MALNUTRITION-INFLAMMATION SCORE IS A USEFUL TOOL IN PERITONEAL DIALYSIS PATIENTS
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Peritoneal Dialysis International, Vol. 26, pp. 705–711 0896-8608/06 $3.00 + .00
Printed in Canada. All rights reserved. Copyright © 2006 International Society for Peritoneal Dialysis
MALNUTRITION–INFLAMMATION SCORE IS A USEFUL TOOL IN
PERITONEAL DIALYSIS PATIENTS
Bariş Afşar,1 Siren Sezer,1 Fatma Nurhan Ozdemir,1 Huseyin Celik,1
Rengin Elsurer,1 and Mehmet Haberal2
Department of Nephrology1 and Department of General Surgery,2
Baskent University Hospital, Ankara, Turkey
♦♦Background: Malnutrition–Inflammation Score (MIS) is patients, and that those correlations were stronger than
a quantitative assessment tool based on Subjective Global those with SGA.
Assessment (SGA) and predicts mortality and morbidity in
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maintenance hemodialysis patients. However, there are not Perit Dial Int 2006; 26:705–711 www.PDIConnect.com
enough data about the use of MIS in peritoneal dialysis
(PD). In this study, relationships between MIS and prospec- KEY WORDS: Malnutrition–Inflammation Score;
tive hospitalization indices, risk of developing peritonitis, Subjective Global Assessment; peritonitis; hospitaliza-
anemia indices, and laboratory and anthropometric param- tion; protein–energy malnutrition; anthropometric
eters were analyzed and compared with SGA in PD. measurements.
♦♦Methods: 50 PD patients (M/F 26/24, age 45.2 ±
14.9 years, mean PD duration 30.8 ± 23.1 months) were in-
cluded. The same physician performed the SGA and MIS
evaluations. Clinical, laboratory, and anthropometric pa-
P rotein–energy malnutrition (PEM) is a common
health problem in end-stage renal disease (ESRD) pa-
tients, and association between malnutrition and out-
rameters were measured.
♦♦Results: 18 patients were classified as SGA-A (without come is evident. Nutritional status of dialysis patients
malnutrition), 24 as SGA-B (with moderate malnutrition), can be assessed by biochemical assays, anthropometry,
and 8 as SGA-C (with severe malnutrition). Increment in protein catabolic rate, and body composition methods.
MIS was concordant with SGA groups A to C (p < 0.0001). Recently, the relationship between malnutrition and in-
Peritonitis rate, number of hospitalizations, total number flammation has received considerable attention and a
of hospitalization days, erythropoietin requirements, strong association between PEM and inflammation has
C-reactive protein (CRP), and ferritin levels were positively been shown in dialysis patients (1,2). These two condi-
correlated with MIS (p < 0.0001). Midarm muscle circum- tions, PEM and inflammation, often occur concomitantly
ference (p = 0.04), albumin (p < 0.0001), prealbumin (p = in hemodialysis patients. Together, they have been re-
0.001), creatinine (p = 0.04), hemoglobin (p = 0.003),
ferred to as the malnutrition–inflammation complex syn-
transferrin (p < 0.0001), and cholesterol (p = 0.009) were
drome (3). Protein-energy malnutrition is also highly
negatively correlated with MIS. Correlation coefficients of
hospitalization indices, peritonitis rate, anemia indices, prevalent among peritoneal dialysis (PD) patients and
erythropoietin requirements, albumin, prealbumin, CRP, Fein et al. confirmed the relationship between indica-
and anthropometric parameters were higher with MIS than tors of malnutrition and measures of inflammation in PD
with SGA. In logistic regression analysis, a higher MIS was patients (4). Subjective Global Assessment (SGA) deter-
independently associated with a higher risk of future hos- mines whether nutrient assimilation has been restricted
pitalization (p = 0.029, odds ratio 2.14, confidence inter- because of decreased food intake, maldigestion or mal-
val 1.082 – 4.146). absorption, whether any effects of malnutrition on organ
♦♦Conclusions: This study demonstrated that MIS signifi- function have occurred, and whether the patients’ dis-
cantly correlated with clinical, nutritional, inflammatory, ease process influences nutrient requirements (5). Both
and anthropometric parameters and anemia indices in PD inflammation and malnutrition affect the clinical con-
Correspondence to: B. Afşar, 3. Cadde 50, Sokak 9/8 06500 dition of dialysis patients and must be assessed in a com-
Bahçelievler, Ankara, Turkey. bined way. For this purpose, a comprehensive scoring
afsarbrs@yahoo.com system called Malnutrition–Inflammation Score (MIS),
Received 11 December 2005; accepted 3 April 2006. which is capable of risk stratifying in hemodialysis
705AFŞAR et al. NOVEMBER 2006 – VOL. 26, NO. 6 PDI
patients in a quantitative way for optimal management, MALNUTRITION–INFLAMMATION SCORE
was developed. Malnutrition–Inflammation Score is
strongly correlated with prospective hospitalizations and The MIS was created using the seven components of
mortality, as well as with measures of nutrition, inflam- the conventional SGA and combining them with three
mation, and anemia in hemodialysis patients (6). How- new elements: body mass index (BMI), serum albumin,
ever, there are not enough data about the use of MIS in and total iron-binding capacity (TIBC) to represent serum
PD. In the present study, relationships between MIS and transferrin (6). The MIS consists of four sections: nutri-
prospective hospitalization indices (hospitalization fre- tional history, physical examination, BMI, and labora-
quency and total hospitalization days), risk of develop- tory values. Each of the 10 components has 4 levels of
ing peritonitis, anemia indices, and laboratory and severity, from 0 (normal) to 3 (severely malnourished).
anthropometric parameters were analyzed and com- The sum of the 10 components varies between 0 and 30.
pared with SGA. A higher score reflects a more severe degree of malnu-
trition and inflammation.
SUBJECTS AND METHODS The history section in MIS includes the above-men-
tioned five components of SGA (6). In our study, we mea-
In total, 50 consecutive PD patients who underwent sured the body weight of PD patients when their
routine controls (male/female 26/24, mean age 45.2 ± abdomen was empty. Weight change was determined as
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14.9 years, mean PD duration 30.8 ± 23.1 months) were change in body weight during the previous 6 months.
included. All patients were willing to participate and were In addition, comorbidity, which includes dialysis vintage
capable of answering the questions. Written informed (number of years on dialysis therapy), was added to the
consent was obtained from all patients. Among the original SGA questionnaire. Other major comorbid con-
50 patients, 46 were on continuous ambulatory PD ditions include congestive heart failure class III or IV,
therapy and 4 patients were on automated PD therapy. full blown AIDS, severe coronary artery disease, moder-
Etiologies of ESRD were as follows: 14% diabetes, 10% ate-to-severe chronic obstructive pulmonary disease,
hypertension, 16% glomerulonephritis, 8% polycystic major neurological sequela, and metastatic malignan-
kidney disease, 14% nephrolithiasis, 14% vesicoureteral cies or recent chemotherapy. Thus, comorbidity is scored
reflux, and 4% amyloidosis. Etiology of ESRD was un- 0 if there are no other medical illnesses and the patient
known in 20% of patients. The same physician performed has undergone hemodialysis therapy (in our study, PD
SGA and MIS evaluations. Peritonitis was defined as a therapy) for less than 1 year; score 1 indicates mild co-
cloudy dialysate with more than 100 white blood cells/µL morbidity, excluding major comorbid conditions, or di-
and 50% or more polymorphonuclear cells. All fluids sus- alysis therapy for 1 – 4 years; score 2 indicates moderate
picious of peritonitis were sent for cell count and cul- comorbidity, including one of the major comorbid con-
ture. Total number of hospitalizations/patient/ ditions listed above or dialysis therapy for more than
6 months, including hospitalizations due to peritonitis, 4 years; and score 3 indicates two or more major comor-
and total days of hospitalizations/patient/6 months, bid conditions.
including days of hospitalizations for peritonitis, dur- Body fat stores and signs of muscle wasting are two
ing the 6-month prospective period were recorded. A variables determined in the physical examination as
simplified peritoneal equilibration test was performed in SGA. A score of 0 through 3, representing normal
for each patient at the time of enrolment in the study to to severe changes, is assigned for each of these two
obtain the dialysate/plasma creatinine concentration components. Presence of edema is the third compo-
ratio at 4 hours of dwell, as described by Twardowski nent of the original SGA physical examination not
et al. (7). used in MIS evaluation (6). Body mass index, a ratio
of weight in kilograms (when abdomen is empty) to
SUBJECTIVE GLOBAL ASSESSMENT height squared (in square meters), is divided into four
graded groups as follows: grade 0: >20 kg/m 2 ;
History used in SGA focuses on five areas: (1) percent- grade 1: 18 – 19.99 kg/m2; grade 2: 16 – 17.99 kg/m2;
age of body weight loss in the previous 6 months, (2) and grade 3:PDI NOVEMBER 2006 – VOL. 26, NO. 6 MIS IN PERITONEAL DIALYSIS
ANTHROPOMETRIC EVALUATION considered statistically significant if two-tailed p value
was less than 0.05. Variables were checked for normal-
Body weight measurement of PD patients was per- ity. Data are shown as mean ±SD and percent. Compari-
formed using an electronic platform scale when their sons between two groups were assessed by means of
abdomens were empty (after draining PD fluid). Biceps t-test for normally distributed continuous variables and
skinfold and triceps skinfold thicknesses (TSF) were mea- Mann–Whitney U test for non-normally distributed con-
sured in triplicate using a conventional skinfold caliper tinuous variables. Comparisons between three groups for
and results were averaged. Midarm circumference (MAC) nonparametric variables were done using Kruskal–Wallis
was measured with a plastic tape. Midarm muscle circum- test. Bonferroni corrected Mann–Whitney U test was used
ference (MAMC) was calculated from the equation MAMC = for post hoc analysis. Pearson’s correlation coefficient r
MAC – (3.1415 × TSF). was used for selected analysis between continuous vari-
ables. We used Spearman’s correlation analysis for non-
LABORATORY AND CLINICAL EVALUATION parametric variables. Multivariate logistic regression
analysis was performed to investigate independent ef-
Laboratory parameters, including hemoglobin, serum fects of individual variables.
albumin, prealbumin, transferrin, blood urea nitrogen,
creatinine, potassium, calcium, phosphorus, total cho- RESULTS
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lesterol, high-density lipoprotein, low-density lipopro-
tein, triglyceride, C-reactive protein (CRP), and Table 1 lists demographic and anthropometric char-
parathyroid hormone levels, were measured at time of acteristics and MISs of the 50 PD patients included in
study enrollment and were analyzed. Serum albumin and the study. No patient died during the study. During the
transferrin concentrations used in MIS were also mea- 6-month period, 4 of the 50 patients were hospitalized
sured at the time of initiation of the study. Blood hemo- 3 times, 9 were hospitalized 2 times, and 17 were hospi-
globin levels were measured in a Coulter STKS flow talized once; 20 were not hospitalized. Mean number and
cytometer (Coulter Electronics, Miami, Florida, USA). duration of hospitalizations were 1.5 ± 0.73 days and
Serum albumin levels were measured by quantitative 23.5 ± 13.6 days respectively in the 30 patients who were
colorimetry (Stanbio Laboratory, San Antonio, Texas, hospitalized. Thirteen patients were not receiving EPO,
USA) by bromcresol green method. Prealbumin levels whereas 37 patients were administered subcutaneous
were measured by immunoturbidimetric assay by PP mod- EPO in doses ranging from 2000 to 15000 U/week. Labo-
ule automatic analyzer (Roche Diagnostics, Mannheim, ratory parameters and EPO requirements of the 50 PD
Germany). A colorimetric method was used to measure patients are shown in Table 2.
serum calcium and phosphorus (Beckman Cx-7 Auto- Patients were divided into three groups depending on
analyzer; Beckman Instruments, Diagnostic Systems the number of peritonitis attacks they suffered during
Group, Brea, California, USA). Serum levels of total cho- the 6-month period: 31 patients did not experience any
lesterol, high-density lipoprotein, low-density lipopro- attacks of peritonitis (group 1), 14 had 1 peritonitis at-
tein, and triglyceride were measured by direct tack (group 2), and 5 had 2 peritonitis attacks (group 3).
quantitative colorimetric method (Human Gesellchaft Mean MIS of groups 1, 2, and 3 was 6.1 ± 4.6, 10.1 ± 3.2,
für Biochemica und Diagnostica mbH, Wiesbaden, Ger- and 14.8 ± 3.1 and was significantly different (p <
many). Turbidimetric latex agglutination method 0.0001). The MISs of each group were compared with
(Biosystems SA, Barcelona, Spain) was used to determine each other by post hoc analysis (Figure 1).
CRP levels. Other biochemical parameters were measured According to SGA results, 18 patients were in SGA-A,
using standard laboratory methods. Presence and num- 24 were in SGA-B, and 8 were in SGA-C. The MIS of these
ber of hospital admissions, episodes of peritonitis, and 3 groups was 13.0 ± 4.3, 15.0 ± 8.5, and 20.0 ± 15.5 re-
erythropoietin (EPO) requirements during the 6-month spectively. Post hoc analysis showed that the MIS of the
prospective period were recorded. No death was recorded SGA groups (SGA-A, SGA-B, and SGA-C) were significantly
during study period. different (p < 0.0001) (data not shown). Correlations for
MIS and SGA with demographic, clinic, and anthropo-
STATISTICS metric data and laboratory data are shown in Tables 3
and 4 respectively.
Statistical analysis was performed using SPSS 10.0 When the presence of hospitalization was accepted
(SPSS Inc, Evanston, Illinois, USA) for Windows as an end point, multivariate logistic regression analy-
(Microsoft, Redmond, Washington, USA). Results were sis showed that only higher MIS was independently
707AFŞAR et al. NOVEMBER 2006 – VOL. 26, NO. 6 PDI
TABLE 1
Demographic and Anthropometric Characteristics and Malnutrition–
Inflammation Scores (MIS) of 50 Peritoneal Dialysis Patients
All patients (n=50) Men (n=26) Women (n=24) p Value
Age (years) 45.2±14.9 44.8±13.5 45.7±16.6 NS
Vintage (dialysis months) 30.8±23.1 30.3±25.3 31.3±21.1 NS
BMI (kg/m2) 25.4±4.8 24.3±3.6 26.6±5.7 NS
Triceps skinfold (mm) 12.2±3.9 10.6±2.9 14.1±4.2 0.002a
Biceps skinfold (mm) 6.5±2.3 5.6±1.8 7.5±2.5 0.006a
MAC (cm) 26.2±4.2 25.3±4.1 27.3±4.2 NS
MAMC (cm) 22.3±3.4 21.9±3.6 22.8±3.2 NS
MIS (range 0–30) 8.1±5.0 7.1±4.9 9.2±4.9 NS
BMI = body mass index; MAC = midarm circumference; MAMC = midarm muscle circumference; NS = nonsignificant.
a Statistically significant.
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TABLE 2
Laboratory Parameters and Erythropoietin Requirements of 50 Peritoneal Dialysis Patients
All patients (n=50) Men (n=26) Women (n=24) p Value
Albumin (g/L) 37.3±4.2 37.1±4.0 37.3±3.2 NS
Prealbumin (g/dL) 31.4±9.8 31.2±7.8 31.5±11.7 NS
CRP (mg/L) 15.3±9.0 12.2±9.2 18.6±15.8 NS
Hemoglobin (g/L) 107.3±19.2 111.4±22.1 102.1±14.3 NS
BUN (mmol/L) 19.48±3.96 19.8±4.28 19.2±3.78 NS
Creatinine (µmol/L) 882.9±249.9 932.9±274.9 833.0±208.3 NS
Calcium (mmol/L) 2.26±0.18 2.27±0.15 2.24±0.18 NS
Phosphorus (mmol/L) 1.54±0.48 1.63±0.45 1.44±0.51 NS
Potassium (mmol/L) 4.4±0.7 4.4±0.8 4.4±0.7 NS
Parathyroid hormone (pmol/L) 26.20±19.45 28.50±23.39 23.62±13.76 NS
Iron (µmol/L) 13.66±5.53 13.59±6.52 13.73±4.27 NS
TIBC (µmol/L) 33.57±7.58 33.89±7.70 33.19±7.58 NS
Ferritin (µg/L) 365.6±275.3 329.0±270.0 407.4±282.6 NS
Transferrin (g/L) 1.94±0.39 2.04±0.37 1.83±0.37 0.04a
Transferrin saturation (%) 41.6±16.2 41.3±19.6 42.0±11.6 NS
Cholesterol (mmol/L) 5.49±1.38 5.31±1.05 5.69±1.67 NS
Triglyceride (g/L) 1.79±0.84 1.67±0.73 1.94±0.94 NS
rHuEPO dose (U/wk) 7020±5705 5923±5649 8208±5641 NS
CRP = C-reactive protein; TIBC = total iron-binding capacity; rHuEPO = recombinant human erythropoietin.
a Statistically significant.
associated with higher risk of future hospitalization (p = Malnutrition–Inflammation Score showed higher nega-
0.029, odds ratio 2.14, confidence interval 1.082 – tive correlation with MAMC, hemoglobin, and serum al-
4.146) (data not shown). bumin, prealbumin, creatinine, transferrin, and
cholesterol levels than SGA.
DISCUSSION Combined occurrence of PEM and inflammation in kid-
ney failure, referred to as malnutrition–inflammation
In the present study, we found that MIS correlated complex syndrome, may be associated with such poor
positively with future peritonitis rate, number of hospi- outcomes as atherosclerotic disease, decreased quality
talizations and total hospitalization days, EPO require- of life, and increased mortality and hospitalization fre-
ments, and serum CRP and ferritin levels better than SGA. quency. In one study, Chung et al. showed that preva-
708PDI NOVEMBER 2006 – VOL. 26, NO. 6 MIS IN PERITONEAL DIALYSIS
and inflammatory status of dialysis patients, and the
reliability of methods for detecting PEM and their prac-
ticability are not convincing (9,10). Methods to measure
the inflammatory state of dialysis patients are not sat-
isfactory (11).
Subjective Global Assessment is a widely used method
to detect PEM in dialysis patients in practice; however,
given the variability of the results in the literature, SGA
cannot be considered a gold standard in nutritional as-
sessment for chronic kidney disease patients (12). Some
authors suggest that there must be a composite score
to represent a more reliable method for evaluation of
nutritional state of dialysis patients. A modified quan-
titative subjective global assessment of nutrition, called
Dialysis Malnutrition Score, was developed for dialysis
patients for this purpose. These authors suggest that
their malnutrition score may be superior to SGA (10).
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Recently, to make the scoring system more comprehen-
sive and quantitative, evaluation criteria for seven Di-
alysis Malnutrition Score components were revised and
Figure 1 — Malnutrition–Inflammation Scores of patients ac-
cording to their 6-month peritonitis attack rates. Group 1 =
three new items were added: BMI, TIBC, and serum al-
no attack of peritonitis during 6-month period; Group 2 = bumin level. It is well known that BMI has a predictive
1 attack of peritonitis during 6-month period; Group 3 = 2 at- value for dialysis mortality (13). Serum TIBC reflects
tacks of peritonitis during 6-month period. serum transferrin concentrations and serum transfer-
rin, which changes with iron loading, inflammation, and
lence of PEM and comorbid disease at the start of PD is gastrointestinal diseases often present in ESRD, corre-
high, and that the simultaneous presence of comorbid lates significantly with nutritional state in dialysis pa-
disease and malnutrition is associated with a high mor- tients. Albumin, which is a negative acute-phase
tality (8). There is no single way to assess nutritional reactant, is an important marker of nutrition in the
TABLE 3
Correlation Coefficients of Two Major Nutritional Scoring Systems, Subjective Global Assessment (SGA) and
Malnutrition–Inflammation Score (MIS), and Pertinent Demographic, Clinical, and Anthropometric Data
Correlation coefficient (r) for SGA (r) p Value MIS (r) p Value
Age +0.323 0.02a 0.230 0.1
Vintage 0.146 0.3 0.07 0.6
Body weight 0.02 0.8 0.112 0.4
BMI 0.242 0.1 0.02 0.8
PD duration 0.245 0.08 0.123 0.4
PET status 0.216 0.1 0.2 0.1
Peritonitis rate +0.349 0.01a +0.608AFŞAR et al. NOVEMBER 2006 – VOL. 26, NO. 6 PDI
TABLE 4
Correlation Coefficients of Two Major Nutritional Scoring Systems, Subjective Global Assessment (SGA) and
Malnutrition–Inflammation Score (MIS), and Pertinent Laboratory Data
Correlation coefficient (r) for SGA (r) p Value MIS (r) p Value
Albumin –0.397 0.04a –0.611PDI NOVEMBER 2006 – VOL. 26, NO. 6 MIS IN PERITONEAL DIALYSIS
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