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Systematic ReviewSystematic Review
Open Access

Epidemiology of lean/non-obese nonalcoholic fatty liver disease in China

A systematic review and meta-analysis

Jianmei Zhang, Xiaocheng Huang, Luying Dong, Yachao Yang and Dehuan Kong
Saudi Medical Journal September 2023, 44 (9) 848-863; DOI: https://doi.org/10.15537/smj.2023.44.9.20230021
Jianmei Zhang
From the Department of Endocrinology and Metabolism (Zhang, Yang); from the Department of Geriatrics (Zhang); from the Department of Health Examination (Huang, Dong), Weihai Municipal Hospital, Shandong University, and from the Department of Endocrinology and Metabolism (Kong), Taian City Central Hospital, Shandong, China.
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  • For correspondence: [email protected]
Xiaocheng Huang
From the Department of Endocrinology and Metabolism (Zhang, Yang); from the Department of Geriatrics (Zhang); from the Department of Health Examination (Huang, Dong), Weihai Municipal Hospital, Shandong University, and from the Department of Endocrinology and Metabolism (Kong), Taian City Central Hospital, Shandong, China.
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Luying Dong
From the Department of Endocrinology and Metabolism (Zhang, Yang); from the Department of Geriatrics (Zhang); from the Department of Health Examination (Huang, Dong), Weihai Municipal Hospital, Shandong University, and from the Department of Endocrinology and Metabolism (Kong), Taian City Central Hospital, Shandong, China.
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Yachao Yang
From the Department of Endocrinology and Metabolism (Zhang, Yang); from the Department of Geriatrics (Zhang); from the Department of Health Examination (Huang, Dong), Weihai Municipal Hospital, Shandong University, and from the Department of Endocrinology and Metabolism (Kong), Taian City Central Hospital, Shandong, China.
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Dehuan Kong
From the Department of Endocrinology and Metabolism (Zhang, Yang); from the Department of Geriatrics (Zhang); from the Department of Health Examination (Huang, Dong), Weihai Municipal Hospital, Shandong University, and from the Department of Endocrinology and Metabolism (Kong), Taian City Central Hospital, Shandong, China.
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Article Figures & Data

Figures

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  • Figure 1
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    Figure 1

    - Flow diagram of the studies’ enrollment and geographical regions of China. A) Flow diagram of the studies’ enrollment by PRISMA. B) The geographical regions of China included in this meta-analysis.

  • Figure 2
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    Figure 2

    - Forest plot for the lean/nonobese NAFLD prevalence by meta-analysis. A) NAFLD prevalence in lean subjects of China. B) NAFLD prevalence in nonobese subjects of China.

  • Figure 3
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    Figure 3

    - Summary of subgroup analysis of NAFLD prevalence by different BMI cut-offs, regions, genders, study year, and population source. A) NAFLD prevalence in lean/nonobese population by different BMI cut-offs, regions, and population source. B) NAFLD prevalence in lean/nonobese population by study year. C) NAFLD prevalence in lean/nonobese men or women of China by different BMI cut-offs. *Sample size refers to the total number of lean/nonobese subjects in the study. BMI: body mass index, CI: confidence interval, NAFLD: nonalcoholic fatty liver disease

  • Appendix 3
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    Appendix 3

    - Funnel plot of publication bias. A) Funnel plot of the 25 original studies included in the analysis. B) Funnel plot of the 25 original studies included in the analysis (black dots) and the missing studies imputed by the trim-and-fill procedure (white dots).

  • Appendix 5
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    Appendix 5

    - Subgroup analysis of NAFLD prevalence in lean/nonobese population by different regions. A) Studies in north China. B) Studies in south China

  • Appendix 6
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    Appendix 6

    - Subgroup analysis of NAFLD prevalence in lean/nonobese Chinese population by source of population. A) Studies based on population. B) Studies based on health check-up.

Tables

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    Table 1

    - Summary of included studies.

    ReferencesRegionPopulationDiagnostics usedNNAFLD prevalence (%)
    OverallIn leanIn nonobese
    Zhang YN et al17ZhejiangHealth checkupUltrasonography6285 10.4% 
    Li C et al18HeilongjiangHealth checkupUltrasonography177950.5%18.3% 
    Wang Q et al19ZhejiangHealth checkupUltrasonography253833.6%13.1% 
    Xu C et al20ZhejiangPopulation basedUltrasonography6905  7.3%
    Wei JL et al21Hong KongPopulation basedH-MRS91128.8% 19.3%
    Zeng J et al22ShanghaiHealth checkupUltrasonography271540.5%21.4%28.1%
    Zheng X et al23ChongqingHealth checkupUltrasonography95924  8.2%
    Luo Z et al24ChongqingHealth checkupUltrasonography34306  3.4%
    Wang L et al25ShanghaiHealth checkupUltrasonography881729.0%7.1% 
    Li Y et al26ZhejiangPopulation basedUltrasonography9767  8.6%
    Li Q et al27ShanghaiPopulation basedUltrasonography2668  10.9%
    Lu Z et al28ZhejiangHealth checkupUltrasonography5916 11.7% 
    Lin H et al29Hong KongPopulation basedH-MRS90428.6%12.5%19.2%
    Wong VWS et al30Hong KongPopulation basedH-MRS56513.8%8.0%11.2%
    Chen CH et al31TaiwanPopulation basedUltrasonography1444  11.5%
    Huang JF et al32TaiwanHealth checkupUltrasonography248344.5% 26.2%
    Hsu CL et al33TaiwanHealth checkupUltrasonography4000  18.5%
    Zou Y et al34ZhejiangHealth checkupUltrasonography12127  17.7%
    You G et al35ShandongHealth checkupUltrasonography2029  16.6%
    Wu L et al36ZhejiangHealth checkupUltrasonography11906  17.2%
    Lu CW et al37TaiwanPopulation basedUltrasonography606  32.2%
    Xiao SJ et al38ChongqingHealth checkupUltrasonography1867622.0% 6.5%
    Lee SW et al39TaiwanHealth checkupUltrasonography200824.5% 10.4%
    Wang Z et al40HubeiHealth checkupUltrasonography2503224.6% 12.2%
    Hu PF et al41ShanghaiPopulation basedUltrasonography371732.7% 16.3%
    • NAFLD: nonalcoholic fatty liver disease, H-MRS: H-magnetic resonance spectroscopy

    • View popup
    Table 2

    - Multivariable meta-regression of included studies to identify heterogeneous sources affecting the prevalence of nonobese nonalcoholic fatty liver disease in China.

    CovariateCoefficientStandard errorLower boundUpper boundP-values
    Study year0.07890.02830.02340.13440.0053*
    Region-0.02880.0646-0.15550.09790.6558
    Population type-0.06770.0442-0.15420.01890.1256
    Diagnostic methods0.06670.0779-0.08600.21930.3920
    BMI cut-offs0.05090.02410.00370.09810.0346*
    Sample size-0.05730.0178-0.0922-0.02240.0013*
    • ↵* Statistically significant. BMI: body mass index

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    Table 3

    - Comparison of characteristics between lean/nonobese and overweight/obese nonalcoholic fatty liver disease patients.

    EventsEstimation of merged valueMean difference
     Lean/nonobeseOverweight/obeseOR (95% CI)I2P-values
    Male52.7%66.4%0.61 (0.44-0.83)89.0%0.0020*
    Hypertension41.4%57.8%0.44 (0.34-0.56)0.0%<0.0001*
    Type 2 diabetes mellitus12.6%15.9%0.88 (0.57-1.34)0.0%0.5427
    Age, years (median range)49.95 (42.60-54.84)50.06 (43.70-56.44)0.27(-0.29-0.84)56.4%0.3506
    Systolic BP (mmHg)128.86 (121.60- 137.81)136.09 (130.40-142.85)-7.34 (-9.22-5.45)79.1%<0.0001*
    Diastolic BP (mmHg)80.48 (77.20- 85.22)84.98 (82.20-91.00)-4.45(-5.88-3.02)55.4%<0.0001*
    Waist circumference(cm)80.63 (76.27 - 85.00)92.73 (90.80-94.00)-12.13 (-14.21-10.04)97.3%<0.0001*
    Fasting plasma glucose(mmol/L)5.53 (4.74-5.91)5.69 (5.23-6.02)-0.17(-0.33-0.01)68.1%0.0379*
    Uric acid (μmol/L)339.14 (305.66- 378.81)365.46 (311.17-415.80)-26.85 (-46.76-6.95)89.0%0.0082*
    Triglycerides (mmol/L)1.63 (1.23-2.02)1.94 (1.81-2.17)-0.30 (-0.51-0.09)70.0%0.0047*
    Total cholesterol(mmol/L)5.14 (4.88-5.40)5.13 (4.93-5.30)-0.005 (-0.06; 0.05)0.0%0.8633
    LDL cholesterol(mmol/L)3.07 (2.83-3.24)3.12 (2.79-3.48)-0.023 (-0.066-0.0196)1.0%0.2866
    HDL cholesterol(mmol/L)1.33 (1.12-1.48)1.26 (1.04-1.35)0.073 (0.005-0.141)88.3%0.0347*
    ALT (IU/L)30.28 (28.21-34.0)33.12 (30.78-37.00)-3.14 (-5.46-0.82)0.0%0.0081*
    GGT (IU/L)29.91 (24.31-35.50)43.68 (40.49-46.87)-13.94 (-31.16-3.27)95.9%0.1124
    • ↵* Indicates statistically significant. The overweight/obese group is the reference group, and the mean difference or OR is calculated as lean/nonobese versus overweight/obese. NAFLD: nonalcoholic fatty liver disease, OR: odds ratio, ALT: alanine aminotransferase, BMI: body mass index, BP: blood pressure, GGT: γ-glutamyl transferase, HDL: high-density lipoprotein cholesterol, LDL: low-density lipoprotein cholesterol, MD: standardized mean difference, CI: confidence interval

    • View popup
    Appendix 1

    - Quality assessment of included studies in the epidemiology of lean/nonobese NAFLD in China using the JBI-prevalence critical appraisal checklist.14

    StudiesQ1Q2Q3Q4Q5Q6Q7Q8Q9
    Zhang et al17YYYYYYYYNA
    Li et al18YYYYYYYYNA
    Wang et al19YYYYYYYYNA
    Xu et al20YYYYYYYYNA
    Wei et al21YYYYYYYYNA
    Zeng et al22YYYYYYYYNA
    Zheng et al23YYYYYYYYNA
    Luo et al24YYYYYYYYNA
    Wang et al25YYYYYYYYNA
    Li et al26YYYYYYYYNA
    Li et al27YYYYYYYYNA
    Lu et al28YYYYYYYYNA
    Lin et al29YYYYYYYYNA
    Wong et al30YYYYYYYYNA
    Chen et al31YYYYYYYYNA
    Huang et al32YYYYYYYYNA
    Hsu et al33YYYYYYYYNA
    You et al34YYYYYYYYNA
    Zou et al35YYYYYYYYNA
    Wu et al36YYYYYYYYNA
    Lu et al37YYYYYYYYNA
    Xiao et al38YYYYYYYYNA
    Lee et al39YYYYYYYYNA
    Wang et al40YYYYYYYYNA
    Hu et al41YYYYYYYYNA
    • Y: yes, N: no, U: unclear, NA: not applicable

    • View popup
    Appendix 2

    - Numbers of citations by each database searched.

    Databases and trial registersCitations
    Pubmed748
    Embase3518
    The Cochrane Library30
    Web of Science4413
    Total8709
    • View popup
    Appendix 4

    - Egger’s test of subgroups for meta-analysis of clinical characteristics between lean (or non-obese) vs. non-lean or (obese) NAFLD patients.

    SubgroupsNumber of studiesP-values
    The proportion of males80.9417
    The prevalence of hypertension30.9795
    Age60.3531
    Systolic pressure60.2077
    Diastolic pressure60.9027
    Waist circumference60.0971
    Fasting plasma glucose level60.8471
    Uric acid level30.5153
    Triglyceride level40.2522
    Total cholesterol level50.8127
    Low-density lipoprotein level60.5453
    High-density lipoprotein level60.4959
    Alanine transaminase30.0774
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Epidemiology of lean/non-obese nonalcoholic fatty liver disease in China
Jianmei Zhang, Xiaocheng Huang, Luying Dong, Yachao Yang, Dehuan Kong
Saudi Medical Journal Sep 2023, 44 (9) 848-863; DOI: 10.15537/smj.2023.44.9.20230021

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Epidemiology of lean/non-obese nonalcoholic fatty liver disease in China
Jianmei Zhang, Xiaocheng Huang, Luying Dong, Yachao Yang, Dehuan Kong
Saudi Medical Journal Sep 2023, 44 (9) 848-863; DOI: 10.15537/smj.2023.44.9.20230021
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Keywords

  • nonalcoholic fatty liver disease
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  • body mass index
  • lean/nonobese NAFLD
  • meta-analysis
  • Chinese population

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