Clinical features and related risk factors of chronic hepatitis B patients with concomitant minimal hepatic steatosis

Xiaoyan MA; Yun CHEN; Jiacheng LIU; Jie LI; Chao WU

doi:10.3969/j.issn.1001-5256.2023.01.010

Volume 39 Issue 1

Jan. 2023

Turn off MathJax

Article Contents

Abstract

References

Article Navigation > Journal of Clinical Hepatology > 2023 > 39(1): 63-69

PDF( 2358 KB)

Clinical features and related risk factors of chronic hepatitis B patients with concomitant minimal hepatic steatosis

DOI: 10.3969/j.issn.1001-5256.2023.01.010

Xiaoyan MA¹,
Yun CHEN²,
Jiacheng LIU³,
Jie LI³,
Chao WU^{3
,
,
,}

1.
Nanjing University Medical School, Nanjing 210008, China
2.
Drum Tower Clinical Medical College of Nanjing Medical University, Nanjing 210008, China
3.
Department of Infectious Diseases, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing 210008, China

Research funding:

National Natural Science Foundation of China General Project (81970545);

National Natural Science Foundation of China General Project (82170609)

More Information

Corresponding author: WU Chao, dr.wu@nju.edu.cn (ORCID: 0000-0002-1657-010X)
Received Date: 2022-07-04
Accepted Date: 2022-09-16
Published Date: 2023-01-20

Abstract

Abstract

Objective To investigate the changes of clinical indices in chronic hepatitis B (CHB) patients with concomitant minimal hepatic steatosis and related factors for minimal hepatic steatosis. Methods A total of 179 CHB patients who underwent liver biopsy in Department of Infectious Diseases, Affiliated Drum Tower Hospital of Nanjing University Medical School, from July 2018 to March 2022 were enrolled, and according to the degree of steatosis, they were divided into non-steatosis group with 98 patients and minimal hepatic steatosis group with 81 patients. Demographic information, clinical data, and liver histopathology data were collected, and related observation indices were compared between the two groups. The independent samples t-test was used for comparison of normally distributed continuous data between two groups, and the Mann-Whitney U test was used for comparison of non-normally distributed continuous data between two groups; the chi-square test was used for comparison of categorical data between groups. A Spearman correlation analysis was performed, and a Logistic regression analysis was used to investigate the risk factors for minimal hepatic steatosis. Results Compared with the non-steatosis group, the minimal hepatic steatosis group had a significantly higher proportion of male patients (69.1% vs 52.0%, χ²=5.390, P < 0.05) and a significantly higher proportion of patients with significant liver fibrosis (43.2% vs 25.5%, χ²=6.234, P < 0.05). Compared with the non-steatosis group, the minimal hepatic steatosis group had significantly higher levels of body mass index (BMI) (23.61±2.95 kg/m² vs 22.13±2.67 kg/m², t=-4.150, P < 0.05), uric acid (UA) [333.0(291.0-375.5) μmol/L vs 287.5(244.8-345.3) μmol/L, Z=-3.620, P < 0.05], triglyceride [0.92 (0.66-1.14) μmol/L vs 0.77 (0.62-1.02) μmol/L, Z=-2.224, P < 0.05], and controlled attenuation parameter (CAP) [234 (214-258) dB/m vs 218 (201-237) dB/m, Z=-2.867, P < 0.05]. In the group with normal body weight, the patients with minimal hepatic steatosis had significantly higher levels of UA (333.0±63.9 μmol/L vs 291.0±72.8 μmol/L, t=-2.395, P < 0.05) a nd HBV DNA [4.44 (3.51-6.79) log₁₀ IU/mL vs 3.42 (3.00-5.03) log₁₀ IU/mL, Z=-2.474, P < 0.05]. BMI (odds ratio [OR]=1.223, 95% confidence interval [CI] : 1.086-1.378, P=0.001) and UA (OR=1.006, 95%CI: 1.002-1.010, P=0.008) were risk factors for minimal hepatic steatosis in CHB patients, and UA (OR=1.007, 95%CI: 1.001-1.013, P=0.022) was a risk factors for minimal hepatic steatosis in CHB patients with normal body weight. Conclusion Compared with the non-steatosis CHB patients, the CHB patients with minimal hepatic steatosis have a significantly higher proportion of patients with significant liver fibrosis and a significantly higher level of CAP. BMI and UA are independent risk factors for minimal hepatic steatosis in CHB patients, and for the CHB patients with normal body weight, elevated UA is closely associated with the onset of minimal hepatic steatosis.
- Hepatitis B, Chronic,
- Non-alcoholic Fatty Liver Disease,
- Risk Factor

FullText(HTML)

References(26)

References

[1]	LI J, ZOU B, YEO YH, et al. Prevalence, incidence, and outcome of non-alcoholic fatty liver disease in Asia, 1999-2019: a systematic review and meta-analysis[J]. Lancet Gastroenterol Hepatol, 2019, 4(5): 389-398. DOI: 10.1016/S2468-1253(19)30039-1.
[2]	ZHENG Q, ZOU B, WU Y, et al. Systematic review with meta-analysis: prevalence of hepatic steatosis, fibrosis and associated factors in chronic hepatitis B[J]. Aliment Pharmacol Ther, 2021, 54(9): 1100-1109. DOI: 10.1111/apt.16595.
[3]	KLEINER DE, BRUNT EM, VAN NATTA M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease[J]. Hepatology, 2005, 41(6): 1313-1321. DOI: 10.1002/hep.20701.
[4]	WANG MM, WANG GS, SHEN F, et al. Hepatic steatosis is highly prevalent in hepatitis B patients and negatively associated with virological factors[J]. Dig Dis Sci, 2014, 59(10): 2571-2579. DOI: 10.1007/s10620-014-3180-9.
[5]	SCHEUER PJ. Classification of chronic viral hepatitis: a need for reassessment[J]. J Hepatol, 1991, 13(3): 372-374. DOI: 10.1016/0168-8278(91)90084-o.
[6]	LAI CL, RATZIU V, YUEN MF, et al. Viral hepatitis B[J]. The Lancet, 2003, 362(9401): 2089-2094. DOI: 10.1016/S0140-6736(03)15108-2.
[7]	SARIN SK, KUMAR M, LAU GK, et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update[J]. Hepatol Int, 2016, 10(1): 1-98. DOI: 10.1007/s12072-015-9675-4.
[8]	LEE MH, YANG HI, LIU J, et al. Prediction models of long-term cirrhosis and hepatocellular carcinoma risk in chronic hepatitis B patients: risk scores integrating host and virus profiles[J]. Hepatology, 2013, 58(2): 546-554. DOI: 10.1002/hep.26385.
[9]	WONG GL, CHAN HL, YU Z, et al. Coincidental metabolic syndrome increases the risk of liver fibrosis progression in patients with chronic hepatitis B-a prospective cohort study with paired transient elastography examinations[J]. Aliment Pharmacol Ther, 2014, 39(8): 883-893. DOI: 10.1111/apt.12658.
[10]	YEN YH, CHANG KC, TSAI MC, et al. Elevated body mass index is a risk factor associated with possible liver cirrhosis across different etiologies of chronic liver disease[J]. J Formos Med Assoc, 2018, 117(4): 268-275. DOI: 10.1016/j.jfma.2017.09.002.
[11]	CHEN YC, HSU CW, JENG WJ, et al. Advanced liver fibrosis is associated with necroinflammatory grade but not hepatic steatosis in chronic hepatitis B patients[J]. Dig Dis Sci, 2021, 66(12): 4492-4500. DOI: 10.1007/s10620-020-06761-x.
[12]	SETO WK, FUNG J, CHEUNG KS, et al. Body-mass index is associated with fibrosis regression during long-term nucleoside analogue therapy in chronic hepatitis B[J]. Aliment Pharmacol Ther, 2016, 44(10): 1071-1079. DOI: 10.1111/apt.13804.
[13]	ZHU L, JIANG J, ZHAI X, et al. Hepatitis B virus infection and risk of non-alcoholic fatty liver disease: A population-based cohort study[J]. Liver Int, 2019, 39(1): 70-80. DOI: 10.1111/liv.13933.
[14]	PAIS R, RUSU E, ZILISTEANU D, et al. Prevalence of steatosis and insulin resistance in patients with chronic hepatitis B compared with chronic hepatitis C and non-alcoholic fatty liver disease[J]. Eur J Intern Med, 2015, 26(1): 30-36. DOI: 10.1016/j.ejim.2014.12.001.
[15]	NAU AL, SOARES JC, SHIOZAWA MB, et al. Clinical and laboratory characteristics associated with dyslipidemia and liver steatosis in chronic HBV carriers[J]. Rev Soc Bras Med Trop, 2014, 47(2): 158-164. DOI: 10.1590/0037-8682-0009-2014.
[16]	YILMAZ B, KOKLU S, BUYUKBAYRAM H, et al. Chronic hepatitis B associated with hepatic steatosis, insulin resistance, necroinflammation and fibrosis[J]. Afr Health Sci, 2015, 15(3): 714-718. DOI: 10.4314/ahs.v15i3.3.
[17]	CHEN Y, CAO D, LI C, et al. A nomogram for discrimination of non- alcoholic fatty liver disease in patients with chronic hepatitis B[J]. Eur J Gastroenterol Hepatol, 2021, 33(1): 69-75. DOI: 10.1097/MEG.0000000000001691.
[18]	YUAN H, YU C, LI X, et al. Serum uric acid levels and risk of metabolic syndrome: a dose-response meta-analysis of prospective studies[J]. J Clin Endocrinol Metab, 2015, 100(11): 4198-4207. DOI: 10.1210/jc.2015-2527.
[19]	HWANG IC, SUH SY, SUH AR, et al. The relationship between normal serum uric acid and nonalcoholic fatty liver disease[J]. J Korean Med Sci, 2011, 26(3): 386-391. DOI: 10.3346/jkms.2011.26.3.386.
[20]	XU CF, YU CH, XU L, et al. High serum uric acid increases the risk for nonalcoholic fatty liver disease: a prospective observational study[J]. PLoS One, 2010, 5(7): e11578. DOI: 10.1371/journal.pone.0011578.
[21]	ZHENG X, GONG L, LUO R, et al. Serum uric acid and non-alcoholic fatty liver disease in non-obesity Chinese adults[J]. Lipids Health Dis, 2017, 16(1): 202. DOI: 10.1186/s12944-017-0531-5.
[22]	ZHOU M, YANG N, XING X, et al. Obesity interacts with hyperuricemia on the severity of non-alcoholic fatty liver disease[J]. BMC Gastroenterol, 2021, 21(1): 43. DOI: 10.1186/s12876-021-01615-w.
[23]	PETTA S, CAMMÀ C, CABIBI D, et al. Hyperuricemia is associated with histological liver damage in patients with non-alcoholic fatty liver disease[J]. Aliment Pharmacol Ther, 2011, 34(7): 757-766. DOI: 10.1111/j.1365-2036.2011.04788.x.
[24]	FERNÁNDEZ RODRÍGUEZ CM, ALLER R, GUTIÉRREZ GARCÍA ML, et al. Higher levels of serum uric acid influences hepatic damage in patients with non-alcoholic fatty liver disease (NAFLD)[J]. Rev Esp Enferm Dig, 2019, 111(4): 264-269. DOI: 10.17235/reed.2019.5965/2018.
[25]	BALLESTRI S, NASCIMBENI F, ROMAGNOLI D, et al. The independent predictors of non-alcoholic steatohepatitis and its individual histological features. : Insulin resistance, serum uric acid, metabolic syndrome, alanine aminotransferase and serum total cholesterol are a clue to pathogenesis and candidate targets for treatment[J]. Hepatol Res, 2016, 46(11): 1074-1087. DOI: 10.1111/hepr.12656.
[26]	DUAN H, ZHANG R, CHEN X, et al. Associations of uric acid with liver steatosis and fibrosis applying vibration controlled transient elastography in the united states: a nationwide cross-section study[J]. Front Endocrinol (Lausanne), 2022, 13: 930224. DOI: 10.3389/fendo.2022.930224.

Relative Articles

[1]	Zhao JinHua, Li JunFeng, Mao XiaoRong. Effect of T-lymphocyte phenotype on immune status in chronic hepatitis B virus infection and its application value[J]. Journal of Clinical Hepatology, 2020, 36(5): 1019-1023. doi: 10.3969/j.issn.1001-5256.2020.05.014
[2]	Chen Bin, Zhang Tao, Zhu WenFang, Peng Jie, Zhang QianQian, Li YunFang, Ding XiuLi. Effect of the warming and heat-clearing method on the percentage of regulatory T lymphocytes/T helper 17 cells in rats with acute-on-chronic liver failure[J]. Journal of Clinical Hepatology, 2018, 34(12): 2642-2647. doi: 10.3969/j.issn.1001-5256.2018.12.026
[3]	Gao WeiHua, Ge KuanXue, Xiang XiaoXing. Association of Th17 cells, regulatory T cells, and their imbalance with nonalcoholic fatty liver disease[J]. Journal of Clinical Hepatology, 2018, 34(6): 1347-1350. doi: 10.3969/j.issn.1001-5256.2018.06.046
[4]	Wang Yan, Huang YouYing, Ma Yan, Guo Feng, Wang XiaoBo, Wang XiaoZhong. Expression features of follicular helper T cells in peripheral blood in patients with chronic hepatitis B[J]. Journal of Clinical Hepatology, 2018, 34(1): 58-62. doi: 10.3969/j.issn.1001-5256.2018.01.012
[5]	Ge KuanXue, Gao WeiHua, Xiang XiaoXing. Association of regulatory T cells, T helper 17 cells, and change in their balance with autoimmune hepatitis[J]. Journal of Clinical Hepatology, 2018, 34(7): 1573-1576. doi: 10.3969/j.issn.1001-5256.2018.07.045
[6]	Li JianYun, Tu ChuanQing, He De, Wang DianWen, Huang Can, Zhang XuYan, Feng Chun. Clinical significance of measurement of T lymphocyte subsets before splenectomy in patients with primary immune thrombocytopenia[J]. Journal of Clinical Hepatology, 2017, 33(1): 150-154. doi: 10.3969/j.issn.1001-5256.2017.01.033
[7]	He JunNan, Zhao ShouSong. Research advances in association between regulatory T cells and hepatitis B virus infection[J]. Journal of Clinical Hepatology, 2016, 32(2): 361-365. doi: 10.3969/j.issn.1001-5256.2016.02.036
[8]	Zhang FeiFei, Chen Hui, Lyu Jun. Role of T-helper cell 17 in the development and progression of hepatocellular carcinoma[J]. Journal of Clinical Hepatology, 2016, 32(8): 1626-1629. doi: 10.3969/j.issn.1001-5256.2016.08.046
[9]	Ji LongShan, Sun XueHua, Zhou ZhenHua, Zhang Xin, Gao YaTing, Gao YueQiu, Li Man. Role of follicular helper T cells in development and progression of liver diseases[J]. Journal of Clinical Hepatology, 2016, 32(6): 1230-1234. doi: 10.3969/j.issn.1001-5256.2016.06.050
[10]	Zhou Yan, Jing Xiang, Zhu ZhengYan. Roles of regulatory T cells and T-helper cells in hepatitis B virus-related liver diseases[J]. Journal of Clinical Hepatology, 2016, 32(10): 1994-1997. doi: 10.3969/j.issn.1001-5256.2016.10.040
[11]	Li CaiDong, Chen XiLian, Duan ZhengJun, Liu XueMei, Wu Bin. Determination of proportions of T cell subsets and levels of interleukin-15 and interleukin-16 in peripheral blood of patients with chronic hepatitis B virus infection and correlation between them[J]. Journal of Clinical Hepatology, 2015, 31(11): 1857-1861. doi: 10.3969/j.issn.1001-5256.2015.11.021
[12]	Shi GuangYing, Ma XiaoYuan, Xie JingDong. Changes in T lymphocyte subsets and cytokines in peripheral blood of patients with primary biliary cirrhosis after treatment with different doses of ursodeoxycholic acid[J]. Journal of Clinical Hepatology, 2015, 31(9): 1447-1451. doi: 10.3969/j.issn.1001-5256.2015.09.020
[13]	Li CaiDong, Chen XiLian, Tian PengFei, Li HuiJun, Wu Bin. Correlation analysis of percentages of T lymphocyte subsets and CD4~+CD25~+ regulatory T cells and HBV DNA level in peripheral blood of chronic hepatitis B patients[J]. Journal of Clinical Hepatology, 2015, 31(4): 541-545. doi: 10.3969/j.issn.1001-5256.2015.04.016
[14]	Wang Yu, Ma ZhiYuan, Guo YongHong, He Yu, Zhang Ying, Xie YuMei, Ma Li, Zhou Yun, Jia ZhanSheng. Investigation of CD4+CXCR5+ follicular helper T cell frequency and expression of related functional molecules in peripheral blood of hepatitis C virus patients[J]. Journal of Clinical Hepatology, 2013, 29(5): 379-382.
[15]	Ding QiaoYun, Yu HaiYing, Sun WeiWei, Pan Jian, Cao XingGuo, Wang Lei. The changes of peripheral blood T-lymphocyte subsets in pediatric severe hepatitis[J]. Journal of Clinical Hepatology, 2011, 27(7): 729-730.

Supplements(0)

Cited By

Cited by

Periodical cited type(8)

1.	蒋丽莎，马洪升. 日归手术——中国日间手术的升华. 华西医学. 2022(02): 161-164 .
2.	雷甜甜，梁鹏，马洪升，蒋丽莎. 四川大学华西医院日归手术管理实践. 广东医学. 2022(10): 1222-1228 .
3.	方宁波，陈伟力. 腹腔镜胆囊切除术日间手术围术期指标观察及患者延迟出院原因分析. 江西医药. 2022(10): 1524-1527 .
4.	刘力玮，郑亚民，刘东斌，王悦华，刘家峰，梁阔，江华，高崇崇，于志浩，徐大华. 日间腹腔镜胆囊切除术的可行性分析. 腹腔镜外科杂志. 2021(05): 359-362 .
5.	杨奕夫，黎柏峰，肖艳. 日间腹腔镜胆囊切除术质量控制的研究进展. 腹腔镜外科杂志. 2020(10): 796-798+800 .
6.	李航，赵礼金. 老年患者腹腔镜胆囊切除日间手术的安全性分析. 中国普通外科杂志. 2019(08): 1012-1017 .
7.	石鑫，秦琦瑜，刘维丽，胥静，王威. “三镜”联合治疗胆囊结石合并肝外胆管结石手术效果及安全性研究. 临床军医杂志. 2018(06): 710-712 .
8.	张少成，张亚辉，徐小梦. 年龄因素对上胆道疾病患者行腹腔镜胆囊切除术安全性的影响. 深圳中西医结合杂志. 2018(06): 184-186 .

Other cited types(1)

Proportional views

Proportional views

通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142

Figures(3) / Tables(5)

Get Citation

PDF

XML

Article Metrics

Article views (1854) PDF downloads(155)

Clinical features and related risk factors of chronic hepatitis B patients with concomitant minimal hepatic steatosis

DOI: 10.3969/j.issn.1001-5256.2023.01.010