association of body fat with inflammation in peritoneal dialysis

Association of Body Fat with Inflammation in PeritonealDialysis

Andresa Marques de Mattos,1,2,3 Paula Payão Ovidio,2 Alceu Afonso Jordão,1

José Abrão Cardeal da Costa,1 and Paula Garcia Chiarello1

Abstract—Peritoneal dialysis (PD) frequently leads to body weight gain, which appears to be apotential cause of the chronic inflammation frequently present in these patients. The consequencesof this inflammation are impaired nutritional status, accelerated atherosclerosis, and increased mo-rtality. To assess the association between inflammation and body fat in female patients treated withPD. Nineteen female patients on PD for at least 6 months with no infectious complications ormalignant or acute inflammatory diseases. Nutritional status was determined by measuring weight,height, body mass index (BMI), waist (WC), and mid-arm circumferences (MAC), mid-arm musclearea, and tricipital fold (TCF). Bioelectrical impedance (BIA) was used to determine body comp-osition. Biochemical evaluation included the determination of serum albumin, urea, creatinine, andC-reactive protein (CRP). The glucose absorbed from the dialysis solution was quantitated. Acco-rding to BMI, two patients were classified as malnourished and ten as overweight/obese. Sixteenindividuals had high WC measurements and 12 had excess body fat (BF) as measured by BIA. HighCRP levels were observed in 12 patients, who had higher WC, MAC, BMI, TCF, and BF measu-rements compared to non-inflamed patients. Positive associations were detected between CRP andBMI, MAC, WC, and TCF. Associations between BF and CRP suggest that adiposity may be apotent exacerbating factor of inflammation in this population, especially visceral fat. Thus, obesitymay be considered to be one more factor responsible for the early atherosclerosis and high cardi-ovascular mortality observed in these patients.

KEY WORDS: peritoneal dialysis; body fat; chronic inflammation; obesity.

INTRODUCTION

Chronic inflammation is highly prevalent inpatients with end-stage renal disease (ESRD) [1]. InEurope and in the USA, about 30–50 % of thesepatients show serological evidence of an activatedinflammatory response based on C-reactive protein(CRP) concentrations [2]. Impaired nutritional status,a poor prognosis, accelerated atherosclerosis, perito-

neal membrane failure, and increased mortality areimportant consequences of chronic inflammation forthese patients [3].

The causes of the presence of inflammation in thispopulation are multifactorial and include a variety offactors related to uremia per se and to the dialysisprocedure, which stimulates the inflammatory responseby activating the production of pro-inflammatory cyto-kines by the macrophages. Recently, excess adiposetissue has been mentioned as another potential causeof chronic inflammation in patients with ESRD [1].

For a long time, adipose tissue has been consideredto be a passive tissue responsible for the storage ofenergy in the form of fat. However, evidence hassuggests that the adipocytes perform important metabol-ic and pro-inflammatory activities in peripheral tissuesby secreting adipokines such as interleukin 6 (IL-6) [4,5]. Interestingly, the secretion of these adipokines differs

1 Department of Internal Medicine, Faculty of Medicine of RibeiraoPreto, University of Sao Paulo, Ribeirao Preto, Brazil

2 Faculty of Medicine of Ribeirao Preto, University of SaoPaulo, Avenue Bandeirantes, 3900, Ribeirao Preto, São Paulo14049-900, Brazil

3 To whom correspondence should be addressed at Faculty ofMedicine of Ribeirao Preto, University of Sao Paulo, AvenueBandeirantes, 3900, Ribeirao Preto, São Paulo 14049-900,Brazil. E-mail: [email protected]

0360-3997/13/0300-0689/0 # 2013 Springer Science+Business Media New York

Inflammation, Vol. 36, No. 3, June 2013 (# 2013)DOI: 10.1007/s10753-013-9593-3

689

between subcutaneous and visceral adipose tissue, thelatter being more active and able to release up to two tothree times more IL-6 than subcutaneous adipose tissue [3].

Several studies have demonstrated the relationshipbetween chronic inflammation and adipose tissue both inobese individuals without renal disease [1] and inindividuals in the pre-dialysis stage [6] and on hemodi-alysis [7]. In one of these studies, the authors demon-strated an increased expression of pro-inflammatorygenes in the abdominal subcutaneous tissue of patientswith advanced chronic renal disease, thus confirming thelink between obesity and inflammation at the cellularlevel in this population [1].

This association is particularly relevant for patientstreated with peritoneal dialysis (PD), since this treatmentfrequently triggers body weight and adipose tissue gain,especially of the visceral type, as a consequence of agenetic polymorphism that affects energy metabolismplus the additional energy originating from the glucoseabsorbed from the peritoneal dialysis solution [4].

However, few studies investigating the association ofchronic inflammation with adipose tissue in patients on PDor evaluating body composition by simple methods such asanthropometry and bioelectrical impedance (BIA) areavailable in the literature. These techniques are consideredto be of low cost, easy to apply, and noninvasive, inaddition to being the methods most frequently used inclinical practice [8]. Additionally, several authors havedemonstrated that BIA shows strong correlation andconcordance with the results of body composition ofESRD patients evaluated by DEXA [9].

In view of these findings and of the highprevalence of obesity among patients on PD, weraised the hypothesis that body fat may influence thechronic inflammation observed in these patients andthus contribute to their increased mortality. Thus, theobjective of the present study was to observe therelationship between serum CRP concentration and bodycomposition and adipose tissue distribution in patients onPD evaluated by simple methods such as anthropometryand BIA.

MATERIALS AND METHODS

Individuals

An observational cross-sectional study was con-ducted on 19 female patients aged 18 years or older andtreated with PD for at least 6 months. Individuals with

infectious complications, malignant diseases, and acuteinflammatory diseases were excluded.

Sixteen patients were on continuous ambulatoryperitoneal dialysis with peritoneal dialysis solutionsbased on glucose and with lactate-corrected pH (Frese-nius Medical Care, Sao Paulo, Brazil). The patientsperformed four to five exchanges per day with 1.0–2.5 lbags. The three patients on automated peritoneal dialysisused solutions with 1.5 and 2.3 % glucose and lactate-corrected pH (Fresenius Medical Care) in four cyclesduring the night.

The study was approved by the Research EthicsCommittee of the University Hospital, College ofMedicine of Ribeirao Preto, University of Sao Paulo,and all patients gave written informed consent toparticipate.

Anthropometric Evaluation

The same trained nutritionist performed the anthro-pometric evaluation of all patients, who were fasting andhad an empty abdominal cavity. Weight was measuredwith a scale with 0.1 kg precision (Filizola S/A, SaoPaulo, Brazil) and height with a stadiometer with 0.1 cmprecision (Alturaexata, Minas Gerais, Brazil). Bodymass index (BMI) was calculated as weight dividedby height squared. A cutoff point of ≥24.9 kg/m2

was used to classify excess weight for adults and a cutoffpoint of ≥27.0 kg/m2 was used to classify excess weight forelderly subjects [10].

Each of the measurements described below wasrepeated three times and the arithmetic mean of thesemeasurements was used as the final results. Waistcircumference (WC) was measured on the umbilical lineusing an inextensible tape with 0.1 cm precision. Mid-arm circumference (MAC) was measured with the sametape on the non-dominant arm in the midpoint betweenthe acromion of the scapula. The tricipital skin fold(TCF) was measured on the non-dominant arm using anadipometer (Lange, Cambridge, MA, USA) according toa standardized technique. Mid-arm muscle area(MAMA) was calculated by the following formula:MAC− (0.3143×[TCF/10]). The standard TCF andMAC values were obtained from the percentile distribu-tion tables of the National Health and NutritionExamination Survey adapted by Frisancho [11].

Body composition was evaluated by tetrapolar BIA(Biodynamics 310 A, Biodynamics Corporation, Seattle,WA, USA) which provides data regarding body water,lean mass, and fat mass, using a current of 800 μA and

690 de Mattos, Ovidio, Jordão, da Costa, and Chiarello

50 kHz. The measurements were performed according tomanufacturer instructions. The cutoff points recommen-ded by Heyward and Wagner [12] were used asreference values to classify fat percentage.

Biochemical Evaluation

Blood samples were collected from the patientsafter a 12-h overnight fast and immediately centrifugedat 3,500×g for 10 min at room temperature. Serum wasseparated and stored at −30 °C.

Serum albumin was determined using a commercialkit (LabTest, Lagoa Santa, Minas Gerais, Brazil). Thereference value used for serum albumin was ≥4.0 g/dL[13]. Serum urea and creatinine were determined usingcommercial kits (LabTest) and Kt/V was calculatedaccording to the formula of Daugirdas [14] using thereference value of ≥1.7 [15].

The amount of glucose absorbed from the perito-neal dialysis solution was determined using the follow-ing formula: 0.89X (g/day)−43 [13], where X is the totalamount of glucose instilled per day. The results arereported as gram/day.

The inflammatory state was assessed on the basis ofCRP levels, which were determined by chemilumines-cence using a commercial kit (Immulite, PDC, Gwy-nedd, UK). The reference value considered was CRP <5.1 mg/dL [16].

Statistical Analysis

The group of patients classified as inflamed wascompared to the groups of patients with no serum signsof inflammation by the unpaired t test. The normality ofthe residues was analyzed by means of a histogram andnormal plot and, in the absence of normal distribution,logarithmic transformation was used.

The Pearson correlation coefficient (r) was used todetermine possible associations between the variables.Data are reported as mean±SD and the level ofsignificance was set at 5 %. All statistical analyses wereperformed with the aid of the SAS 9 software [17].

RESULTS

The mean age of the patients was 56.0±14.9 years andtheir mean time of PD treatment was 31.2±34.9 months.The most frequent causes of ESRD were diabetes mellitus(n06), systemic arterial hypertension (n05), polycystickidney disease (n04), and unknown (n04).

The nutritional status of the patients was classifiedaccording to BMI, with 10.0 % (n02) of the individualsbeing malnourished and 52.6 % (n010) being over-weight or obese. Based on MAMA measurement, leanmass depletion was detected in 31.6 % (n06) of theindividuals. Sixteen patients (84.2 %) had WC measure-ments above recommended values. The results of BIAdemonstrated that 12 patients (63.1 %) had excess bodyweight (Table 1). Fourteen patients (73.3 %) hadhypoalbuminemia and about 63 % (n012) had serumCRP levels ≥5.1 mg/L (Table 2).

Table 1. Anthropometric and body composition variables of the patients participating in the study

Mean SD Minimum Median Maximum

Waist circumference (cm) 95.9 14.1 59.5 97.7 119.5Mid-arm circumference (cm) 30.1 5.1 20.0 29.8 38.0Mid-arm muscle area (cm) 22.4 3.4 16.5 22.9 27.9BMI (kg/m2) 27.0 5.5 16.3 27.0 36.5Tricipital skin fold (mm) 24.3 12.6 7.3 26.4 42.0Body fat (kg) 20.1 7.6 6.1 20.0 37.0Lean mass (kg) 44.1 8.1 23.6 45.7 57.1Total water (L) 32.7 5.5 21.9 32.3 44.6Phase angle (degrees) 5.4 2.2 3.4 5.1 14.4

BMI body mass index

Table 2. Clinical and biochemical characteristics of the patients part-icipating in the study

Mean±SD

Urea (mg/dL) 98.5±31.0Creatinine (mg/dL) 7.4±2.0Kt/V 2.2±1.0Albumin (g/dL) 3.7±4.0Absorbed glucose (g/day) 293.0±139.0C-reactive protein (mg/L) 10.1±12.7

691Body Fat and Inflammation

In order to compare inflamed patients and patientswith no serum signs of inflammation regarding anthro-pometric and body composition parameters, the patientswere divided into groups according to CRP level.However, no differences in clinical or biochemicalcharacteristics were observed between groups (Table 3).

The patients with high CRP levels also had higherWC, MAC, BMI, TCF, and body fat values than patientswith no biochemical evidence of the presence ofinflammation. The parameters related to lean massquantitation did not differ between groups (Table 4).

A positive association was observed between CRPand some anthropometric parameters such as BMI (r00.75;p00.0005) (Fig. 1), MAC (r00.52; p<0.02), WC (r00.81;p<0.0001) (Fig. 1), and TCF (r00.49; p00.03). Anassociation was also detected between glucose absorbedfrom the PD fluid and WC (r00.48; p<0.05) (Fig. 2).

DISCUSSION

The main findings of the present study were excessweight and body fat in the abdominal region of female

patients on PD. The presence of chronic inflammationwas also observed in most of these patients and wasassociated with excess weight and body fat, especiallyvisceral fat.

The presence of malnutrition in patients on PD iswidely accepted, although a growing prevalence ofexcess weight and body fat has been observed in thesepatients by several authors. In a study on PD patients,Chow et al. [18] detected malnutrition in 14 % of themand excess weight in 50.9 % according to BMI.

The mean BMI of ESRD patients has beenprogressively increasing since the late 1980s. In Aus-tralia and New Zealand, the mean BMI of patientsstarting PD increased from 22.1 to 26.0 kg/m2. The sameincrease was reported in the USA, where BMI mean was25.7 kg/m2 in 1995 and 27.5 kg/m2 in 2002. During thisperiod, the prevalence of obesity increased from 33 to63 % and the increase in mean BMI in patients withESRD was twice that observed in the general NorthAmerican population [19].

This alarming growth of the prevalence of obesityin the population on dialysis may be attributed to manyreasons, including the increased prevalence of obesity in

Table 3. Comparison of the clinical and biochemical characteristics of patients with and without signs of inflammation

CRP ≥5.1 mg/L CRP <5.1 mg/L p value

Number of patients (n) 12 7 –Age (years) 57.9±13.1 52.9±18.3 nsTime on dialysis (months) 21.5±24.4 47.9±45.4 nsUrea (mg/dL) 107.3±35.9 84.7±14.5 nsCreatinine (mg/dL) 7.4±2.1 7.2±2.1 nsKt/V 2.1±0.6 2.4±1.9 nsAlbumin (g/dL) 3.6±4.3 3.8±0.4 nsAbsorbed glucose (g/day) 308.9±128.9 253.5±173.5 ns

CRP C-reactive protein, ns nonsignificant

Table 4. Comparison of the anthropometric parameters and body composition of the groups of patients with and without signs of inflammation

CRP ≥5.1 mg/L CRP <5.1 mg/L p value

Waist circumference (cm) 102.6±9.6 83.2±13.0 0.002Mid-arm circumference (cm) 32.2±3.9 25.7±4.3 0.003Mid-arm muscle area (cm) 23.1±2.2 21.1±5.1 nsBMI (kg/m2) 29.7±4.3 21.8±3.9 0.001Tricipital skin fold (mm) 29.0±11.0 14.4±9.7 0.01Body fat (kg) 23.7±6.7 13.9±5.2 0.004Lean mass (kg) 45.5±4.8 41.0±12.1 nsTotal water (L) 33.9±4.5 29.8±6.6 nsPhase angle (deg) 4.7±0.8 6.6±3.5 ns

CRP C-reactive protein, BMI body mass index, ns nonsignificant


the general population, the marked risk of progressionfrom chronic renal disease to ESRD in obese patients,and the lower probability of obese patients on dialysisreceiving a kidney transplant [20].

A gradual reduction of total body nitrogen seems tooccur in these patients along with the dialysis treatmentwhich is reflected by the loss of lean mass, as observedin the present study. Thus, the increase in body weightobserved in most individuals may occur due to adiposetissue [21, 22].

Di Gioia et al. [22] used BIA to evaluate the bodycomposition of patients treated with PD and observedexcess body weight in their study sample. Theirobservation is in agreement with the results of thepresent study, in which the abdominal region was themain site of localization of excess adipose tissue. This isalso reported by others [2–23].

This progressive accumulation of adipose tissue,especially in the abdominal region, is the result ofcontinuous glucose absorption during PD treatment [23],

as detected by the association of energy absorbed fromthe glucose present in the PD fluid with abdominalcircumference in the present study. PD patients areexposed daily to standard dialysis solutions containingabout 10–40 times more glucose than the bloodstream(1,360 to 3,860 mg/dL) which can supply 100 to 200 gglucose within 24 h [18].

Cho et al. [18] demonstrated the occurrence of agreater fat accumulation during the first year oftreatment, although the mechanisms by which thesepatients rapidly accumulate adipose tissue are not clear.Wang et al. [24], after associating patients on PDcarrying the UCP2 del/del genotype with increased bodyfat during the first year of treatment, recently suggestedthe participation of the UCP2 gene in the expenditure ofexcess energy in an environment with a high glucoseconcentration.

Adipose tissue is an active system capable ofsynthesizing and secreting adipokines such as IL-6 andleptin, which attract macrophages for infiltration among

Fig. 2. Association between glucose absorbed from the peritoneal dialysis solution and abdominal circumference.

Fig. 1. Association between C-reactive protein and anthropometric parameters.


the adipocytes, leading to the release of more cytokinesand inflammatory mediators [1]. Axelsson et al. [2]observed that adipose tissue is an important source ofIL-6 production in patients with ESRD, contributingabout 20 % of the total circulating concentration of thiscytokine, which is responsible for the stimulation ofCRP production by the liver [25]. In the present sample,63 % of the patients had elevated serum CRP levels,prevalence similar to that reported in other studies [2].

Positive associations between inflammation andbody fat have been reported in the literature [4–27] andwere also observed in the present study. Nihi et al. [5]investigated associations between inflammation andbody fat in patients on hemodialysis treatment anddetected positive correlations between CRP and BMIand body fat, in agreement with the results of the presentstudy. The authors suggested that chronic inflammationmay be more associated with excess weight and body fatthan with malnutrition.

A study conducted on patients with chronic renaldisease before dialysis investigated possible geneticchanges related to subcutaneous adipose tissue in thisgroup and detected changes in the expression ofinflammatory genes in this tissue. The authors concludedthat the presence of adipose tissue in combination withimpaired renal function contributes to the systemicinflammation of these patients [27].

The results of the present study showed that theanthropometric and body composition parameters thatreflect the quantity of adipose tissue were higher ininflamed patients than in subjects with normal CRPconcentrations, although no difference was observedbetween groups in the parameters regarding lean mass.Axelsson et al. [2] also detected significant differencesin the quantity of total body and visceral fat evaluated byDEXA in patients with ESRD divided into inflamed andnon-inflamed groups.

A study in which patients with stage 3 and 4chronic renal disease were followed for 12 monthsdemonstrated that changes in CRP concentrations arepositively associated with changes in the markers ofadiposity in this group after adjustment for confound-ing factors such as age, gender, and glomerularfiltration rate. The magnitude of this association wasthe observed increase in CRP concentration of 1.94and 0.45 for each increased BMI and WC unit,respectively [1].

A different aspect of the present study was the useof two different indicators of adiposity: one reflectingthe total quantity of BF and the other indicating visceral

fat. Both exceeded normal values in the patients studied,especially those presenting serum signs of inflammation,and were correlated with CRP, in agreement withliterature data [5].

Evidence suggests that the differential distributionof adipose tissue has an impact on the secretion of pro-inflammatory cytokines and may contribute to theinflammatory state in a general manner [1]. Additionally,the inflammatory activity seems to differ according tothe body localization of adipose tissue, with visceral fatbeing more active than subcutaneous fat [2]. However,the mechanisms responsible for this difference are stillunknown and future studies are needed to interpret thedata obtained thus far [5].

Many studies have demonstrated that inflammatorymarkers such as CRP are strong and independentpredictors of mortality for individuals with ESRD [2].Adipose tissue has been pointed out as a potential causeof the systemic inflammation observed in this group [1].This association is quite important for patients on PDsince the beginning of treatment is accompanied by aweight and body fat gain [4].

The present results agree with data available in theliterature, suggesting that nutritional evaluation per-formed with simple methods can produce reliableresults. These findings motivate a search for clinicaland nutritional strategies aiming at fat and body weightloss in order to reduce or improve the state of chronicinflammation observed in patients on PD, thus contrib-uting to a reduction of mortality and an improvement ofquality of life in this group.

ACKNOWLEDGMENTS

The authors thank National Council for Scientificand Technological Development (CNPq) for grantsupport.

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association of body fat with inflammation in peritoneal dialysis

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