Relationship Between the Hemoglobin, Albumin, Lymphocyte Count, Platelet Count (HALP) Score and Type 2 Diabetes Retinopathy

Figures & data

Table 1 Comparison of General Data and Laboratory-Related Indicators in All Patients

Variable	NDR (N=388)	DR (N=286)	Statistics	P value
Gender (male)	233 (60.1%)	163 (60.0%)	0.636	0.425
Age (years)	56 (45, 64)	60 (52, 67)	−4.290	<0.001
Course of disease (years)	6(1, 10.5)	12 (7,20)	−8.925	<0.001
History of smoking (yes)	131 (33.8%)	72 (25.2%)	5.769	0.016
History of drinking (yes)	119 (30.6%)	72 (25.2%)	2.448	0.118
SBP (mmHg)	131.27±17.28	136.61± 19.83	−3.728	<0.001
DBP (mmHg)	82.11± 10.73	80 (73,88)	−1.381	0.167
BMI (Kg/m^2)	26.27 (23.99, 28.56)	25.6 (23.38, 28.27)	−1.961	0.050
HGB (10^9/L)	144.37±14.9	140.13±16.12	3.521	<0.001
LYM (10^9/L)	1.91 (1.55, 2.37)	1.71 (1.39, 2.17)	−4.231	<0.001
PLT (10^9/L)	220 (189, 259)	221.5 (190, 267)	−0.321	0.749
HbA1c (%)	8.8 (7.25, 10.65)	8.9 (8, 10.2)	−0.993	0.321
FBG (mmol/L)	8.13 (6.26, 10.92)	8.46 (6.14, 10.97)	−0.261	0.794
ALT (U/L)	20.95 (14.3, 28.1)	17.5 (13.2, 24.3)	−3.449	0.001
AST (U/L)	19.9 (16.35, 24.15)	18.95 (15.9, 24.3)	−1.227	0.220
ALB (g/L)	41.9 (39.5, 44.4)	40.7 (38.3, 43.4)	−4.537	<0.001
Cr (umol/L)	63.15 (54.5, 71.95)	63.7 (56.4, 74.7)	−1.300	0.193
UA (umol/L)	308.4 (263.4, 369.95)	287.2 (242.2, 344.9)	−3.203	0.001
BUN (mmol/L)	5.1 (4.25, 6.1)	5.35 (4.6, 6.5)	−3.589	<0.001
eGFR (mL/min)	102 (93.89, 111.55)	97.3 (90.19, 107.23)	−4.069	<0.001
TC (mmol/L)	4.68 (3.86, 5.47)	4.46 (3.69, 5.39)	−1.463	0.143
TG (mmol/L)	1.53 (1.07,2.25)	1.17 (0.86,1.73)	−4.971	<0.001
HDL-C (mmol/L)	1.03 (0.89, 1.23)	1.11 (0.95, 1.32)	−3.567	<0.001
LDL-C (mmol/L)	3.06 (2.45, 3.61)	2.93 (2.29, 3.6)	−1.577	0.115
HALP score	50.32 (40.85, 66.33)	43.83 (33.39, 56.84)	−5.472	<0.001

Abbreviations: DR, diabetic retinopathy; NDR, non-diabetic retinopathy; SBP, systolic blood pressure; DBP, diastolic blood pressure; BMI, body mass index; HbA1c, glycated hemoglobin; FBG, fasting blood glucose; ALB, albumin; AST, aspartate aminotransferase; ALT, alanine transaminase; HGB, hemoglobin; LYM, lymphocyte count; PLT, platelet count; Cr, blood creatinine; UA, blood uric acid; BUN, blood urea nitrogen; eGFR, Glomerular filtration rate; TC, total cholesterol; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 1 Comparison of HALP score in two groups of all patients.

Note: ***Denotes significance at a P value of <0.001.

Abbreviations: DR, diabetic retinopathy; NDR, non-diabetic retinopathy; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Table 2 Comparison of General Data and Laboratory-Related Indicators in Male Patients

Variable	NDR (N=233)	DR (N=163)	Statistics	P value
Age (years)	54 (43, 62)	60 (51.5, 67)	−4.303	<0.001
Course of disease (years)	6 (1, 10)	12 (8,20)	−8.021	<0.001
History of smoking (yes)	95 (40.8%)	50 (30.7%)	4.213	0.04
History of drinking (yes)	85 (36.5%)	49 (30.1%)	1.765	0.184
SBP (mmHg)	130.11±16.53	133 (120, 148)	−2.469	0.014
DBP (mmHg)	82.29± 10.68	81.16±10.94	1.028	0.305
BMI (Kg/m^2)	26.4 (24.22, 28.38)	25.41 (23.33, 27.79)	−2.238	0.025
HGB (10^9/L)	149 (140, 156)	143.18±15.47	−3.278	0.001
LYM (10^9/L)	1.84 (1.48, 2.31)	1.73±0.55	−2.978	0.003
PLT (10^9/L)	214 (187, 245)	216 (184.5, 260.5)	−0.245	0.807
HbA1c (%)	8.7 (7.1, 10.6)	9.1 (8,10.45)	−1.515	0.130
FBG (mmol/L)	7.99 (6.2, 11.2)	8.28 (6.03, 10.95)	−0.525	0.599
ALT (U/L)	21.7 (14.7, 29)	17.7 (13.35, 24.25)	−3.297	0.001
AST (U/L)	19.6 (16.5, 23.4)	19 (15.95, 23.2)	−1.020	0.308
ALB (g/L)	42.1 (39.9, 44.5)	40.56±3.92	−4.308	<0.001
Cr (umol/L)	65.7 (59.3, 74.4)	67.5 (60, 77.6)	−0.888	0.375
UA (umol/L)	322.4 (270.8, 384.6)	286.2 (247.55, 344.35)	−3.560	<0.001
BUN (mmol/L)	5.2 (4.4, 6.2)	5.5 (4.7, 6.9)	−2.740	0.006
eGFR (mL/min)	103.76 (94.55, 113.77)	98.31 (90.05, 107.33)	−4.123	<0.001
TC (mmol/L)	4.58 (3.8, 5.29)	4.3 (3.62, 5.145)	−1.585	0.113
TG (mmol/L)	1.41 (1.04,2.12)	1.08 (0.81,1.54)	−4.929	<0.001
HDL-C (mmol/L)	1.01 (0.87, 1.19)	1.09 (0.94, 1.24)	−3.043	0.002
LDL-C (mmol/L)	2.97±0.88	2.81 (2.24, 3.4)	−1.510	0.131
HALP score	51.21 (42.51, 67)	43.93 (35.37, 56.13)	−4.638	<0.001

Abbreviations: DR, diabetic retinopathy; NDR, non-diabetic retinopathy; SBP, systolic blood pressure; DBP, diastolic blood pressure; BMI, body mass index; HbA1c, glycated hemoglobin; FBG, fasting blood glucose; ALB, albumin; AST, aspartate aminotransferase; ALT, alanine transaminase; HGB, hemoglobin; LYM, lymphocyte count; PLT, platelet count; Cr, blood creatinine; UA, blood uric acid; BUN, blood urea nitrogen; eGFR, Glomerular filtration rate; TC, total cholesterol; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 2 Comparison of HALP score in two groups of male patients.

Note: ***Denotes significance at a P value of <0.001.

Abbreviations: DR, diabetic retinopathy; NDR, non-diabetic retinopathy; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Table 3 Comparison of General Data and Laboratory-Related Indicators in Female Patients

Variable	NDR (N=155)	DR (N=123)	Statistics	P value
Age (years)	59 (50.5, 66.5)	60 (52, 66.5)	−0.682	0.495
Course of disease (years)	5 (1, 13)	12 (6, 19.5)	−4.344	<0.001
History of smoking (yes)	36 (23.2%)	22 (17.9%)	1.184	0.276
History of drinking (yes)	34 (21.9%)	23 (18.7%)	0.441	0.507
SBP (mmHg)	133±18.26	138.53±19.34	−2.442	0.015
DBP (mmHg)	81.83± 10.83	80 (73, 90)	−0.662	0.508
BMI (Kg/m^2)	26.25 (23.72, 28.92)	25.76 (23.42, 29.1)	−0.483	0.629
HGB (10^9/L)	137 (129, 147)	136.1±16.14	−1.041	0.298
LYM (10^9/L)	2.04 (1.7, 2.39)	1.73 (1.48, 2.34)	−3.276	0.001
PLT (10^9/L)	233 (197, 271)	232 (201, 269)	−0.094	0.925
HbA1c (%)	8.9 (7.35, 10.7)	8.7 (7.95, 9.9)	−0.321	0.748
FBG (mmol/L)	8.19 (6.35, 10.45)	8.6 (6.78, 10.97)	−0.898	0.369
ALT (U/L)	18.8 (14.1, 27.3)	17.4 (13.2, 24.2)	−1.358	0.175
AST (U/L)	20 (16, 25.1)	18.9 (15.8, 25.45)	−0.715	0.475
ALB (g/L)	41.76±3.84	40.9 (38.65, 43.35)	−1.857	0.063
Cr (umol/L)	55.7 (51.1, 66.4)	59.3 (52.35, 69.65)	−1.457	0.145
UA (umol/L)	289 (248.35, 344.1)	291.6 (235.45, 343.8)	−0.664	0.507
BUN (mmol/L)	4.9 (4.1, 5.8)	5.2 (4.55, 6.3)	−2.477	0.013
eGFR (mL/min)	99.07 (92.6, 106.64)	97.41±14.45	−1.437	0.151
TC (mmol/L)	4.83 (3.99, 5.75)	4.87±1.29	−0.556	0.578
TG (mmol/L)	1.76 (1.14,2.34)	1.33 (1.04, 2.07)	−2.160	0.031
HDL-C (mmol/L)	1.05 (0.94, 1.25)	1.13 (0.96, 1.36)	−1.863	0.062
LDL-C (mmol/L)	3.24±0.95	3.13±0.97	1.022	0.308
HALP score	49.38 (38.6, 61.33)	43.69 (32.14, 57.46)	−2.951	0.003

Abbreviations: DR, diabetic retinopathy; NDR, non-diabetic retinopathy; SBP, systolic blood pressure; DBP, diastolic blood pressure; BMI, body mass index; HbA1c, glycated hemoglobin; FBG, fasting blood glucose; ALB, albumin; AST, aspartate aminotransferase; ALT, alanine transaminase; HGB, hemoglobin; LYM, lymphocyte count; PLT, platelet count; Cr, blood creatinine; UA, blood uric acid; BUN, blood urea nitrogen; eGFR, Glomerular filtration rate; TC, total cholesterol; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 3 Comparison of HALP score in two groups of female patients.

Note: **Denotes significance at a P value of <0.01.

Abbreviations: DR, diabetic retinopathy; NDR, non-diabetic retinopathy; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Table 4 Trend Test of HALP Score and DR in T2DM Patients

Mantel-Haenszel Chi-square Trend Test
	Groups	A	B	C	D	Linear trend	Pearson related
All patients	DR	57.1%	42.0%	36.7%	33.9%	X^2=22.153 P<0.001	R=−0.169 P<0.001
Male patients	DR	57.6%	39.4%	37.4%	30.3%	X^2=16.547 P=0.001	R=−0.190 P<0.001
Female patients	DR	56.5%	44.3%	35.7%	40.6%	X^2=6.657 P=0.084	R=−0.127 P=0.035

Abbreviation: DR, diabetic retinopathy.

Table 5 Multi-Factor Regression Analysis of DR in All T2DM Patients

	B	SE	Wals	P	OR	95% (CI)
HALP score	−0.017	0.005	10.987	0.001	0.983	0.974–0.993
Age	−0.018	0.012	2.207	0.137	0.983	0.960–1.006
Course of disease	0.083	0.013	39.056	<0.001	1.087	1.059–1.116
History of smoking	0.266	0.194	1.876	0.171	1.304	0.892–1.907
SBP	0.018	0.005	13.677	<0.001	1.018	1.009–1.028
BUN	0.204	0.062	11.019	0.001	1.227	1.087–1.384
HDL-C	0.528	0.352	2.255	0.133	1.696	0.851–3.379
ALT	−0.005	0.007	0.382	0.536	0.996	0.981–1.010
UA	−0.002	0.001	3.821	0.051	0.998	0.995–1.020
eGFR	0.002	0.009	0.061	0.804	1.002	0.985–1.020
TG	−0.056	0.064	0.770	0.380	0.946	0.835–1.071

Abbreviations: SBP, systolic blood pressure; ALT, alanine transaminase; UA, blood uric acid; BUN, blood urea nitrogen; eGFR, Glomerular filtration rate; HDL-C, high-density lipoprotein cholesterol; TG, triglycerides; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Table 6 Multi-Factor Regression Analysis of DR in Male Patients

	B	SE	Wals	P	OR	95% (CI)
HALP score	−0.014	0.007	4.218	0.040	0.986	0.974–0.999
Age	−0.016	0.016	0.978	0.323	0.984	0.954–1.016
Course of disease	0.111	0.020	32.288	<0.001	1.117	1.075–1.161
SBP	0.018	0.007	6.978	0.008	1.019	1.005–1.033
BUN	0.200	0.085	5.569	0.018	1.221	1.034–1.442
HDL-C	0.645	0.511	1.593	0.207	1.906	0.700–5.189
History of smoking	0.260	0.250	1.081	0.299	1.297	0.795–2.115
BMI	0.004	0.038	0.013	0.910	1.004	0.932–1.082
ALT	−0.006	0.009	0.436	0.509	0.994	0.976–1.012
SUA	−0.003	0.002	3.701	0.054	0.997	0.994–1.000
eGFR	0.002	0.012	0.018	0.893	1.002	0.978–1.026
TG	−0.213	0.127	2.846	0.092	0.808	0.630–1.035

Abbreviations: SBP, systolic blood pressure; ALT, alanine transaminase; UA, blood uric acid; BUN, blood urea nitrogen; eGFR, Glomerular filtration rate; HDL-C, high-density lipoprotein cholesterol; BMI, body mass index; TG, triglycerides; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Table 7 Multi-Factor Regression Analysis of DR in Female Patients

	B	SE	Wals	P	OR	95% (CI)
HALP score	−0.021	0.008	7.045	0.008	0.980	0.965–0.995
Course of disease	0.044	0.016	7.676	0.006	1.045	1.013–1.078
SBP	0.014	0.007	3.980	0.046	1.014	1.000–1.028
BUN	0.195	0.091	4.614	0.032	1.216	1.017–1.453
TG	0.051	0.085	0.356	0.550	1.052	0.891–1.243

Abbreviations: SBP, systolic blood pressure; BUN, blood urea nitrogen; TG, triglycerides; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 4 The nonlinear relationship between HALP score and DR in all patients.

Abbreviations: DR, diabetic retinopathy; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 5 The nonlinear relationship between HALP score and DR in male patients.

Abbreviations: DR, diabetic retinopathy; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 6 The nonlinear relationship between HALP score and DR in female patients.

Abbreviations: DR, diabetic retinopathy; HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Table 8 Diagnostic Value of HALP Score and Combined Diagnostic Mode for DR in T2DM Patients

	Variable	AUC	95% (CI)	P-value	Cutoff	Sensitivity (%)	Specificity (%)
All patients	HALP score	0.623	0.580–0.666	P<0.001	45.83	55.6%	63.4%
	Diagnostic model	0.730	0.692–0.786	P<0.001	−0.5251	73.4%	61.1%
Male patients	HALP score	0.637	0.582–0.692	P<0.001	45.08	52.8%	69.5%
	Diagnostic model	0.761	0.713–0.808	P<0.001	−0.0066	58.3%	80.3%
Female patients	HALP score	0.603	0.536–0.671	P=0.003	41.86	48.8%	68.4%
	Diagnostic model	0.684	0.621–0.746	P<0.001	−0.1734	65%	67.7%

Abbreviations: HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 7 Diagnostic value of HALP score and combined diagnostic model for DR in all patients.

Abbreviations: HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 8 Diagnostic value of HALP score and combined diagnostic model for DR in male patients.

Abbreviations: HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.

Figure 9 Diagnostic value of HALP score and combined diagnostic model for DR in female patients.

Abbreviations: HALP score, hemoglobin, albumin, lymphocyte count, platelet count score.