Editorial Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Feb 21, 2024; 30(7): 636-643
Published online Feb 21, 2024. doi: 10.3748/wjg.v30.i7.636
Muscle strength and non-alcoholic fatty liver disease/metabolic-associated fatty liver disease
Xuan-Yu Hao, Kai Zhang, Xing-Yong Huang, Fei Yang, Department of Gastroenterology, Endoscopic Center, Shengjing Hospital of China Medical University, Shenyang 110004, Liaoning Province, China
Si-Yu Sun, Department of Gastroenterology, Endoscopic Center, Engineering Research Center of Ministry of Education for Minimally Invasive Gastrointestinal Endoscopic Techniques, Shengjing Hospital of China Medical University, Shenyang 110004, Liaoning Province, China
ORCID number: Xuan-Yu Hao (0000-0003-0880-2633); Kai Zhang (0000-0002-0355-3415); Xing-Yong Huang (0009-0002-0620-3645); Fei Yang (0000-0001-7550-8675); Si-Yu Sun (0000-0002-7308-0473).
Author contributions: Sun SY and Zhang K were involved in the study conception and design; Hao XY, Zhang K, Huang XY and Yang F wrote the manuscript; Sun SY performed critical revision of the article for important intellectual content; all authors approved the final version of the article.
Supported by National Natural Science Foundation of China, No. 82000625; and the Doctoral Scientific Research Foundation of Liaoning Province, No. 2020-BS-109.
Conflict-of-interest statement: The authors declare that there are no conflicts of interest.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Si-Yu Sun, MD, PhD, Chief Doctor, Director, Professor, Department of Gastroenterology, Endoscopic Center, Engineering Research Center of Ministry of Education for Minimally Invasive Gastrointestinal Endoscopic Techniques, Shengjing Hospital of China Medical University, No. 36 Sanhao Street, Shenyang 110004, Liaoning Province, China. sun-siyu@163.com
Received: December 5, 2023
Peer-review started: December 5, 2023
First decision: December 7, 2023
Revised: December 12, 2023
Accepted: January 22, 2024
Article in press: January 22, 2024
Published online: February 21, 2024

Abstract

This editorial comments on an article published in a recent issue of World Journal of Gastroenterology, entitled “Association of low muscle strength with metabolic dysfunction-associated fatty liver disease: A nationwide study”. We focused on the association between muscle strength and the incidence of non-alcoholic fatty liver disease (NAFLD) and metabolic-associated fatty liver disease (MAFLD), as well as the mechanisms underlying the correlation and related clinical applications. NAFLD, which is now redefined as MAFLD, is one of the most common chronic liver diseases globally with an increasing prevalence and is characterized by malnutrition, which may contribute to decreased muscle strength. Reduction of muscle strength reportedly has a pathogenesis similar to that of NAFLD/ MAFLD, including insulin resistance, inflammation, sedentary behavior, as well as insufficient vitamin D. Multiple studies have focused on the relationship between sarcopenia or muscle strength and NAFLD. However, studies investigating the relationship between muscle strength and MAFLD are limited. Owing to the shortage of specific medications for NAFLD/MAFLD treatment, early detection is essential. Furthermore, the relationship between muscle strength and NAFLD/MAFLD suggests that improvements in muscle strength may have an impact on disease prevention and may provide novel insights into treatments including dietary therapy, as well as tailored physical activity.

Key Words: Muscle strength, Non-alcoholic fatty liver disease, Metabolic-associated fatty liver disease, Sarcopenia, Insulin resistance, Inflammation

Core Tip: The relationship between muscle strength and the incidence of non-alcoholic fatty liver disease (NAFLD) and metabolic-associated fatty liver disease (MAFLD), as well as the mechanisms underlying the correlation and related clinical applications were discussed. Muscle strength may play an imperative role in the incidence and development of NAFLD/MAFLD and interventions to improve muscle strength in the management of NAFLD/MAFLD may provide novel insights into the treatment of these diseases.



INTRODUCTION

As an imperative component of human health and a crucial predictor of physical function, muscle strength has drawn great interest in the areas of disease prediction and treatment[1,2]. Non-alcoholic fatty liver disease (NAFLD), recently renamed metabolic-associated fatty liver disease (MAFLD), with liver biopsy as the gold standard for diagnosis, is a common chronic liver disease, and its prevalence is still increasing, representing a global healthcare burden[3,4]. NAFLD/ MAFLD is characterized by malnutrition, which may contribute to decreased muscle mass, strength, and sarcopenia[5,6]. NAFLD encompasses a broad disease spectrum ranging from non-alcoholic fatty liver to cirrhosis, which is a representative cause of sarcopenia due to protein and energy metabolic disorders[7,8].

Sarcopenia is now defined as low muscle strength combined with low muscle quantity or quality with or without poor physical performance after revision by the European Working Group on Sarcopenia in Older People 2[9]. However, the measurements for diagnosis of sarcopenia differs according to clinical practice and research. In addition, some studies have utilized the previous definition of sarcopenia, which focused only on decreased muscle mass and not on low muscle strength. Multiple studies have focused on the association between sarcopenia or muscle strength and NAFLD; however, studies on the relationship between muscle strength and MAFLD are rare. As the primary parameter for sarcopenia in the updated definition, decreased muscle strength has also been suggested as a better predictor of mortality and poor disease outcomes than has muscle mass in previous studies[9-11]. Thus, further exploration of the association between low muscle strength and NAFLD/MAFLD is necessary. Muscle strength is usually measured using grip strength, which is noninvasive, low-cost, uncomplicated, and has been validated reliably in research and clinical practice[12]. Lower limb strength can also be measured when grip strength is not available[13].

MUSCLE STRENGTH AND NAFLD/MAFLD

In a recent issue of World Journal of Gastroenterology, Lee et al[14] published an absorbing article titled “Association of low muscle strength with metabolic dysfunction-associated fatty liver disease: A nationwide study”. This study verified a significant relationship between muscle strength and MAFLD in the general Korean population. The present cross-sectional study examined 31649 participants aged ≥ 19 years who took part in the Korea National Health and Nutrition Examination Survey between 2015 and 2018. Of the enrolled participants, 29.3% had MAFLD diagnosed using the hepatic steatosis index and the presence of metabolic risk factors. The muscle strength of the participants was defined by relative handgrip strength and divided into quartiles. Multivariate logistic regression analysis revealed that the prevalence of MAFLD was higher in the lower muscle strength quartiles. The lowest quartile exhibited a 3.12-fold increased risk of MAFLD compared to that in the highest quartile. A significantly elevated odds ratio for MAFLD was also observed in the lower muscle strength quartiles in a dose-dependent manner. These associations persisted across all subgroups, including age, obesity, and diabetes mellitus. Patients with MAFLD in the highest quartile also had increased risks of severe liver fibrosis compared to those in the other quartiles. The study indicated that decreased muscle strength was related to a dose-dependent higher risk of MAFLD as well as to a high probability of liver fibrosis in participants with MAFLD.

Studies that have explored the association between muscle strength and NAFLD are presented in Table 1. The relationship between NAFLD and low muscle strength was demonstrated in a cross-sectional study by Gan et al[15]. The occurrence of NAFLD was higher in the sarcopenic state, and this risk was further elevated if obesity was present. The results also showed that low muscle strength, measured using weight-adjusted handgrip strength, was positively, independently, and significantly associated with NAFLD. An association between low muscle strength and increased incidence of NAFLD has been detected in the Korean population[16-19]. Similar findings have been validated in the Chinese population and HIV-infected men in Italy, as well as in the male patients diagnosed with type 2 diabetes mellitus[20-23]. Further, low muscle strength was related to a higher incidence of severe NAFLD in a prospective study using data derived from the UK Biobank[24]. These results indicated that lower muscle strength was significantly associated with an increased incidence of severe NAFLD. In another study by Kang et al[25], decreased muscle strength was independently related to the incidence and progression of NAFLD in a Korean population. Additionally, grip strength was inversely associated with NAFLD severity in a United States population[26,27]. Furthermore, higher muscle strength was independently related to lower all-cause and cardiovascular mortality after full adjustment in patients with NAFLD in a United States population[28]. Muscle strength was independently associated with long-term all-cause mortality in participants with NAFLD in a study conducted in Thailand[29]. However, few studies have compared the predictive value of muscle strength in NAFLD and MAFLD.

Table 1 Studies fucus on the relationship between muscle strength and non-alcoholic fatty liver disease.
Ref.
Study design
Subjects
Sample size and gender [female; n (%)]
Mean age (yr)
Strength position/measures
Outcome
Gan et al[15], 2020Cross-sectional studyGeneral adults in China3536 (71.3)51.72 for participants without NAFLD/55.2 for participants with NAFLDHandgrip strength (kg)/electronic hand dynamometerIncidence of NAFLD
Lee et al[16], 2018Cross-sectional studyGeneral adults in Korea8001 (55.5)49.9Handgrip strength (kg)/digital grip strength dynamometerIncidence of NAFLD
Kim et al[17], 2019Cross-sectional studyMen aged ≥ 50 yr and postmenopausal women in Korea4103 (53.8)61.9 for men without NAFLD/59.5 for men with NAFLD/61.8 for women without NAFLD/62 for women with NAFLDHandgrip strength (kg)/digital grip strength dynamometerIncidence of NAFLD
Cho et al[18], 2021Cross-sectional studyMiddle-aged adults in Korea5272 (68.2)57.1Handgrip strength (kg)/digital grip strength dynamometerIncidence of NAFLD
Lee et al[19], 2022Cross-sectional studyGeneral adults in Korea19852 (62.5)45.8 for men/48.3 for womenHandgrip strength (kg)/digital grip strength dynamometerIncidence of NAFLD
Debroy et al[20], 2019Cross-sectional studyAdults living with HIV and receiving treatment in Italy169 (0)56.8Handgrip strength (kg)/handheld dynamometerIncidence of NAFLD
Meng et al[21], 2016Cross-sectional studyGeneral adults in China20957(49)41.2Handgrip strength (kg)/electronic hand-grip dynamometerIncidence of NAFLD
Bulur et al[22], 2023Cross-sectional studyMiddle-aged male patients diagnosed with type 2 diabetes mellitus145 (0)55.2hand muscle strength (kg)/hydraulic dynamometerIncidence of NAFLD
Wang et al[23], 2021Cross-sectional studySenior hospital staff in China578 (84.1)72.9 for men without NAFLD/68.9 for men with NAFLD/62.9 for women without NAFLD/67.5 for women with NAFLDHandgrip strength (kg)/hydraulic hand dynamometerIncidence of NAFLD
Petermann-Rocha et al[24], 2022prospective studyGeneral adults in Scotland, England and Wales333295 (55)56.6Handgrip strength (kg)/hydraulic hand dynamometerIncidence of severe NAFLD
Kang et al[25], 2020Cross-sectional studyGeneral adults in Korea13502 (57.6)45.6Handgrip strength (kg)/digital grip strength dynamometerIncidence and severity of NAFLD
Park et al[26], 2020Cross-sectional studyGeneral adults in the USA3922 (58.1)45 for men/46.9 for womenHandgrip strength (kg)/digital grip strength dynamometerIncidence and severity of NAFLD
Zhao et al[27], 2023Cross-sectional studyGeneral adults in the USA8888 (50.43)46.07Handgrip strength (kg)/digital grip strength dynamometerIncidence and severity of NAFLD
Kim et al[28], 2023Cross-sectional studyGeneral adults with NAFLD in the USA4655 (46.9)48Handgrip strength (kg)/digital grip strength dynamometerAll-cause and cause-specific mortality in NAFLD
Charatcharoenwitthaya et al[29], 2022Observational studyGeneral adults with NAFLD in the Thailand7083 (69.4)49.3Handgrip strength (kg)/digital dynamometerAll-cause mortality in NAFLD
POTENTIAL MECHANISM FOR THE RELATIONSHIP BETWEEN MUSCLE STRENGTH AND NAFLD/MAFLD

The potential mechanisms that may explain the relationship between muscle strength, NAFLD/MAFLD, and cirrhosis have yet to be explored. Insulin resistance may play a crucial role in the inverse relationship between muscle strength and NAFLD/MAFLD. Skeletal muscle is the primary target organ of insulin-stimulated glucose disposal; therefore, a reduction in muscle strength may exacerbate insulin resistance, which is a crucial pathogenic component of NAFLD/MAFLD, through hepatic fat accumulation, inflammation, and energy metabolism alteration[30-32]. Insulin resistance in turn aggravates proteolysis and itself leads to muscle depletion[33]. Several inflammatory mechanisms related to NAFLD, such as cirrhosis, have been identified[34,35]. As a characteristic of NAFLD, dysfunction of adipocyte lipolysis is suggested to lead to ectopic fat accumulation in hepatic parenchyma as well as skeletal muscle[36,37]. Higher levels of inflammatory markers, including C-reactive protein, interleukin (IL)-6, and tumor necrosis factor-α, observed in populations with lower muscle strength indicated that decreased muscle strength may be associated with NAFLD/MAFLD and cirrhosis based on inflammation[38]. Elevated levels of proinflammatory cytokines may result in muscle degradation by reducing the muscle response to insulin and insulin-like growth factor-1[39]. Alterations in myokines (such as irisin, IL-6, myostatin, and adiponectin) secreted by skeletal muscle may be involved in NAFLD/MAFLD development through their influence on hepatic fat accumulation[40]. A previous study found that decreased muscle strength was related to lower vitamin D levels and that vitamin D supplementation contributed to muscle strength preservation[41,42]. Epidemiological data also support that vitamin D is associated with the incidence of NAFLD and that the vitamin D/vitamin D receptor axis is involved in the modulation of inflammatory and metabolic pathways related to MAFLD[43,44]. Decreased muscle strength is related to physical disability and functional decline as well as sedentary behavior, which is related to the development of NAFLD/MAFLD[45-47].

CLINICAL IMPLICATION

Recovery from decreased muscle strength may decrease complications and improve survival in individuals with fatty liver disease[10,48]. Because sarcopenia is related to nutritional status, dietary therapy based on optimal nutritional intake has been suggested for its treatment in fatty liver disease and cirrhosis[49]. Supplementation with branched-chain amino acids and adequate energy in conjunction with a protein-enriched dietary intake has been recommended for individuals with liver cirrhosis[50]. As a non-pharmacological and innovative strategy, proper physical activity can be effective in recovering lost muscle strength. A previous study illustrated that progressive resistance training could increase muscle strength and improve general performance, including functional exercise capacity, mental health, and body composition, in patients with cirrhosis[51]. Furthermore, implementation of tailored physical activity may improve outcomes in patients awaiting liver transplantation[52]. A recent meta-analysis indicated that combining protein supplementation with resistance training is advisable for optimizing muscle strength[53]. The findings of a cross-sectional study suggested that adherence to an anti-inflammatory nutrient pattern, characterized by a high intake of polyunsaturated fat, monounsaturated fat, copper, vitamin E, and omega-3 fatty acids was associated with reduced odds of low muscle strength, which indicated that anti-inflammatory pattern might be a therapeutic approach for decreased muscle strength[54]. Despite the beneficial impact of physical activity on muscle strength, specific exercise training guidelines for individuals with fatty liver disease and cirrhosis are lacking in terms of the amount, intensity, and forms of exercise in clinical practice[55,56]. Electrical stimulation has also emerged as a popular modality for enhancing muscle strength among athletes and fitness enthusiasts; however, the lack of standardized protocols pertaining to its specific implementation remains a challenge[57].

The correlation between muscle strength and NAFLD/MAFLD might provide a fresh perspective for treatment owing to the lack of specific medications[58]. Although there are no specific pharmacotherapeutic interventions for reduced muscle strength to date, multiple efforts have already been made, including a variety of clinical trials that focused on pharmacological interventions for sarcopenia[59,60]. Several drugs have been investigated for their ability to augment muscle strength based on different molecular targets. Bimagrumab, a fully human monoclonal antibody targeting the MSTN-ActRII pathway, was found to be useful for increasing muscle strength in patients with sarcopenia in phase 2 clinical trials[61]. However, in a clinical trial performed by Rooks et al[62], bimagrumab demonstrated no positive effect on muscle strength. Medications targeting the renin–angiotensin system, such as inhibitors of angiotensin-converting enzyme, have also been found to influence the decline in muscle strength[63]. The efficacy of dipeptidyl peptidase-4 inhibitors for enhancing muscle strength in geriatric patients with type 2 diabetes mellitus was investigated in a recent retrospective cohort study[64]. Furthermore, several studies have demonstrated the potential benefits of testosterone for improving muscle strength. The most recent Clinical Practice Guideline by the Endocrine Society suggested that testosterone treatment can enhance muscle strength in men with hypogonadism[65]. A meta-analysis also found that intramuscular testosterone replacement therapy is effective in improving muscle strength in middle-aged and older men[66]. In addition, owing to their beneficial effects on muscle strength, exercise mimetics, which can induce energy expenditure without changes in activity, have been recognized as a potential therapeutic strategy[67].

CONCLUSION

In summary, muscle strength has an imperative function in the incidence of NAFLD/MAFLD and may serve as a potential predictor for early diagnosis, as well as a better means of evaluating NAFLD/MAFLD. Interventions based on muscle strength may provide novel insights into the treatment of NAFLD/MAFLD.

Footnotes

Provenance and peer review: Invited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Gastroenterology and hepatology

Country/Territory of origin: China

Peer-review report’s scientific quality classification

Grade A (Excellent): A

Grade B (Very good): 0

Grade C (Good): 0

Grade D (Fair): 0

Grade E (Poor): 0

P-Reviewer: Cigrovski Berkovic M, Croatia S-Editor: Lin C L-Editor: A P-Editor: Chen YX

References
1.  Volaklis KA, Halle M, Meisinger C. Muscular strength as a strong predictor of mortality: A narrative review. Eur J Intern Med. 2015;26:303-310.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 158]  [Cited by in F6Publishing: 143]  [Article Influence: 15.9]  [Reference Citation Analysis (0)]
2.  Benfica PDA, Aguiar LT, Brito SAF, Bernardino LHN, Teixeira-Salmela LF, Faria CDCM. Reference values for muscle strength: a systematic review with a descriptive meta-analysis. Braz J Phys Ther. 2018;22:355-369.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 27]  [Cited by in F6Publishing: 24]  [Article Influence: 4.0]  [Reference Citation Analysis (0)]
3.  Le MH, Yeo YH, Li X, Li J, Zou B, Wu Y, Ye Q, Huang DQ, Zhao C, Zhang J, Liu C, Chang N, Xing F, Yan S, Wan ZH, Tang NSY, Mayumi M, Liu X, Rui F, Yang H, Yang Y, Jin R, Le RHX, Xu Y, Le DM, Barnett S, Stave CD, Cheung R, Zhu Q, Nguyen MH. 2019 Global NAFLD Prevalence: A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2022;20:2809-2817.e28.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 66]  [Cited by in F6Publishing: 205]  [Article Influence: 102.5]  [Reference Citation Analysis (2)]
4.  Chandan S, Deliwala S, Khan SR, Mohan BP, Dhindsa BS, Bapaye J, Goyal H, Kassab LL, Kamal F, Sayles HR, Kochhar GS, Adler DG. EUS-guided versus percutaneous liver biopsy: A comprehensive review and meta-analysis of outcomes. Endosc Ultrasound. 2023;12:171-180.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Reference Citation Analysis (0)]
5.  Berná G, Romero-Gomez M. The role of nutrition in non-alcoholic fatty liver disease: Pathophysiology and management. Liver Int. 2020;40 Suppl 1:102-108.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 80]  [Cited by in F6Publishing: 107]  [Article Influence: 26.8]  [Reference Citation Analysis (0)]
6.  Robinson S, Granic A, Sayer AA. Nutrition and Muscle Strength, As the Key Component of Sarcopenia: An Overview of Current Evidence. Nutrients. 2019;11.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 31]  [Cited by in F6Publishing: 52]  [Article Influence: 10.4]  [Reference Citation Analysis (0)]
7.  Kim HY, Jang JW. Sarcopenia in the prognosis of cirrhosis: Going beyond the MELD score. World J Gastroenterol. 2015;21:7637-7647.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 84]  [Cited by in F6Publishing: 80]  [Article Influence: 8.9]  [Reference Citation Analysis (0)]
8.  Paternostro R, Trauner M. Current treatment of non-alcoholic fatty liver disease. J Intern Med. 2022;292:190-204.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 23]  [Cited by in F6Publishing: 31]  [Article Influence: 15.5]  [Reference Citation Analysis (0)]
9.  Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M; Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16-31.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 6053]  [Cited by in F6Publishing: 5637]  [Article Influence: 1127.4]  [Reference Citation Analysis (0)]
10.  Schaap LA, van Schoor NM, Lips P, Visser M. Associations of Sarcopenia Definitions, and Their Components, With the Incidence of Recurrent Falling and Fractures: The Longitudinal Aging Study Amsterdam. J Gerontol A Biol Sci Med Sci. 2018;73:1199-1204.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 176]  [Cited by in F6Publishing: 223]  [Article Influence: 44.6]  [Reference Citation Analysis (0)]
11.  Wu M, Wei Y, Lv J, Guo Y, Pei P, Li J, Du H, Yang L, Chen Y, Sun X, Zhang H, Chen J, Chen Z, Yu C, Li L; China Kadoorie Biobank Collaborative Group. Associations of muscle mass, strength, and quality with all-cause mortality in China: a population-based cohort study. Chin Med J (Engl). 2022;135:1358-1368.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
12.  Ibrahim K, May C, Patel HP, Baxter M, Sayer AA, Roberts H. A feasibility study of implementing grip strength measurement into routine hospital practice (GRImP): study protocol. Pilot Feasibility Stud. 2016;2:27.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 70]  [Cited by in F6Publishing: 59]  [Article Influence: 7.4]  [Reference Citation Analysis (0)]
13.  Mentiplay BF, Perraton LG, Bower KJ, Adair B, Pua YH, Williams GP, McGaw R, Clark RA. Assessment of Lower Limb Muscle Strength and Power Using Hand-Held and Fixed Dynamometry: A Reliability and Validity Study. PLoS One. 2015;10:e0140822.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 194]  [Cited by in F6Publishing: 259]  [Article Influence: 28.8]  [Reference Citation Analysis (0)]
14.  Lee GB, Huh Y, Lee SH, Han B, Kim YH, Kim DH, Kim SM, Choi YS, Cho KH, Nam GE. Association of low muscle strength with metabolic dysfunction-associated fatty liver disease: A nationwide study. World J Gastroenterol. 2023;29:5962-5973.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
15.  Gan D, Wang L, Jia M, Ru Y, Ma Y, Zheng W, Zhao X, Yang F, Wang T, Mu Y, Zhu S. Low muscle mass and low muscle strength associate with nonalcoholic fatty liver disease. Clin Nutr. 2020;39:1124-1130.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 31]  [Cited by in F6Publishing: 50]  [Article Influence: 10.0]  [Reference Citation Analysis (0)]
16.  Lee K. Relationship Between Handgrip Strength and Nonalcoholic Fatty Liver Disease: Nationwide Surveys. Metab Syndr Relat Disord. 2018;16:497-503.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 12]  [Cited by in F6Publishing: 12]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
17.  Kim BJ, Ahn SH, Lee SH, Hong S, Hamrick MW, Isales CM, Koh JM. Lower hand grip strength in older adults with non-alcoholic fatty liver disease: a nationwide population-based study. Aging (Albany NY). 2019;11:4547-4560.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 24]  [Cited by in F6Publishing: 27]  [Article Influence: 6.8]  [Reference Citation Analysis (0)]
18.  Cho J, Lee I, Park DH, Kwak HB, Min K. Relationships between Socioeconomic Status, Handgrip Strength, and Non-Alcoholic Fatty Liver Disease in Middle-Aged Adults. Int J Environ Res Public Health. 2021;18.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 13]  [Article Influence: 4.3]  [Reference Citation Analysis (0)]
19.  Lee SB, Kwon YJ, Jung DH, Kim JK. Association of Muscle Strength with Non-Alcoholic Fatty Liver Disease in Korean Adults. Int J Environ Res Public Health. 2022;19.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 4]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
20.  Debroy P, Lake JE, Malagoli A, Guaraldi G. Relationship between Grip Strength and Nonalcoholic Fatty Liver Disease in Men Living with HIV Referred to a Metabolic Clinic. J Frailty Aging. 2019;8:150-153.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 5]  [Reference Citation Analysis (0)]
21.  Meng G, Wu H, Fang L, Li C, Yu F, Zhang Q, Liu L, Du H, Shi H, Xia Y, Guo X, Liu X, Bao X, Su Q, Gu Y, Yang H, Bin Yu, Wu Y, Sun Z, Niu K. Relationship between grip strength and newly diagnosed nonalcoholic fatty liver disease in a large-scale adult population. Sci Rep. 2016;6:33255.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 32]  [Cited by in F6Publishing: 35]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
22.  Bulur A, Sivritepe R. The Association between Non-Alcoholic Fatty Liver Disease and Dynapenia in Men Diagnosed with Type 2 Diabetes Mellitus. Healthcare (Basel). 2023;11.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 2]  [Reference Citation Analysis (2)]
23.  Wang YM, Zhu KF, Zhou WJ, Zhang Q, Deng DF, Yang YC, Lu WW, Xu J, Yang YM. Sarcopenia is associated with the presence of nonalcoholic fatty liver disease in Zhejiang Province, China: a cross-sectional observational study. BMC Geriatr. 2021;21:55.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 11]  [Article Influence: 3.7]  [Reference Citation Analysis (0)]
24.  Petermann-Rocha F, Gray SR, Forrest E, Welsh P, Sattar N, Celis-Morales C, Ho FK, Pell JP. Associations of muscle mass and grip strength with severe NAFLD: A prospective study of 333,295 UK Biobank participants. J Hepatol. 2022;76:1021-1029.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 37]  [Cited by in F6Publishing: 36]  [Article Influence: 18.0]  [Reference Citation Analysis (0)]
25.  Kang S, Moon MK, Kim W, Koo BK. Association between muscle strength and advanced fibrosis in non-alcoholic fatty liver disease: a Korean nationwide survey. J Cachexia Sarcopenia Muscle. 2020;11:1232-1241.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 12]  [Article Influence: 3.0]  [Reference Citation Analysis (0)]
26.  Park SH, Kim DJ, Plank LD. Association of grip strength with non-alcoholic fatty liver disease: investigation of the roles of insulin resistance and inflammation as mediators. Eur J Clin Nutr. 2020;74:1401-1409.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 8]  [Cited by in F6Publishing: 14]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
27.  Zhao X, Shi X, Gu H, Zhou W, Zhang Q. Association between handgrip strength, nonalcoholic fatty liver disease, advanced hepatic fibrosis and its modifiers: Evidence from the NHANES database of the USA. J Gastroenterol Hepatol. 2023;38:1734-1742.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Reference Citation Analysis (0)]
28.  Kim D, Dennis BB, Wijarnpreecha K, Cholankeril G, Ahmed A. Muscle strength in non-alcoholic fatty liver disease and all-cause and cause-specific mortality. Liver Int. 2023;43:513-516.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 1]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
29.  Charatcharoenwitthaya P, Karaketklang K, Aekplakorn W. Muscle strength, but not body mass index, is associated with mortality in patients with non-alcoholic fatty liver disease. J Cachexia Sarcopenia Muscle. 2022;13:2393-2404.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 6]  [Article Influence: 3.0]  [Reference Citation Analysis (0)]
30.  Abdul-Ghani MA, DeFronzo RA. Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotechnol. 2010;2010:476279.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 292]  [Cited by in F6Publishing: 364]  [Article Influence: 26.0]  [Reference Citation Analysis (0)]
31.  Lee SH, Park SY, Choi CS. Insulin Resistance: From Mechanisms to Therapeutic Strategies. Diabetes Metab J. 2022;46:15-37.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 49]  [Cited by in F6Publishing: 147]  [Article Influence: 73.5]  [Reference Citation Analysis (0)]
32.  Fujii H, Kawada N;  Japan Study Group Of Nafld Jsg-Nafld. The Role of Insulin Resistance and Diabetes in Nonalcoholic Fatty Liver Disease. Int J Mol Sci. 2020;21.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 45]  [Cited by in F6Publishing: 109]  [Article Influence: 27.3]  [Reference Citation Analysis (0)]
33.  Bhanji RA, Narayanan P, Allen AM, Malhi H, Watt KD. Sarcopenia in hiding: The risk and consequence of underestimating muscle dysfunction in nonalcoholic steatohepatitis. Hepatology. 2017;66:2055-2065.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 142]  [Cited by in F6Publishing: 158]  [Article Influence: 22.6]  [Reference Citation Analysis (0)]
34.  Peiseler M, Schwabe R, Hampe J, Kubes P, Heikenwälder M, Tacke F. Immune mechanisms linking metabolic injury to inflammation and fibrosis in fatty liver disease - novel insights into cellular communication circuits. J Hepatol. 2022;77:1136-1160.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 113]  [Article Influence: 56.5]  [Reference Citation Analysis (0)]
35.  Engelmann C, Clària J, Szabo G, Bosch J, Bernardi M. Pathophysiology of decompensated cirrhosis: Portal hypertension, circulatory dysfunction, inflammation, metabolism and mitochondrial dysfunction. J Hepatol. 2021;75 Suppl 1:S49-S66.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 49]  [Cited by in F6Publishing: 116]  [Article Influence: 38.7]  [Reference Citation Analysis (0)]
36.  Bali T, Chrysavgis L, Cholongitas E. Metabolic-Associated Fatty Liver Disease and Sarcopenia. Endocrinol Metab Clin North Am. 2023;52:497-508.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
37.  Chen Y, Zhang P, Lv S, Su X, Du Y, Xu C, Jin Z. Ectopic fat deposition and its related abnormalities of lipid metabolism followed by nonalcoholic fatty pancreas. Endosc Ultrasound. 2022;11:407-413.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
38.  Tuttle CSL, Thang LAN, Maier AB. Markers of inflammation and their association with muscle strength and mass: A systematic review and meta-analysis. Ageing Res Rev. 2020;64:101185.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 96]  [Cited by in F6Publishing: 215]  [Article Influence: 53.8]  [Reference Citation Analysis (0)]
39.  Fernández-Mincone T, Contreras-Briceño F, Espinosa-Ramírez M, García-Valdés P, López-Fuenzalida A, Riquelme A, Arab JP, Cabrera D, Arrese M, Barrera F. Nonalcoholic fatty liver disease and sarcopenia: pathophysiological connections and therapeutic implications. Expert Rev Gastroenterol Hepatol. 2020;14:1141-1157.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 8]  [Cited by in F6Publishing: 8]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
40.  Li AA, Kim D, Ahmed A. Association of Sarcopenia and NAFLD: An Overview. Clin Liver Dis (Hoboken). 2020;16:73-76.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 20]  [Cited by in F6Publishing: 31]  [Article Influence: 7.8]  [Reference Citation Analysis (0)]
41.  Visser M, Deeg DJ, Lips P; Longitudinal Aging Study Amsterdam. Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): the Longitudinal Aging Study Amsterdam. J Clin Endocrinol Metab. 2003;88:5766-5772.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 797]  [Cited by in F6Publishing: 727]  [Article Influence: 34.6]  [Reference Citation Analysis (0)]
42.  Bo Y, Liu C, Ji Z, Yang R, An Q, Zhang X, You J, Duan D, Sun Y, Zhu Y, Cui H, Lu Q. A high whey protein, vitamin D and E supplement preserves muscle mass, strength, and quality of life in sarcopenic older adults: A double-blind randomized controlled trial. Clin Nutr. 2019;38:159-164.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 61]  [Cited by in F6Publishing: 64]  [Article Influence: 12.8]  [Reference Citation Analysis (0)]
43.  Barchetta I, Angelico F, Del Ben M, Baroni MG, Pozzilli P, Morini S, Cavallo MG. Strong association between non alcoholic fatty liver disease (NAFLD) and low 25(OH) vitamin D levels in an adult population with normal serum liver enzymes. BMC Med. 2011;9:85.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 215]  [Cited by in F6Publishing: 224]  [Article Influence: 17.2]  [Reference Citation Analysis (0)]
44.  Barchetta I, Cimini FA, Cavallo MG. Vitamin D and Metabolic Dysfunction-Associated Fatty Liver Disease (MAFLD): An Update. Nutrients. 2020;12.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 33]  [Cited by in F6Publishing: 63]  [Article Influence: 15.8]  [Reference Citation Analysis (0)]
45.  Ramsey KA, Rojer AGM, D'Andrea L, Otten RHJ, Heymans MW, Trappenburg MC, Verlaan S, Whittaker AC, Meskers CGM, Maier AB. The association of objectively measured physical activity and sedentary behavior with skeletal muscle strength and muscle power in older adults: A systematic review and meta-analysis. Ageing Res Rev. 2021;67:101266.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 87]  [Article Influence: 29.0]  [Reference Citation Analysis (0)]
46.  Li R, Xia J, Zhang XI, Gathirua-Mwangi WG, Guo J, Li Y, McKenzie S, Song Y. Associations of Muscle Mass and Strength with All-Cause Mortality among US Older Adults. Med Sci Sports Exerc. 2018;50:458-467.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 138]  [Cited by in F6Publishing: 188]  [Article Influence: 31.3]  [Reference Citation Analysis (0)]
47.  Kim D, Vazquez-Montesino LM, Li AA, Cholankeril G, Ahmed A. Inadequate Physical Activity and Sedentary Behavior Are Independent Predictors of Nonalcoholic Fatty Liver Disease. Hepatology. 2020;72:1556-1568.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 39]  [Cited by in F6Publishing: 60]  [Article Influence: 15.0]  [Reference Citation Analysis (0)]
48.  Zhao Q, Yin Y, Deng Y. Metabolic associated fatty liver disease and sarcopenia additively increase mortality: a real-world study. Nutr Diabetes. 2023;13:21.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
49.  Fox R, Stenning K, Slee A, Macnaughtan J, Davies N. Sarcopenia in liver cirrhosis: Prevalence, pathophysiology and therapeutic strategies. Anal Biochem. 2022;647:114581.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
50.  European Association for the Study of the Liver. EASL Clinical Practice Guidelines on nutrition in chronic liver disease. J Hepatol. 2019;70:172-193.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 394]  [Cited by in F6Publishing: 483]  [Article Influence: 96.6]  [Reference Citation Analysis (1)]
51.  Aamann L, Dam G, Borre M, Drljevic-Nielsen A, Overgaard K, Andersen H, Vilstrup H, Aagaard NK. Resistance Training Increases Muscle Strength and Muscle Size in Patients With Liver Cirrhosis. Clin Gastroenterol Hepatol. 2020;18:1179-1187.e6.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 35]  [Cited by in F6Publishing: 41]  [Article Influence: 10.3]  [Reference Citation Analysis (0)]
52.  Jones JC, Coombes JS, Macdonald GA. Exercise capacity and muscle strength in patients with cirrhosis. Liver Transpl. 2012;18:146-151.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 92]  [Cited by in F6Publishing: 97]  [Article Influence: 8.1]  [Reference Citation Analysis (0)]
53.  Gielen E, Beckwée D, Delaere A, De Breucker S, Vandewoude M, Bautmans I; Sarcopenia Guidelines Development Group of the Belgian Society of Gerontology and Geriatrics (BSGG). Nutritional interventions to improve muscle mass, muscle strength, and physical performance in older people: an umbrella review of systematic reviews and meta-analyses. Nutr Rev. 2021;79:121-147.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 50]  [Cited by in F6Publishing: 90]  [Article Influence: 30.0]  [Reference Citation Analysis (0)]
54.  Bagheri A, Hashemi R, Heshmat R, Motlagh AD, Esmaillzadeh A. Patterns of Nutrient Intake in Relation to Sarcopenia and Its Components. Front Nutr. 2021;8:645072.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 2]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
55.  Kim D, Konyn P, Cholankeril G, Ahmed A. Physical Activity Is Associated With Nonalcoholic Fatty Liver Disease and Significant Fibrosis Measured by FibroScan. Clin Gastroenterol Hepatol. 2022;20:e1438-e1455.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 20]  [Cited by in F6Publishing: 45]  [Article Influence: 22.5]  [Reference Citation Analysis (0)]
56.  Romero-Gómez M, Zelber-Sagi S, Trenell M. Treatment of NAFLD with diet, physical activity and exercise. J Hepatol. 2017;67:829-846.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 614]  [Cited by in F6Publishing: 708]  [Article Influence: 101.1]  [Reference Citation Analysis (0)]
57.  Mukherjee S, Fok JR, van Mechelen W. Electrical Stimulation and Muscle Strength Gains in Healthy Adults: A Systematic Review. J Strength Cond Res. 2023;37:938-950.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
58.  Ferguson D, Finck BN. Emerging therapeutic approaches for the treatment of NAFLD and type 2 diabetes mellitus. Nat Rev Endocrinol. 2021;17:484-495.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 97]  [Cited by in F6Publishing: 192]  [Article Influence: 64.0]  [Reference Citation Analysis (0)]
59.  Kwak JY, Kwon KS. Pharmacological Interventions for Treatment of Sarcopenia: Current Status of Drug Development for Sarcopenia. Ann Geriatr Med Res. 2019;23:98-104.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 45]  [Cited by in F6Publishing: 72]  [Article Influence: 14.4]  [Reference Citation Analysis (0)]
60.  Feike Y, Zhijie L, Wei C. Advances in research on pharmacotherapy of sarcopenia. Aging Med (Milton). 2021;4:221-233.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 23]  [Cited by in F6Publishing: 18]  [Article Influence: 6.0]  [Reference Citation Analysis (0)]
61.  Rooks D, Praestgaard J, Hariry S, Laurent D, Petricoul O, Perry RG, Lach-Trifilieff E, Roubenoff R. Treatment of Sarcopenia with Bimagrumab: Results from a Phase II, Randomized, Controlled, Proof-of-Concept Study. J Am Geriatr Soc. 2017;65:1988-1995.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 115]  [Cited by in F6Publishing: 97]  [Article Influence: 13.9]  [Reference Citation Analysis (0)]
62.  Rooks D, Swan T, Goswami B, Filosa LA, Bunte O, Panchaud N, Coleman LA, Miller RR, Garcia Garayoa E, Praestgaard J, Perry RG, Recknor C, Fogarty CM, Arai H, Chen LK, Hashimoto J, Chung YS, Vissing J, Laurent D, Petricoul O, Hemsley S, Lach-Trifilieff E, Papanicolaou DA, Roubenoff R. Bimagrumab vs Optimized Standard of Care for Treatment of Sarcopenia in Community-Dwelling Older Adults: A Randomized Clinical Trial. JAMA Netw Open. 2020;3:e2020836.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 44]  [Cited by in F6Publishing: 56]  [Article Influence: 14.0]  [Reference Citation Analysis (0)]
63.  Onder G, Penninx BW, Balkrishnan R, Fried LP, Chaves PH, Williamson J, Carter C, Di Bari M, Guralnik JM, Pahor M. Relation between use of angiotensin-converting enzyme inhibitors and muscle strength and physical function in older women: an observational study. Lancet. 2002;359:926-930.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 233]  [Cited by in F6Publishing: 214]  [Article Influence: 9.7]  [Reference Citation Analysis (0)]
64.  Sencan C, Dost FS, Ates Bulut E, Isik AT. DPP4 inhibitors as a potential therapeutic option for sarcopenia: A 6-month follow-up study in diabetic older patients. Exp Gerontol. 2022;164:111832.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
65.  Bhasin S, Brito JP, Cunningham GR, Hayes FJ, Hodis HN, Matsumoto AM, Snyder PJ, Swerdloff RS, Wu FC, Yialamas MA. Testosterone Therapy in Men With Hypogonadism: An Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2018;103:1715-1744.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 786]  [Cited by in F6Publishing: 809]  [Article Influence: 134.8]  [Reference Citation Analysis (0)]
66.  Skinner JW, Otzel DM, Bowser A, Nargi D, Agarwal S, Peterson MD, Zou B, Borst SE, Yarrow JF. Muscular responses to testosterone replacement vary by administration route: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle. 2018;9:465-481.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 40]  [Cited by in F6Publishing: 44]  [Article Influence: 7.3]  [Reference Citation Analysis (0)]
67.  Cento AS, Leigheb M, Caretti G, Penna F. Exercise and Exercise Mimetics for the Treatment of Musculoskeletal Disorders. Curr Osteoporos Rep. 2022;20:249-259.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 3]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]