Association of neutrophil-lymphocyte ratio with cardiovascular and all-cause mortality in patients receiving chronic hemodialysis: Systematic review and meta-analysis

Table 1 Baseline characteristics of the study population from the included studies, n (%)/mean ± SD

Ref.	Type of study	Follow-up in years	Sample size	Age in years	Males	BMI (Kg/m²)	Serum albumin (g/dL)	Absolute neutrophil value (109/L)	Absolute lymphocytes value (109/L)	Total leukocytes (109/L)
Erdem et al[13]	P	1	59	55.6 ± 44	35 (59)	26.91 ± 6	3.85 ± 0.383	4.30 ± 1.57a	1.27 ± 0.35a	6.35 ± 1.6a
Abe et al[14]	P	N/A	86	57.6 ± 11.5	58 (67.4)	22.0 ± 4.0	3.5 ± 0.5	4.1 ± 1.7a	1.1 ± 0.4a	6.0 ± 2a
Neuen et al[15]	R	5	170	54 ± 11	102 (60)	26 ± 1.5	3.4 ± 0.13a	5.1 ± 1.7a	1.7 ± 0.57a	7.7 ± 0.59
Ouellet et al[16]	R	2	5782	62.5 ± 15.2a	3180(55)a	N/A	3.72 ± 0.48a	64.5 ± 10.7a	22.22 ± 9.01a	7.26 ± 2.56a
Yaprak et al[17]	P	N/A	80	56.8 ± 18.1	32 (40)	N/A	3.64 ± 0.47	3.904 ± 1.543	1.44 ± 0.5	N/A
Sato et al[18]	R	2	78	63.4 ± 11.7	51 (65.4)	23.4 ± 3.9	3.2 ± 0.5	N/A	N/A	6.3 ± 2.18a
Li et al[19]	P	N/A	268	48.7 ± 10.9	149 (55)	N/A	3.63 ± 0.35	N/A	N/A	N/A
Xiang et al[20]	P	6	355	58.0 ± 14.9a	220 (62)	21.5 ± 3.30	4 ± 0.9a	4.0 ± 0.3a	1.2 ± 0.09a	5.89 ± 0.39a
Woziwodzka et al[21]	P	5	84	61.5 ± 4.38	50 (59.5)	25.1 ± 1.21	4.2 ± 0.11a	N/A	N/A	6.9 ± 0.48a
Balboul et al[22]	R	N/A	554	67.6 ± 14.2	66 (12)	26.7 ± 6.0	3.47 ± 0.6	4.8 ± 0.52	1.3 ± 0.14	7.0 ± 0.59
Kular et al[23]	R	N/A	224	65.8 ± 14.4a	133 (59)	N/A	3.36 ± 6.32	4.67 ± 2.99a	0.903 ± 0.49	6.16 ± 3.18a
Oguz et al[24]	P	N/A	123	61 ± 15.6a	75 (61)	N/A	3.47 ± 0.65a	4.8 ± 3.1a	0.99 ± 0.89	6.6 ± 4.6a
Zhang et al[25]	P	5.9	360	60 ± 3.17	201 (56)	N/A	4.05 ± 0.08	4.05 ± 0.34a	1.17 ± 0.112a	N/A
Lano et al[6]	P	2	183	65.5 ± 16.3a	106(58)a	N/A	3.78 ± 0.56	4.3 ± 1.8a	1.29 ± 0.58a	6.9 ± 5.0a
Wang et al[26]	R	3	185	56.3 ± 13.8a	88 (47.6)	N/A	3.878 ± 0.36a	N/A	N/A	N/A
Parmelia et al[27]	P	1	186	56.3 ± 11.1	110 (59)	N/A	N/A	3.9 ± 0.38a	1.3 ± 0.12a	6.2 ± 0.38
Wang et al[28]	R	4.83	240	63.4 ± 13.7	161 (67)	N/A	3.754 ± 0.42a	N/A	N/A	N/A
Zhang et al[29]	R	7	303	53.7 ± 13.17	184 (61)	N/A	4 ± 0.23	4.1 ± 1.1	1.3 ± 0.3a	N/A
He et al[30]	P	N/A	168	55.4 ± 15.1a	101 (60)	N/A	4.15 ± 0.55	4.51 ± 1.84	1.38 ± 0.56a	N/A

^aP < 0.05.

BMI: Body mass index; R: Retrospective; P: Prospective; N/A: Not applicable.

Table 2 Baseline characteristics of the study population from the included studies

Ref.	Total Platelets (109/L)	NLR	Hb (g/dL)	S Ferritin (ng/mL)	S Creatinine (mg/dL)	Smoking	HTN	Stroke	DM	CRP (mg/dL)
Erdem et al[13]	222 ± 64	3.51 ± 0.95a	11.15 ± 0.9	N/A	9.75 ± 2.5	N/A	N/A	N/A	N/A	N/A
Abe et al[14]	206 ± 59	3.72 ± 4.9a	8.8 ± 1.3	148.9 ± 180.8	10.2 ± 3.4	16 (18.6)	N/A	21 (24.4)	N/A	N/A
Neuen et al[15]	N/A	3 ± 0.28a	10.8 ± 1.5a	483 ± 98	N/A	32 (19)	N/A	6 (3.5)	117 (69)a	N/A
Ouellet et al[16]	N/A	3.84 ± 3.27a	N/A	N/A	N/A	N/A	N/A	231 (4)	3007(52)a	N/A
Yaprak et al[17]	174 ± 56	2.52 ± 0.91	10.6 ± 1.5	1015 ± 513	7.68 ± 2.46	N/A	N/A	N/A	N/A	1.36 ± 2.00
Sato et al[18]	202 ± 92a	4.09 ± 6.94a	8.9 ± 1.3	82.6 ± 119.9	10.1 ± 3.2	N/A	77 (98.7)	7 (9.0)	N/A	0.24 ± 1.41a
Li et al[19]	N/A	3.36 ± 1.65	11.49 ± 1.27	N/A	10.33 ± 1.9	71 (26.5)	N/A	N/A	49 (18.3)	N/A
Xiang et al[20]	N/A	3.22 ± 0.3a	10.68 ± 1.52	0.15 ± 0.05a	11.46 ± 3.19	85 (23.9)	262 (74)	N/A	66 (18.6)	N/A
Woziwodzka et al[21]	N/A	3 ± 0.37	N/A	N/A	5 ± 0.43	20 (23.8)	71 (84.5)	3 (3.6)	25 (29.8)	7.4 ± 3.26
Balboul et al[22]	182 ± 16.4	3.55 ± 0.6	10.4 ± 1.5	N/A	6.42 ± 2.4	N/A	N/A	N/A	61	1.19 ± 0.65
Kular et al[23]	N/A	6.9 ± 8.4a	10.5 ± 1.5	N/A	N/A	71 (32)a	182 (81)	49 (22)a	120 (54)	N/A
Oguz et al[24]	174 ± 78	6.49 ± 7.88a	9.87 ± 1.65	1024 ± 1206a	N/A	49 (40)	93 (76)	N/A	53 (43)a	74 ± 96.82a
Zhang et al[25]	171.5 ± 15.3a	3.42 ± 0.4a	11.2 ± 0.35a	N/A	N/A	N/A	N/A	N/A	N/A	64 ± 30.63
Lano et al[6]	199 ± 83a	4.01 ± 2.6a	10.7 ± 1.2	562 ± 462	N/A	104 (57)	159 (87)	N/A	73 (40)	N/A
Wang et al[26]	N/A	3.365 ± 0.98a	10.99 ± 1.8	N/A	N/A	N/A	N/A	N/A	N/A	N/A
Parmelia et al[27]	192.5 ± 12.27	3.2 ± 0.37a	10.3 ± 0.36	N/A	11.3 ± 3.3	N/A	146 (92)	N/A	31 (19.5)	N/A
Wang et al[28]	N/A	3.31 ± 1.36a	10.57 ± 1.85a	N/A	7.01 ± 2.86	N/A	N/A	N/A	N/A	N/A
Zhang et al[29]	172 ± 13.62a	3.22 ± 0.35a	10.6 ± 1.0	182 ± 71.64	11.3 ± 65.74	43 (14.19)	252 (83)	N/A	80 (26.4)	N/A
He et al[30]	198.03 ± 80.9a	3.63 ± 1.80a	10.4 ± 2.26	228.9 ± 350.9a	11.2 ± 3.8	N/A	23 (13.7)	N/A	44 (26.2)	N/A

^aP < 0.05.

Hb: Hemoglobin; NLR: Neutrophil-lymphocyte ratio; S: Serum; HTN: Hypertension; DM: Diabetes mellitus; CRP: C-reactive protein; N/A: Not available.

Table 3 Subgroup analysis of the included studies on the association of neutrophil-lymphocyte ratio with all-cause mortality

Variables	Number of studies	No. of patients	aHR (95%CI)	P value	I2
Study design
Prospective	5	786	1.63 (1.66-2.27)	0.004	67.1
Retrospective	6	7111	1.17 (1.07-1.29)	0.0008	87.7
Sample size
≥ 200	5	7131	1.11 (1.02-1.21)	0.016	81.6
< 200	6	766	1.35 (1.16-1.56)	< 0.0001	52
Age (years)
≥ 57	5	6722	1.07 (1.00-1.14)	0.048	72.2
< 57	6	1175	1.42 (1.21-1.67)	< 0.0001	57.4
Males%
≥ 60%	4	719	1.30 (1.16-1.46)	< 0.0001	45.5
< 60%	7	7178	1.14 (1.03-1.25)	0.008	79.2
Diabetes (%)
≥ 30	4	6730	1.14 (1.04-1.25)	0.008	91.2
< 30	5	1009	1.62 (1.20-2.19)	0.001	69.5
NLR
≥ 3.5	5	6806	1.08 (1.02-1.14)	0.01	71.8
2.5-3.5	6	1091	1.54 (1.33-1.78)	< 0.0001	14
Hemoglobin (g/dL)
≥ 10.5	5	1045	1.37 (1.06-1.76)	0.02	91
< 10.5	4	986	1.17 (1.00-1.36)	0.04	75.8
Creatinine (mg/dL)
≥ 7.7	5	1003	1.42 (1.16-1.73)	0.0006	60.7
< 7.7	3	718	1.43 (0.77-2.67)	0.26	64
Serum albumin (g/dL)
≥ 3.5	6	6685	1.53 (1.21-1.94)	0.0004	57.6
< 3.5	4	1026	1.13 (1.03-1.24)	0.007	90.6
Serum ferritin (ng/mL)
≥ 340	3	418	1.29 (1.11-1.49)	0.0008	56.4
< 340	2	381	1.34 (1.09-1.64)	0.004	< 0.0001

NLR: Neutrophil-lymphocyte ratio; HR: Hazard ratio.

Table 4 Meta-regression analysis of variables associated with all-cause mortality and cardiovascular mortality

Variables	Number of studies	Coefficient estimate	95%CI	P value
All-cause mortality
Age	11	-0.02	-0.03 to 0.01	< 0.0001
Males	11	0.005	-0.003 to 0.01	0.22
BMI	4	-0.05	-0.23 to 0.12	0.55
Hypertension	6	0.002	-0.005 to 0.01	0.5
Diabetes	9	-0.005	-0.01 to 0.0006	0.08
CRP	4	0.1	-0.03 to 0.23	0.13
Hemoglobin	9	0.08	-0.08 to 0.24	0.32
Serum creatinine	6	0.06	-0.02 to 0.13	0.17
Serum ferritin	5	0.0004	-0.0001 to 0.0009	0.12
Serum albumin	10	0.17	-0.13 to 0.47	0.26
Smoking	5	-0.02	-0.06 to 0.02	0.28
Cardiovascular mortality
Age	4	-0.02	-0.04 to 0.004	0.01
Males	4	0.005	0.003 to 0.008	< 0.0001
Diabetes	4	-0.004	-0.01 to 0.006	0.43
Hemoglobin	4	0.26	-0.04 to 0.56	0.09
Serum albumin	4	0.54	-0.75 to 1.83	0.41

BMI: Body mass index; CRP: C-reactive protein