The risk factors for cardiovascular disease and chronic kidney disease in patients with nonalcoholic fatty liver disease in Saudi Arabia

Walaa Mohammedsaeed; Abdullah Al Malki; Salma Alsayed

doi:10.15537/smj.2025.46.5.20240901

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Table 1

- Clinical and biochemical characteristics of patients with and without non-alcoholic fatty liver disease (N=1500).

Parameters	Without NAFLD (n=765)	With NAFLD (n=735)	P-values
Age (years)	34.54±11.23	55.55±12.21	0.001^**
Gender (male/female)	375/390	355/380	-
FBG (mmol/L)	4.9±1.31	6.5±1.41	0.001^**
HbA1c (%)	4.69±1.29	5.7±1.11	<0.001^**
LDL-C (mmol/L)	2.22±0.31	2.22±0.40	>0.05
HDL-C (mmol/L)	1.55±0.82	1.11±0.21	<0.001^**
Total cholesterol (mmol/L)	4.78±1.23	5.88±1.41	<0.001^**
Triglycerides (mmol/L)	1.2±1.13	2.5±1.10	0.001^**
AIP = log (TG/HDL-C).	0.11±0.10	0.3±0.11^*	0.002^**
BMI (kg/m²)	24.5±5.55	26.5±6.55^†	<0.001^**
hs-CRP(mg/l)	2.5±1.32	3.9±1.16	0.001^**
Albumin (g/dL)	5.9±1.99	3.0±0.3	0.002^**
Total protein (g/dL)	7.5±1.87	5.3±1.2	<0.001^**
AST (IU/L)	15.4±5.55	44.11±10.24	0.002^**
ALT(IU/L)	20.3±10.26	55.12±12.14	<0.001^**
ALP (IU/L)	55.5±11.12	77±10.16	0.001^**
AST: ALT ratio	0.79±0.12	1.5±0.10	>0.05
Total bilirubin (mg/dL)	0.69±0.12	0.69±0.11	>0.05
Serum creatinine(mg/dL)	0.4±0.11	1.6±0.51	<0.001^**
Urine creatinine (mg/dL)	65.5±10.11	300±20.51	<0.001^**
Urine albumin (mg/dL)	1.8±0.16	35.5±7.16	<0.001^**
GFR (mL/min/1.73m²)	138±10.21	70±8.11^‡	<0.001^**
Urine albumin-to-creatinine ratio (mg/g)	27.7±6.11	116.7±11.12^§	<0.001^**
Creatine phosphokinase (mcg/L)	15.5±5.21	60.43±10.11	0.002^**

Values are presented as mean ± standard deviation (SD). P-values obtained from the independent student t-test.

NAFLD: nonalcoholic fatty liver disease, FBG: fasting blood glucose, HbA1c: hemoglobin A1c, HDL-C: high density lipoprotein, LDL-C: low-density lipoprotein, hs-CRP: high-sensitivity C-reactive protein, AIP: atherogenic index of plasma, BMI: body mass index, AST: aspartate transaminase, ALT: alanine transaminase, ALP: alkaline phosphatase, GFR: glomerular filtration rate

↵* AIP of >0.21, high risk of CVD.
↵^† BMI of 25.0-29.9 kg/m² (overweight).
↵^‡ G2= GFR of 60-89 (mildly decreased).
↵^§ A2= UACR of 30-300 (moderately increased).
↵** P-value of <0.001

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Table 2

- Clinical and biochemical characteristics of patients with non-alcoholic fatty liver disease (n=735), 4-time intervals were recorded throughout the follow-up period.

Parameters	2018-2019	2019-2020	2020-2021	2021-2022	2022-2023	P-values
FBG (mmol/L)	6.5±1.41	6.5±1.51	6.8±1.61	6.8±1.81	7.5±1.61	0.001^**
HbA1c (%)	5.7±1.11	5.7±1.12	5.87±1.13	5.87±1.16	6.3±1.13	<0.001^**
HDL-C (mmol/L)	1.11±0.21	1.01±0.11	1.0±0.11	1.0±0.11	0.8±0.11	<0.001^**
Total cholesterol (mmol/L)	5.88±1.41	5.98±1.51	6.1±1.61	6.5±1.51	6.7±1.67	0.05^*
Triglycerides (mmol/L)	2.5±1.10	2.9±1.15	3.1±1.15	3.6±1.17	4.1±1.18	0.03^*
AIP = log (TG/HDL-C).	0.3±0.11	0.4±0.12	0.5±0.16	0.5±0.20	0.6±0.17	0.002^**
BMI (kg/m²)	26.5±6.55	28.5±7.55	29.5±6.45	29.5±6.55	29.6±6.65	0.05^*
hs-CRP(mg/l)	3.9±1.16	4.0±1.6	6.0±1.8	6.4±1.9	7.0±1.9	0.01^*
Albumin (g/dL)	3.0±0.3	2.8±0.8	2.5±0.3	2.2±0.4	2.0±0.4	0.02^*
AST:ALT ratio	1.5±0.10	1.6±0.10	1.6±0.15	1.7±0.15	1.8±0.15	>0.05
Serum creatinine(mg/dL)	1.6±0.51	1.7±0.61	1.9±0.51	1.9±0.55	2.0±0.66	0.04^*
GFR (mL/min/1.73m²)	70±8.11	69±7.11	58±9.11	56±9.14	50±9.17	0.04^*
Urine albumin-to-creatinine ratio mg/g	116.7±11.12	119.6±11.16	130.6±13.18	150.2±16.11	166.8±18.28	0.001^**
The incidences of CVD, and CKD were recorded throughout the follow-up period for 735 NAFLD patients, n (%)
Incidences of CVD	0 (0.0)	55 (7.5)	68 (9.4)	70 (9.5)	73 (9.9)	267 (36.3)
Incidences of CKD	0 (0.0)	50 (6.8)	64 (8.7)	73 (9.9)	80 (10.9)	267 (36.3)

Values are presented mean ± standard deviation (SD) or numbers and percentages (%). P-values were obtained from a 2-way ANOVA.

NAFLD: Nonalcoholic fatty liver disease, FBG: fasting blood glucose, HbA1c: hemoglobin A1c, HDL-C: high density lipoprotein, LDL-C: low-density lipoprotein, hs-CRP: high-sensitivity C-reactive protein, AIP: atherogenic index of plasma, BMI: body mass index, AST: aspartate transaminase, ALT: alanine transaminase, ALP: alkaline phosphatase, eGFR: estimated glomerular filtration rate, CVD: cardiovascular disease, CKD: chronic kidney disease

↵* P-value of <0.05,
↵** p-value of <0.001.

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Table 3
- The percentage of individuals at high risk of chronic kidney disease or cardiovascular disease with non-alcoholic fatty liver disease in the year 2018-2019 (n=735).
Risk of diseases n (%)
CKD events 189 (25.7)
CVD events 216 (29.4)
The incidences of CKD or CVD with NAFLD (n=735) after 4 years of follow-up
CKD events 267 (36.3)
CVD events 267 (36.3)
Values are presented as numbers and percentages (%).
NAFLD: non-alcoholic fatty liver disease, CKD: chronic kidney disease, CVD: cardiovascular disease

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Table 4

- Correlation of non-alcoholic fatty liver disease with glomerular filtration rate, chronic kidney disease grade, the incidence of albuminuria, atherogenic index of plasma categories, and the incidence of dyslipidemia.

NAFLD	GFR			Grade CKD						Albuminuria
Participants (n=735)	<60	>60	P-value^*	Grade 1	Grade 2	Grade 3	Grade 4	Grade 5	P-value^*	A1	A2	A3	P-value^*
NAFLD patients at 2018-2019	245 (33.3)	490 (66.7)	0.02	417 (56.7)	313 (42.6)	5 (0.7)	0 (0.0)	0 (0.0)	0.03	355 (48.3)	375 (51.0)	5 (0.7)	0.02
NAFLD patients after 4 years follow up	390 (53.1)	345 (46.9)		225 (30.6)	370 (50.3)	100 (13.6)	35 (4.8)	5 (0.7)		300 (40.8)	385 (52.4)	50 (6.8)
Participants (n=735)	Lipid			AIP (risk of CVD)
Participants (n=735)	Dyslipidemia	Normal	P-value^*	Low risk	Intermediate risk	High risk	P-value^*
NAFLD patients at 2018-2019	325 (44.2)	410 (55.8)	0.05	410 (55.8)	300 (40.8)	25 (3.4)	0.04
NAFLD patients after 4 years follow up	370 (50.3)	365 (49.7)	0.05	305 (41.5)	370 (50.3)	60 (8.2)	0.04

Values are presented as numbers and percentages (%).

Grade CKD groups: p-value for Grade 1 vs other groups. Albuminuria groups: p-value for A1 vs other groups. AIP (risk of CVD) groups: p-value for low-risk vs other groups. NAFLD: nonalcoholic fatty liver disease, GFR: glomerular filtration rate, CKD: chronic kidney disease, CVD: cardiovascular disease, AIP: atherogenic index of plasma

↵* Chi-square test. AIP of <0.11 low risk of CVD, whereas AIP values between 0.11-0.21= intermediate risk, AIP >0.21= high risk of CVD.

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Table 5

- Logistic regression to cardiovascular disease and chronic kidney disease in patients with non-alcoholic fatty liver disease.

Parameters	CVD		CKD
Parameters	Odds ratio (95% CI)	P-values	Odds ratio (95% CI)	P-values
Age (years)
Young (30-44)	2.11 (1.13-3.19)	>0.05	2.16 (1.33-3.12)	>0.05
Middle-age (45-59)	5.66 (2.193-5.99)	0.05^*	2.66 (1.53-3.52)	>0.05
Older adults (60-80)	6.11 (3.13-7.19)	0.04^*	6.16 (2.93-7.11)	0.04^*
FBG (mmol/L)	1.96 (0.93-2.19)	>0.05	5.86 (3.73-7.12)	0.03^*
HDL-C (mmol/L)	-7.76 (3.23-8.79)	0.04^*	-0.56 (0.43-0.99)	>0.05
Total cholesterol (mmol/L)	7.33 (3.93-8.99)	0.03^*	1.13 (0.95-1.99)	>0.05
Triglycerides (mmol/L)	8.22 (3.93-10.39)	0.02^*	0.96 (0.93-1.19)	>0.05
AIP = log (TG/HDL-C)	9.16 (2.93-11.99)	0.01^*	1.22 (0.83-2.10)	>0.05
BMI (kg/m²)	5.96 (2.93-6.29)	0.04^*	1.34 (0.55-1.89)	>0.05
hs-CRP(mg/l)	5.97 (2.43-6.79)	0.04^*	8.88 (3.93-9.90)	0.01^*
Albumin (g/dL)	0.92 (0.90-1.91)	>0.05	-5.96 (3.93-7.99)	0.05^*
Total protein (g/dL)	1.76 (0.99-2.29)	>0.05	3.46 (1.33-4.09)	>0.05
AST (IU/L)	6.36 (2.93-8.99)	0.02^*	7.26 (2.93-9.39)	0.01^*
ALT(IU/L)	1.26 (0.73-2.29)	>0.05	1.33 (0.73-1.99)	>0.05
ALP (IU/L)	2.16 (1.93-3.89)	>0.05	4.36 (1.93-4.99)	>0.05
Creatine phosphokinase (mcg/L)	9.46 (3.93-11.49)	0.03^*	2.33 (1.23-3.11)	>0.05

Logistic regression analysis with odds ratio (OR) and 95% confidence interval (CI). NAFLD: nonalcoholic fatty liver disease, CKD: chronic kidney disease, CVD: cardiovascular diseases, FBG: fasting blood glucose, HDL-C: high density lipoprotein, hs-CRP: high-sensitivity C-reactive protein, AIP: atherogenic index of plasma, BMI: body mass index, AST: aspartate transaminase, ALT: alanine transaminase, ALP: Alkaline phosphatase