Diet-Related Inflammation is Associated with Malnutrition-Inflammation Markers in Maintenance Hemodialysis Patients: Results of a Cross-Sectional Study in China Using Dietary Inflammatory Index

Figures & data

Table 1 Baseline Characteristics of MHD Patients

Variable	Total	Tertile 1 (DII ≤ −0.0483)	Tertile 2 (−0.0483 < DII < 1.718)	Tertile 3 (DII ≥ 1.718)	P-value
Continuous variables
Participant number	161	53	55	53
(Mean ± SD)
Age (year) *	59.99 ± 13.61	57.94 ± 14.03	60.82 ± 14.51	61.19 ± 12.15	0.406
K+ (mmol/L) *	4.71 ± 0.54	4.70 ± 0.54	4.70 ± 0.50	4.71 ± 0.58	0.990
P (mmol/L) *	1.91 ± 0.41	1.90 ± 0.41	1.91 ± 0.37	1.91 ± 0.46	0.976
(Median [IQR])
Dialysis vintage (yrs)^†	3.00(1.00, 7.00)	4.00(1.00, 8.50)	3.00(1.58, 7.00)	3.00(1.00, 6.50)	0.605
DII^†	0.60(−0.80, 2.32)	−1.41(−2.34, −0.80)	0.60(0.33, 1.25)	3.13(2.32, 3.96)	<0.0001
PLR (%)^†	161.58(140.90, 207.16)	158.53(140.43, 201.16)	154.91(138.53, 190.43)	186.22(147.93, 244.53)	0.044
HB (g/L)^†	111.00(99.51, 118.42)	109.63(96.80, 116.88)	112.67(103.86, 119.43)	110.33(98.27, 119.29)	0.226
Cr (umol/L)^†	870.25(765.67, 983.13)	888.38(794.50, 1007.88)	856.00(743.67, 967.60)	870.40(742.90, 987.40)	0.378
Urea (mmol/L)^†	25.50(22.07, 28.99)	25.50(22.69, 28.42)	25.24(21.11, 29.20)	25.88(22.07, 29.52)	0.879
Ca (mmol/L)^†	2.24(2.11, 2.37)	2.24(2.12, 2.36)	2.22(2.10, 2.37)	2.29(2.09, 2.40)	0.998
ALB (g/L)^†	39.60(37.27, 40.92)	40.30(38.12, 41.30)	39.12(36.80, 40.47)	39.60(37.13, 40.64)	0.069
TP (g/L)^†	68.06(64.31, 70.54)	67.70(64.12, 70.22)	68.34(64.96, 70.64)	68.08(64.26, 70.63)	0.758
TC (mmol/L)^†	3.73(3.14, 4.37)	3.66(2.97, 4.37)	3.75(3.25, 4.23)	3.79(3.22, 4.51)	0.732
Serum total iron binding capacity (umol/L)^†	38.73(35.01, 44.35)	39.02(34.34, 46.56)	38.67(35.20, 44.25)	39.00(35.16, 44.26)	0.899
Transferrin saturation (%)^†	31.43(23.59, 39.44)	33.40(22.01, 41.33)	30.70(24.24, 35.86)	31.98(23.31, 41.71)	0.441
CRP (mg/L)^†	3.29(1.37, 7.20)	1.30(0.69, 2.41)	2.93(1.86, 4.35)	8.60(6.58, 13.95)	< 0.0001
NLR (%)^†	4.18(3.27, 5.73)	3.90(2.87, 5.11)	4.451(3.49, 5.52)	4.120(3.36, 6.42)	0.099
Na+ (mmol/L)^†	139.00(138.00, 140.00)	139.14(138.05, 140.31)	139.00(138.33, 140.00)	138.55(137.86, 140.05)	0.334
TG (mmol/L)^†	1.36(0.95, 1.91)	1.12(0.82, 1.91)	1.41(1.03, 2.07)	1.34(1.02, 1.84)	0.081
PTH (pg/mL)^†	372.82(210.56, 633.35)	365.80(217.38, 740.82)	359.75(208.40, 525.56)	408.09(183.22, 695.79)	0.684
Categorical variables (%)
Male/ female^‡	50.93%/49.07%	49.06%/50.94%	43.64%/56.36%	60.38%/39.62%	0.208
BMI (kg/m2) θ					0.125
Underweight (< 18.5)		16.98%	5.45%	9.43%
Normal (18.5–24.9)		69.81%	78.18%	66.04%
Overweight (25–29.9)		13.21%	14.55%	22.64%
Obese (> 30)		0.00%	1.82%	1.89%
MIS (%) θ					<0.0001
< 8		50.94%	40.00%	3.77%
8–18		49.06%	60.00%	94.34%
19–30		0.00%	0.00%	1.89%

Notes: *One-way ANOVA test; ^†Kruskal–Wallis H-test; ^‡chi-square test; θ Goodman-Kruskal GammaTest. Statistically significant at P < 0.05.

Abbreviations: DII, dietary inflammatory index; CRP, c-reactive protein; HB, Hemoglobin; Cr, serum creatinine; Urea, serum urea; ALB, albumin; TP, total protein; TG, tri-glyceride; TC, total cholesterol; PTH, parathyroid hormone; BMI, body mass index; NLR, neutrophil-to-lymphocyte ratio; PLR, platelet-to-lymphocyte ratio; MIS, malnutrition-inflammation score.

Figure 1 Flow diagram for study participants.

Abbreviation: MHD, maintenance hemodialysis.

Table 2 Distribution of Food Parameter of MHD Patients

Food Parameter/ Day	Total	Tertile 1	Tertile 2	Tertile 3	P-value
(Mean ± SD)
Total fat (g)*	35.22 ± 13.52	38.82 ± 15.50	33.53 ± 12.26	33.37 ± 12.11	0.06
MUFA (g)*	12.37 ± 5.01	13.66 ± 5.65	11.58 ± 4.29	11.90 ± 4.87	0.069
Vitamin E (mg)*	11.01 ± 3.42	12.35 ± 3.72	10.63 ± 3.31	10.07 ± 2.82	0.001
Zn (mg)*	12.39 ± 3.18	13.72 ± 3.41	12.16 ± 2.76	11.29 ± 2.93	<0.0001
(Median [IQR])
Energy (kcal)^†	1398.58(1180.07,1691.58)	1583.75(1376.89,1852.30)	1362.19(1158.92,1589.14)	1321.39(1063.60,1531.50)	<0.0001
Carbohydrate (g)^†	196.18(150.94,242.83)	218.92(193.28,273.41)	185.73(146.46,225.61)	173.06(137.60,214.09)	<0.0001
Protein (g)^†	72.87(58.79,92.13)	82.43(60.97,101.31)	72.87(60.90,86.33)	68.78(54.25,88.58)	0.105
Saturated fat (g)^†	8.79(6.49,11.52)	9.42(6.97,11.97)	9.34(6.63,11.02)	7.93(6.35,11.93)	0.535
Fibre (g)^†	23.00(15.02,30.20)	26.24(18.70,31.42)	23.27(13.23,30.38)	17.82(12.25,23.41)	<0.0001
Mg (mg)^†	359.17(319.97,410.30)	396.37(360.44,452.16)	358.18(324.20,405.62)	323.65(297.29,363.84)	<0.0001
Omega-6 fatty acids (g)^†	13.32(9.53,17.39)	15.14(11.84,21.26)	11.37(8.51,15.06)	12.12(9.32,15.87)	0.002
PUFA (g)^†	8.55(5.39,11.82)	9.97(6.22,12.92)	8.44(4.58,11.68)	7.80(5.46,10.58)	0.207
VitaminB1(thiamin) (mg)^†	1.01(0.74,1.38)	1.16(0.85,1.52)	0.99(0.75,1.32)	0.92(0.67,1.35)	0.181
Riboflavin (mg)^†	1.22(0.95,1.49)	1.36(1.08,1.58)	1.24(0.96,1.52)	1.03(0.89,1.29)	0.002
Niacin (mg)^†	31.24(24.89,37.29)	34.73(26.83,40.79)	29.49(25.00,35.70)	30.34(21.65,33.49)	0.006
Se (μg)^†	33.77(27.93,43.53)	36.08(28.57,50.63)	35.19(27.93,42.02)	32.10(26.87,42.14)	0.235
Vitamin B12 (μg)^†	1.60(1.15,2.28)	1.84(1.04,2.34)	1.67(1.22,2.14)	1.56(1.07,2.36)	0.755
Cholesterol (mg)^†	125.00(82.24,182.07)	136.18(92.38,186.94)	121.49(85.25,179.47)	115.18(71.46,193.81)	0.766
Fe (mg)^†	19.03(16.87,22.26)	21.91(17.86,25.32)	19.03(16.94,21.59)	17.43(15.42,19.93)	<0.0001
Trans fat (g)^†	0.18(0.08,0.41)	0.29(0.14,0.49)	0.15(0.08,0.32)	0.14(0.06,0.31)	0.028
Alcohol (g)^†	0.00(0.00,0.00)	0.00(0.00,0.00)	0.00(0.00,0.00)	0.00(0.00,0.00)	0.737
β-carotene (μg)^†	3999.68(2496.03,5335.18)	4062.30(2727.99,5335.18)	4037.20(2680.57,5495.60)	3965.47(2325.66,5260.69)	0.144
Omega-3 fatty acids (g)^†	0.97(0.75,1.52)	1.33(0.81,2.23)	0.93(0.67,1.32)	0.94(0.60,1.48)	0.007
Vitamin C (mg)^†	59.92(36.08,71.88)	62.08(45.78,69.91)	63.28(36.41,88.57)	53.97(32.16,67.40)	0.235
Vitamin A (RE)^†	421.35(279.62,521.56)	443.96(339.08,503.56)	434.01(269.79,575.39)	396.70(260.88,491.70)	0.229

Notes: *One-way ANOVA test; ^†Kruskal–Wallis H-test. Statistically significant at P < 0.05.

Abbreviations: PUFA, polyunsaturated fatty acids; MUFA, monounsaturated fatty acid.

Table 3 Association Between Dietary Inflammatory Index and Malnutrition-Inflammation Markers Among Hemodialysis Patients

DII Groups	Model 1						Model 2
	MIS	CRP (mg/L)	ALB (g/L)	HB (g/L)	NLR (%)	PLR (%)	MIS	CRP (mg/L)	ALB (g/L)	HB (g/L)	NLR (%)	PLR (%)
Continuous
β	0.58	0.70	−0.16	0.04	0.12	0.10	0.61	0.54	−0.10	0.01	0.14	0.03
95% CI	(0.46, 0.68)	(0.58, 0.80)	(−0.30, -0.01)	(−0.11, 0.20)	(−0.04, 0.28)	(−0.20, 0.26)	(0.51, 0.69)	(0.46, 0.63)	(−0.27, 0.09)	(−0.15, 0.18)	(−0.06, 0.30)	(−0.15, 0.22)
P-value	<0.0001	<0.0001	0.054	0.617	0.12	0.197	<0.0001	<0.0001	0.213	0.923	0.076	0.698
Tertile 1
β	−0.04	0.04	0.04	−0.13	−0.32	−0.16	−0.01	−0.18	0.03	−0.13	−0.37	−0.30
95% CI	(−0.30, 0.21)	(−0.28, 0.33)	(−0.25, 0.32)	(−0.39, 0.16)	(−0.578, -0.02)	(−0.48, 0.14)	(−0.30, 0.27)	(−0.54, 0.22)	(−0.25, 0.33)	(−0.42, 0.14)	(−0.61, -0.13)	(−0.57, 0.02)
P-value	0.78	0.784	0.804	0.361	0.019	0.252	0.929	0.224	0.854	0.369	0.008	0.037
Tertile 2
β	0.39	0.29	0.01	0.01	0.03	−0.05	0.41	0.28	0.03	−0.06	−0.03	−0.14
95% CI	(0.11, 0.60)	(0.06, 0.51)	(−0.28, 0.30)	(−0.28, 0.28)	(−0.23, 0.31)	(−0.32, 0.23)	(0.12, 0.64)	(−0.01, 0.50)	(−0.26, 0.29)	(−0.34, 0.23)	(−0.29, 0.29)	(−0.42, 0.21)
P-value	0.004	0.031	0.957	0.932	0.824	0.732	0.003	0.045	0.848	0.697	0.82	0.318
Tertile 3
β	0.60	0.55	−0.32	−0.14	0.01	−0.05	0.58	0.66	−0.23	−0.13	0.19	−0.01
95% CI	(0.39, 0.76)	(0.27, 0.75)	(−0.55, -0.06)	(−0.39, 0.13)	(−0.29, 0.31)	(−0.31, 0.22)	(0.36, 0.76)	(0.43, 0.83)	(−0.47, 0.08)	(−0.37, 0.12)	(−0.12, 0.43)	(−0.28, 0.23)
P-value	<0.0001	<0.0001	0.019	0.325	0.966	0.699	<0.0001	<0.0001	0.116	0.394	0.197	0.935

Notes: Model 1: unadjusted; Model 2: age, BMI, gender, and dialysis vintage were adjusted.

Abbreviations: CRP, c-reactive protein; HB, Hemoglobin; ALB, albumin; NLR, Neutrophil-to-lymphocyte ratio; PLR, platelet-to-lymphocyte ratio; MIS, malnutrition-inflammation score.

Table 4 Multivariate Logistic Regression Analysis with MIS Status as Outcome

	Multivariate Model α		Multivariate Model β
Variables	Odds Ratio (95% CI)	P value	Odds Ratio (95% CI)	P value
CRP	1.05 (1.01, 1.10)	0.021	1.06 (1.01, 1.11)	0.012
DII	2.413 (1.17, 4.99)	0.017	3.06 (1.39, 6.69)	0.005

Notes: α Variables included in the analysis were CRP and DII; βVariables included in the analysis were CRP, DII, age, gender, BMI and dialysis vintage.

Abbreviations: DII, dietary inflammatory index; CRP, c-reactive protein; BMI, body mass index.