Association of apolipoprotein E gene polymorphism with end-stage renal disease and hyperlipidemia in patients on long-term hemodialysis

Figures & data

Table 1. Distribution of apoE alleles and genotypes in ESRD patients on hemodialysis and controls.

	ESRD patients (n = 109)	Controls (n = 97)	p
e2	7 (0.03)	13 (0.06)
e3	107 (0.73)*	94 (0.82)	<0.001
e4	51 (0.24)*	22 (0.12)
E2/E2	0 (0)	0 (0)
E2/E3	5 (0.05)	10 (0.10)
E2/E4	2 (0.02)	3 (0.03)	<0.001
E3/E3	53 (0.48)*	65 (0.67)
E3/E4	49 (0.45)*	19 (0.20)
E4/E4	0 (0)	0 (0)

Notes: Values are expressed as number (frequency). Differences in genotype and allele distribution were tested by means chi-square test.

*Significant differences.

apoE: apolipoprotein E; e2, e3 and e4: apoE alleles; E2/E2, E2/E3, E2/E4, E3/E3, E3/E4 and E4/E4: apoE genotypes; and ESRD: end-stage renal disease.

Table 2. Disease association analyses according to apoE polymorphism in ESRD patients.

	Odds ratio (95% CI)	p*
e2	0.473 (0.181–1.235)	0.093
e3	Reference group
e4	0.491 (0.277–0.870)	0.009
E2/E3	0.613 (0.197–1.904)	0.285
E2/E4	0.818 (0.132–5.074)	0.600
E3/E3	Reference group
E3/E4	0.316 (0.166–0.601)	<0.001

Notes: Values are expressed as odds ratio (confidence interval).

*p (ESRD patients versus controls, e3 as reference allele and E3E3 as reference genotype).

apoE: apolipoprotein E; e2, e3 and e4: apoE alleles; E2/E3, E2/E4, E3/E3 and E3/E4: apoE genotypes; and ESRD: end-stage renal disease.

Table 3. Lipids, apolipoproteins, lipoprotein particles and inflammation in ESRD patients on hemodialysis according to the apoE alleles.

Parameters	e2 (n = 7)	e3 (n = 107)	e4 (n = 51)
Age (years)	46.58 ± 16.56	43.88 ± 14.80	48.21 ± 13.80
Hs-CRP (mg/L)	7.71 ± 11.22	5.76 ± 8.16	5.77 ± 5.91
TC (g/L)	1.75 ± 0.39**	1.51 ± 0.21	1.64 ± 0.34‡
TG (g/L)	1.46 ± 0.44	1.57 ± 0.40	1.60 ± 0.32
HDL-C (g/L)	0.44 ± 0.13	0.43 ± 0.09	0.41 ± 0.09†
LDL-C (g/L)	1.02 ± 0.28***	0.77 ± 0.18	0.91 ± 0.31§
LDL-p (g/L)	0.97 ± 0.29***	0.71 ± 0.18	0.85 ± 0.30‡
TC/HDL-C	4.16 ± 1.00*	3.65 ± 0.73	4.15 ± 1.04‡
LDL-C/HDL-C	2.43 ± 0.75**	1.87 ± 0.55	2.32 ± 0.87‡
ApoAI (g/L)	1.25 ± 0.34	1.17 ± 0.19	1.17 ± 0.23†
ApoB (g/L)	0.91 ± 0.25	0.79 ± 0.24	0.87 ± 0.25
ApoE (mg/L)	0.06 ± 0.02	0.05 ± 0.02	0.05 ± 0.03
ApoB/ApoAI	0.76 ± 0.24	0.69 ± 0.24	0.76 ± 0.22
LpAI (g/L)	0.46 ± 0.13	0.39 ± 0.17	0.37 ± 0.15†
LpAI:AII (g/L)	0.78 ± 0.35	0.78 ± 0.21	0.80 ± 0.25
Lp(a) (g/L)	0.18 ± 0.11	0.20 ± 0.12	0.21 ± 0.15
t-Hcy (µmol/L)	39.68 ± 11.62	41.78 ± 9.33	41.49 ± 8.27
PON activity (UI/mL)	89.96 ± 69.41	116.22 ± 82.13	124.48 ± 90.45

Notes: Values are expressed as means ± SD.

*p < 0.05, **p < 0.01 and ***p < 0.001 (e2 vs. e3 alleles), †p < 0.05 (e2 vs. e4 alleles), ‡p < 0.01 and §p < 0.001 (e3 vs. e4 alleles).

apo: apolipoproteins; e2, e3 and e4: apoE alleles; ESRD: end-stage renal disease; HDL-C: high density lipoprotein-cholesterol; Hs-CRP: high sensitivity C-reactive protein; LDL-C: low-density lipoprotein-cholesterol; LDL-p: pure LDL-cholesterol; Lp: lipoprotein particles; PON: paraoxonase; t-Hcy: total homocystein; and TG: triglycerides.

Table 4. Lipids, apolipoproteins, lipoprotein particles and inflammation in ESRD patients on hemodialysis according to the apoE genotypes.

Parameters	Apoe3 containing genotypes (E3/E3 + E2/E3) (n = 58)	Apoe4-containing genotypes (E3/E4 + E2/E4) (n = 51)
Age (years)	44.28 ± 14.83	48.14 ± 14.14
Hs-CRP (mg/L)	6.76 ± 9.01	5.10 ± 5.57
TC (g/L)	1.53 ± 0.23	1.67 ± 0.35**
TG (g/L)	1.53 ± 0.39	1.62 ± 0.34
HDL-C (g/L)	0.43 ± 0.09	0.41 ± 0.09
LDL-C (g/L)	0.80 ± 0.20	0.94 ± 0.31**
LDL-p (g/L)	0.73 ± 0.19	0.88 ± 0.31**
TC/HDL-C	3.70 ± 0.75	4.18 ± 1.06**
LDL-C/HDL-C	1.93 ± 0.57	2.36 ± 0.88**
ApoAI (g/L)	1.15 ± 0.21	1.20 ± 0.24
ApoB (g/L)	0.79 ± 0.24	0.90 ± 0.25*
ApoE (mg/L)	0.05 ± 0.02	0.05 ± 0.03
ApoB/ApoAI	0.70 ± 0.23	0.76 ± 0.23
LpAI (g/L)	0.39 ± 0.17	0.39 ± 0.15
LpAI:AII (g/L)	0.76 ± 0.24	0.82 ± 0.24
Lp(a) (g/L)	0.22 ± 0.14	0.19 ± 0.12
t-Hcy (µmol/L)	41.35 ± 9.06	41.49 ± 9.22
PON activity (UI/mL)	111.03 ± 78.94	123.71 ± 90.91

Notes: Values are expressed as means ± SD.

*p < 0.05 and **p < 0.01.

Apoe4-containing genotypes include E3/E4 and E2/E4 and apoe3 containing genotypes include E3/E3 and E2/E3.

apo: apolipoproteins; ESRD: end-stage renal diseases; HDL-C: high-density lipoprotein-cholesterol; Hs-CRP: high-sensitivity C-reactive protein; LDL-C: low-density lipoprotein cholesterol; LDL-p: pure LDL-cholesterol; Lp: lipoprotein particles; PON: paraoxonase; t-Hcy: total homocystein; and TG: triglycerides.

Table 5. ApoE allele frequencies in Moroccan healthy subjects.

Studies	N	e2 (%)	e3 (%)	e4 (%)
Our study (MHS)	97	6.7	82	11
Valveny et al. (MHS)24	660*	4.0	86	10
Kacemi et al. (MHS)25	168	5.0	84	11
Bennouar et al. (MHS)26	141	7.0	80	13

Notes: e2, e3 and e4: apoE alleles; MHS: Moroccan healthy subjects; and N: number of patients. *Number included other populations.

Table 6. ApoE allele frequencies in Morrocan healthy subjects and Arab populations.

Studies	N	e2 (%)	e3 (%)	e4 (%)
Our study (MHS)	97	6.7	82.0	11.0
Al-Muhanna et al. (AHD)27	42	6.0	87.0	7.0
Al-Yahyaee et al. (AHS)28	162	5.2	88.6	6.2
Al-Shammari et al. (AHS)29	106	5.7	85.4	9.0

Notes: e2, e3 and e4: apoE alleles; AHD: Arab hemodialysis patients; AHS: Arab healthy subjects; MHS: Moroccan healthy subjects; and N: number of patients.

Table 7. ApoE allele frequencies in ESRD patients, Arab and no-Arab ESRD populations.

Studies	N	e2 (%)	e3 (%)	e4 (%)
Our study (HD)	109	3.2	73.4	23.4
Al-Muhanna et al. (AHD)27	42	6.0	87.0	7.0
Liberopoulos et al. (NAHD)13	301	6.8	85.7	7.5
Zahálková et al. (NAHD)30	87	8.1	83.8	8.1
Oda et al. (NAHD)31	485	5.8	85.1	9.1

Notes: e2, e3 and e4: apoE alleles; AHD: Arab hemodialysis patients; HD: hemodialysis patients; NAHD: no-Arab hemodialysis patients; and N: number of patients.

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