regression constant a2in the posterior leg segments from a0determined from the adjacent anterior segment and the posterior segment skin temperature. Posterior segment tissue heat contents were then determined from the quadratic version of Equation 1. Average segment tissue temperatures were determined by Equation 2: In another publication we described the derivation and limitations of these equations. 
"Deep temperature," measured on the ball of the foot, was assumed to represent the entire foot. Foot heat content thus was calculated by multiplying foot temperature by the mass of the foot and the specific heat of muscle. Average temperatures of the thigh and lower leg (calf and foot) were calculated by weighting values from each of the nine segments in proportion to their estimated masses. The right and left legs were treated comparably throughout this study, so we assumed that average tissue temperatures in the two limbs were similar.
Arm tissue temperature and heat content were calculated from parabolic tissue temperature regressions and the above equations. In the arms, we assumed full radial symmetry and thus did not separately calculate posterior segment values. Adductor pollicis temperature was assumed to represent that of the entire hand. Hand heat content thus was calculated by multiplying adductor pollicis temperature by the mass of the hand and the specific heat of muscle. As in the leg, average temperatures of the arm and forearm (forearm and hand) were calculated by weighting values from each of the three segments in proportion to their estimated masses.
Changes in trunk and head heat content were modeled simply by multiplying the weight of the trunk and head by the change in core temperature and the average specific heat of human tissues. Trunk and head weight was estimated by subtracting the calculated weight of the extremities (from the radial integration) from the total weight of each patient.
Afterdrop was defined as the decrease in core temperature after discontinuation of bypass. Similarly, the afterdrop time was defined by the period from the end of bypass until the minimum postbypass core temperature was observed. Results are expressed as means +/- SDs.
Morphometric and demographic characteristics of the patients were generally similar in each temperature group, although leg weight and peripheral fraction of the body mass were significantly greater in the patients cooled to 27 [degree sign]C. Most of the patients assigned to 31 [degree sign]C had coronary artery grafts, whereas most of those assigned to 27 [degree sign]C had a Ross procedure (Table 1).
The 31 [degree sign]C Group
Cooling required 66 +/- 40 min, and bypass lasted 128 +/- 4 min. Core temperature at the onset of bypass, [almost equal to] 1 h after induction of anesthesia, was 35.2 +/- 0.5 [degree sign]C, and decreased to a minimum of 30.8 +/- 1 [degree sign]C. The average peripheral tissue temperature at the onset of bypass was 34.2 +/- 0.9 [degree sign]C, decreased to a minimum of 31.9 +/- 1.4 [degree sign]C, and subsequently increased to 34 +/- 1.4 [degree sign]C at the end of bypass. Vasodilation occurred at 35.9 +/- 1 [degree sign]C after 21 +/- 4 min of rewarming. The core-to-peripheral tissue temperature gradient was 3.5 +/- 1.8 [degree sign]C at the end of rewarming. The core-temperature afterdrop was 1.5 +/- 0.4 [degree sign]C and lasted 40 +/- 12 min after bypass (Figure 1, Table 2). It was associated with a 0.9 +/- 0.9 [degree sign]C increase in peripheral tissue temperature. By the end of the afterdrop, 62% of the patients were again vasoconstricted.
Peripheral (arm and leg) tissue heat content at the onset of pump cooling was 923 +/- 180 kcal, whereas core (trunk and head) heat content was 1,414 +/- 288 kcal. Peripheral and core heat contents decreased 54 +/- 28 and 177 +/- 70 kcal, respectively, during bypass cooling. Total body heat content thus decreased 231 +/- 93 kcal. During pump rewarming, peripheral heat content increased to 7 +/- 27 kcal below precooling values, whereas core heat content increased to 94 +/- 33 kcal above precooling values. Body heat content at the end of rewarming was thus 87 +/- 42 kcal more than at the onset of cooling (Figure 2). Two patients in this group required small amounts of nitroglycerin during bypass.
The 27 [degree sign]C Group
Cooling required 114 +/- 46 min, and bypass lasted 180 +/- 44 min. Core temperature at the onset of bypass, [almost equal to] 1 h after induction of anesthesia, was 35.5 +/- 0.5 [degree sign]C and decreased to a minimum of 27.2 +/- 1.3 [degree sign]C. The average peripheral tissue temperature at the onset of bypass was 34.9 +/- 1.1 [degree sign]C, decreased to a minimum of 29.8 +/- 1.7 [degree sign]C, and subsequently increased to 32.8 +/- 2.1 [degree sign]C at the end of bypass. Vasodilation occurred at 36.6 +/- 1 [degree sign]C after 44 +/- 30 min of rewarming. The core-to-peripheral tissue temperature gradient was 4.6 +/- 1.9 [degree sign]C at the end of rewarming. The core temperature afterdrop was 2.3 +/- 0.9 [degree sign]C and lasted 56 +/- 15 min after bypass (Figure 1, Table 2). It was associated with a 1.5 +/- 0.9 [degree sign]C increase in peripheral tissue temperature. By the end of the afterdrop, 87% of the patients were again vasoconstricted.
Peripheral (arm and leg) tissue heat content at the onset of pump cooling was 1,144 +/- 299 kcal, whereas core heat content was 1,150 +/- 248 kcal. Peripheral and core heat contents decreased 170 +/- 72 and 249 +/- 50 kcal, respectively, during bypass cooling. Total body heat content thus decreased 419 +/- 94 kcal. During pump rewarming, core heat content increased to 66 +/- 23 kcal above precooling values, whereas peripheral heat content remained 70 +/- 42 kcal below precooling values. Body heat content at the end of rewarming was thus 4 +/- 52 kcal less than at the onset of cooling (Figure 2). One patient in this group required a small amount of nitroglycerin during bypass.
Our first tissue temperature measurements were somewhat delayed because positioning and connecting the approximately 30 thermocouples required for this study required [almost equal to] 30 min. By the time active cooling was initiated, about 1 h after induction of anesthesia, core (trunk and head) temperature was already near 35.5 [degree sign]C. This initial hypothermia presumably resulted from a core-to-peripheral redistribution of body heat, and the slight increase in peripheral tissue temperature in the 15 min before onset of cooling is consistent with this explanation. As intended, the cardiopulmonary bypass pump heat exchanger markedly reduced core temperature, and therefore core heat content, during cooling. The pump then returned core temperature to normothermic values near 37.5 [degree sign]C in each group. The core temperature triggering vasodilation (threshold) was near 36 [degree sign]C, which is consistent with previous observations. 
Peripheral tissue temperature also decreased markedly during cardiopulmonary bypass cooling. However, peripheral temperature and heat content in the extremities decreased considerably less than in the core. Tissue heat content decreased significantly more in patients in the 27 [degree sign]C group than in those in the 31 [degree sign]C group. Rewarming effectively repleted peripheral heat content in the patients in the 31 [degree sign]C group, but not in those cooled to 27 [degree sign]C. The core-to-peripheral tissue temperature gradients after rewarming were 3.5 +/- 1.8 [degree sign]C in the warmer patients and 4.6 +/- 1.9 [degree sign]C in the cooler patients, thus differing by about 1 [degree sign]C.
Afterdrop after accidental hypothermia results from a combination of conduction [21,22]and convection. [12,23]Conductive heat loss causes hypothermia when cold peripheral tissues continue to extract heat from the core, a noncirculatory heat transfer that can be demonstrated in a bag of gelatin or isolated leg of beef. Convection contributes to afterdrop when cutaneous warming provokes vasodilation in still-cold peripheral tissues, with subsequent recirculation of cold blood to the relatively warm core. The magnitude of afterdrop and the relative contribution of each mechanism depend on many factors, including the duration of hypothermia, rate at which cooling occurred, and the type of rewarming. [13,23,25,26]
Although both conduction and convection surely contribute to afterdrop after cardiopulmonary bypass, it is likely that convection dominates, as it does after induction of anesthesia. [10,11]Both mechanisms, however, depend entirely on the core-to-peripheral tissue temperature gradient. (The Second Law of Thermodynamics specifies that heat flows only down at temperature gradient). This gradient differed only by about 1 [degree sign]C in the patients in the 27 [degree sign]C and 31 [degree sign]C groups. However, the normal gradient is not zero, because otherwise heat could not be dissipated from the core; even in vasodilated persons, the gradient is near 2 [degree sign]C. The difference between the core-to-peripheral gradient and the normal (dilated) gradient was thus [almost equal to] 50% greater in the patients in the 27 [degree sign]C group. As might be expected from this difference, the afterdrop was [almost equal to] 35% greater in the colder patients. Redistribution of body heat was associated with significant peripheral tissue warming, with the warming being about 40% greater in the patients cooled to 27 [degree sign]C. A similar failure to fully rewarm and redistribution has been observed before; however, only one or two temperatures were evaluated in each study, which precluded accurate estimates of peripheral tissue heat content. [5,28,29]
Patients in our study were not randomly assigned to 31 [degree sign]C or 27 [degree sign]C. Cardiac surgical patients at the University of Vienna are routinely cooled to [almost equal to] 31 [degree sign]C; those assigned to 27 [degree sign]C were selected because the surgeons anticipated more difficult repairs. Consistent with this selection process, bypass times lasted nearly 1 h longer in the colder group. It is likely that the difference in bypass times contributed as much to the results as the temperature differences. Similarly, leg weight and the peripheral fraction of the total body mass was significantly greater in these patients, perhaps reflecting progression of their underlying disease. Results in the two groups therefore should be compared with caution because bypass temperatures were not randomly assigned and the patients in each group may not have been comparable.
Temperature and heat content changes within a group should also be extrapolated cautiously to other circumstances because they depend closely on body structure, duration and rate of warming and cooling, and the use of anesthetics and other vasoactive medications. For example, the afterdrop would likely have been substantially greater in the 27 [degree sign]C patients had they not been warmed to a plateau temperature 15 min longer than the patients cooled to 31 [degree sign]C. Conversely, the magnitude of the afterdrop would presumably have been reduced had rewarming been prolonged or vasodilating medications been given. Afterdrop magnitude also is less in pediatric patients, presumably because a smaller fraction of their body mass is peripheral. The methods described in this study can be used to quantify the effects of these and similar interventions on body heat content and distribution.
We did not try to estimate heat loss through the cardiopulmonary bypass machine because this is only one of many sources of heat loss and gain. Similarly, we did not measure heat flux or oxygen consumption because they were unlikely to accurately estimate systemic heat balance under the study conditions. Furthermore, we had no way of evaluating the perhaps substantial radiative and evaporative losses from within the surgical incisions. Consequently, we could not confirm that changes in core and peripheral tissue heat contents equaled the difference between metabolic rate and heat loss. Results were comparable with each measure of body heat content in previous studies, but it remains possible that core temperature was inhomogeneous during bypass. A consistent gradient within trunk tissues and the head would not affect our estimates of heat content changes. To the extent that temperature gradients changed during bypass, however, our estimates may be erroneous. Some error is likely, especially during the rapid perturbations induced by cardiopulmonary bypass, but our heat content estimates during the relatively steady state periods at the end of cooling, rewarming, and redistribution are likely to be reasonably accurate.
In conclusion, average peripheral tissue temperatures failed to fully rewarm by the end of bypass in the patients in the 27 [degree sign]C group, even though the rewarming period to plateau was 15 min longer than in the warmer patients. The core-to-peripheral tissue temperature gradient was thus [almost equal to] 1 [degree sign]C greater in the colder patients. Consistent with this difference, their afterdrop was about 35% greater than in the patients maintained at 31 [degree sign]C during bypass. Peripheral tissue warming during this body heat redistribution was about 40% greater in the colder patients. Under the circumstances of this study, cooling to 31 [degree sign]C was associated with better peripheral tissue rewarming and less afterdrop.