Cited by 363Gut microbiota and healthNutrition and Health in AgingMuscle Physiology and Disorders

The DOI matches its Crossref record; 115 of the 116 references it cites were found in a registry or an index.

Understanding the gut microbiota and sarcopenia: a systematic review

Open access

Liu, Chaoran, Cheung, Wing‐Hoi, Li, Jie, Chow, Simon Kwoon‐Ho, Yu, Jun, Wong, Sunny Hei, Ip, Margaret, Sung, Joseph Jao Yiu, Wong, Ronald Man Yeung·2021·Journal of Cachexia, Sarcopenia and Muscle

DOI 10.1002/jcsm.12784PMC PMC8718038

Open this paper in CoChat — free account

Abstract

Background: Gut microbiota dysbiosis and sarcopenia commonly occur in the elderly. Although the concept of the gut–muscle axis has been raised, the casual relationship is still unclear. This systematic review analyses the current evidence of gut microbiota effects on muscle/sarcopenia. Methods: A systematic review was performed in PubMed, Embase, Web of Science, and The Cochrane Library databases using the keywords (microbiota* OR microbiome*) AND (sarcopen* OR muscle). Studies reporting the alterations of gut microbiota and muscle/physical performance were analysed. Results: A total of 26 pre‐clinical and 10 clinical studies were included. For animal studies, three revealed age‐related changes and relationships between gut microbiota and muscle. Three studies focused on muscle characteristics of germ‐free mice. Seventy‐five per cent of eight faecal microbiota transplantation studies showed that the recipient mice successfully replicated the muscle phenotype of donors. There were positive effects on muscle from seven probiotics, two prebiotics, and short‐chain fatty acids (SCFAs). Ten studies investigated on other dietary supplements, antibiotics, exercise, and food withdrawal that affected both muscle and gut microbiota. Twelve studies explored the potential mechanisms of the gut–muscle axis. For clinical studies, 6 studies recruited 676 elderly people (72.8 ± 5.6 years, 57.8% female), while 4 studies focused on 244 young adults (29.7 ± 7.8 years, 55.4% female). The associations of gut microbiota and muscle had been shown in four observational studies. Probiotics, prebiotics, synbiotics, fermented milk, caloric restriction, and exercise in six studies displayed inconsistent effects on muscle mass, function, and gut microbiota. Conclusions: Altering the gut microbiota through bacteria depletion, faecal transplantation, and various supplements was shown to directly affect muscle phenotypes. Probiotics, prebiotics, SCFAs, and bacterial products are potential novel therapies to enhance muscle mass and physical performance. Lactobacillus and Bifidobacterium strains restored age‐related muscle loss. Potential mechanisms of microbiome modulating muscle mainly include protein, energy, lipid, and glucose metabolism, inflammation level, neuromuscular junction, and mitochondrial function. The role of the gut microbiota in the development of muscle loss during aging is a crucial area that requires further studies for translation to patients.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1002/jcsm.12784

Cites

115 of 115 references verified0 citation errors · 0 not checkable

Statistics

Figure 1 Study search and selection process.CC BY-NC-ND · PubMed Central

Figure 2 The molecular signalling pathways of gut microbiota and skeletal muscle: the noxious bacterial metabolites (indoxyl sulfate and LPS) and absence of gut microbiota (black) induced muscle atrophy. 39 , 94 , 95 , 97 , 99 , 100 , 102 Indoxyl sulfate and LPS caused muscle atrophy and inflammation by activating the PI3K/AKT, NF‐κB, and MAPKs (p38, JNK, ERK) signalling pathways to up‐regulate Atrogin‐1/MAFbx and MuRF1 genes encoding E3 ubiquitin ligases, and inflammatory cytokines. AMPK–FoxO3–Atrogin‐1/MuRF1 cascade and BCAAs catabolism were activated in the bacteria depletion condition. The expressions of IGF1, myogenin, and MyoD were reduced, and myostatin was increased. NMJ function and mitochondrial function were widely impaired. Supplements with probiotics, SCFAs, or germ‐free transplanted models showed (red) the suppression of GR and excessive AMPK activation, attenuated inflammation levels, mitochondrial and NMJ function repair, as well as increased the expressions of muscle growth‐related genes (IGF1, myogenin, SIK1) to maintain muscle mass and functions. 32 , 39 , 47 , 80 For abbreviations of the main text, please see Table S3.CC BY-NC-ND · PubMed Central

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042
The Effect of Riding as an Alternative Treatment for Children with Cerebral Palsy: A Systematic Review and Meta-Analysis
Wang, G., Ma, R., Qiao, G., Wada, K., Aizawa, Y., & Satoh, T. (2015) · Integrative Medicine International · doi:10.1159/000368408 · Cited by 18,762
Sarcopenia: revised European consensus on definition and diagnosis
Cruz-Jentoft, A. J., Bahat, G., Bauer, J., Boirie, Y., Bruyère, O., Cederholm, T., Cooper, C., Landi, F., Rolland, Y., Sayer, A. A., et al. (2019) · Age and Ageing · doi:10.1093/ageing/afy169 · Cited by 13,818
Initial sequencing and comparative analysis of the mouse genome
Mouse Genome Sequencing Consortium (2002) · Nature · doi:10.1038/nature01262 · Cited by 7,187
Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment
Chen, L.-K., Woo, J., Assantachai, P., Auyeung, T.-W., Chou, M.-Y., Iijima, K., Jang, H. C., Kang, L., Kim, M., Kim, S., et al. (2020) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2019.12.012 · Cited by 7,070
Gut microbiota in human metabolic health and disease
Fan, Y., & Pedersen, O. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0433-9 · Cited by 4,724
Sarcopenia
Cruz-Jentoft, A. J., & Sayer, A. A. (2019) · The Lancet · doi:10.1016/s0140-6736(19)31138-9 · Cited by 3,905
Mechanisms underlying the resistance to diet-induced obesity in germ-free mice
Bäckhed, F., Manchester, J. K., Semenkovich, C. F., & Gordon, J. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605374104 · Cited by 2,615
The FNIH Sarcopenia Project: Rationale, Study Description, Conference Recommendations, and Final Estimates
Studenski, S. A., Peters, K. W., Alley, D. E., Cawthon, P. M., McLean, R. R., Harris, T. B., Ferrucci, L., Guralnik, J. M., Fragala, M. S., Kenny, A. M., et al. (2014) · The Journals of Gerontology: Series A · doi:10.1093/gerona/glu010 · Cited by 2,545
Gut microbiota-derived metabolites as key actors in inflammatory bowel disease
Lavelle, A., & Sokol, H. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0258-z · Cited by 2,015
Prebiotics: Definition, Types, Sources, Mechanisms, and Clinical Applications
Davani-Davari, D., Negahdaripour, M., Karimzadeh, I., Seifan, M., Mohkam, M., Masoumi, S. J., Berenjian, A., & Ghasemi, Y. (2019) · Foods · doi:10.3390/foods8030092 · Cited by 1,848
The healthcare costs of sarcopenia in the United States
Janssen, I., Shepard, D. S., Katzmarzyk, P. T., & Roubenoff, R. (2004) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52014.x · Cited by 1,546
Gut microbial metabolites as multi-kingdom intermediates
Krautkramer, K. A., Fan, J., & Bäckhed, F. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0438-4 · Cited by 1,398
Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health
Oliphant, K., & Allen-Vercoe, E. (2019) · Microbiome · doi:10.1186/s40168-019-0704-8 · Cited by 1,327
Summary comments
Rosenberg, I. H. (1989) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/50.5.1231 · Cited by 1,234
Gut microbiota and aging
O’Toole, P. W., & Jeffery, I. B. (2015) · Science · doi:10.1126/science.aac8469 · Cited by 1,202
Sarcopenia and its association with falls and fractures in older adults: A systematic review and meta-analysis
Yeung, S. S. Y., Reijnierse, E. M., Pham, V. K., Trappenburg, M. C., Lim, W. K., Meskers, C. G. M., & Maier, A. B. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12411 · Cited by 1,115
A practical guide to amplicon and metagenomic analysis of microbiome data
Liu, Y., Qin, Y., Chen, T., Lu, M., Qian, X., Guo, X., & Bai, Y. (2020) · Protein & Cell · doi:10.1007/s13238-020-00724-8 · Cited by 931
An overview of sarcopenia: facts and numbers on prevalence and clinical impact
von Haehling, S., Morley, J. E., & Anker, S. D. (2010) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1007/s13539-010-0014-2 · Cited by 888
Age-related decrease in physical activity and functional fitness among elderly men and women
Milanovic, Z., Jorgić, B., Trajković, N., Sporis, Pantelić, S., & James (2013) · Clinical Interventions in Aging · doi:10.2147/cia.s44112 · Cited by 779 · cited 1×
“Resistance exercise is the primary non-pharmacological approach to improve muscle mass and function,(13) but elderly patients often have poor adherence(14) and lack physical fitness for long-term sustainability.(15) The increment of protein intake,”
Background
Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children
Blanton, L. V., Charbonneau, M. R., Salih, T., Barratt, M. J., Venkatesh, S., Ilkaveya, O., Subramanian, S., Manary, M. J., Trehan, I., Jorgensen, J. M., et al. (2016) · Science · doi:10.1126/science.aad3311 · Cited by 735 · cited 5×
“body mass through magnetic resonance (MR) and dualenergy X-ray absorptiometry (DXA).(36,37,41,43,45,47,56) Twelve studies evaluated size and types of myofibres, muscle metabolites, and target genes of muscle growth and atrophy.”
BackgroundInfluential
The Role of Inflammation in Age-Related Sarcopenia
Dalle, S., Rossmeislova, L., & Koppo, K. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.01045 · Cited by 668
Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review.
the IOF-ESCEO Sarcopenia Working Group, Beaudart, C., Dawson, A., Shaw, S. C., Harvey, N. C., Kanis, J. A., Binkley, N., Reginster, J. Y., Chapurlat, R., Chan, D. C., et al. (2017) · Osteoporosis International · doi:10.1007/s00198-017-3980-9 · Cited by 602
The gut microbiota influences skeletal muscle mass and function in mice
Lahiri, S., Kim, H., Garcia-Perez, I., Reza, M. M., Martin, K. A., Kundu, P., Cox, L. M., Selkrig, J., Posma, J. M., Zhang, H., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aan5662 · Cited by 580
Gut Microbiota–Derived Short-Chain Fatty Acids Promote Poststroke Recovery in Aged Mice
Lee, J., d’Aigle, J., Atadja, L. A., Quaicoe, V. A., Honarpisheh, P., Ganesh, B. P., Hassan, A. F., Graf, J., Petrosino, J. F., Putluri, N., et al. (2020) · Circulation Research · doi:10.1161/circresaha.119.316448 · Cited by 567
Short-chain fatty acids as potential regulators of skeletal muscle metabolism and function
Frampton, J. E., Murphy, K. G., Frost, G. S., & Chambers, E. S. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0188-7 · Cited by 552
Sarcopenia: burden and challenges for public health
Beaudart, C., Rizzoli, R., Bruyère, O., Reginster, J., & Biver, E. (2014) · Archives of Public Health · doi:10.1186/2049-3258-72-45 · Cited by 523
Differences in gut microbiota profile between women with active lifestyle and sedentary women
Bressa, C., Bailén-Andrino, M., Pérez-Santiago, J., González-Soltero, R., Pérez, M., Montalvo-Lominchar, M. G., Maté-Muñoz, J. L., Domínguez, R., Moreno, D., & Larrosa, M. (2017) · PLOS ONE · doi:10.1371/journal.pone.0171352 · Cited by 501
Does nutrition play a role in the prevention and management of sarcopenia?
Robinson, S. M., Reginster, J. Y., Rizzoli, R., Shaw, S. C., Kanis, J. A., Bautmans, I., Bischoff-Ferrari, H., Bruyère, O., Cesari, M., Dawson-Hughes, B., et al. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2017.08.016 · Cited by 491
Engineered E. coli Nissle 1917 for the delivery of matrix-tethered therapeutic domains to the gut
Praveschotinunt, P., Duraj‐Thatte, A., Gelfat, I., Bahl, F., Chou, D. B., & Joshi, N. S. (2019) · Nature Communications · doi:10.1038/s41467-019-13336-6 · Cited by 467
An inflammation-targeting hydrogel for local drug delivery in inflammatory bowel disease
Zhang, S., Ermann, J., Succi, M. D., Zhou, A., Hamilton, M. J., Cao, B., Korzenik, J. R., Glickman, J. N., Vemula, P. K., Glimcher, L. H., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa5657 · Cited by 467
Microbial shifts in the aging mouse gut
Langille, M. G., Meehan, C. J., Koenig, J. E., Dhanani, A. S., Rose, R. A., Howlett, S. E., & Beiko, R. G. (2014) · Microbiome · doi:10.1186/s40168-014-0050-9 · Cited by 437
Gut Microbiota, Muscle Mass and Function in Aging: A Focus on Physical Frailty and Sarcopenia
Ticinesi, A., Nouvenne, A., Cerundolo, N., Catania, P., Prati, B., Tana, C., & Meschi, T. (2019) · Nutrients · doi:10.3390/nu11071633 · Cited by 418
Interaction Between Obesity and the Gut Microbiota: Relevance in Nutrition
Delzenne, N. M., & Cani, P. D. (2011) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-072610-145146 · Cited by 418
Functional Characterization of Novel Faecalibacterium prausnitzii Strains Isolated from Healthy Volunteers: A Step Forward in the Use of F. prausnitzii as a Next-Generation Probiotic
Martín, R., Miquel, S., Benevides, L., Bridonneau, C., Robert, V., Hudault, S., Chain, F., Berteau, O., Azevedo, V., Chatel, J. M., et al. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01226 · Cited by 398
Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2019
von Haehling, S., Morley, J. E., Coats, A. J. S., & Anker, S. D. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12501 · Cited by 389
Interventions for Treating Sarcopenia: A Systematic Review and Meta-Analysis of Randomized Controlled Studies
Yoshimura, Y., Wakabayashi, H., Yamada, M., Kim, H., Harada, A., & Arai, H. (2017) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2017.03.019 · Cited by 365
The histone deacetylase inhibitor butyrate improves metabolism and reduces muscle atrophy during aging
Walsh, M. E., Bhattacharya, A., Sataranatarajan, K., Qaisar, R., Sloane, L., Rahman, M. M., Kinter, M., & Van Remmen, H. (2015) · Aging Cell · doi:10.1111/acel.12387 · Cited by 334
Fecal Microbiota Composition and Frailty
van Tongeren, S. P., Slaets, J. P. J., Harmsen, H. J. M., & Welling, G. W. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.10.6438-6442.2005 · Cited by 333 · cited 1×
“prausnitzii, and Bacteroides/Prevotella ratio declined sharply and Enterobacteriaceae increased in the frail old people.(107) Active adults had higher muscle mass, functions,”
Background
Economic Impact of Hospitalizations in US Adults with Sarcopenia
Goates, S., Du, K., Arensberg, M. B., Gaillard, T. R., Guralnik, J. M., & Pereira, S. L. (2019) · The Journal of Frailty & Aging · doi:10.14283/jfa.2019.10 · Cited by 301
Lactobacillus plantarum TWK10 Supplementation Improves Exercise Performance and Increases Muscle Mass in Mice
Chen, Y.-M., Wei, L., Chiu, Y.-S., Hsu, Y.-J., Tsai, T.-Y., Wang, M.-F., & Huang, C.-C. (2016) · Nutrients · doi:10.3390/nu8040205 · Cited by 297
Minerals and Sarcopenia; The Role of Calcium, Iron, Magnesium, Phosphorus, Potassium, Selenium, Sodium, and Zinc on Muscle Mass, Muscle Strength, and Physical Performance in Older Adults: A Systematic Review
van Dronkelaar, C., van Velzen, A., Abdelrazek, M., van der Steen, A., Weijs, P. J. M., & Tieland, M. (2018) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2017.05.026 · Cited by 279
Restoring Specific Lactobacilli Levels Decreases Inflammation and Muscle Atrophy Markers in an Acute Leukemia Mouse Model
Bindels, L. B., Beck, R., Schakman, O., Martin, J. C., De Backer, F., Sohet, F. M., Dewulf, E. M., Pachikian, B. D., Neyrinck, A. M., Thissen, J.-P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037971 · Cited by 278
p-Cresyl Sulfate Promotes Insulin Resistance Associated with CKD
Koppe, L., Pillon, N. J., Vella, R., Croze, M. L., Pelletier, C. C., Chambert, S., Massy, Z. A., Glorieux, G., Vanholder, R. C., Dugenet, Y., et al. (2012) · Journal of the American Society of Nephrology · doi:10.1681/asn.2012050503 · Cited by 275
Phlorizin ameliorates obesity-associated endotoxemia and insulin resistance in high-fat diet-fed mice by targeting the gut microbiota and intestinal barrier integrity
Zhang, X., Chen, J., Kang, Y., Peng, L., Xie, J., Gou, X., Peng, T., & Tang, L. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1842990 · Cited by 273
Toll‐like receptor 4 mediates lipopolysaccharide‐induced muscle catabolism via coordinate activation of ubiquitin‐proteasome and autophagy‐lysosome pathways
Doyle, A., Zhang, G., Fattah, E. A. A., Eissa, N. T., & Li, Y. (2011) · The FASEB Journal · doi:10.1096/fj.10-164152 · Cited by 256
Lactobacillus and Bifidobacterium Improves Physiological Function and Cognitive Ability in Aged Mice by the Regulation of Gut Microbiota
Ni, Y., Yang, X., Zheng, L., Wang, Z., Wu, L., Jiang, J., Yang, T., Ma, L., & Fu, Z. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201900603 · Cited by 255
Regulation of Skeletal Muscle Function by Amino Acids
Kamei, Y., Hatazawa, Y., Uchitomi, R., Yoshimura, R., & Miura, S. (2020) · Nutrients · doi:10.3390/nu12010261 · Cited by 254
Age-Associated Changes in Gut Microbiota and Dietary Components Related with the Immune System in Adulthood and Old Age: A Cross-Sectional Study
Salazar, N., Arboleya, S., Fernández-Navarro, T., Reyes‐Gavilán, C. G. D. L., González, S., & Gueimonde, M. (2019) · Nutrients · doi:10.3390/nu11081765 · Cited by 241
Health Care Costs Associated With Muscle Weakness: A UK Population-Based Estimate
Pinedo‐Villanueva, R., Westbury, L. D., Syddall, H. E., Sanchez-Santos, M. T., Dennison, E. M., Robinson, S. M., & Cooper, C. C. (2018) · Calcified Tissue International · doi:10.1007/s00223-018-0478-1 · Cited by 222
Effect of a Prebiotic Formulation on Frailty Syndrome: A Randomized, Double-Blind Clinical Trial
Buigues, C., Fernández-Garrido, J., Pruimboom, L., Hoogland, A., Navarro-Martínez, R., Martínez-Martínez, M., Verdejo, Y., Mascarós, M., Peris, C., & Cauli, O. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060932 · Cited by 222
Gut bacteria are critical for optimal muscle function: a potential link with glucose homeostasis
Nay, K., Jollet, M., Goustard, B., Baati, N., Vernus, B., Pontones, M., Lefeuvre-Orfila, L., Bendavid, C., Rué, O., Mariadassou, M., et al. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00521.2018 · Cited by 215
Microbiome potentiates endurance exercise through intestinal acetate production
Okamoto, T., Morino, K., Ugi, S., Nakagawa, F., Lemecha, M., Ida, S., Ohashi, N., Sato, D., Fujita, Y., & Maegawa, H. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00510.2018 · Cited by 210
Efficacy of Whey Protein Supplementation on Resistance Exercise–Induced Changes in Lean Mass, Muscle Strength, and Physical Function in Mobility-Limited Older Adults
Chalé, A., Cloutier, G. J., Hau, C., Phillips, E. M., Dallal, G. E., & Fielding, R. A. (2013) · The Journals of Gerontology: Series A · doi:10.1093/gerona/gls221 · Cited by 208
Neurogenesis and prolongevity signaling in young germ-free mice transplanted with the gut microbiota of old mice
Kundu, P., Lee, H. U., Garcia-Perez, I., Tay, E. X. Y., Kim, H., Faylon, L. E., Martin, K. A., Purbojati, R., Drautz-Moses, D. I., Ghosh, S., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aau4760 · Cited by 201
Muscle wasting: The gut microbiota as a new therapeutic target?
Bindels, L. B., & Delzenne, N. M. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.06.021 · Cited by 198
Metabolic alterations by indoxyl sulfate in skeletal muscle induce uremic sarcopenia in chronic kidney disease
Sato, E., Mori, T., Mishima, E., Suzuki, A., Sugawara, S., Kurasawa, N., Saigusa, D., Miura, D., Morikawa, T., Saito, R., et al. (2016) · Scientific Reports · doi:10.1038/srep36618 · Cited by 195
Effect of Intestinal Microbiota on Exercise Performance in Mice
Hsu, Y.-J., Chiu, C. C., Li, Y. P., Huang, W. C., Huang, Y. T., Huang, C., & Chuang, H.-L. (2014) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000000644 · Cited by 192
Indoxyl sulfate potentiates skeletal muscle atrophy by inducing the oxidative stress-mediated expression of myostatin and atrogin-1
Enoki, Y., Watanabe, H., Arake, R., Sugimoto, R., Imafuku, T., Tominaga, Y., Ishima, Y., Kotani, S., Nakajima, M., Tanaka, M., et al. (2016) · Scientific Reports · doi:10.1038/srep32084 · Cited by 188
Gut Microbial, Inflammatory and Metabolic Signatures in Older People with Physical Frailty and Sarcopenia: Results from the BIOSPHERE Study
Picca, A., Ponziani, F. R., Calvani, R., Marini, F., Biancolillo, A., Coelho‐Júnior, H. J., Gervasoni, J., Primiano, A., Putignani, L., CHIERICO, F. D., et al. (2019) · Nutrients · doi:10.3390/nu12010065 · Cited by 181
Gut Dysbiosis and Muscle Aging: Searching for Novel Targets against Sarcopenia
Picca, A., Fanelli, F., Calvani, R., Mulè, G., Pesce, V., Sisto, A., Pantanelli, C., Bernabei, R., Landi, F., & Marzetti, E. (2018) · Mediators of Inflammation · doi:10.1155/2018/7026198 · Cited by 181
Muscle strength is increased in mice that are colonized with microbiota from high-functioning older adults
Fielding, R. A., Reeves, A. R., Jasuja, R., Liu, C. K., Barrett, B. B., & Lustgarten, M. S. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.110722 · Cited by 171
Self-citation
Pharmacological interventions for treatment of sarcopenia: Current status of drug development for sarcopenia
Kwak, J. Y., & Kwon, K.-S. (2019) · Annals of Geriatric Medicine and Research · doi:10.4235/agmr.19.0028 · Cited by 171
Aerobic Exercise Training with Brisk Walking Increases Intestinal Bacteroides in Healthy Elderly Women
Morita, E., Yokoyama, H., Imai, D., Takeda, R., Ota, A., Kawai, E., Hisada, T., Emoto, M., Suzuki, Y., & Okazaki, K. (2019) · Nutrients · doi:10.3390/nu11040868 · Cited by 169
Potential therapeutic interventions for chronic kidney disease‐associated sarcopenia via indoxyl sulfate‐induced mitochondrial dysfunction
Enoki, Y., Watanabe, H., Arake, R., Fujimura, R., Ishiodori, K., Imafuku, T., Nishida, K., Sugimoto, R., Nagao, S., Miyamura, S., et al. (2017) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12202 · Cited by 158
Epidemiologic and methodologic problems in determining nutritional status of older persons. Proceedings of a conference. Albuquerque, New Mexico, October 19-21, 1988.
(1989) · PubMed · Cited by 154
Young versus aged microbiota transplants to germ-free mice: increased short-chain fatty acids and improved cognitive performance
Lee, J., Venna, V. R., Durgan, D. J., Shi, H., Hudobenko, J., Putluri, N., Petrosino, J. F., McCullough, L. D., & Bryan, R. M. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1814107 · Cited by 151
Effectiveness of Creatine Supplementation on Aging Muscle and Bone: Focus on Falls Prevention and Inflammation
Candow, D. G., Forbes, S. C., Chilibeck, P. D., Cornish, S. M., Antonio, J., & Kreider, R. B. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8040488 · Cited by 149
Beneficial bacteria inhibit cachexia
Varian, B. J., Goureshetti, S., Poutahidis, T., Lakritz, J. R., Levkovich, T., Kwok, C., Teliousis, K., Ibrahim, Y. M., Mirabal, S., & Erdman, S. E. (2016) · Oncotarget · doi:10.18632/oncotarget.7730 · Cited by 146
Effect of Lactobacillus plantarum TWK10 on Exercise Physiological Adaptation, Performance, and Body Composition in Healthy Humans
Huang, W.-C., Lee, M., Lee, C., Ng, K., Hsu, Y.-J., Tsai, T., Young, S.-L., Lin, J., & Huang, C. (2019) · Nutrients · doi:10.3390/nu11112836 · Cited by 140
Gut microbiota can transfer fiber characteristics and lipid metabolic profiles of skeletal muscle from pigs to germ-free mice
Yan, H., Diao, H., Xiao, Y., Li, W., Yu, B., He, J., Yu, J., Zheng, P., Mao, X., Luo, Y., et al. (2016) · Scientific Reports · doi:10.1038/srep31786 · Cited by 138
Self-citation
The relationship between sarcopenia and fragility fracture—a systematic review
Wong, R. M. Y., Wong, H., Zhang, N., Chow, S. K., Chau, W., Wang, J., Chim, Y. N., Leung, K., & Cheung, W. (2019) · Osteoporosis International · doi:10.1007/s00198-018-04828-0 · Cited by 131
Self-citation
Multiple Levels of Influence on Older Adults' Attendance and Adherence to Community Exercise Classes
Hawley-Hague, H., Horne, M., Campbell, M., Demack, S., Skelton, D. A., & Todd, C. J. (2013) · The Gerontologist · doi:10.1093/geront/gnt075 · Cited by 129
Aging and sarcopenia associate with specific interactions between gut microbes, serum biomarkers and host physiology in rats
Siddharth, J., Chakrabarti, A., Pannérec, A., Karaz, S., Morin-Rivron, D., Masoodi, M., Feige, J. N., & Parkinson, S. J. (2017) · Aging · doi:10.18632/aging.101262 · Cited by 127
Lactobacillus paracasei PS23 decelerated age-related muscle loss by ensuring mitochondrial function in SAMP8 mice
Chen, L.-H., Huang, S.-Y., Huang, K.-C., Hsu, C.-C., Yang, K.-C., Li, L.-A., Chan, C.-H., & Huang, H.-Y. (2019) · Aging · doi:10.18632/aging.101782 · Cited by 117
Kefir Supplementation Modifies Gut Microbiota Composition, Reduces Physical Fatigue, and Improves Exercise Performance in Mice
Hsu, Y.-J., Huang, W.-C., Lin, J.-S., Chen, Y.-M., Ho, S.-T., Huang, C.-C., & Tung, Y.-T. (2018) · Nutrients · doi:10.3390/nu10070862 · Cited by 116
Is sarcopenia associated with an increased risk of all-cause mortality and functional disability?
Kelley, G. A., & Kelley, K. S. (2017) · Experimental Gerontology · doi:10.1016/j.exger.2017.06.008 · Cited by 109
Creatine Supplementation and Skeletal Muscle Metabolism for Building Muscle Mass- Review of the Potential Mechanisms of Action
Farshidfar, F., Pinder, M. A., & Myrie, S. B. (2017) · Current Protein and Peptide Science · doi:10.2174/1389203718666170606105108 · Cited by 104
Special considerations of antibiotic prescription in the geriatric population
Beckett, C. L., Harbarth, S., & Huttner, B. D. (2014) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2014.08.018 · Cited by 103
Lactobacillus salivarius Subspecies salicinius SA-03 is a New Probiotic Capable of Enhancing Exercise Performance and Decreasing Fatigue
Lee, M., Hsu, Y.-J., Ho, H.-H., Hsieh, S., Kuo, Y., Sung, H., & Huang, C. (2020) · Microorganisms · doi:10.3390/microorganisms8040545 · Cited by 100
Uremic metabolites impair skeletal muscle mitochondrial energetics through disruption of the electron transport system and matrix dehydrogenase activity
Thome, T., Salyers, Z. R., Kumar, R. A., Hahn, D., Berru, F. N., Ferreira, L. F., Scali, S. T., & RYAN, T. E. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00098.2019 · Cited by 92
Protective Effects of Ghrelin on Fasting-Induced Muscle Atrophy in Aging Mice
Wu, C.-S., Wei, Q., Wang, H., Kim, D. M., Balderas, M., Wu, G., Lawler, J., Safe, S., Guo, S., Devaraj, S., et al. (2020) · The Journals of Gerontology: Series A · doi:10.1093/gerona/gly256 · Cited by 81
Metabolic Perturbations from Step Reduction in Older Persons at Risk for Sarcopenia: Plasma Biomarkers of Abrupt Changes in Physical Activity
Saoi, M., Li, A., McGlory, C., Stokes, T., von Allmen, M., Phillips, S. M., & Britz‐McKibbin, P. (2019) · Metabolites · doi:10.3390/metabo9070134 · Cited by 75
Targeted Depletion of Bacteria from Mixed Populations by Programmable Adhesion with Antagonistic Competitor Cells
Ting, S., Martínez‐García, E., Huang, S., Bertolli, S. K., Kelly, K. A., Cutler, K. J., Su, E. D., Zhi, H., Tang, Q., Radey, M. C., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.05.006 · Cited by 75
Implications of the human microbiome in inflammatory bowel diseases
Bakhtiar, S. M., LeBlanc, J. G., Salvucci, E., Ali, A., Martín, R., Langella, P., Chatel, J., Miyoshi, A., Bermúdez‐Humarán, L. G., & Azevedo, V. (2013) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12111 · Cited by 74
A Critical Mutualism – Competition Interplay Underlies the Loss of Microbial Diversity in Sedentary Lifestyle
Castellanos, N. P., Díez, G. G., Almagro, C. A., Bailén, M., Bressa, C., González-Soltero, R., Pérez, M., & Larrosa, M. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.03142 · Cited by 74
Physical fitness in community‐dwelling older adults is linked to dietary intake, gut microbiota, and metabolomic signatures
Castro-Mejía, J. L., Khakimov, B., Krych, Ł., Bülow, J., Bechshøft, R. L., Højfeldt, G. W., Mertz, K. H., Garne, E. S., Schacht, S. R., Ahmad, H. F., et al. (2020) · Aging Cell · doi:10.1111/acel.13105 · Cited by 72
Anti-fatigue property of the oyster polypeptide fraction and its effect on gut microbiota in mice
Xiao, M., Lin, L., Chen, H., Ge, X., Huang, Y., Zheng, Z., Li, S., Pan, Y., Liu, B., & Zeng, F. (2020) · Food & Function · doi:10.1039/d0fo01713b · Cited by 69
Metronidazole Causes Skeletal Muscle Atrophy and Modulates Muscle Chronometabolism
Manickam, R., Oh, H. Y. P., Tan, C. K., Paramalingam, E., & Wahli, W. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082418 · Cited by 66
Metabolites related to gut bacterial metabolism, peroxisome proliferator‐activated receptor‐alpha activation, and insulin sensitivity are associated with physical function in functionally‐limited older adults
Lustgarten, M. S., Price, L. L., Chalé, A., & Fielding, R. A. (2014) · Aging Cell · doi:10.1111/acel.12251 · Cited by 64
Effects of Three-Month Intake of Synbiotic on Inflammation and Body Composition in the Elderly: A Pilot Study
Neto, J. V., de Melo, C., & Ribeiro, S. M. L. (2013) · Nutrients · doi:10.3390/nu5041276 · Cited by 59
Toxoplasma gondii infection triggers chronic cachexia and sustained commensal dysbiosis in mice
Hatter, J. A., Kouche, Y. M., Melchor, S. J., Ng, K., Bouley, D. M., Boothroyd, J. C., & Ewald, S. E. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204895 · Cited by 58
Effect of Caloric Restriction on BMI, Gut Microbiota, and Blood Amino Acid Levels in Non-Obese Adults
Zou, H., Wang, D., Ren, H., Chen, P., Fang, C., Shi, Z., Zhang, P., Wang, J., Wang, J., Cai, K., et al. (2020) · Nutrients · doi:10.3390/nu12030631 · Cited by 51
Indoxyl sulfate induces myotube atrophy by ROS-ERK and JNK-MAFbx cascades
Changchien, C., Lin, Y., Cheng, Y., Chang, H., Peng, Y., & Chen, Y. (2019) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2019.02.023 · Cited by 50
Quorum sensing molecules as a novel microbial factor impacting muscle cells
Spiegeleer, A. D., Elewaut, D. S., Noortgate, N. J. V. D., Janssens, Y., Debunne, N., Langenhove, S. V., Govindarajan, S., Spiegeleer, B. M. J. D., & Wynendaele, E. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.165646 · Cited by 50
Supplementation of nano-bubble curcumin extract improves gut microbiota composition and exercise performance in mice
Chen, Y., Chiu, W., Chiu, Y., Li, T., Sung, H., & Hsiao, C.-Y. (2020) · Food & Function · doi:10.1039/c9fo02487e · Cited by 50
Contemporary Applications of Fecal Microbiota Transplantation to Treat Intestinal Diseases in Humans
Staley, C. M., Khoruts, A., & Sadowsky, M. J. (2017) · Archives of Medical Research · doi:10.1016/j.arcmed.2017.11.006 · Cited by 48
Independent and Interactive Effects of Habitually Ingesting Fermented Milk Products Containing Lactobacillus casei Strain Shirota and of Engaging in Moderate Habitual Daily Physical Activity on the Intestinal Health of Older People
Aoyagi, Y., Amamoto, R., Park, S. J., Honda, Y., Shimamoto, K., Kushiro, A., Tsuji, H., Matsumoto, H., Shimizu, K., Miyazaki, K., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01477 · Cited by 48
Exercise Training Combined with Bifidobacterium longum OLP-01 Supplementation Improves Exercise Physiological Adaption and Performance
Huang, W.-C., Hsu, Y.-J., Huang, C., Liu, H., & Lee, M. (2020) · Nutrients · doi:10.3390/nu12041145 · Cited by 48
AChRs Degeneration at NMJ in Aging-Associated Sarcopenia–A Systematic Review
Bao, Z., Cui, C., Chow, S. K., Qin, L., Wong, R. M. Y., & Cheung, W. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.597811 · Cited by 48
Self-citation
The Associations between Circulating Bile Acids and the Muscle Volume in Patients with Non-alcoholic Fatty Liver Disease (NAFLD)
Kobayashi, Y., Hara, N., Sugimoto, R., Mifuji‐Moroka, R., Tanaka, H., Eguchi, A., Iwasa, M., Hasegawa, H., Iwata, K., Takei, Y., et al. (2017) · Internal Medicine · doi:10.2169/internalmedicine.56.7796 · Cited by 47
The double‐edged sword of endoplasmic reticulum stress in uremic sarcopenia through myogenesis perturbation
Jheng, J.-R., Chen, Y.-S., Ao, U. I., Chan, D., Huang, J., Hung, K., Tarng, D.-C., & Chiang, C. (2018) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12288 · Cited by 47
Gut microbiota composition influences outcomes of skeletal muscle nutritional intervention via blended protein supplementation in posttransplant patients with hematological malignancies
Ren, G., Zhang, J., Li, M., Tang, Z., Yang, Z., Cheng, G., & Wang, J. (2020) · Clinical Nutrition · doi:10.1016/j.clnu.2020.04.030 · Cited by 41
The effects of whey and soy proteins on growth performance, gastrointestinal digestion, and selected physiological responses in rats
Wróblewska, B., Juśkiewicz, J., Kroplewski, B., Jurgoński, A., Wasilewska, E. M., Złotkowska, D., & Markiewicz, L. H. (2018) · Food & Function · doi:10.1039/c7fo01204g · Cited by 39
Basal Diet Determined Long-Term Composition of the Gut Microbiome and Mouse Phenotype to a Greater Extent than Fecal Microbiome Transfer from Lean or Obese Human Donors
Rodriguez, D. M., Benninghoff, A. D., Aardema, N. D. J., Phatak, S., & Hintze, K. J. (2019) · Nutrients · doi:10.3390/nu11071630 · Cited by 37
Supplementation with Saccharomyces boulardii Increases the Maximal Oxygen Consumption and Maximal Aerobic Speed Attained by Rats Subjected to an Incremental-Speed Exercise
Soares, A. D. N., Wanner, S. P., Morais, E. S. S., Hudson, A. S. R., Martins, F. S., & Cardoso, V. N. (2019) · Nutrients · doi:10.3390/nu11102352 · Cited by 35
Investigation of the Diet-Gut-Muscle Axis in the Osteoporotic Fractures in Men Study
Barger, K., Langsetmo, L., ORWOLL, E. S., & Lustgarten, M. S. (2020) · The journal of nutrition health & aging · doi:10.1007/s12603-020-1344-1 · Cited by 35
Dysbacteriosis‐induced LPS elevation disturbs the development of muscle progenitor cells by interfering with retinoic acid signaling
Song, J., Wang, C., Long, D., Li, Z., You, L., Brand‐Saberi, B., Wang, G., & Yang, X. (2020) · The FASEB Journal · doi:10.1096/fj.201902965r · Cited by 34
Heritability and Clinical Determinants of Serum Indoxyl Sulfate and p-Cresyl Sulfate, Candidate Biomarkers of the Human Microbiome Enterotype
Viaene, L., Thijs, L., Jin, Y., Liu, Y., Gu, Y., Meijers, B. K. I., Claes, K. J., Staessen, J. A., & Evenepoel, P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0079682 · Cited by 34
Supplementation with Beef Extract Improves Exercise Performance and Reduces Post-Exercise Fatigue Independent of Gut Microbiota
Hsu, T.-H., Chiu, C.-C., Wang, Y.-C., Chen, T.-H., Chen, Y.-H., Lee, Y.-P., Hung, S.-W., Wu, C.-P., & Chuang, H.-L. (2018) · Nutrients · doi:10.3390/nu10111740 · Cited by 20
Lactobacillus curvatus CP2998 Prevents Dexamethasone-Induced Muscle Atrophy in C2C12 Myotubes
KATSUKI, R., SAKATA, S., Nakao, R., Oishi, K., & Nakamura, Y. (2019) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.65.455 · Cited by 20
Exercise with food withdrawal at thermoneutrality impacts fuel use, the microbiome, AMPK phosphorylation, muscle fibers, and thyroid hormone levels in rats
Giacco, A., Paoli, G. D., Simiele, R., Caterino, M., Ruoppolo, M., Bloch, W., Kraaij, R., Uitterlinden, A. G., Santillo, A., Senese, R., et al. (2020) · Physiological Reports · doi:10.14814/phy2.14354 · Cited by 19
Impact of perinatal prebiotic consumption on gestating mice and their offspring: a preliminary report
Desbuards, N., Gourbeyre, P., Haure‐Mirande, J., Darmaun, D., Champ, M. M. J., & Bodinier, M. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511004363 · Cited by 18
Proteome and microbiota analysis highlight Lactobacillus plantarum TWK10 supplementation improves energy metabolism and exercise performance in mice
Chen, Y., Liao, C., Huang, Y., Chen, M., Huang, C., Chen, W.-C., & Chiu, Y. (2020) · Food Science & Nutrition · doi:10.1002/fsn3.1635 · Cited by 14

Research works printed but not linked: 1

Das Neves RX, 2017, Germ free mice accelerate cachexia‐associated cancer, Cancer Res, 77

Sorted by citations

Epidemiology of sarcopenia: Prevalence, risk factors, and consequences
Yuan, S., & Larsson, S. C. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155533 · Cited by 1,114
Skeletal muscle oxidative stress and inflammation in aging: Focus on antioxidant and anti-inflammatory therapy
Chen, M., Wang, Y., Deng, S., Lian, Z., & Yu, K. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.964130 · Cited by 187
Gut microbiota–bile acid–skeletal muscle axis
Mancin, L., Wu, G. D., & Paoli, A. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2022.10.003 · Cited by 183
Sarcopenia in youth
Jung, H. N., Jung, C. H., & Hwang, Y. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155557 · Cited by 163
Fat infiltration in skeletal muscle: Influential triggers and regulatory mechanism
Wang, L., Valencak, T. G., & Shan, T. (2024) · iScience · doi:10.1016/j.isci.2024.109221 · Cited by 149

See all 363

Authors: Liu, C., Cheung, W., Li, J., Chow, S. K., Yu, J., Wong, S. H., Ip, M., Sung, J. J. Y., & Wong, R. M. Y.
Affiliations: Chinese University of Hong Kong (HK)
Corresponding author: Wong, Ronald Man Yeung
ORCID: Liu, Chaoran
Cheung, Wing‐Hoi
Li, Jie
Chow, Simon Kwoon‐Ho
Yu, Jun
Wong, Sunny Hei
Ip, Margaret
Sung, Joseph Jao Yiu
Wong, Ronald Man Yeung
Venue: Journal of Cachexia, Sarcopenia and Muscle
Publisher: Wiley
Published: 2021-09-14
Volume: 12
Issue: 6
Pages: 1393-1407
ISSN: 2190-5991 (ISSN-L)
2190-6009
DOI: 10.1002/jcsm.12784
PMC: PMC8718038
OpenAlex: W3201032809
Cited by: 363
References: 116
Citations by year: 2026: 75 · 2025: 96 · 2024: 82 · 2023: 75 · 2022: 31 · 2021: 4
FWCI: 5.04
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Journal of Cachexia Sarcopenia and Muscle (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: gut microbiota, sarcopenia, gut-muscle axis, muscle mass, muscle function, aging, probiotics, prebiotics, short-chain fatty acids, fecal microbiota transplantation, germ-free mice, Lactobacillus, Bifidobacterium, caloric restriction, physical activity, physical performance, inflammation, mitochondrial function, neuromuscular junction
MeSH terms: Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Aged, Animals, Female, Humans, Male, Mice, Sarcopenia, Prebiotics, Synbiotics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Understanding the gut microbiota and sarcopenia: a systematic review

Abstract

Overview

Integrity signals

Figures

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks