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Association Between Low Muscle Mass and Non-alcoholic Fatty Liver Disease Diagnosed Using Ultrasonography, Magnetic Resonance Imaging Derived Proton Density Fat Fraction, and Comprehensive NAFLD Score in Korea
Hun Ju Lee, Jae Seung Chang, Jhii Hyun Ahn, Moon Young Kim, Kyu-Sang Park, Yeon-Soon Ahn, Sang Baek Koh
J Prev Med Public Health. 2021;54(6):412-421.   Published online October 22, 2021
DOI: https://doi.org/10.3961/jpmph.21.387
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  • 4 Web of Science
  • 5 Crossref
AbstractAbstract AbstractSummary PDFSupplementary Material
Objectives
Non-alcoholic fatty liver disease (NAFLD) is an increasingly prevalent metabolic disease. Muscle is known to influence NAFLD development. Therefore, this study aimed to determine the relationships among low muscle mass, NAFLD, and hepatic fibrosis using various definitions of low muscle mass and NAFLD diagnostic methods, including magnetic resonance imaging-based proton density fat fraction (MRI-PDFF).
Methods
This cross-sectional study included 320 participants (107 males, 213 females) from the Korean Genome and Epidemiology Study on Atherosclerosis Risk of Rural Areas in the Korean General Population cohort. Muscle mass was assessed using whole-body dual-energy X-ray absorptiometry and adjusted for the height squared, body weight, and body mass index (BMI). NAFLD was diagnosed using ultrasonography (US), MRI-PDFF, and the comprehensive NAFLD score (CNS). Hepatic fibrosis was assessed using magnetic resonance elastography. Multivariable logistic and linear regression analyses were performed to determine the aforementioned associations.
Results
According to US, 183 participants (57.2%) had NAFLD. Muscle mass adjusted for body weight was associated with NAFLD diagnosed using US (odds ratio [OR], 3.00; 95% confidence interval [CI], 1.70 to 5.31), MRI-PDFF (OR, 2.00; 95% CI, 1.13 to 3.53), and CNS (OR, 3.39; 95% CI, 1.73 to 6.65) and hepatic fibrosis (males: β=-0.070, p<0.01; females: β=-0.037, p<0.04). Muscle mass adjusted for BMI was associated with NAFLD diagnosed by US (OR, 1.71; 95% CI, 1.02 to 2.86) and CNS (OR, 1.95; 95% CI, 1.04 to 3.65), whereas muscle mass adjusted for height was not associated with NAFLD.
Conclusions
Low muscle mass was associated with NAFLD and liver fibrosis; therefore, maintaining sufficient muscle mass is important to prevent NAFLD. A prospective study and additional consideration of muscle quality are needed to strengthen the findings regarding this association.
Summary
Korean summary
비알콜성 간질환은 대사질환 중 하나로 적은 근육양과의 연관성이 지속적으로 제시되었으나, 기존 연구들에서 일관되지 않은 결과를 보여주었다. KoGES-ARIRANG 코호트의 320명을 대상으로 초음파·MRI-PDFF·CNS 진단기준을 사용하여 단면연구를 수행한 결과, 세 진단기준에서 모두 적은 근육량과 비알콜성 간질환 사이에 연관성이 나타났다.

Citations

Citations to this article as recorded by  
  • Prevalence of Sarcopenia and Its Defining Components in Non-alcoholic Fatty Liver Disease Varies According to the Method of Assessment and Adjustment: Findings from the UK Biobank
    Christine L. Freer, Elena S. George, Sze-Yen Tan, Gavin Abbott, David Scott, Robin M. Daly
    Calcified Tissue International.2024; 114(6): 592.     CrossRef
  • Prevalence and outcome of sarcopenia in non-alcoholic fatty liver disease
    Suprabhat Giri, Prajna Anirvan, Sumaswi Angadi, Ankita Singh, Anurag Lavekar
    World Journal of Gastrointestinal Pathophysiology.2024;[Epub]     CrossRef
  • Association between Regional Body Muscle Mass and Non-Alcoholic Fatty Liver Disease: An Observational Study Using Data from the REACTION Study
    Jing Du, Shizhan Ma, Li Fang, Meng Zhao, Zhongshang Yuan, Yiping Cheng, Jiajun Zhao, Xiude Fan, Qingling Guo, Zhongming Wu
    Journal of Personalized Medicine.2023; 13(2): 209.     CrossRef
  • Predicting Habitual Use of Wearable Health Devices Among Middle-aged Individuals With Metabolic Syndrome Risk Factors in South Korea: Cross-sectional Study
    Jaeyoung Ha, Jungmi Park, Sangyi Lee, Jeong Lee, Jin-Young Choi, Junhyoung Kim, Sung-il Cho, Gyeong-Suk Jeon
    JMIR Formative Research.2023; 7: e42087.     CrossRef
  • Osteosarcopenia in NAFLD/MAFLD: An Underappreciated Clinical Problem in Chronic Liver Disease
    Alessandra Musio, Federica Perazza, Laura Leoni, Bernardo Stefanini, Elton Dajti, Renata Menozzi, Maria Letizia Petroni, Antonio Colecchia, Federico Ravaioli
    International Journal of Molecular Sciences.2023; 24(8): 7517.     CrossRef
Relationship Between Non-alcoholic Fatty Liver Disease and Decreased Bone Mineral Density: A Retrospective Cohort Study in Korea
Jisun Sung, Seungho Ryu, Yun-Mi Song, Hae-Kwan Cheong
J Prev Med Public Health. 2020;53(5):342-352.   Published online July 17, 2020
DOI: https://doi.org/10.3961/jpmph.20.089
  • 3,791 View
  • 143 Download
  • 9 Crossref
AbstractAbstract PDF
Objectives
The aim of this retrospective cohort study was to investigate whether non-alcoholic fatty liver disease (NAFLD) was associated with incident bone mineral density (BMD) decrease.
Methods
This study included 4536 subjects with normal BMD at baseline. NAFLD was defined as the presence of fatty liver on abdominal ultrasonography without significant alcohol consumption or other causes. Decreased BMD was defined as a diagnosis of osteopenia, osteoporosis, or BMD below the expected range for the patient’s age based on dual-energy X-ray absorptiometry. Cox proportional hazards models were used to estimate the hazard ratio of incident BMD decrease in subjects with or without NAFLD. Subgroup analyses were conducted according to the relevant factors.
Results
Across 13 354 person-years of total follow-up, decreased BMD was observed in 606 subjects, corresponding to an incidence of 45.4 cases per 1000 person-years (median follow-up duration, 2.1 years). In the model adjusted for age and sex, the hazard ratio was 0.65 (95% confidence interval, 0.51 to 0.82), and statistical significance disappeared after adjustment for body mass index (BMI) and cardiometabolic factors. In the subgroup analyses, NAFLD was associated with a lower risk of incident BMD decrease in females even after adjustment for confounders. The direction of the effect of NAFLD on the risk of BMD decrease changed depending on BMI category and body fat percentage, although the impact was statistically insignificant.
Conclusions
NAFLD had a significant protective effect on BMD in females. However, the effects may vary depending on BMI category or body fat percentage.
Summary

Citations

Citations to this article as recorded by  
  • Anti-osteoporotic treatments in the era of non-alcoholic fatty liver disease: friend or foe
    Maria Eleni Chondrogianni, Ioannis Kyrou, Theodoros Androutsakos, Christina-Maria Flessa, Evangelos Menenakos, Kamaljit Kaur Chatha, Yekaterina Aranan, Athanasios G. Papavassiliou, Eva Kassi, Harpal S. Randeva
    Frontiers in Endocrinology.2024;[Epub]     CrossRef
  • Association between body fat and bone mineral density in Korean adults: a cohort study
    Hyunjung Yoon, Eunju Sung, Jae-Heon Kang, Cheol-Hwan Kim, Hocheol Shin, Eunsol Yoo, Minyoung Kim, Mi Yeon Lee, Sujeong Shin
    Scientific Reports.2023;[Epub]     CrossRef
  • Liver fibrosis is associated with impaired bone mineralization and microstructure in obese individuals with non-alcoholic fatty liver disease
    Ilaria Barchetta, Carla Lubrano, Flavia Agata Cimini, Sara Dule, Giulia Passarella, Arianna Dellanno, Alberto Di Biasio, Frida Leonetti, Gianfranco Silecchia, Andrea Lenzi, Maria Gisella Cavallo
    Hepatology International.2023; 17(2): 357.     CrossRef
  • Non-Alcoholic Fatty Liver Disease and Bone Tissue Metabolism: Current Findings and Future Perspectives
    Oxana M. Drapkina, Anastasia Yu. Elkina, Anna F. Sheptulina, Anton R. Kiselev
    International Journal of Molecular Sciences.2023; 24(9): 8445.     CrossRef
  • Nonalcoholic Fatty Liver Disease Is Associated With Decreased Bone Mineral Density in Adults: A Systematic Review and Meta‐Analysis
    Ying‐Hao Su, Kuo‐Liong Chien, Shu‐Hua Yang, Wei‐Tso Chia, Jen‐Hau Chen, Yen‐Ching Chen
    Journal of Bone and Mineral Research.2023; 38(8): 1092.     CrossRef
  • The National Consensus statement on the management of adult patients with non-alcoholic fatty liver disease and main comorbidities
    Marina V. Maevskaya, Yulia V. Kotovskaya, Vladimir T. Ivashkin, Olga N. Tkacheva, Ekaterina A. Troshina, Marina V. Shestakova, Valeriy V. Breder, Natalia I. Geyvandova, Vladimir L. Doshchitsin, Ekaterina N. Dudinskaya, Ekaterina V. Ershova, Khava B. Kodzo
    Terapevticheskii arkhiv.2022; 94(2): 216.     CrossRef
  • Nonalcoholic fatty liver disease and osteoporosis: A potential association with therapeutic implications
    Ilias D. Vachliotis, Athanasios D. Anastasilakis, Antonis Goulas, Dimitrios G. Goulis, Stergios A. Polyzos
    Diabetes, Obesity and Metabolism.2022; 24(9): 1702.     CrossRef
  • Hepatic fibrosis is associated with an increased rate of decline in bone mineral density in men with nonalcoholic fatty liver disease
    Ji Won Yoon, Min Joo Kim, Goh-Eun Chung, Jong In Yang, Jeong Yoon Yim, Jin Ju Kim, Sun Mie Kim, Min-Sun Kwak
    Hepatology International.2021; 15(6): 1347.     CrossRef
  • NAFLD Associated Comorbidity
    L. B. Lazebnik, S. V. Turkina
    Experimental and Clinical Gastroenterology.2021; (10): 5.     CrossRef
Comparison of Computed Tomography-based Abdominal Adiposity Indexes as Predictors of Non-alcoholic Fatty Liver Disease Among Middle-aged Korean Men and Women
Jongmin Baek, Sun Jae Jung, Jee-Seon Shim, Yong Woo Jeon, Eunsun Seo, Hyeon Chang Kim
J Prev Med Public Health. 2020;53(4):256-265.   Published online June 18, 2020
DOI: https://doi.org/10.3961/jpmph.20.140
  • 5,003 View
  • 164 Download
  • 3 Crossref
AbstractAbstract PDFSupplementary Material
Objectives
We compared the associations of 3 computed tomography (CT)-based abdominal adiposity indexes with non-alcoholic fatty liver disease (NAFLD) among middle-aged Korean men and women.
Methods
The participants were 1366 men and 2480 women community-dwellers aged 30-64 years. Three abdominal adiposity indexes—visceral fat area (VFA), subcutaneous fat area (SFA), and visceral-to-subcutaneous fat ratio (VSR)—were calculated from abdominal CT scans. NAFLD was determined by calculating the Liver Fat Score from comorbidities and blood tests. An NAFLD prediction model that included waist circumference (WC) as a measure of abdominal adiposity was designated as the base model, to which VFA, SFA, and VSR were added in turn. The area under the receiver operating characteristic curve (AUC), integrated discrimination improvement (IDI), and net reclassification improvement (NRI) were calculated to quantify the additional predictive value of VFA, SFA, and VSR relative to WC.
Results
VFA and VSR were positively associated with NAFLD in both genders. SFA was not significantly associated with NAFLD in men, but it was negatively associated in women. When VFA, SFA, and VSR were added to the WC-based NAFLD prediction model, the AUC improved by 0.013 (p<0.001), 0.001 (p=0.434), and 0.009 (p=0.007) in men and by 0.044 (p<0.001), 0.017 (p<0.001), and 0.046 (p<0.001) in women, respectively. The IDI and NRI were increased the most by VFA in men and VSR in women.
Conclusions
Using CT-based abdominal adiposity indexes in addition to WC may improve the detection of NAFLD. The best predictive indicators were VFA in men and VSR in women.
Summary

Citations

Citations to this article as recorded by  
  • Relationship between Non-Alcoholic Fatty Liver Disease and Visceral Fat Measured by Imaging-Based Body Composition Analysis: A Systematic Review
    Ker Ming Seaw, Christiani Jeyakumar Henry, Xinyan Bi
    Livers.2023; 3(3): 463.     CrossRef
  • Stratifying the risk of ovarian cancer incidence by histologic subtypes in the Korean Epithelial Ovarian Cancer Study (Ko‐EVE)
    Soseul Sung, Youjin Hong, Byoung‐Gie Kim, Ji‐Yeob Choi, Jae Weon Kim, Sang‐Yoon Park, Jae‐Hoon Kim, Yong‐man Kim, Jong‐Min Lee, Tae Jin Kim, Sue K. Park
    Cancer Medicine.2023; 12(7): 8742.     CrossRef
  • Correlation between CT Abdominal Anthropometric Measurements and Liver Density in Individuals with Non-Alcoholic Fatty Liver Disease
    Dragoș Constantin Cucoranu, Marian Pop, Raluca Niculescu, Vlad Vunvulea, Irina-Bianca Kosovski, Radu-Ovidiu Togănel, Eliza Russu, Adrian Vasile Mureșan, Răzvan-Andrei Licu, Anca Bacârea
    Medicina.2023; 59(3): 500.     CrossRef
A Cohort Study on Risk Factors for Chronic Liver Disease: Analytic Strategies Excluding Potentially Incident Subjects.
Moo Song Lee, Dae Sung Kim, Dong Hyun Kim, Jong Myun Bae, Myung Hee Shin, Yoon Ok Ahn
Korean J Prev Med. 1999;32(4):452-458.
  • 2,093 View
  • 27 Download
AbstractAbstract PDF
OBJECTIVES
The authors conducted the study to evaluate bias when potentially diseased subjects were included in cohort members while analyzing risk factors of chronic liver diseases. METHODS: Total of 14,529 subjects were followed up for the incidence of liver diseases from January 1993 to June 1997. We have used databases of insurance company with medical records, cancer registry, and death certificate data to identify 102 incident cases. The cohort members were classified into potentially diseased group(n=2,217) when they were HBsAg positive, serum GPT levels higher than 40 units, or had or has liver diseases in baseline surveys. Cox' model were used for potentially diseased group, other members, and total subjects, respectively. RESULTS: The risk factors profiles were similar for total and potentially diseased subjects: HBsAg positivity, history of acute liver disease, and recent quittance of smoking or drinking increased the risk, while intake of pork and coffee decreased it. For the potentially diseased, obesity showed marginally significant protective effect. Analysis of subjects excluding the potentially diseased showed distinct profiles: obesity increased the risk, while quitting smoking or drinking had no association. For these intake of raw liver or processed fish or soybean paste stew increased risk; HBsAg positivity, higher levels of liver enzymes and history of acute liver diseases increased the risk. CONCLUSIONS: The results suggested the potential bias in risk ratio estimates when potentially diseased subjects were included in cohort study on chronic liver diseases, especially for lifestyles possibly modified after disease onset. The analytic strategy excluding potentially diseased subjects was considered appropriate for identifying risk factors for chronic liver diseases.
Summary
A Case-Control Study of Primary Liver Cancer and Liver Disease History.
Dong Hyun Kim, Byung Joo Park, Keun Young Yoo, Yoon Ok Ahn, Hyo Suk Lee, Chung Yong Kim, Sang Il Lee, Moo Song Lee, Hyung Sik Ahn, Heon Kim, Tae Soo Park
Korean J Prev Med. 1994;27(2):217-225.
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  • 20 Download
AbstractAbstract PDF
The relationship between past liver disease history and the risk of primary liver cancer was analyzed in a hospital-based case-control study conducted in Seoul on 165 patients with histologically or serologically confirmed hepatocellular carcinoma and individually age-and sex-matched 165 controls in hospital for ophthalmologic, ontologic, or nasopharyngeal problems. Significant association were observed for liver diseases occurring 5 or more years before liver cancer diagnosis[OR, 4.9;97% confidence interval(CI), 1.6~14.0) and family history of liver disease(OR, 9.0;95% CI, 2.1~38.8). These associations were mot appreciably modified by allowance for major identified potential confounding factors, From these results, it is possible to speculate that liver cell injuries caused by Considering the significant effect of family history of liver diseases on PLCA risk after adjusting past liver disease history, there might be genetic susceptibility in the carcinogenic mechanism of liver cancer. Further investigations are needed to clarify the effect of family history of liver disease on PLCA risk.
Summary
A Study on the Status of Seeking Intervention among the Workers with Health Problems Identified by the Workers' Periodic Health Examination.
Hee Kwan Cheong, Joung Soon Kim, Ok Ryun Moon, Hyun Sul Lim
Korean J Prev Med. 1992;25(4):343-356.
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AbstractAbstract PDF
Authors studied the workers' knowledge about the health problems detected through the previous workers' periodic health examination, content of follow-up management and actions taken for their health problem detected on previous health examination. From June to September 1992, workers' periodic health examination was performed on workers employed in 10 companies located in 2 middle-sized Korean cities. A questionnaire survey was done for 150 workers who reported to have D2 result of either hypertension or liver disorder at the previous workers' periodic health examination done in 1991. The results are as follows; 1. Of 160 workers who had D2 result of either hypertension or liver disorder in previous examination one year before, only 85 workers(51.3%, 43 workers with hypertension, 38 workers with live disorder) responded that they have such disorders. The other 65 workers responded to questionnaire were all those with C results. Respondents' knowledge about their diagnoses was relatively precise (95.2% in hypertension group, 94.6% in liver disorder group) but knowledge about classification of diseases was poor. 2. The main efforts to solve the health problem was self management (26 spells, 55.3%), visiting clinic or hospital (6 spells, 12.8%), use of herb medicine (2 spells, 4.3%) and use of drug store (2 spells, 4.3%) in hypertension group. In liver disorder group, 30 spells (71.4%) relied on self management, 6 spells (14.3%) on hospital or clinic and 9 spells (21.4%) had no effort to improve the health problem. Content of self management was low salt diet, quit smoking, regular exercise and quit alcohol drinking in order. Avoidance of salt in diet was high in hypertension group and quitting alcohol drinking was high in liver disorder group. In those with self management, 80.7% of hypertension group and 83.3% of liver disorder group continued previous effort. Those, however, who utilized clinic or hospital, only 16.7% and 50.0% were still visiting hospital or clinic. 3. Fifty seven percent of hypertension group and 64.3% of liver disorder group was presently smoking, 8.5% and 11.9% reduced smoking and 21.3% and 14.3% stopped smoking. Forty nine percent of hypertension group and 28.6% of liver disorder group was presently drinking. Reduced alcohol intake was reported in 29.8% and 40.5%, 12.8% and 23.8% stopped alcohol drinking. Sixty six percent of hypertension group and 73.8% of liver disorder group did no regular exercise, but 12.8% and 11.9% of each group increased their physical exercise for last one year. Forty three percent of hypertension group and 38.1% of liver disorder group was overweight (defined by bodymass index greater or equal than 25). Reduced body weight was reported in 17.2% and 16.7% of each group. Reduced dietary salt intake was high in hypertension group (51.5%). The study results suggest that follow-up management after workers' periodic health examination is not satisfactory. In order to improve this situation, adequate information on the result of the workers' periodic health examination should be distributed to each worker group with health education and counselling.
Summary

JPMPH : Journal of Preventive Medicine and Public Health