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NDT Advance Access published online on August 23, 2007
Nephrology Dialysis Transplantation, doi:10.1093/ndt/gfm436
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© The Author [2007]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Resting energy expenditure and thermal balance during isothermic and thermoneutral haemodialysis—heat production does not explain increased body temperature during haemodialysis

Jirí Horácek1, Sylvie Dusilová Sulková2,3, Magdalena Fortová4, Frantisek Lopot4, Marta Kalousová3, Lubos Sobotka2, Jirí Chaloupka5, Vladimír Tesar6, Ales Zák7 and Tomás Zima3

1Department of Internal Medicine II and 2Department of Gerontology and Metabolism, Charles University Prague, Faculty of Medicine and University Hospital Hradec Králové, Hradec Králové, 3Institute of Clinical Chemistry and Laboratory Diagnostics, 4Internal Department Strahov, Charles University Prague, 1st Faculty of Medicine and University Hospital Prague, Prague, 5Department of Occupational Health, Charles University Prague, Faculty of Medicine and University Hospital Hradec Králové, Hradec Králové, 6Department of Nephrology and 74th Department of Medicine, Charles University Prague, 1st Faculty of Medicine and University Hospital Prague, Prague, Czech Republic.

Correspondence and offprint requests to: Prof. Sylvie Dusilová Sulková, Department of Gerontology and Metabolism, Charles University Prague, Faculty of Medicine and University Hospital Hradec Králové, Email: sulkovas{at}volny.cz



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 
Background. During routine haemodialysis (HD) body temperature increases, which contributes to haemodynamic instability. The relative roles of increased heat production and/or incomplete heat transfer are not fully elucidated. Concomitant measurement of heat production and heat transfer may help to assess the factors determining thermal balance during HD.

Methods. Thirteen stable non-diabetic maintenance HD patients were investigated during two HD procedures (isothermic, dT = 0, no change of body temperature; thermoneutral, dE = 0, no energy transfer between blood and dialysate), using a blood temperature monitor (BTM) in active mode. Energy transfer, blood and dialysate temperature, and relative blood volume change (dBV) were continuously recorded, and resting energy expenditure (REE; Deltatrac Datex) was measured repeatedly during each procedure. Fourteen healthy persons served as controls for REE comparison.

Results. In isothermic HD, median energy removal was 218 kJ/4 h HD (= heat flow –15.1 W). This cooling correlated with dBV induced by ultrafiltration ({rho} = 0.731, P < 0.01). There was no difference in dBV between isothermic (7.7%) and thermoneutral (8.1%) HD. Predialysis REE was 82.8 W/1.73 m2, not different from controls. No variation in REE during HD was observed, except a small and transient increase after a light meal (5 and 4%). In the time course of REE, no difference between the procedures was found.

Conclusions. Our findings suggest that stable maintenance HD patients have REE not different from healthy controls, that HD procedure per se does not significantly increase REE and that neither isothermic nor thermoneutral regimen has any influence on metabolic rate. Therefore, body temperature elevation during routine HD may rather be due to decreased heat removal. With the use of BTM in active mode, body temperature can be kept stable (isothermic HD), which requires active cooling. This negative energy transfer is proportional to decrease in blood volume induced by ultrafiltration.

Keywords: blood temperature monitor; isothermic haemodialysis; resting energy expenditure; thermal balance; thermoneutral haemodialysis; ultrafiltration



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 
There has been increasing interest in the thermoregulatory processes during haemodialysis (HD) in the last few years as thermal dysequilibrium is one of the major deviations from homeostasis during routine HD procedure, influencing greatly the haemodynamic stability in response to ultrafiltration [1–5].

Normally, the stability of body temperature is controlled by equilibrium between heat production and heat removal from the body. Heat elimination is mediated by perspiration, convection and radiation; they are capable of mutual compensation. None of these three components is directly measurable. On the other hand, heat production may be estimated using indirect calorimetry because it corresponds to energy expenditure.

HD procedure may affect the steady state between heat production and heat removal in several ways. First, there is a heat exchange between blood and dialysate in haemodialyser. Changes in heat dissipation from skin surface due to changes in skin perfusion may also be important. Finally, an increase in metabolic rate (i.e. increased heat production) during HD has been suggested.

During routine HD, dialysis solution temperature is constant and no information about the real energy transfer is available. However, using a BTM device (Blood Temperature Monitor, Fresenius, Bad Homburg, Germany) the extracorporeal energy transfer during HD can be monitored, which offers a unique opportunity to quantify the heat loss. Moreover, the simultaneous registration of extracorporeal energy transfer together with the measurement of resting energy expenditure (REE) might provide more information about the thermoregulatory processes during HD.

The BTM works in active or passive mode. During HD, two special sensors continuously measure the blood temperature both in arterial and venous extracorporeal lines and this process is highly standardized and precise. In passive mode, the energy transfer is only registered. In active mode, the dialysate temperature is continuously adjusted on the ‘biofeedback’ principle. This biofeedback allows to keep a pre-set body temperature (regimen T) or to reach a pre-set energy transfer (regimen E), respectively [1,3,5].

In this study, both energy production and energy transfer were studied during two distinct thermal regimens of HD (isothermic HD and thermoneutral HD). Isothermic HD (dT = 0) keeps a stable body temperature. Thermoneutral HD (dE = 0) means no thermal transfer in the dialyser.

Our assumption was that if measured REE increased during both settings, then HD itself would be responsible for increased heat production and its accumulation during HD. If a change in REE occurred in one setting only, it would be related to the respective thermal balance, not to HD procedure itself (e.g. a change in REE in response to the change in body temperature). If REE remained stable in both thermal HD regimes, then thermal balance would be dependent on extracorporeal heat flow.

We were also interested in possible relationship between thermal balance and relative blood volume changes (dBV) in response to ultrafiltration, as Rosales et al. [6] and Schneditz et al. [7] have previously described a close link between these variables.

An accessory aim of the study was to compare the REE in our patients with a control group because of equivocal data on REE in dialysed patients in the literature.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 Acknowledgements
 References
 
Thirteen chronic HD patients (7 men and 6 women; aged 59.8 ± 13.5 years, length of HD treatment 3.4 ± 2.2 years) were studied prospectively (Table 1). The patients were clinically stable, with no signs of inflammation or heart failure. No patients with diabetes mellitus, or those treated with glucocorticoids, thyroid hormones or ß-blockers were included. The control group of healthy subjects consisted of 4 men and 10 women with an average age of 41.3 ± 20.5 years. All subjects were informed about the study procedure and its aim, and expressed their informed consent.


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  		Table 1. Baseline characteristics of haemodialysis patients (n = 13)

 
Patients were observed during two HD procedures with different thermal balance, i.e. during isothermic (‘cool’) and thermoneutral (‘warm’) HD. Isothermic HD has been defined as dT = 0, i.e. body temperature remained constant during HD because the excess heat produced during HD was convected out of the body (the energy balance of the procedure was negative). In contrast, thermoneutral HD has been defined as dE = 0, i.e. no energy is lost in the extracorporal circuit and body temperature increases [1,2]. Both thermal regimens were continuously kept under control by BTM module (Fresenius, Bad Homburg, Germany) in active regimen, with HD monitor 4008S.

Other HD characteristics remained identical in both regimens: low-flux steam sterilized polysulphone dialyzer 1.6 m2, two G15 dialysis needles, blood flow rate 300 ml/min, dialysate flow rate 500 ml/min, composition of dialysis solution: c(Na+) 140 mmol/l, c(K+) 3 mmol/l, c(Ca2+) 1.75 mmol/l and c(HCO3–) 32 mmol/l with no glucose, duration of HD 4 h, constant ultrafiltration rate and identical total amount of ultrafiltrate. The interval between measurements was one week (mid-week dialysis), afternoon shift. All patients had a well-functioning native arteriovenous fistula (proven by regular assessment of vascular access blood flow by thermodilution).

REE was measured by indirect calorimetry (metabolic monitor Deltatrac Datex, Helsinki, Finland) using ventilated canopy. Patients were completely at rest during the whole HD procedure, lying supine in a quiet room with a temperature of 24°C–25°C. The measurement started at least 3 h after the last meal; however, no specific long-term food intake limitations were imposed to either control subjects or HD patients. The first measurement was performed before each HD, after 30 min of rest in supine position. It was then repeated 4 times: 10, 70, 110 and 215 min after the start of HD. The fourth measurement (110 min) followed shortly after a light meal (two rolls and non-sweetened tea, ~1000 kJ). Thus, REE was measured five times during each HD session.

In each indirect calorimetry procedure, oxygen consumption (VO2) and CO2 production (VCO2) were registered for 10 min at 1 min intervals after 3 min of adaptation period. The average of these 10 measurements was taken as the result. Respiratory quotient (RQ = VCO2/VO2) and resting energy expenditure (REE; Weir formula) were calculated by the device [8]. The measured REE values were compared with the values of basal metabolic rate (BMR) estimated from Harris–Benedict formula [9].

In HD patients, blood pressure (BP), heart rate (HR) and respiration rate (RR) were recorded before dialysis and at 30 min intervals during both procedures. Temperature in arterial blood line (Tart), venous blood line (Tven) and dialysate temperature (Tdial) as well as relative changes of intravascular volume (dBV; Critline; On-line Diagnostics, Riverdale, USA) [10] were recorded continuously throughout the study. Temperature in arterial blood line (Tart) measured by BTM is acceptable representative of mixed body temperature [1,5], provided the recirculation is measured and included into calculation, as it was in our practice.

Pre-dialysis blood samples were drawn from inserted dialysis needle just before starting HD. During HD, samples were taken from arterial blood line in the 70th min of HD. Post-dialysis blood samples were taken using slow-flow method from arterial blood line. The samples were kept on ice for ~30 min, and then centrifuged at –4°C at 3000g. Thereafter, serum was kept at –20°C until the laboratory assays were performed (max. 8 weeks).

Serum urea and albumin concentrations were assayed using autoanalyser Kodak Ektachem 700XR and haematocrit levels using Critline device. For pre-albumin, immunoturbidimetric assay was used (Tinaquant-Prealbumin, Roche). To compare the magnitude of biological response to both procedures, pregnancy-associated plasma protein A (PAPP-A) was measured by TRACE (Time Resolved Amplified Cryptate Emission) technology based on non-radiating energy transfer. Commercial kit for PAPP-A determination (BRAHMS GmbH, Berlin, Germany) contains two different monoclonal antibodies—one is conjugated with europium cryptate and the other with fluorescent agent XL 665. The antigen (PAPP-A) present in serum samples is sandwiched between two conjugates. The fluorescent signal measured during the formation of the antigen–antibody complex by the KRYPTOR analyser (BRAHMS GmbH, Berlin, Germany) is proportional to the antigen concentration. Cyclic GMP (cGMP) as a marker of hydration was determined with competitive EIA using standard kits (Cayman Chemicals, USA). Concentration of non-esterified fatty acids (NEFA) was determined using the enzymatic-colorimetric method (NEFA, Randox Laboratories, UK); they were selected for their supportive information about metabolic response during HD.

For statistical analysis, non-parametric tests were employed, as the assumptions for parametric tests were not consistently met. Data were expressed as medians (with 1st and 3rd quartiles). For comparisons between the control and HD groups, Mann–Whitney test was used. The two distinct thermodynamic regimens within the HD group were compared using Wilcoxon test for paired data. For variation of repeated measurements during HD, Friedman test was used, with subsequent Dunnett or Student–Newman–Keuls (SNK) test for significant difference between the individual measurements, as appropriate. Relations between variables were evaluated by non-parametric correlation analysis (Spearman {rho}). SigmaStat® statistical software package, version 3.1 (Jandel Corp., San Rafael, USA), was used for calculations, and P < 0.05 was considered statistically significant.



   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 Acknowledgements
 References
 
Thermal balance during thermoneutral and isothermic haemodialysis
As expected, there was a significant difference in thermal balance between the HD procedures (Table 2). During thermoneutral HD, in accord with its definition, there was nearly no heat transfer between blood and dialysate, and continuous increase in arterial and venous line temperature was observed. During isothermic HD, dialysate temperature was continuously decreasing, which was paralleled by venous line temperature. The thermal balance of the procedure was clearly negative (–218 kJ removed in 4 h; heat flow –15.1 W). In spite of this, there was a minor (though statistically significant) increase in arterial line temperature. While the difference in thermal balance and in venous line temperature was clearly apparent from the 30th min of HD, arterial line temperature (best reflecting core temperature) became significantly different only after the 210th min. Median difference in dialysate temperature till the end of both procedures was 1.9°C with a starting dialysate temperature of 36.5°C in both settings, and final values of 35.2°C and 37.1°C in isothermic and thermoneutral HD, respectively.


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  		Table 2. Thermal parameters and relative decrease in blood volume in the course of isothermic (dT = 0) and thermoneutral (dE = 0) HD

 
Changes in intravascular volume (dBV)
There was no difference between the changes of intravascular volume (dBV) (–8.1 vs –7.7% in isothermic and thermoneutral HD, respectively, NS) (Table 2). In isothermic HD, significant correlation ({rho} = 0.731, P < 0.01) was found between dBV and total amount of heat removed (Figure 1). In thermoneutral HD, no clear-cut relationship between dBV and body temperature increase was found.


Figure 1
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  		Fig. 1. Correlation of intravascular volume decrease (induced by ultrafiltration and measured by Critline device) and total thermal energy transferred into extracorporeal circuit (measured by BTM device) during 4 h of isothermic HD. Spearman (non-parametric) correlation: {rho} = 0.731; P < 0.01.

 
Haemodynamic stability
Both in isothermic and thermoneutral settings, blood pressure (systolic, diastolic and mean) remained stable and no symptomatic hypotension was observed. Also, there was no significant difference in the heart rate at any time point between the procedures, in spite of a minor (but significant) overall increase during thermoneutral HD (Table 3).


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  		Table 3. Blood pressure (BP) and heart rate (HR) in the course of isothermic (dT = 0) and thermoneutral (dE = 0) HD

 
Selected biochemical variables
Serum urea concentrations were used for Kt/V calculations, and dialysis adequacy (eKt/V 1.3 or more) was confirmed. Blood concentrations of circulating volume marker, cGMP, metalloproteinase PAPP-A as marker of a complex biological response to extracorporeal procedure [11] and non-esterified fatty acids (NEFA) in the course of both procedures are summarized in Table 4.


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  		Table 4. Selected biochemical variables in the course of isothermic (dT = 0) and thermoneutral (dE = 0) HD

 
There was a significant decrease in cGMP level in both settings, and in the 70th min this decrease was relatively greater than that of intravascular volume. Inflammatory marker PAPP-A increased after the start of dialysis, as expected, and returned to pre-treatment value. The sharp rise of NEFA in the 70th min was similar in both procedures, as was the subsequent decrease. No significant difference between isothermic and thermoneutral HD was found in any of these investigated parameters.

Indirect calorimetry (REE and RQ)
REE values remained stable in the course of both HD regimens (Table 5) except a small and transient (though significant) increase after the light meal (110 min). RQ was slowly but significantly declining during both HD regimens. However, this decline was abolished after the carbohydrate meal. Significant negative correlation ({rho} = –0.451, P < 0.05) was found between the change in RQ and in NEFA level during both HD settings.


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  		Table 5. Indirect calorimetry in the course of isothermic (dT = 0) and thermoneutral (dE = 0) haemodialysis

 
The values of pre-dialysis REE were generally stable within the same patient; median difference between the two measurements (i.e. before isothermic and thermoneutral HD) was 4.7% (4.1% when expressed as REE per 1.73 m2). Therefore, the mean of two pre-dialysis values in every patient was used for comparison with healthy controls. As summarized in Table 6, there was no difference in REE between HD patients and controls (in absolute values, or expressed in watts per standardized body surface area, or as percentage of BMR).


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  		Table 6. Indirect calorimetry—comparison of HD patients (n = 13) and control group (n = 14)

 


   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
Acknowledgements
 References
 
In our study, heat production together with heat removal were being monitored in the course of two different thermal HD regimens. One of the compared regimens was isothermic HD that, with respect to thermal balance, makes HD as close as possible to physiological homeostasis because it prevents the increase in body temperature. The haemodynamic benefit of isothermic HD has been proven by Maggiore et al. [2] in a multicentre study and their conclusion has generally been accepted but still has remained underused [12].

In isothermic HD, the energy balance is negative. In two previous studies a quantitative relationship was found between ultrafiltration and energy transfer [6,7]. A similar conclusion can be drawn from our data: (cumulative) heat energy removal correlates well with (cumulative) decrease in intravascular volume (Figure 1). Furthermore, in our study ultrafiltration as well as blood volume decrease were considerably lower than in published studies, but this correlation was of similar strength. In our patients, the energy loss per 1% of body weight change corresponded to 5.6% of measured pre-dialysis REE, which is in perfect agreement with 6% estimation of Rosales et al. [6] despite considerably lower ultrafiltration volume in our patients. Also, our heat flow (15 W) is in accord with Schneditz et al. [7], who observed extracorporeal heat flow of 20 W (with a mean dBV of 15% in his patients).

According to ‘volume hypothesis’ [1], the accumulation of heat in the body during conventional HD is a consequence of vasoconstriction, which is a regulatory haemodynamic response to decreasing intravascular volume due to ultrafiltration. Vasoconstriction leads to skin hypoperfusion, thus impairing heat dissipation. In order to prevent the rise in body temperature, the accumulated heat must be removed in another way, i.e. by heat transfer from blood into dialysate in dialyser. As vasoconstriction is presumably proportional to the loss of circulating volume, the necessary amount of heat removed is proportional to the loss of intravascular volume, too. Our findings are in accord with this ‘volume hypothesis’, and lend further support to it in a novel setting, with smaller changes in intravascular volume, and no important changes in blood pressure.

Quite recently, van der Sande et al. [13, 14] were first to show that in isothermic HD some thermal energy had to be removed (to keep body temperature constant) even in isovolaemic HD without any measured cutaneous perfusion changes. They concluded that ‘volume hypothesis’ does not provide full explanation for heat accumulation during HD, and more factors, so far poorly understood, may be involved. In our setting, ultrafiltration was always used, therefore we cannot comment on this.

Twenty years ago Monteon et al. [15] demonstrated no important difference in energy expenditure between healthy subjects and stable patients undergoing maintenance HD. Their results were later supplemented with reports of increased REE precipitated by inflammation [16, 17] or accentuated hyperparathyroidism [18], but also of decreased expenditure in simple (non-inflammatory) malnutrition [19]; all these measurements were performed on non-dialysis days. Pre-dialysis REE in our patients did not vary on repeated measurement within 1 week, and it was not different from healthy controls (though our control group was not pair-matched). Our patients had no symptoms/signs of inflammation/infection or malnutrition.

There are scarce data on time course of REE during HD and we have found no (full-text) report comparing different thermal HD regimens in this aspect. Ikizler et al. [20] described an increased REE in the course of HD, but the inflammatory status of patients was not reported, their dialysis solution contained 11 mmol/l glucose, and also in other aspects their method was different from ours.

Also, studies comparing pre- and post-dialysis values of measured REE are scarce. An abstract by Lange et al. from 1995 was cited in [1] suggesting an average increase in REE by 8.6% (but with a high SD of 8.8%) during ‘cool’ HD, while during ‘warm’ HD it was 12.4% (SD 9.7%). These results are difficult to discuss as no full-text paper on these patients, with other important methodological data, has since appeared. Van der Sande et al. [13] found no change in REE before and after isothermic and thermoneutral HD (in both regimens with or without ultrafiltration). Our study gives further support to their measurements, providing original data on REE not only before and after, but also during the course of HD. However, this stability does not preclude mild changes in REE when more intensive cooling is applied, as observed by Rokyta et al. [21] in their critically ill patients.

In our setting, HD was standard ‘low-flux’ procedure, using standard dialysis solution, where endotoxin concentrations were kept below the safety values recommended by European pharmacopoeia. There was no difference between isothermic and thermoneutral HD in serum PAPP-A levels, indicating that thermal balance does not influence the biological response to dialysis.

Our secondary (though rather surprising) finding was continuously decreasing RQ in the course of both HD regimens. Ikizler et al. [20] described a similar trend, while van der Sande et al. [13] found no difference in RQ before vs after HD. Our finding may tentatively be explained by corresponding variations in NEFA concentrations and/or metabolism. Preferential NEFA oxidation decreases RQ, while glucose oxidation has the opposite effect. In the first hour of both HD regimens an increase in NEFA levels was found, followed by a decline but not to the baseline values. Theoretically, we might ascribe the initial rise of NEFA to heparin (2000 U administered at the beginning of HD), a well-known activator of lipoprotein lipase. More importantly, NEFA may also be mobilized by fasting during HD, possibly aggravated by glucose loss into dialysate. This hypothesis would be supported by their decline following a light (carbohydrate-containing) meal. While NEFA levels were decreasing after the light meal, the observed decline in RQ was stopped, and RQ then remained stable in spite of a temporary increase in oxygen consumption and REE. Also, there was a correlation between the changes in NEFA levels and in RQ during HD. We have found no data on NEFA dynamics during HD in the available literature.

We are also not aware of any study describing the changes of vasoactive hormones during isothermic and thermoneutral HD. The sharp (and expected) decrease in cGMP, corresponding to the loss of circulating fluid volume, was not different between isothermic and thermoneutral HD, indicating no important difference in the fluid shifts between these procedures.

In conclusion, our findings suggest that stable-maintenance HD patients have REE not different from healthy controls, that HD procedure per se does not significantly increase REE and that neither isothermic nor thermoneutral regimen has any influence on metabolic rate. Therefore, body temperature elevation during routine HD may rather be due to decreased heat removal. With the use of BTM in active mode, body temperature can be kept stable (isothermic HD), which requires active cooling. This negative energy transfer is proportional to decrease in blood volume induced by ultrafiltration.



   Acknowledgements
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
References
 
This study was supported by the research projects ‘MZO 0021620819’ and ‘MZO 00179906’, Czech Republic. We are grateful to Dr Jirina Soukupova for her valuable laboratory work, to Ing. Petr Moucka for his technical support and consultations and to Dr Jan Blaha for recruitment of patients.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 

  1. Lange H, Schwickardi M, Hermann W, Dahmen G, Issing J, Krämer M, Kuhlmann U. Effects of dialysate temperature on resting metabolic rate (RMR) during extracorporeal hemodialysis (HD) in ESRD [abstract]. Int J Artif Organs (1995) 18:425.
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Received for publication: 13. 2.07
Accepted in revised form: 11. 6.07


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