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1 Department of Physiology, The Medical School, University of Birmingham, Birmingham B15 2TT, UK2 Department of Physiology, University College Cork, Cork, Ireland
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Abstract |
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40% reduction in heart rate (HR), 10% fall in mean arterial blood pressure (MABP), and decreased glomerular filtration rate (GFR) by 50% and 5% in euthermic and acclimatized rats, respectively. At 25°C, urine flow increased some two-fold and absolute and fractional sodium excretions by 4- to 6-fold in the euthermic rats and to a lesser extent in the cold acclimatized rats, while basal levels of fluid excretion were higher in the acclimatized rats. A loss of pulsatility in the RSNA signal with cooling was seen in both groups. One of the factors contributing to modest hypotension during acute hypothermia is a reduction in RSNA. There was a progressive fall in the proportion of RSNA power at HR frequency with cooling of 20% in euthermic and 80% in acclimatized rats. All variables were restored to basal levels on rewarming in both groups of rats. We conclude that natriuresis and diuresis in euthermic rats during hypothermia is a consequence of a reduction in nephron reabsorption, reduced urine osmolality and possibly altered patterning of RSNA. In acclimatized rats, the response was modified by altered renal haemodynamics and/or hormonal influences induced by chronic cold exposure to minimize the hypothermic stress on renal function.
(Received 21 January 2004;
accepted after revision 29 April 2004; first published online 29 April 2004)
Corresponding author S. Egginton: Department of Physiology, The Medical School, University of Birmingham, Vincent Drive, Birmingham B15 2TT, UK. Email: s.egginton{at}bham.ac.uk
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Introduction |
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As mean arterial blood pressure (MABP) remains nearly constant at lower temperatures, despite a large fall in the cardiac output (Granberg, 1991), the lower RBF must reflect an increased RVR. This would result primarily from an increased resistance of afferent arterioles, due to a combination of higher blood viscosity and increased vasoconstriction (Chapman et al. 1975; Withey et al. 1976; Broman & Källskog, 1995). During hypothermia there may be an increase in the plasma and urinary concentrations of catecholamines (Granberg, 1991), and also an increased responsiveness to noradrenaline in various vascular beds (Speziali et al. 1994). However, a later report (Broman et al. 1998a) showed that cold-induced renal vasoconstriction is not due to an increased renal sympathetic nerve activity (RSNA) or catecholamine-mediated activation of renal 
1-adrenoceptors. Nonetheless, altered patterning of renal nerve discharge could be another factor leading to the raised RVR during hypothermia. It is also important to acknowledge that the renal sympathetic nerves also innervate the tubules, and may therefore modulate tubular fluid reabsorption under hypothermic conditions (Baraja et al. 1992).
Rodents have warm and cold receptors in the skin which display distinct firing rate responses when stimulated. Generally, the static discharge activity peaks at skin temperatures of 25–27°C for cold receptors and 40–45°C for warm receptors (Spray, 1986), with maximum tonic activity at 31°C and 42°C, respectively (Hellon et al. 1975). Afferent impulses from the thermal receptors are integrated within the higher brain centres to modulate RSNA so as to ensure appropriate renal function, with the level of integrated RSNA reflecting a balance between actively discharging and silent renal nerve fibres (DiBona & Jones, 1998) that are recruited by changes in temperature. It may well be that chronic stimulation of these receptors, as may occur during acclimation to winter conditions, could reset and alter the pattern and sensitivity of the evoked responses.
This study was designed to examine the effects of acute hypothermia on parallel changes in cardiovascular homeostasis and renal function, and to determine whether they correlated with any altered patterning of RSNA. Responses were compared with rats exposed to lower environmental temperature and shortened photoperiod as we hypothesized that chronic cold exposure, akin to hibernating/winter conditions, would alter the neuro-hormonal responses to an acute hypothermic challenge.
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Methods |
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Surgical preparation
Gaseous anaesthesia, 4% halothane in oxygen, was gradually replaced with I.V. administration of a mixture of chloralose and urethane (32 and 450 mg kg–1; Sigma, UK), approximately 0.7 ml given over 35 min during which the halothane concentration was reduced to 0% and the oxygen switched off, followed by 0.05 ml every 30 min, in saline (150 mmol NaCl) at a rate of 3 ml h–1 via the right femoral vein. The animals were tracheotomised to aid spontaneous ventilation. Mean arterial blood pressure (MABP) and heart rate (HR) were measured via the right femoral artery catheter interfaced to a pressure transducer (MLT105, Precision, UK), with cannula patency maintained using heparinized saline [20 U heparin (ml saline)–1]. Blood pressure signals were amplified (PowerLab, AD Instruments, UK) and together with heart rate signals were recorded on a microcomputer (iMac DV) running a data acquisition program (CHART 4) at a sampling rate of 1000 Hz. Animals were placed on a plate containing a system of tubes through which water was pumped and it was connected to a control unit to alter the water temperature such that core temperature (Tc), which was measured via an oesophageal thermistor (Thermocouple, UK) could be raised or lowered. Experiments were started 90 min after completion of surgery to allow the animal to stabilize renal function and renal nerve activity. At the end of each experiment, the animals were killed with an overdose of sodium pentobarbitone (Rhone-Merieux, Ireland). Half the rats were used to study the effect of hypothermia on renal function and the other half for recording renal nerve activity, in both cases euthermic and acclimatized groups consisted of n= 7 and n= 6 rats, respectively.
Basal levels of all variables were determined at Tc= 37°C (normal core temperature), a moderate level of hypothermia at Tc= 31°C (temperature at which shivering becomes evident and of maximum cold receptor activity), severe hypothermia at Tc= 25°C (temperature of clinical relevance and above the point of cardiac arrhythmias (Broman & Källskog, 1995) and on rewarming back to Tc= 37°C. The core temperature was changed, gradually, at a rate of 3°C every 15 min, and rats were maintained for 30 min at each appropriate Tc for data collection. It took 1–1.5 h to reduce the core temperature to 25°C and a further 1–1.5 h to rewarm to Tc= 37°C.
Renal function
The left kidney was exposed through a flank incision, and a catheter inserted into the left proximal ureter for the sampling of urine. A 2 ml bolus of inulin (Sigma, UK) in saline was given as a primer (15 mg ml–1) immediately after surgery, followed by an infusion of saline containing 15 mg ml–1 inulin at 3 ml h–1 throughout the remainder of the experiment. A series of four 15 min urine collections and four blood samples (from the femoral artery) were taken at Tc= 37°C, on cooling to 31°C, at 25°C and on rewarming to 37°C, respectively. Blood samples, 0.4 ml were taken, centrifuged 13 500 g at 20°C, the plasma samples removed and thereafter the red cells were resuspended in an equivalent volume of saline and injected back into the circulation. Urine and plasma inulin concentrations were analysed as described previously (Johns & Manitius, 1986) using spectrophotometer analysis (Labsystems Multiskan MS 4.0, UK) at a wavelength of 640 nm. Plasma and urine electrolytes were assayed using a flame photometer (Corning model 410C; Fisher Scientific, Leicestershire, UK). Urine osmolality was measured by the freezing point depression technique on an osmometer (Advanced Micro-Osmometer, Model 3MO, Vitech Scientific Ltd, Partridge Green, W. Sussex, UK). Urine flow (UV), absolute sodium excretion (UNaV) and fractional sodium excretion (FENa) were estimated, and glomerular filtration rate (GFR) was calculated as clearance of inulin.
Renal nerve activity
Following cannulation of the bladder, the left kidney was exposed through a flank incision and its ureter cannulated. A renal nerve bundle was identified, isolated at the angle between the aorta and left renal artery, placed on bipolar electrodes and sealed using silicone gel 932A & 932B (Wacker, Germany).
RSNA was recorded using an optically isolated amplifier (Grayden Electronics, UK) and fed through filters set at 0.1 Hz and 1 kHz to remove low and high frequency noise. The amplified nerve signal was fed onto the microcomputer, via an I/O board, running a data acquisition program written in LabView (version 3.0). RSNA was then rectified, integrated and expressed in millivolts (mV) over 1 s intervals (sampled at a rate of 1000 Hz), with a mean value estimated over each 3.5 min data collection. The amount of integrated RSNA recorded in the present study represents a combination of both afferent and efferent nerve activity, but any contribution of afferent activity is likely to be very low, being in the order of µV s–1 (Kopp & DiBona, 1992) compared with mV s–1 in the present study. Further, the greater random firing of the afferent fibres would make virtually no contribution to the power spectral signal (Davis & Johns, 1995), which is our main area of interest. Thirty minutes after the animal was killed, a background noise level of RSNA was recorded as postmortem nerve activity, which was later subtracted from the results to reveal the dynamic RSNA.
Blood pressure (BP) and RSNA signals were then transformed and expressed in the frequency domain, using microprocessors and software from LabView that allowed the application of Fourier transformation to generate a power spectrum from 1 to 10 Hz, from a 60 s high frequency (1 kHz) sample. This recording was divided into three 20 s samples, which were further subdivided into two halves. Next, 210 points from each half was passed through a Hanning filter to minimize the interference from noise by avoiding spectral leakage. A power spectrum for each variable was calculated and the sum of the three parts determined. Over this range, there was a prominent peak, usually between 6 and 8 Hz, at normal core temperature (Tc= 37°C), that corresponded to HR frequency, with a smaller peak appearing in the range of respiration frequency (Davis & Johns, 1996). The total power in a spectrum was derived as the area under the curve from 0 to 10 Hz. The power at HR frequency for RSNA was determined by finding the maximum peak in the power spectra of BP that corresponds to heart rate frequency (± 0.1 Hz) and using this value to define power in the RSNA signal. Absolute power at heart rate (mV2) was determined by measuring the power in the renal nerve spectra at HR frequency. The percentage power at HR frequency was calculated as a fraction of total power that occurred at HR frequency.
Statistical analysis
All data represent the average value calculated from individual rats and are expressed as mean ±S.E.M. Statistical evaluation was performed using factorial and repeated measures (hierarchical) analysis of variance (ANOVA), with Fisher's protected least squares difference (PLSD) to estimate the posthoc significance (StatView; SAS Institute, Cary, NC, USA). Statistical significance was accepted at P < 0.05.
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Results |
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There was a progressive decrease in HR and MABP in both euthermic and acclimatized rats with cooling. Figure 1 shows that there was 40% reduction in HR at 25°C (253 ± 6 b.p.m.) versus basal levels taken at 37°C (428 ± 6 b.p.m.) (P < 0.001), while there was 10% reduction of MABP at 25°C (99 ± 2 mmHg) versus 37°C (107 ± 2 mmHg) (P < 0.01) in euthermic rats. Basal levels of HR and MABP at 37°C for the acclimatized rats were not significantly different from those of euthermic animals (424 ± 12 b.p.m. and 112 ± 1 mmHg, respectively). Reduction of Tc to 25°C in the acclimatized rats resulted in 35% reduction in HR (271 ± 5 b.p.m.) (P < 0.001) and 15% reduction in MABP (94 ± 3 mmHg) (P < 0.001) versus 37°C. At Tc= 25°C, bradycardia in euthermic rats was more pronounced than acclimatized rats (P < 0.05). In both groups MABP and HR returned at or above precooling levels on rewarming (Fig. 1).
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Basal values for GFR were similar in euthermic and acclimatized rats at Tc= 37°C. Chronic cold exposure produced increased baseline levels of UV, UNaV, FENa and decreased baseline level of urine osmolality in acclimatized rats when compared to the euthermic group. Urine osmolality was 18% lower (P < 0.05) in acclimatized rats at Tc= 37°C compared to euthermic animals, which reduced further by 50%(P < 0.01) and 40%(P < 0.001) in euthermic and acclimatized rats at Tc= 25°C, respectively, with almost complete recovery on rewarming. Reduction of Tc produced a progressive decrease in GFR of 50%(P < 0.05) at 25°C in euthermic rats, whereas in acclimatized rats, there was an abrupt decrease in GFR at 31°C by 65% (P < 0.01) but thereafter increased with further cooling to 25°C (Table 1) reaching a level no different from basal, and to a degree that was significantly higher than euthermic rats at that Tc. In euthermic rats, there was a twofold increase in UV (P < 0.05), a four to eightfold increase in UNaV (P < 0.05) and FENa (P < 0.01) at Tc= 25°C versus basal levels taken at Tc= 37°C. A different pattern of response was observed in acclimatized rats in that there was an initial increase in urine osmolality with reduced levels of UNaV and FENa at Tc= 31°C. This was followed by a 35% decrease (P < 0.01) in urine osmolality, 20% increase in UV, 35% increase in UNaV and 50% increase in FENa (P < 0.01) with further cooling to a core temperature of 25°C (Table 1).
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RSNA, percentage power at HR frequency, total power and absolute power were all normalized to 100% at Tc= 37°C. RSNA reduced by 10%(P < 0.05) and 20%(P < 0.05) in euthermic and acclimatized rats, respectively, at Tc= 25°C (Table 2). Figure 2 shows that there was a change in pulsatility in the nerve signal as temperature was reduced to 25°C that was restored on rewarming. There was a reduction in percentage power at HR frequency in both groups of rats at Tc= 25°C, but the magnitude of the fall in the acclimatized rats was fourfold greater than that of euthermic rats (Fig. 3 and Table 2) despite an attenuated bradycardia in euthermic rats. RSNA at HR frequency in euthermic rats was reduced by 20% but in acclimatized rats it was reduced by 80% (P < 0.01) at 25°C versus basal levels taken at 37°C (Figs 2 and 3 and Table 2). There was a fall in total power of RSNA at Tc= 25°C, 20% and 40%(P < 0.05) in euthermic and acclimatized rats, respectively, while absolute power of RSNA at HR frequency was also reduced (20% in euthermic and 35% in cold-acclimatized rats, P < 0.05). However, on rewarming to 37°C there was an overshoot in some variables into a value significantly higher than basal levels (Table 2).
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Discussion |
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During acute hypothermia, RSNA decreased in both euthermic and acclimatized rats at 25°C but to a greater extent in the acclimatized rats, which could have contributed to the larger fall in blood pressure in these rats. At Tc= 31°C MABP and RSNA were not altered in either group suggesting that the decreases in these parameters at 25°C were due to central nervous system control mediated via the autonomic nervous system. RSNA has been used as an index of overall sympathetic nerve responses, but it does not rule out the possibility that as regional differences following physiological challenges in cardiac and renal nerves have been reported (Matsukawa et al. 1993). Of note was the observation that the RSNA showed a decreased pulsatility in the signal at heart rate frequency with cooling, presumably resulting from an altered patterning from the central nervous system, that approched control levels on rewarming. Exactly how the underlying mechanisms cause these changes is unclear at present. It has been suggested in other studies that hypothermia produces non-uniform and differential responses in activity of peripheral sympathetic nerves such that the cardiac-related pattern of renal, splanchnic and lumbar sympathetic activity is altered, despite the presence of pulse-synchronous activity in arterial baroreceptor afferent nerves (Kenney et al. 1999).
The marked bradycardia during hypothermia has been attributed to multiple factors including a direct effect of temperature on SA node discharge (Schneider & Gillis, 1966), a fall in cardiac output, an increased total peripheral resistance (Granberg, 1991), a reduction in metabolic rate with core temperature (Wong, 1983) and/or an increase in the degree of vagal tone (Zheng et al. 1996). It was evident that prior cold-acclimatization and subsequent induction of hypothermia to 25°C in acclimatized rats resulted in a less pronounced bradycardia when compared to the euthermic group suggesting an adaptive mechanism that involved either an altered central drive or peripheral responsiveness. Interestingly, the process of cold acclimatization did not change the core temperature or body mass of the acclimatized rats as reported in a previous study (Deveci et al. 2001), which would suggest that the adaptive response was driven by activity of peripheral temperature sensors in the skin.
In an earlier report from our laboratory (Deveci & Egginton, 1999), total renal blood flow (RBF) was found to be reduced in both euthermic and acclimatized rats by 40% during acute hypothermia, and would reflect an increase in RVR. As MABP remained nearly constant at Tc= 25°C in the present study, the fall in GFR was most probably due to an increased tone in the resistance arterioles, which would reduce glomerular filtration pressure and hence filtration rate. In spite of the fall in filtration rate, the reduced Tc caused progressive increases in UNaV and FENa, and this was most probably a consequence of the decreased temperature on energy requiring sodium reabsorptive processes at the proximal tubule and the thick limb of the ascending loop of Henle. This would be supported by the observation of a decreased osmolality in the urine with cooling, and is consistent with other studies reporting hypothermia to decrease antidiuretic hormone (ADH) secretion (Broman et al. 1998b) and to cause a redistribution of blood flow to different organs (Giesbrecht & Bristow, 1997; Hultström et al. 2003). Even though there was a decrease in RSNA at Tc= 25°C in both groups of rats, it is unlikely that a change of this magnitude could play a major role in causing the large changes in fluid excretion at lower temperatures.
Studies in adult animals have demonstrated an activation of sympathetic nervous system (Bruck, 1992; Zeisberger, 1998; DiBona, 2003), renin–angiotensin and vasopressin systems during cold exposure (Cassis, 1993; Toner & McArdle, 1996) that could alter the sensitivity of the neuro-hormonal balance regulating body fluid volume and fluid excretion in acclimatized rats. In the acclimatized rats, the fall in GFR at Tc = 31°C probably reflected an increased RVR, but further cooling to Tc of 25°C associated with a raised GFR would be indicative of a further change in the balance between the afferent and efferent arteriolar resistances. The fall in UV and UNaV at Tc= 31°C may be a consequence of the large reduction in filtered load, but at Tc = 25°C the higher GFR would have contributed to an increase in UNaV, UV and FENa in addition to a direct effect of temperature on the reabsorptive process of the tubular epithelial cells. This would suggest that there was a transition of regulatory control of renal haemodynamics between moderate and severe hypothermia in the acclimatized rats.
The RSNA spectral analysis demonstrated that in both groups of rats there were falls in total power, absolute power at HR frequency and percentage power of RSNA at HR frequency at Tc= 25°C which were greater in acclimatized than euthermic rats. One possible explanation is that in the former group of rats there was a decreased defence response, that is, an increased sympathetic tone leading to vasoconstriction on chronic exposure to cold. There is evidence in the literature to suggest several adaptive adjustments during cold acclimation including a range of morphometric changes (Deveci & Egginton, 2002), elevations in obligatory and regulatory non-shivering thermogenesis (Chaffee & Roberts, 1971; Jansky, 1979), increases in sympathetic innervation of brown adipose tissue (Himms-Hagen, 1990), enhanced metabolic activity (Jansky, 1979) and elevations in plasma and tissue catecholamines (Leduc, 1961; Young et al. 1982). Some of the RSNA variables did not return to precooling levels immediately on rewarming, indeed, there was an initial overshoot when compared with the normal core Tc. It is probable that the altered patterning of the nerve signal was not fully compensated over this period and would require a longer time to regain basal levels.
In this study we focused mainly on percentage power at HR frequency at different temperatures, in an attempt to correlate neural patterning with the cardiovascular changes. Previous work had shown 50% fall in respiratory frequency during hypothermia in both euthermic and acclimatized rats that could be due to decreased inspiratory neuronal activity and/or unloading of pulmonary stretch receptors. As the responses were similar in both groups of animals, it was suggested that the adaptive response evoking thermogenesis in acclimatized rats could be limited by oxygen delivery (Egginton et al. 2001). However, it is important to note that the change in HR peak was more profound than that at the respiration peak, indicating a possible redistribution of power across the spectrum during hypothermia. This compliments the systemic response to hypothermia, where the reduced metabolic rate lessens the respiratory drive, but the impaired cardiac contractility and increased afterload (Schneider & Gillis, 1966) would suggest that redistribution of neural outflow was required to increase activity of the cardiac sympathetic fibres in a compensatory manner. The decreased total power in both groups of rats during hypothermia suggests that the central drive modulates the sympathetic tone to the kidneys for renal homeostasis during adverse conditions.
The findings of the present study indicate that there are autonomic, cardiovascular and renal adaptive mechanisms operative on reducing core temperature below 31°C contributing to a differential response between the euthermic and acclimatized rats. Natriuresis and diuresis is most likely a consequence of a temperature-induced reduction in reabsorptive activity of the tubular epithelial cells of the nephron, decreased urine osmolality and with minor contributions from the renal sympathetic nerves. In acclimatized rats, hormones and/or some other autonomic reorientation induced by chronic cold exposure and concomitant reduction in photoperiod appears to modify the responses and minimize the stress to the acute hypothermic challenge in relation to renal function.
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References |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Baraja L, Liu L & Powers K (1992). Anatomy of the renal innervation: intrarenal aspects and ganglia of origin. Can J Physiol Pharmacol 70, 735–749.[Medline]
Boylan
JW
&
Hong
SK (1966). Regulation of renal function in hypothermia. Am J Physiol
211, 1371–1378.
Broman M & Källskog Ö (1995). The effects of hypothermia on renal function and haemodynamics in the rat. Acta Physiol Scand 153, 179–184.[Medline]
Broman M, Källskog Ö, Kopp UC & Wolgast M (1998a). Influence of the sympathetic nervous system on renal function during hypothermia. Acta Physiol Scand 163, 241–249.[CrossRef][Medline]
Broman M, Källskog Ö, Nygren K & Wolgast M (1998b). The role of antidiuretic hormone in cold-induced diuresis in the anaesthetized rat. Acta Physiol Scand 162, 475–480.[CrossRef][Medline]
Bruck K (1992). Neonatal thermal regulation. In Fetal and Neonatal Physiology, ed. Polin, RA, Fox, WWÍ, pp. 488–515. Saunders, Philadelphia.
Cassis LA (1993). Role of angiotensin II in brown adipose thermogenesis during cold acclimation. Am J Physiol 265, E860–E865.
Chaffee RR & Roberts JC (1971). Temperature acclimation in birds and mammals. Annu Rev Physiol 33, 155–202.[CrossRef][Medline]
Chapman BJ, Munday KA & Withey WR (1975). Arterial blood pressure changes and renal blood flow during hypothermia. J Physiol 244, 91P–92P.
Davis G & Johns EJ (1995). Renal sympathetic nerve responses to somato-sensory nerve stimulation in normotensive rats. J Auton Nerv Syst 54, 59–70.[CrossRef][Medline]
Davis G & Johns EJ (1996). Renal nerve responses to somatic nerve activation in stroke-prone spontaneously hypertensive rats. J Auton Nerv Syst 61, 209–217.[CrossRef][Medline]
Deveci D & Egginton S (1999). Development of the fluorescent microsphere technique for quantifying regional blood flow in small mammals. Exp Physiol 84, 615–630.[Abstract]
Deveci D & Egginton S (2002). The effects of reduced temperature and photoperiod on body composition in hibernator and non-hibernator rodents. J Therm Biol 27, 467–478.[CrossRef]
Deveci D, Stone PC & Egginton S (2001). Differential effect of cold acclimation on blood composition in rats and hamsters. J Comp Physiol [B] 171, 135–143.[CrossRef][Medline]
DiBona
GF (2003). Thermoregulation. Am J Physiol Regul Integr Comp Physiol
284, R277–R279.
DiBona
GF
&
Jones
SY (1998). Reflex effects on components of synchronized renal sympathetic nerve activity. Am J Physiol
275, F441–F446.
Egginton S, Fairney JA & Bratcher J (2001). Effect of acute and chronic cooling on cardio-respiratory integration in rodents. J Physiol (Proceedings) 532, 19P.
Giesbrecht GG & Bristow GK (1997). Recent advances in hypothermia research. Ann N Y Acad Sci 813, 663–675.[Medline]
Granberg PO (1991). Human physiology under cold exposure. Arctic Med Res 50, 23–27.
Hellon
RF, Hensel
H
&
Schafer
K (1975). Thermal receptors in the scrotum of the rat. J Physiol
248, 349–357.
Himms-Hagen J (1990). Brown adipose tissue thermogenesis: interdisciplinary studies. FASEB J 4, 2890–2898.[Abstract]
Hultström M, Jansson L, Bodin B, Andersson A & Källskog Ö (2003). Moderate hypothermia and organ blood flow in anaesthetized rats: Effects of adenosine and adrenergic receptor inhibition. FASEB J 17, A1266.
Jansky L (1979). Nonshivering thermogenesis. Cesk Fysiol 28, 97–107.[Medline]
Johns EJ & Manitius J (1986). An investigation into the alpha-adrenoceptor mediating renal nerve-induced calcium reabsorption by the rat kidney. Br J Pharmacol 89, 91–97.[Medline]
Kenney
MJ, Claassen
DE, Fels
RJ
&
Saindon
CS (1999). Cold stress alters characteristics of symapthetic nerve discharge bursts. J Appl Physiol
87, 732–742.
Kopp UC & DiBona GF (1992). The neural control of renal function. In: The Kidney: Physiology and Pathophysiology, Vol. 33 ed. Giebisch, S, pp. 1157–1204. Raven press, New York.
Leduc J (1961). Catecholamine production and release in exposure and acclimation to cold. Acta Physiol Scand 183, 1–101.[CrossRef]
Matsukawa
K, Ninomiya
I
&
Nishiura
N (1993). Effects of anesthesia on cardiac and renal sympathetic nerve activities and plasma catecholamines. Am J Physiol
265, R792–R797.
Schneider
FH
&
Gillis
CN (1966). Hypothermic potentiation of chronotropic response of isolated atria to sympathetic nerve stimulation. Am J Physiol
211, 890–896.
Segar
WE, Riley
PA
&
Barila
TG (1956). Urinary composition during hypothermia. Am J Physiol
185, 528–532.
Speziali G, Russo P, Davis DA & Wagerle LC (1994). Hypothermia enhances contractility in cerebral arteries of newborn lambs. J Surg Res 57, 80–84.[CrossRef][Medline]
Spray DC (1986). Cutaneous temperature receptors. Annu Rev Physiol 48, 625–638.[CrossRef][Medline]
Toner MM & McArdle WD (1996). Physiological adjustments of man to the cold. In Human Performance Physiology and Environmental Medicine at Terrestrial Extremes, ed. Pandolf, KB, Sawka, MN, Gonzalez, RR, pp. 361–400. Benchmark, Indianapolis.
Withey WR, Chapman BJ & Munday KA (1976). Distribution of blood flow in the hypothermic (27 degrees C) dog kidney. Clin Sci Mol Med 51, 583–588.
Wong KC (1983). Physiology and pharmacology of hypothermia. West J Med 138, 227–232.[Medline]
Young JB, Saville E, Rothwell NJ, Stock MJ & Landsberg L (1982). Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue of the rat. J Clin Invest 69, 1061–1071.
Zeisberger E (1998). Biogenic amines and thermoregulatory changes. Brain Res 115, 159–176.
Zheng F, Kidd C & Bowser-Riley F (1996). Effects of moderate hypothermia on baroreflex and pulmonary chemoreflex heart rate response in decerebrate ferrets. Exp Physiol 81, 409–420.[Abstract]
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, n= 14), acclimatized rats (
, n= 12). *P < 0.05, **P < 0.01, ***P < 0.001 versus 37°C, #P < 0.05 versus euthermic at same Tc (ANOVA). The data from renal function and RSNA experiments have been grouped together.
