Association between nonalcoholic fatty liver disease and osteoporosis in elderly patients

Qian XUE; Chunling JIA; Jingtong WANG

doi:10.12449/JCH240813

Volume 40 Issue 8

Aug. 2024

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Article Navigation > Journal of Clinical Hepatology > 2024 > 40(8): 1585-1590

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Association between nonalcoholic fatty liver disease and osteoporosis in elderly patients

DOI: 10.12449/JCH240813

Department of Gerontology，Peking University People’s Hospital，Beijing 100044，China

Research funding:

National Project of Multidisciplinary Diagnosis and Treatment of Major Diseases (2020);

International Institute of Population Health, Peking University Health Science Center (JKCJ202102)

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Corresponding author: WANG Jingtong， wangjingtong11@163.com （ORCID： 0000-0002-8203-1323）
Received Date: 2023-11-23
Accepted Date: 2024-01-23
Published Date: 2024-08-25

Abstract

Abstract

Objective To investigate the association between nonalcoholic fatty liver disease （NAFLD） and osteoporosis in elderly patients. Methods A total of 824 patients， aged ≥60 years， who were hospitalized in Department of Gerontology， Peking University People’s Hospital， from June 2016 to April 2023 were enrolled， with 398 patients in the osteoporosis group and 426 in the non-osteoporosis group. Related data were collected from all subjects， including general information， blood biochemical parameters， liver ultrasound， and bone mineral density measured by dual-energy X-ray examination. 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 variables； a binary Logistic regression analysis was used to investigate the independent risk factors for osteoporosis. Results Compared with the non-osteoporosis group， the osteoporosis group had a significantly higher age， a significantly higher proportion of female patients or patients with diabetes， and a significantly lower body mass index （all P<0.05）. The osteoporosis group had a significantly higher proportion of patients with NAFLD than the non-osteoporosis group （36.2% vs 24.6%， χ²=12.878， P<0.001）. Compared with the non-osteoporosis group， the osteoporosis group had significantly lower levels of hemoglobin， uric acid， and albumin and significantly higher levels of total cholesterol， low-density lipoprotein cholesterol （LDL-C）， bone-specific alkaline phosphatase， and tartrate-resistant acid phosphatase （all P<0.05）. The binary Logistic regression analysis showed that old age （odd ratio ［OR］=1.040， 95% confidence interval ［CI］： 1.015‍ ‍—‍ ‍1.066， P=0.002）， female sex （OR=4.089， 95%CI： 2.607‍ ‍—‍ ‍6.411， P<0.001）， NAFLD （OR=1.697， 95%CI： 1.076‍ ‍—‍ ‍2.678， P=0.023）， diabetes （OR=1.509， 95%CI： 1.008‍ ‍—‍ ‍2.260， P=0.046）， and LDL-C （OR=1.431， 95%CI： 1.010‍ ‍—‍ ‍2.029， P=0.044） were independent risk factors for osteoporosis in elderly patients. Considering the impact of diabetes on the research findings， a subgroup analysis was performed for the patients without diabetes， and the results showed that NAFLD （OR=1.573， 95%CI： 1.015‍ ‍—‍ ‍2.439， P=0.043） was an independent risk factor for osteoporosis in the elderly patients without diabetes. Conclusion NAFLD， old age， and female sex are independent risk factors for osteoporosis in elderly patients.
- Non-Alcoholic Fatty Liver Disease,
- Osteoporosis,
- Aged

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References

[1]	SERIOLO B, PAOLINO S, CASABELLA A, et al. Osteoporosis in the elderly[J]. Aging Clin Exp Res, 2013, 25( Suppl 1): S27- S29. DOI: 10.1007/s40520-013-0107-9.
[2]	ABBASI M, FARZAM SA, MAMAGHANI Z, et al. Relationship between metabolic syndrome and its components with bone densitometry in postmenopausal women[J]. Diabetes Metab Syndr, 2017, 11( Suppl 1): S73- S76. DOI: 10.1016/j.dsx.2016.12.008.
[3]	SHANBHOGUE VV, FINKELSTEIN JS, BOUXSEIN ML, et al. Association between insulin resistance and bone structure in nondiabetic postmenopausal women[J]. J Clin Endocrinol Metab, 2016, 101( 8): 3114- 3122. DOI: 10.1210/jc.2016-1726.
[4]	National Workshop on Fatty Liver and Alcoholic Liver Disease, Chinese Society of Hepatology. Guidelines for management of nonalcoholic fatty liver disease[J]. J Clin Hepatol, 2010, 26( 2): 120- 124. 中华医学会肝脏病学分会脂肪肝和酒精性肝病学组. 非酒精性脂肪性肝病诊疗指南[J]. 临床肝胆病杂志, 2010, 26( 2): 120- 124.
[5]	JIN R, WANG XX, LIU F, et al. Research advances in pharmacotherapy for nonalcoholic fatty liver disease[J]. J Clin Hepatol, 2022, 38( 7): 1634- 1640. DOI: 10.3969/j.issn.1001-5256.2022.07.033. 靳睿, 王晓晓, 刘峰, 等. 非酒精性脂肪性肝病的药物治疗进展[J]. 临床肝胆病杂志, 2022, 38( 7): 1634- 1640. DOI: 10.3969/j.issn.1001-5256.2022.07.033.
[6]	PAN BJ, CAI J, ZHAO PP, et al. Relationship between prevalence and risk of osteoporosis or osteoporotic fracture with non-alcoholic fatty liver disease: A systematic review and meta-analysis[J]. Osteoporos Int, 2022, 33( 11): 2275- 2286. DOI: 10.1007/s00198-022-06459-y.
[7]	CUI R, SHENG H, RUI XF, et al. Low bone mineral density in Chinese adults with nonalcoholic fatty liver disease[J]. Int J Endocrinol, 2013, 2013: 396545. DOI: 10.1155/2013/396545.
[8]	MOON SS, LEE YS, KIM SW. Association of nonalcoholic fatty liver disease with low bone mass in postmenopausal women[J]. Endocrine, 2012, 42( 2): 423- 429. DOI: 10.1007/s12020-012-9639-6.
[9]	UPALA S, JARUVONGVANICH V, WIJARNPREECHA K, et al. Nonalcoholic fatty liver disease and osteoporosis: A systematic review and meta-analysis[J]. J Bone Miner Metab, 2017, 35( 6): 685- 693. DOI: 10.1007/s00774-016-0807-2.
[10]	MANTOVANI A, DAURIZ M, GATTI D, et al. Systematic review with meta-analysis: Non-alcoholic fatty liver disease is associated with a history of osteoporotic fractures but not with low bone mineral density[J]. Aliment Pharmacol Ther, 2019, 49( 4): 375- 388. DOI: 10.1111/apt.15087.
[11]	KAYA M, IŞıK D, BEŞTAŞ R, et al. Increased bone mineral density in patients with non-alcoholic steatohepatitis[J]. World J Hepatol, 2013, 5( 11): 627- 634. DOI: 10.4254/wjh.v5.i11.627.
[12]	VACHLIOTIS ID, ANASTASILAKIS AD, GOULAS A, et al. Nonalcoholic fatty liver disease and osteoporosis: A potential association with therapeutic implications[J]. Diabetes Obes Metab, 2022, 24( 9): 1702- 1720. DOI: 10.1111/dom.14774.
[13]	MARCUCCI G, DOMAZETOVIC V, NEDIANI C, et al. Oxidative stress and natural antioxidants in osteoporosis: Novel preventive and therapeutic approaches[J]. Antioxidants(Basel), 2023, 12( 2): 373. DOI: 10.3390/antiox12020373.
[14]	SHI Y, LIU XY, JIANG YP, et al. Monotropein attenuates oxidative stress via Akt/mTOR-mediated autophagy in osteoblast cells[J]. Biomed Pharmacother, 2020, 121: 109566. DOI: 10.1016/j.biopha.2019.109566.
[15]	SUN S, XU MH, ZHUANG PJ, et al. Effect and mechanism of vitamin D activation disorder on liver fibrosis in biliary atresia[J]. Sci Rep, 2021, 11: 19883. DOI: 10.1038/s41598-021-99158-3.
[16]	DRAPKINA OM, ELKINA AY, SHEPTULINA AF, et al. Non-alcoholic fatty liver disease and bone tissue metabolism: Current findings and future perspectives[J]. Int J Mol Sci, 2023, 24( 9): 8445. DOI: 10.3390/ijms24098445.
[17]	LIU W, YUAN J, SU ZY, et al. Relationship between bone metabolism and insulin resistance in male type 2 diabetes mellitus patients from community with different body mass indexes[J]. J Clin Intern Med, 2018, 35( 3): 173- 176. DOI: 10.3969/j.issn.1001-9057.2018.03.009. 刘薇, 原晶, 苏志燕, 等. 不同体重指数的社区男性2型糖尿病患者骨代谢与胰岛素抵抗的相关性研究[J]. 临床内科杂志, 2018, 35( 3): 173- 176. DOI: 10.3969/j.issn.1001-9057.2018.03.009.
[18]	ZENG R, HUANG SY, LIAO SB. Study on the influential factors of lumbar osteoporosis in postmenopausal women with type 2 diabetes mellitus[J]. Chin J Osteoporos, 2021, 27( 11): 1620- 1625. DOI: 10.3969/j.issn.1006-7108.2021.11.012. 曾荣, 黄淑玉, 廖世波. 绝经后女性2型糖尿病患者腰椎骨质疏松的影响因素研究[J]. 中国骨质疏松杂志, 2021, 27( 11): 1620- 1625. DOI: 10.3969/j.issn.1006-7108.2021.11.012.
[19]	GAO M, LI SL. The research progress in the relationship between serum uric acid and osteoporosis[J]. Chin J Osteoporos, 2016, 22( 5): 641- 646. DOI: 10.3969/j.issn.1006-7108.2016.05.026. 高萌, 李社莉. 血尿酸与骨质疏松症关系的研究进展[J]. 中国骨质疏松杂志, 2016, 22( 5): 641- 646. DOI: 10.3969/j.issn.1006-7108.2016.05.026.
[20]	ZHAO N, LI SM, FANG XX, et al. Study of the relationship between bone mineral density and serum uric acid in senile diabetic patients[J]. Chin J Osteoporos, 2014, 20( 7): 784- 788. DOI: 10.3969/j.issn.1006-7108.2014.07.013. 赵娜, 李素梅, 方星星, 等. 老年糖尿病患者骨密度与血尿酸水平的相关研究[J]. 中国骨质疏松杂志, 2014, 20( 7): 784- 788. DOI: 10.3969/j.issn.1006-7108.2014.07.013.
[21]	ESTEP M, ABAWI M, JARRAR M, et al. Association of obestatin, ghrelin, and inflammatory cytokines in obese patients with non-alcoholic fatty liver disease[J]. Obes Surg, 2011, 21( 11): 1750- 1757. DOI: 10.1007/s11695-011-0475-1.
[22]	YAN DD, WANG J, HOU XH, et al. Association of serum uric acid levels with osteoporosis and bone turnover markers in a Chinese population[J]. Acta Pharmacol Sin, 2018, 39( 4): 626- 632. DOI: 10.1038/aps.2017.165.
[23]	HAN W, BAI XJ, WANG N, et al. Association between lumbar bone mineral density and serum uric acid in postmenopausal women: A cross-sectional study of healthy Chinese population[J]. Arch Osteoporos, 2017, 12( 1): 50. DOI: 10.1007/s11657-017-0345-0.
[24]	ZHANG BW, LEI T. Obesity and osteoporosis[J]. Int J Endocrinol Metab, 2010, 30( 4): 242- 244. DOI: 10.3760/cma.j.issn.1673-4157.2010.04.008. 张宝伟, 雷涛. 肥胖与骨质疏松[J]. 国际内分泌代谢杂志, 2010, 30( 4): 242- 244. DOI: 10.3760/cma.j.issn.1673-4157.2010.04.008.
[25]	ASPRAY TJ, HILL TR. Osteoporosis and the ageing skeleton[J]. Subcell Biochem, 2019, 91: 453- 476. DOI: 10.1007/978-981-13-3681-2_16.
[26]	FENG C, XU ZW, TANG XJ, et al. Estrogen-related receptor α: A significant regulator and promising target in bone homeostasis and bone metastasis[J]. Molecules, 2022, 27( 13): 3976. DOI: 10.3390/molecules27133976.
[27]	MA YZ, WANG YP, LIU Q, et al. 2018 China guideline for the diagnosis and treatment of senile osteoporosis[J]. Chin J Gerontol, 2019, 39( 11): 2557- 2575. DOI: 10.3969/j.issn.1005-9202.2019.11.001. 马远征, 王以朋, 刘强, 等. 中国老年骨质疏松诊疗指南(2018)[J]. 中国老年学杂志, 2019, 39( 11): 2557- 2575. DOI: 10.3969/j.issn.1005-9202.2019.11.001.

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Association between nonalcoholic fatty liver disease and osteoporosis in elderly patients

DOI: 10.12449/JCH240813

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