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NDT Advance Access originally published online on January 5, 2007
Nephrology Dialysis Transplantation 2007 22(3):839-844; doi:10.1093/ndt/gfl705
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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

Serum and cellular interleukin-6 in haemodialysis patients: relationship with energy expenditure

Maria A. Kamimura1, Sergio A. Draibe2, Maria A. Dalboni2, Miguel Cendoroglo2, Carla M. Avesani2, Silvia R. Manfredi2, Maria E. F. Canziani2 and Lilian Cuppari1

1Nutrition Program, Federal University of São Paulo, São Paulo and 2Division of Nephrology, Federal University of São Paulo, São Paulo, Brazil

Correspondence and offprint requests to: Lilian Cuppari, PhD, Affiliate Professor, Division of Nephrology, Federal University of São Paulo, Rua Pedro de Toledo, 282 Cep: 04039-000 São Paulo, SP, Brazil. Email: lilian{at}dis.epm.br



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 
Background. Inflammation is a highly prevalent condition among end-stage renal disease (ESRD) patients and it has been implicated with several metabolic derangements. Considering the harmful effect of hypermetabolism on nutritional status and clinical outcomes of ESRD patients, we aimed to investigate the relationship between proinflammatory cytokine interleukin-6 (IL-6) and energy expenditure in this population.

Methods. This cross-sectional study enrolled 80 adult haemodialysis patients for the evaluation of serum IL-6 and energy expenditure. The production of IL-6 by peripheral blood mononuclear cells (PBMCs) (spontaneous and endotoxin-stimulated production) was examined in a subgroup of 30 haemodialysis patients and in 11 healthy control subjects. IL-6 was measured by immunoenzymatic assay. The resting energy expenditure was evaluated by means of indirect calorimetry. Body composition was assessed by bioelectrical impedance analysis and skinfold thicknesses.

Results. Serum IL-6 [6.3 (2.2–163.5) pg/ml] correlated positively with age (R = 0.26; P = 0.02) and C-reactive protein (R = 0.31; P < 0.01). Resting energy expenditure correlated positively with lean body mass (R = 0.68; P < 0.001) and BMI (R = 0.44; P < 0.001), and negatively with Kt/V (R = –0.37; P < 0.01). In the multivariate analysis, controlling for age and lean body mass, serum IL-6 was positively associated with resting energy expenditure (n = 80; ß = 2.4; P = 0.01). The production of IL-6 by PBMCs did not reach statistically significant differences between patients and controls [spontaneous production 6541 (96–7739) pg/ml vs 3410 (50–7806) pg/ml, respectively; and stimulated production 6530 (579–7671) pg/ml vs 5304 (1527–7670) pg/ml, respectively]. IL-6 secreted by monocytes showed no association with either serum IL-6 or resting energy expenditure.

Conclusion. Serum IL-6 was associated with an increase of energy expenditure in haemodialysis patients.

Keywords: energy expenditure; haemodialysis; inflammation; interleukin-6; monocytes



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 
End-stage renal disease (ESRD) is associated with an inflammatory state characterized by elevated circulating levels of proinflammatory cytokines such as interleukin-6 (IL-6), which has been recognized as a predictor of mortality in both incident and prevalent dialysis patients [1,2]. Although the causes of elevated IL-6 in ESRD patients are not fully understood, various uraemia and dialysis-related factors may contribute [3]. In fact, previous studies show that more than 30% of the patients on dialysis have elevated circulating IL-6 levels. In addition, it has been suggested that ESRD patients have overproduction of proinflammatory cytokines by peripheral blood mononuclear cells (PBMCs) [4,5].

Much interest has been focused on IL-6 in ESRD due to its complex spectrum of biological activities, including the role of mediating the development of malnutrition [6,7]. Although the pathophysiological link between inflammation and malnutrition has not been clearly elucidated, it has been shown that serum IL-6 induces protein catabolism [8], lipolysis [9], insulin resistance and suppression of appetite [10]. Additionally, it has been suggested that the release of cytokines by PBMCs is associated with hypermetabolism in other diseases conditions [11–13]. In chronic kidney disease, although the role of high acute phase protein levels on elevated energy expenditure has been evidenced [14,15], it remains unclear whether a similar association exists with cytokines.

Considering the harmful effect of elevated energy expenditure on nutritional status and on clinical outcomes of ESRD patients [16], we aimed to investigate the relationship of serum and monocyte-derived IL-6 with energy expenditure in patients undergoing haemodialysis.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 Acknowledgements
 References
 
Patients
This cross-sectional cohort included 80 patients (51 males/29 females) on maintenance haemodialysis at the Dialysis Unit of the Federal University of São Paulo – Oswaldo Ramos Foundation (São Paulo, SP, Brazil). The exclusion criteria were age below 18 years, length of haemodialysis below 2 months, altered thyroid or hepatic functions, diabetes and active malignance. Patients were dialysed for 4 h thrice a week using acetate or polysulfone membranes. The majority of the patients were being treated with human recombinant erythropoietin, iron saccharate and a vitamin complex, and none was taking hormones, a corticosteroid or immunosuppressive drugs. A subgroup of 30 haemodialysis patients and 11 healthy subjects was submitted to cytokine production assessment. All control subjects had normal kidney and thyroid functions, and none of them was taking any medication.

This study was approved by the University Ethical Advisory Committee, and all participants provided written informed consent.

Resting energy expenditure
Resting energy expenditure was assessed on a non-dialysis day by indirect calorimetry using an open circuit ventilated computerized metabolic system (Vmax series 29n; SensorMedics Corp; Yorba Linda, CA, USA). The oxygen and carbon dioxide sensors were calibrated before each resting energy expenditure measurement with the use of mixed reference gases of known composition. All subjects were previously instructed to refrain from any unusual physical activity for a 24-h period prior to the test and to sleep at the same time as usual in the night before the resting energy expenditure measurement. They were admitted to the clinic at 8:00 a.m. after an overnight fast of 12 h. After resting for 30 min in a recumbent position, subjects breathed for 30 min through a clear plastic canopy over their heads in a quiet dimly lit thermo neutral room. They were instructed to avoid hyperventilation, fidgeting or falling asleep during the test. Oxygen consumption and carbon dioxide production were measured at 1-min intervals and the mean of the last 20 min was used to calculate the resting energy expenditure according to the Weir's equation without using urinary urea nitrogen [17].

Anthropometry and body composition
Nutritional assessment was performed 15–30 min after the dialysis session on the day before the indirect calorimetry test. Subjects were weighed with light clothes and without shoes on a platform manual scale balance (Filizola®, São Paulo, Brazil). Body mass index (BMI) was calculated as body weight divided by squared height. Lean body mass was assessed by bioelectrical impedance analysis using a single frequency tetrapolar technique with an electrical current of 800 µA at 50 kHz (BIA 101 Quantum, RJL Systems, Detroit, USA). The electrodes were placed in the standard positions (two electrodes placed on the hand and wrist and another two positioned on the foot and ankle) on the opposite side of vascular access, with the subject in the supine position. The software Fluids & Nutrition (version 3.0) provided by the manufacturer was used to estimate the lean body mass.

Skinfold measurements at four standard sites (biceps, triceps, subscapular and suprailiac) were performed for determining body fat, since this method seems to be superior to bioelectrical impedance analysis for the measurement of this compartment in haemodialysis patients [18]. Body density was calculated from the sum of the four skinfold measurements according to Durnin and Womersley [19], and the percentage of body fat was then calculated by Siri's equation [20].

Subjective global assessment
The subjective global assessment was used to evaluate the overall protein-energy nutritional status. It includes assessing the patient's history of weight loss, presence of anorexia, vomiting, oedema/ascite, grade of muscle wasting and loss of subcutaneous fat. Based on these data, each patient was scored as follows: 1 = well-nourished, 2 = mild-moderately malnourished or 3 = severely malnourished [21].

Laboratory data
Fasting blood samples for glucose, bicarbonate, thyroid stimulating hormone, serum albumin, intact parathyroid hormone and C-reactive protein were drawn on the interdialytic day. Serum creatinine and urea were obtained from the monthly routine exam (predialysis session). Serum glucose, creatinine and urea were determined using a standard autoanalyser. Bicarbonate was measured by an automated potentiometer (normal range: 23–27 mmol/l), thyroid stimulating hormone by immunofluorometric assay (normal range: 0.3–4.0 µIU/ml) and serum albumin by green bromcresol technique (normal range: 2.5–4.0 g/dl). Intact parathyroid hormone and high-sensitivity C-reactive protein were determined by immunochemiluminescence. Aliquots of serum collected on the interdialytic day (just before the indirect calorimetry test) were frozen and stored at –70°C and by using a commercially available enzyme-linked immunosorbent assay, IL-6 (BD Biosciences Pharmingen, USA) and adiponectin (Linco Research, USA) were measured. Kt/V was determined according to the K/DOQI guideline [22].

Cytokine production
PBMCs were also obtained on the same day of the indirect calorimetry test. Blood was layered on a Ficoll–Hypaque gradient and centrifuged at 1200 rpm for 25 min. Cells were washed 3 times in sterile, pyrogen-free saline, and were suspended at 5 x 106/ml in RPMI (Sigma Chemical Co.) Aliquots of PBMCs from each patient with 1 x 106 cells/ml were incubated with RPMI (spontaneous production) and RPMI plus 500 ng/ml of Escherichia coli endotoxin (stimulated production) for 24 h in CO2 at 37°C. After incubation, the cells were kept at –70°C until analysis. Immunoenzymatic assays were performed to assess the production of IL-6 (BD Biosciences Pharmingen, USA).

Statistical analysis
Data are expressed as mean ± SD. Variables that did not present normal distribution are presented in median and ranges. Spearman's correlation was used for the univariate analysis among the study parameters. In order to evaluate the factors affecting REE among HD patients, stepwise multiple linear regression analysis was applied, including those variables that correlated significantly with REE or those that might influence REE. Differences with P < 0.05 were considered statistically significant. The statistical analyses were conducted using the True Epistat software (Texas, USA, 1995).



   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 Acknowledgements
 References
 
Total haemodialysis patients
Table 1 depicts the main characteristics of the patients. The age ranged from 18 to 76 years, and the length of dialysis therapy from 2 months to 13 years. Hypertensive nephrosclerosis was the main aetiology of chronic kidney disease corresponding to 35% (n = 24), followed by undetermined causes in 28% (n = 22), chronic glomerulonephritis in 15% (n = 12), and other causes accounted for 28% (n = 22). Patients were adequately dialysed according to Kt/V. BMI was within the normal range (18.5–24.9 kg/m2) in 75% of the patients, 20% had BMI ≥ 25 kg/m2 and 5% had BMI < 18.5 kg/m2. According to subjective global assessment, 69.2% of the patients were well-nourished, 24.4% were mild to moderately malnourished and 6.4% were severely malnourished. Serum IL-6 was not significantly different between well-nourished and malnourished patients [5.4 (2.2–163.5) pg/ml and 7.7 (2.2–30.3) pg/ml, respectively]. Forty-eight percent of the patients had C-reactive protein values higher than 0.5 mg/dl and 31.3% had values ≥1.0 mg/dl. In the univariate analysis, serum IL-6 was positively associated with age (R = 0.26; P = 0.02) and with C-reactive protein (R = 0.31; P < 0.01). No association was observed between serum IL-6 and length of dialysis, Kt/V, adiponectin, albumin, body composition parameters or resting energy expenditure. Resting energy expenditure correlated positively with lean body mass (R = 0.68; P < 0.001) and BMI (R = 0.44; P < 0.001), and negatively with Kt/V (R = –0.37; P = 0.001). Multivariate linear regression was used to analyse parameters that explained the variability in serum IL-6 and resting energy expenditure. We found that body fat was the determinant of serum IL-6 (ß = 0.98; SE = 0.41; P = 0.02), and explained 7.3% of the IL-6 variations when adjusted for age. The determinants of resting energy expenditure of the haemodialysis patients are shown in Table 2. As can be seen, together with the well-known determinants such as age and lean body mass, serum IL-6 was an independent determinant of resting energy expenditure.


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  		Table 1. Demographic, clinical and nutritional characteristics of the patients

 

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  		Table 2. Multiple linear regression analysis using resting energy expenditure as a dependent variable (n = 80; R2 = 0.58)

 
Cytokine production study groups
The subgroup of 30 haemodialysis patients was not significantly different from the total haemodialysis group regarding age, length of dialysis, Kt/V, body composition, C-reactive protein, serum IL-6 and resting energy expenditure (analysis not shown). The main characteristics of the subgroup of haemodialysis patients and of the healthy control group are presented in Table 3. As can be seen, C-reactive protein and serum IL-6 levels were significantly higher in haemodialysis patients. No difference was observed regarding body composition and resting energy expenditure. The spontaneous IL-6 production in the haemodialysis group tended to be increased in comparison with the healthy group, however, it did not reach statistical significance (Table 3). The stimulated production of IL-6 was similar between the groups (P = 0.22). While in the healthy group IL-6 production increased after cell stimulation by endotoxin, in haemodialysis patients the spontaneous and stimulated productions of IL-6 were similarly high and comparable with that of the stimulated production of the healthy group. Spontaneous IL-6 correlated positively with stimulated IL-6 in the haemodialysis group (R = 0.67; P < 0.01), and this association was much stronger among healthy individuals (R = 0.85; P < 0.01). IL-6 derived by PBMCs of the patients showed no association with serum IL-6 and C-reactive protein levels. In addition, IL-6 production did not show any association with variables such as age, length of dialysis, albumin, subjective global assessment, body composition or resting energy expenditure. In regards to serum IL-6 in this subgroup of patients, a positive correlation was found with age (R = 0.51; P < 0.01), C-reactive protein (R = 0.51; P < 0.01) and body fat (R = 0.42; P = 0.02). Similarly to the total haemodialysis group, the resting energy expenditure in this subgroup of patients correlated positively with lean body mass (R = 0.77; P < 0.001) and BMI (R = 0.42; P = 0.02), and inversely with Kt/V (R = –0.61; P < 0.001). Among healthy subjects, resting energy expenditure was positively associated only with lean body mass (R = 0.86; P < 0.001).


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  		Table 3. Main characteristics of the cytokine production study groups

 


   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
Acknowledgements
 References
 
Despite many advances in medical care over the past decades, the mortality is still elevated among ESRD patients [23]. High cytokine levels [1] and, more recently, increased resting energy expenditure [16] have shown to contribute to this condition. In the present study, we demonstrated a linkage between circulating IL-6 levels and energy expenditure in haemodialysis patients.

The resting energy expenditure of haemodialysis patients has shown to be equal or higher than that of healthy individuals [24–27]. Although some aspects of loss of renal function may contribute to reducing energy metabolism in chronic kidney disease patients [28,29], comorbid conditions, such as diabetes [30] and hyperparathyroidism [31], seem to exert an effect increasing resting energy expenditure of these patients. The current analysis demonstrating that a single measurement of IL-6 in serum was a determinant of resting energy expenditure in haemodialysis patients supports the previous findings by our group that suggested the role of inflammation increasing resting energy expenditure of non-dialysed chronic kidney disease patients [14,15]. By using C-reactive protein as an inflammatory marker, Avesani et al. [14] showed that subclinical inflammation was sufficient to increase resting energy expenditure of these patients. Furthermore, a subsequent analysis showed that after treatment of acute infection of the patients, the reduction on C-reactive protein levels (median from 2.05 to 0.35 mg/dl) was accompanied by 13% reduction of resting energy expenditure [15].

The exact mechanisms involving inflammation and resting energy expenditure cannot be fully identified, but it seems reasonable to speculate that protein catabolism caused by inflammation might be implicated in the increase of resting energy expenditure. In fact, the association of IL-6 and reduced muscle mass measured by computed tomography has been observed in haemodialysis patients [8]. The lack of association between circulating IL-6 and lean body mass in the present study may possibly be due to the low sensitive method used for assessing lean body mass and the cross-sectional design of the study.

The spontaneous IL-6 production by PBMCs in haemodialysis patients tended to be elevated in comparison to healthy controls, which is in accordance with previous studies that show overproduction of cytokines by monocytes in uraemic patients [4,5]. Regarding the stimulated IL-6 production, the rates were comparable between haemodialysis and controls in our study. This finding is supported by some investigators [32] but contradict others who found significantly reduced cytokine release by PBMCs after cell stimulation [33]. It is noteworthy that studies vary in terms of type and doses of endotoxin for cell activation, cell-collection period (before, during or after dialysis, or non-dialysis day), cell culture duration, dosage techniques, and type of dialysis membrane used. Moreover, in this complex pathological condition such as chronic kidney disease, we cannot exclude the possible intrinsic alterations of signalling pathways and immune defectiveness of the patients [32]. In fact, we observed that while in the healthy group, stimulated IL-6 production was higher than the spontaneous production, in the haemodialysis group the IL-6 production showed no change after cell stimulation, suggesting the cells of the patients were hyporesponsive to exogenous stimuli. Some authors have indeed reported an impaired endotoxin-induced IL-6 release from PBMCs of haemodialysis patients [34]. Yet, a recent study showed that the ability of haemodialysis patients to secrete tumour necrosis factor (TNF-{alpha}), interleukin-1 (IL-1ß) and IL-6 by stimulated monocytes decreased progressively according to length of dialysis therapy [33]. However, the fact that spontaneous production of IL-6 tended to be already elevated in haemodialysis patients suggests that the monocytes might be chronically activated and subsequently refractory to any further stimulation. In particular, blood interaction with dialyser membrane may chronically activate PBMCs of haemodialysis patients [35].

The dysregulation of cytokine production is involved in several clinically relevant acute and chronic complications of dialysis treatment, including fever, hypotension, sleep disorders, dialysis-related amyloidosis, impaired immunity, bone disease and anaemia [36]. Moreover, in other diseases, an association of cytokine production by PBMCs with energy expenditure has been suggested. In cachectic patients with pancreatic cancer, elevated resting energy expenditure was found in patients with enhanced spontaneous production of TNF-{alpha} and IL-6 [11]. Roubenoff et al. [12] demonstrated in patients with rheumatoid arthritis that TNF-{alpha} and IL-1ß production was higher than in controls and, more importantly, explained 20% of the variability in resting energy expenditure. In our haemodialysis patients the IL-6 production by PBMCs, showed no association with the resting energy expenditure. The reasons for this lack of relationship are not clear. It is of note that the cellular production of IL-6 was not associated with serum IL-6 as well. A combination of many factors related to disturbances in the cytokine network may overcome the association between monocyte-derived IL-6 and serum levels of IL-6 in haemodialysis patients. Moreover, the proportional contribution of different sources of IL-6 in the circulation of the human is unclear. For instance, in the last few years, adipose tissue has emerged as an additional important source of systemic IL-6 [37]. Mohamed-Ali et al. [38] showed that fat release of IL-6 may account for up to 35% of IL-6 in plasma. Accordingly, in the current study, body fat was an independent determinant of circulating IL-6 in haemodialysis patients. Axelsson et al. [39] also found a positive association between body fat and circulating IL-6 in chronic kidney disease patients.

In conclusion, serum IL-6, but not production of IL-6 by monocytes, was associated with increase of energy expenditure in haemodialysis patients. Attempts to better understand the mechanisms involved in the relationship between cytokines and energy metabolism in ESRD population are still necessary.



   Acknowledgements
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
References
 
This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (Fapesp) and Oswaldo Ramos Foundation, and is dedicated to the memory of Nelma Scheyla José dos Santos.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 

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Received for publication: 21. 6.06
Accepted in revised form: 31.10.06


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H. A. Haugen, L.-N. Chan, and F. Li
Indirect Calorimetry: A Practical Guide for Clinicians
Nutr Clin Pract, August 1, 2007; 22(4): 377 - 388.
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