NGAL (Neutrophil Gelatinase-Associated Lipocalin) as an early biomarker of nephropathy in patients with type 2 diabetes

Figures & data

Table 1. Demographics features and anthropometric measures of the study groups.

	Group A (n = 100)		Group B (n = 100)		Group C (n = 100)		Test of Sig.			p
	No.	%	No.	%	No.	%
Sex
Male	21	21.0	11	11.0	23	23.0	χ^2= 5.521			0.063
Female	79	79.0	89	89.0	77	77.0
Age (years)
Min.–Max.	32.0–70.0		38.0–70.0		44.0–70.0		F= 21.404*			<0.001*
Mean ± SD.	50.20 ± 10.65		54.34 ± 8.76		58.72 ± 8.02
Median (IQR)	50.0(44.0–58.5)		54.5(49.0–60.0)		58.0(52.0–65.0)
Sig. bet. groups.	p1 = 0.005*, p2 <0.001*, p3 = 0.003*
Anthropometric measurement	Group A (n = 100)		Group B (n = 100)		Group C (n = 100)			F	p
Weight (kg)
Min.–Max.	52.0–138.0		61.0–111.0		47.0–131.0			7.625*	0.001*
Mean ± SD.	82.75 ± 14.67		86.63 ± 12.30		90.39 ± 14.41
Median (IQR)	84.0 (73.0–90.50)		88.0 (77.0–96.0)		90.0 (83.50–97.0)
Sig. bet. groups.	p1 = 0.118, p2 <0.001*, p3=.134
WC (cm)								30.958*	<0.001*
Min.–Max.	72.0–136.0		77.0–130.0		72.0–134.0
Mean ± SD.	96.46 ± 14.37		103.74 ± 13.21		111.30 ± 12.35
Median (IQR)	96.50 (85.0–106.5)		105.5 (94.0–114.0)		112.0(104.0–120.0)
Sig. bet. groups.	p1 <0.001*, p2 <0.001*, p3 <0.001*
BMI (kg/m2)								20.079*	<0.001*
Min.–Max.	21.26–44.55		23.24–43.36		20.08–46.65
Mean ± SD.	29.51 ± 4.64		32.16 ± 4.56		33.72 ± 5.04
Median (IQR)	28.89 (26.59–32.27)		32.15 (28.93–35.72)		33.03 (31.56–36.72)
Sig. bet. groups.	p1 <0.001*, p2 <0.001*, p3 = 0.055

p: P-value for comparing between the studied groups.

p1: P-value for comparing between Group A and Group B.

p2: P-value for comparing between Group A and Group C.

p3: P-value for comparing between Group B and Group C.

*:Statistically significant at p ≤ 0.05.

Table 2. Comparing between the study groups as regard Glycemic parameters, lipid profile, serum creatinine and GFR.

Glycemic parameter	Group-A (100)	Group-B (100)			Group-C (100)	F		p
FPG (mg/dl)
Min.–Max.	82.0–387.0	75.0–315.0			78.0–345.0	11.628*		<0.001*
Mean± SD.	139.72 ± 53.62	157.72 ± 48.24			176.75 ± 60.37
Median (IQR)	125.0 (109.0–150.5)	145.50 (128.0–176.5)			174.0 (123.0–234.0)
Sig. bet. groups.	p1 = 0.051,p2 <0.001*,p3 = 0.037*
HbA1c (%)
Min.–Max.	4.83–13.30	5.90–12.90			5.53–14.40	33.637*		<0.001*
Mean± SD.	7.29 ± 1.69	8.38 ± 1.48			9.12 ± 1.60
Median (IQR)	6.80(6.40–7.65)	8.10(7.40–8.60)			9.20(7.95–10.05)
Sig. bet. groups.	p1 <0.001*,p2 <0.001*,p3 = 0.003*
Lipid profile
Total cholesterol (mg/dl)
Min.–Max.	133.0–295.0		127.0–310.0	118.0–387.0		40.371*	<0.001*
Mean± SD.	181.80 ± 29.28		196.36 ± 27.77	229.93 ± 53.84
Median (IQR)	179.50 (165.0–190.0)		198.0 (183.5–210.0)	224.0 (191.5–266.0)
Sig. bet. groups.	p1 = 0.023*,p2 <0.001*,p3 <0.001*
Triglycerides (mg/dl)
Min.–Max.	74.0–235.0		77.0–596.0	65.70–354.0		18.746*	<0.001*
Mean± SD.	134.24 ± 33.19		151.19 ± 57.38	176.48 ± 53.25
Median (IQR)	134.0 (113.0–147.5)		144.0 (124.0–171.5)	165.0 (146.0–198.5)
Sig. bet. groups.	p1 = 0.040*,p2 <0.001*,p3 = 0.001*
LDL (mg/dl)
Min.–Max.	50.0–196.0		54.0–180.50	46.0–313.0		50.602*	<0.001*
Mean± SD.	99.64 ± 28.79		121.44 ± 22.53	149.59 ± 48.80
Median (IQR)	93.0 (81.50–104.5)		124.0 (112.1–135.0)	147.5 (114.0–180.0)
Sig. bet. groups.	p1 <0.001*,p2 <0.001*,p3 <0.001*
HDL (mg/dl)
Min.–Max.	24.0–69.0		30.0–91.10	22.0–71.0		40.606*	<0.001*
Mean±SD.	54.43 ± 10.30		43.85 ± 7.83	44.44 ± 9.68
Median (IQR)	56.50 (47.50–63.0)		42.0 (39.50–46.0)	41.0 (38.0–51.50)
Sig. bet. groups.	p1 <0.001*,p2 <0.001*,p3 = 0.894
Serum Creatinine
Min.–Max.	0.59–1.40		0.70–2.53	0.70–5.90		149.601*	<0.001*
Mean± SD.	0.93 ± 0.18		1.13 ± 0.28	2.10 ± 1.12
Median (IQR)	0.90(0.80–1.01)		1.10 (1.0–1.20)	1.70 (1.40–2.50)
Sig. bet. groups.	p1 <0.001*,p2 <0.001*,p3 <0.001*
GFR
Min.–Max.	38.0–113.80		20.10–109.90	6.90–101.0		159.820*	<0.001*
Mean± SD.	78.65 ± 17.74		59.99 ± 14.53	35.51 ± 18.84
Median (IQR)	82.65 (64.90–91.50)		57.70 (51.40–70.25)	32.80 (22.30–43.10)
Sig. bet. groups.	p1 <0.001*,p2 <0.001*,p3 <0.001*

p: P-value for comparing between the studied groups.

p1: P-value for comparing between Group A and Group B.

p2: P-value for comparing between Group A and Group C.

p3: P-value for comparing between Group B and Group C.

*:Statistically significant at p ≤ 0.05.

Table 3. Comparing among the study groups regarding serum NGAL and urinary NGAL.

	Group A (n = 100)	Group B (n = 100)	Group C (n = 100)	F	p
Serum NGAL
Min.–Max.	7.79–14.22	6.93–15.32	9.15–38.81	232.767*	<0.001*
Mean± SD.	10.17 ± 1.72	10.76 ± 2.0	19.07 ± 5.0
Median (IQR)	9.66 (8.71–11.13)	10.48 (9.20–12.18)	19.39 (16.36–21.12)
Sig. bet. groups.	p1 = 0.404,p2 <0.001*,p3 <0.001*
Urinary NGAL
Min.–Max.	9.34–20.52	9.88–23.78	11.68–25.28	33.633*	<0.001*
Mean± SD.	14.86 ± 2.54	15.98 ± 3.33	18.33 ± 3.24
Median (IQR)	14.62 (13.55–16.61)	15.47 (13.55–17.98)	17.44 (16.22–20.48)
Sig. bet. groups.	p1 = 0.027*, p2 <0.001*, p3 <0.001*

2: Chi- square testing.

F: F for ANOVA testing, pairwise comparing bet. Every 2 groups were by Post Hoc Testing (Tukey).

p: between the studied groups.

p1: Groups A and B.

p2: Groups A and C.

p3: Groups B and C.

*:Statistically significant at p ≤ 0.05.

Group A:Normoalbuminuria, equivalent to urine ACR <30 mg/g.

Group B:Moderately elevated albuminuria, equivalent to ACR 30–300 mg/g.

Group C:Severely elevated albuminuria, equivalent to ACR >300 mg/g to <2500 mg/g.

Figure 1. ROC curve for Serum NGAL (ng/ml) and urinary NGAL (ng/ml) to discriminate between moderately/severely albuminuria (group B + C) (n = 200) from normoalbuminuria (group A) (n = 100).

Table 4. Univariate and multi-variate logistic regression analyses for the factors impacting moderately/severely albuminuria (group B+ C) (n = 200).

	Univariate		^#Multivariate
	p	OR (95%C.I)	p	OR (95%C.I)
Female	0.399	1.298 (0.708–2.380)
Age (years)	<0.001*	1.073 (1.044–1.102)	0.731	1.007 (0.966–1.051)
WC (cm)	<0.001*	1.058 (1.038–1.079)	0.249	1.045 (0.970–1.126)
BMI (kg/m^2)	<0.001*	1.167 (1.102–1.235)	0.647	0.948 (0.754–1.192)
HbA1c (%)	<0.001*	1.930 (1.572–2.369)	0.003*	1.453 (1.136–1.858)
Triglycerides (mg/dl)	<0.001*	1.018 (1.011–1.026)	0.809	0.999 (0.989–1.009)
LDL (mg/dl)	<0.001*	1.036 (1.025–1.046)	0.132	1.011 (0.997–1.024)
HDL (mg/dl)	<0.001*	0.898 (0.872–0.924)	<0.001*	0.922 (0.889–0.957)
GFR (mL/min/1.73 m^2)	<0.001*	0.925 (0.909–0.942)	0.001*	0.936 (0.901–0.973)
Serum NGAL (ng/ml)	<0.001*	1.445 (1.295–1.613)	0.031*	1.213 (1.018–1.446)
Urinary NGAL (ng/ml)	<0.001*	1.274 (1.164–1.394)	0.782	1.021 (0.882–1.182)
Fundus examination
No DR		1.000		1.000
NPDR	<0.001*	11.831(6.154–22.743)	0.982	1.014 (0.306–3.366)
PDR	0.997	–	0.998	–

#: All parameters with P-value <0.05 was comprised in the multi-variate.

*: Statistical significance at p ≤ 0.05.

$: for each 0.1 sCr.