Baseline moderate-range albuminuria is associated with protection against severe COVID-19 pneumonia

doi:10.4239/wjd.v13.i12.1154

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World Journal of Diabetes

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Baishideng Publishing Group Inc, 7041 Koll Center Parkway, Suite 160, Pleasanton, CA 94566, USA

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World J Diabetes. Dec 15, 2022; 13(12): 1154-1167
Published online Dec 15, 2022. doi: 10.4239/wjd.v13.i12.1154

Table 1 Clinical and demographic characteristics of patients with type 2 diabetes, with and without coronavirus disease 2019 infection

	Patients without COVID-19 infection, n = 144	Patients with COVID-19 infection, n = 65	P value
Age (yr), mean (SD)	63.9 (9.9)	59.8 (9.2)	0.005¹
Median (IQR)	65 (57-71)	61 (53-66)	0.005¹
Sex, female, n (%)	50 (34.7)	32 (49.2)	0.066²
Population group, n (%)			0.067²
Jews	63 (44.7)	20 (30.8)
Arabs	78 (55.3)	45 (69.2)
BMI (kg/m²), mean (SD)	30.7 (5.9)	32.1 (4.6)	0.09¹
Median (IQR)	30.3 (27.4-33.8)	31.6 (29.1-34.7)	0.09¹
Diabetes duration (yr), median (IQR)	13 (8-17.8)	10 (5.5-14.5)	0.031³
eGFR (mL/min/1.73 m² body surface area) at baseline, median (IQR)	85.4 (62.2-97.6)	91.9 (75.3-101.0)	0.033³
HbA1c (%), median (IQR)	7.6 (6.5-9.1)	7.4 (6.6-9.1)	1.00³
Metformin, n (%)	110 (76.9)	56 (86.2)	0.14²
DPP-4 inhibitors, n (%)	29 (20.1)	18 (27.7)	0.28²
Sulfonylurea, n (%)	8 (5.6)	7 (10.8)	0.25⁴
SGLT2 inhibitors, n (%)	36 (25.0)	18 (27.7)	0.73²
GLP-1 agonists, n (%)	25 (17.4)	12 (18.5)	1.00²
Basal insulin, n (%)	60 (41.7)	18 (27.7)	0.064²
Prandial insulin, n (%)	30 (21.0)	6 (9.2)	0.047²
Current smoking, n (%)	48 (33.3)	4 (6.2)	< 0.001²
No albuminuria, n (%)	65 (45.1)	45 (69.2)	0.002²
Albuminuria < 30 mg/g, n (%)	79 (54.9)	20 (30.8)	0.005³
Albuminuria 30-300 mg/g, n (%)	65 (45.1)	14 (21.5)
Albuminuria > 300 mg/g, n (%)	14 (9.7)	6 (9.2)
Retinopathy, n (%)	21 (21.4)	7 (15.2)	0.50²
NLR_max at hospitalization, median (IQR)	4.0 (2.5-7.8)	6.5 (2.6-10.0)	0.12³
CRP (mg/L) at admission, median (IQR)	9.7 (4.8-45.4)	71.8 (12.2-145.9)	< 0.001³
CRP_max (mg/L) at hospitalization, median (IQR)	11.3 (5.2-68.1)	86.6 (12.2-167.6)	< 0.001³
eGFR (mL/min/1.73 m² body surface area) at hospitalization, median (IQR)	86.0(62.2-96.0)	92.1(76.2-100.8)	0.030³
Albumin, median (IQR)	3.8 (3.4-4.0)	3.6(3.2-3.9)	0.026¹

¹Independent sample t-test.

²Chi-square test.

³Mann-Whitney test.

⁴Fisher’s exact test.

COVID-19: Coronavirus disease 2019; IQR: Interquartile range; BMI: Body mass index; HbA1c: Glycosylated hemoglobin; eGFR: Estimated glomerular filtration rate; DPP-4: Dipeptidyl-peptidase 4; SGLT2: Sodium/glucose cotransporter 2; GLP-1: Glucagon-like peptide 1; NLR_max: Maximum neutrophil:lymphocyte ratio; CRP: C-reactive protein; CRP_max: Maximum C-reactive protein.

Table 2 Clinical and demographic characteristics of patients type 2 diabetes and coronavirus disease 2019 infection, with and without albuminuria

	Diabetic patients without baseline albuminuria, n = 45	Diabetic patients with baseline albuminuria, n = 20	P value
Age (yr), mean (SD)	58.7 (9.2)	62.2 (9.0)	0.16¹
Median (IQR)	60.0 (50.5-65.0)	63.0 (56.5-68.8)	0.16¹
Sex, female, n (%)	21 (46.7)	11 (55.0)	0.60²
Population group, n (%)			0.77²
Jews	13 (28.9)	7 (35.0)
Arabs	32 (71.1)	13 (65.0)
BMI (kg/m²), mean (SD)	31.6 (4.5)	33.2 (4.6)	0.19¹
Median (IQR)	30.9 (28.6-33.7)	32.3 (29.7-35.9)	0.19¹
Diabetes duration (yr), median (IQR)	10.0 (5.5-14.0)	11.0 (5.3-17.0)	0.25¹
eGFR (mL/min/1.73 m² body surface area) at baseline, median (IQR)	90.5 (77.8-99.5)	95.3 (69.6-101.1)	0.90³
HbA1c (%), median (IQR)	7.2 (6.6-8.4)	8.9 (7.3-10.4)	0.02³
Metformin, n (%)	41 (91.1)	15 (75)	0.12⁴
DPP-4 inhibitors, n (%)	15 (33.3)	3 (15)	0.15²
Sulfonylurea, n (%)	5 (11.1)	2 (10)	1.00⁴
SGLT2 inhibitors, n (%)	15 (33.3)	3 (15)	0.15²
GLP-1 agonists, n (%)	8 (17.8)	4 (20)	1.00⁴
Basal insulin, n (%)	8 (17.8)	10 (50)	0.015²
Prandial insulin, n (%)	2 (4.4)	4 (20)	0.067⁴
Current smoking, n (%)	2 (4.4)	2 (10)	0.58⁴
Retinopathy, n (%)	4 (12.9)	3 (20)	0.67⁴
NLR_max, median (IQR)	6.2 (2.5-9.4)	6.7 (2.6-18.0)	0.48³
CRP (mg/L) at admission, median (IQR)	90.4 (10.9-153.6)	43.9 (12.5-106.8)	0.33³
CRP_max (mg/L) at hospitalization, median (IQR)	92.8 (11.4-171.3)	61.0 (12.5-157.3)	0.60³
eGFR (mL/min/1.73 m² body surface area) at hospitalization, median (IQR)	90.3 (77.0-98.4)	94.3 (67.8-101)	0.76³
Albumin, median (IQR)	3.6 (3.3-4.0)	3.6 (3.1-3.9)	0.25¹

¹Independent sample t-test.

²Chi-square test.

³Mann-Whitney test.

⁴Fisher’s exact test.

IQR: Interquartile range; BMI: Body mass index; HbA1c: Glycosylated hemoglobin; eGFR: Estimated glomerular filtration rate; DPP-4: Dipeptidyl-peptidase 4; SGLT2: Sodium/glucose cotransporter 2; GLP-1: Glucagon-like peptide 1; NLR_max: Maximum neutrophil:lymphocyte ratio; CRP: C-reactive protein; CRP_max: Maximum C-reactive protein.

Table 3 Clinical and demographic characteristics of patients with type 2 diabetes, with mild or moderate versus severe or critical coronavirus disease 2019 pneumonia

	Mild-moderate COVID-19 pneumonia, n = 34	Severe-critical COVID-19 pneumonia, n = 31	P value
Age (yr), mean (SD)	58.6 (10.0)	61.2 (8.1)	0.26¹
Median (IQR)	59.5 (50.8-65.3)	63 (57.0-67.0)	0.26¹
Sex, female, n (%)	20 (58.8)	12 (38.7)	0.14²
Population group, n (%)			1.00²
Jews	10 (29.4)	10 (32.3)
Arabs	24 (70.6)	21 (67.7)
BMI (kg/m²), mean (SD)	31.4 (3.8)	32.8 (5.2)	0.22¹
Median (IQR)	31.2 (28.9-33.6)	31.7 (29.3-36.1)	0.22¹
Diabetes duration (yr), median (IQR)	9.5 (4.8-12.5)	11 (7-17)	0.13³
eGFR (mL/min/1.73 m² body surface area) at baseline, median	90.4 (74.9-105.5)	93.3 (76.0-100.3)	0.78³
HbA1C (%), median (IQR)	7.4 (6.6-9.1)	7.4 (6.6-9.4)	0.93³
Metformin, n (%)	30 (88.2)	26 (83.9)	0.73⁴
DPP-4, n (%)	10 (29.4)	8 (25.8)	0.79²
Sulfonylurea, n (%)	5 (14.7)	2 (6.5)	0.43⁴
SGLT2 inhibitors, n (%)	11 (32.4)	7 (22.6)	0.42²
GLP-1 agonists, n (%)	5 (14.7)	7 (22.6)	0.53²
Basal insulin, n (%)	8 (23.5)	10 (32.3)	0.58²
Prandial insulin, n (%)	3 (8.8)	3 (9.7)	1.00⁴
Current smoking, n (%)	4 (11.8)	0 (0)	0.12⁴
No albuminuria, n (%)	21 (61.8)	24 (77.4)	0.19²
			2-sided
			0.14²
			1-sided
Albuminuria < 30 mg/g, n (%)	13 (38.2)	7 (22.6)	0.145³
Albuminuria < 30 mg/g, n (%)	13 (38.2)	7 (22.6)	2-sided
Albuminuria 30-300 mg/g, n (%)	8 (23.5)	6 (19.4)	0.073³
Albuminuria > 300 mg/g, n (%)	5 (14.7)	1 (3.2)	1-sided
Retinopathy, n (%)	4 (16.7)	3 (13.6)	1.00⁴
NLR_max median (IQR)	2.7 (1.7-8.5)	9.2 (5.7-15.4)	< 0.001³
CRP (mg/L) at admission, median (IQR)	15.4 (5.1-80.9)	122.1 (70.8-177.2)	< 0.001³
CRP_max (mg/L) at hospitalization, median (IQR)	15.4 (5.1-86.2)	142.3 (87.1-205.1)	< 0.001³
eGFR (mL/min/1.73 m² body surface area) at hospitalization, median (IQR)	91.2 (76.0-105.0)	93.3 (76.5-100.3)	0.90³
Albumin (g/dL), mean (SD)	3.8 (0.4)	3.3 (0.4)	< 0.001¹
Median (IQR)	3.9 (3.6-4.1)	3.3 (3.1-3.5)	< 0.001¹

¹Independent sample t-test.

²Chi-square test.

³Mann-Whitney test.

⁴Fisher’s exact test.

Table 4 Multivariable logistic regression analysis performed to determine the risk factors for severe coronavirus disease 2019 infection (n = 65)

		OR	95%CI	P value
Model 1	Sex (female vs male)	0.30	0.10-0.93	0.038
Baseline characteristics	Age (yr)	1.03	0.98-1.09	0.28
R-square: 14.4%	BMI (kg/m²)	1.12	0.99-1.28	0.073
Model 2	Sex (female vs male)	0.57	0.15-2.16	0.41
Baseline characteristics	Age (yr)	1.02	0.94-1.11	0.62
R-square: 34.4%	BMI (kg/m²)	1.14	0.96-1.35	0.13
	HbA1c (%)	0.85	0.59-1.23	0.39
	Baseline eGFR (mL/min/ 1.73 m² of body surface area)	1.02	0.98-1.07	0.28
	NLR_max	1.18	1.05-1.33	0.007
Model 3	Sex (female vs male)	0.42	0.09-1.94	0.27
Baseline characteristics	Age (yr)	1.08	0.97-1.20	0.18
R-square = 46.9%	BMI (kg/m²)	1.24	1.01-1.53	0.040
	HbA1c (%)	1.04	0.67-1.61	0.89
	Baseline eGFR (mL/min/1.73 m² of body surface area)	1.04	0.99-1.09	0.12
	NLR_max	1.20	1.06-1.37	0.005
	Albuminuria	0.09	0.01-0.62	0.015

OR: Odds ratio; CI: Confidence intervals; BMI: Body mass index; HbA1c: Glycosylated hemoglobin; eGFR: Estimated glomerular filtration rate; NLR_max: Maximum neutrophil:lymphocyte ratio; CRP: C-reactive protein; IQR: Interquartile range.

Table 5 Multivariable logistic regression analysis performed to determine the risk factors for bacterial infection (n = 144)

		OR	95%CI	P value
Model 1	Sex (female vs male)	1.88	0.70-5.05	0.21
Baseline characteristics	Age (yr)	0.98	0.93-1.02	0.34
R-square: 2.8%	BMI (kg/m²)	0.95	0.88-1.04	0.27
Model 2	Sex (female vs male)	7.23	1.57-33.23	0.011
Baseline characteristics	Age (yr)	1.00	0.92-1.09	0.97
R-square: 54.0%	BMI (kg/m²)	0.94	0.84-1.05	0.26
	HbA1c (%)	1.19	0.88-1.60	0.25
	Baseline eGFR (mL/min/1.73 m² of body surface area)	1.05	1.01-1.08	0.013
	NLR_max	1.36	1.21-1.54	< 0.001
Model 3	Sex (female vs male)	7.26	1.58-33.44	0.011
Baseline characteristics	BMI (kg/m²)	0.94	0.84-1.05	0.26
R-square: 54.0%	Age (yr)	1.00	0.92-1.09	0.98
	HbA1c (%)	1.19	0.87-1.61	0.28
	Baseline eGFR (mL/min/1.73 m² of body surface area)	1.05	1.01-1.08	0.012
	NLR_max	1.37	1.21-1.55	< 0.001
	Albuminuria	1.12	0.32-3.96	0.86

OR: Odds ratio; CI: Confidence intervals; BMI: Body mass index; HbA1c: Glycosylated hemoglobin; eGFR: Estimated glomerular filtration rate; NLR_max: Maximum neutrophil:lymphocyte ratio.

Citation: Bashkin A, Shehadeh M, Shbita L, Namoura K, Haiek R, Kuyantseva E, Boulos Y, Yakir O, Kruzel-Davila E. Baseline moderate-range albuminuria is associated with protection against severe COVID-19 pneumonia. World J Diabetes 2022; 13(12): 1154-1167
URL: https://www.wjgnet.com/1948-9358/full/v13/i12/1154.htm
DOI: https://dx.doi.org/10.4239/wjd.v13.i12.1154