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Review

A Narrative Review of Gut-Muscle Axis and Sarcopenia: The Potential Role of Gut Microbiota

ORCID Icon, &
Pages 1263-1273 | Published online: 13 Apr 2021

References

  • Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.
  • Chen LK, Woo J, Assantachai P, et al. Asian working group for sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc. 2020;21:300–307.
  • Shafiee G, Keshtkar A, Soltani A, Ahadi Z, Larijani B, Heshmat R. Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies. J Diabetes Metab Disord. 2017;16:21.
  • Fox B, Henwood T, Schaap L, et al. Adherence to a standardized protocol for measuring grip strength and appropriate cut-off values in adults over 65 years with sarcopenia: a systematic review protocol. JBI Database System Rev Implement Rep. 2015;13:50–59.
  • Van Ancum JM, Alcazar J, Meskers C, Nielsen BR, Suetta C, Maier AB. Impact of using the updated EWGSOP2 definition in diagnosing sarcopenia: a clinical perspective. Arch Gerontol Geriatr. 2020;90:104125.
  • Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: european consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39:412–423.
  • Lauretani F, Russo CR, Bandinelli S, et al. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol (1985). 2003;95:1851–1860.
  • Martone AM, Marzetti E, Salini S, et al. Sarcopenia identified according to the EWGSOP2 definition in community-living people: prevalence and clinical features. J Am Med Dir Assoc. 2020.
  • Kim M, Won CW. Prevalence of sarcopenia in community-dwelling older adults using the definition of the European Working Group on Sarcopenia in Older People 2: findings from the Korean Frailty and Aging Cohort Study. Age Ageing. 2019;48:910–916.
  • Waltz TB, Fivenson EM, Morevati M, et al. Sarcopenia, aging and prospective interventional strategies. Curr Med Chem. 2018;25:5588–5596.
  • Liguori I, Russo G, Aran L, et al. Sarcopenia: assessment of disease burden and strategies to improve outcomes. Clin Interv Aging. 2018;13:913–927.
  • Chen J, Douglass J, Prasath V, et al. The microbiome and breast cancer: a review. Breast Cancer Res Treat. 2019;178:493–496.
  • Li J, Jia H, Cai X, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32:834–841.
  • Dave M, Higgins PD, Middha S, Rioux KP. The human gut microbiome: current knowledge, challenges, and future directions. Transl Res. 2012;160:246–257.
  • Jager R, Zaragoza J, Purpura M, et al. Probiotic administration increases amino acid absorption from plant protein: a placebo-controlled, randomized, double-blind, multicenter, crossover study. Probiotics Antimicrob Proteins. 2020.
  • Ford AC, Harris LA, Lacy BE, et al. Systematic review with meta-analysis: the efficacy of prebiotics, probiotics, synbiotics and antibiotics in irritable bowel syndrome. Aliment Pharmacol Ther. 2018;48(10):1044–1060. doi:10.1111/apt.15001
  • Mangiola F, Nicoletti A, Gasbarrini A, Ponziani FR. Gut microbiota and aging. Eur Rev Med Pharmacol Sci. 2018;22:7404–7413.
  • Kim S, Jazwinski SM. The gut microbiota and healthy aging: a mini-review. Gerontology. 2018;64:513–520.
  • Seifi N, Safarian M, Nematy M, Rezvani R, Khadem-Rezaian M, Sedaghat A. Effects of synbiotic supplementation on energy and macronutrients homeostasis and muscle wasting of critical care patients: study protocol and a review of previous studies. Trials. 2020;21:221.
  • Fielding RA, Reeves AR, Jasuja R, Liu C, Barrett BB, Lustgarten MS. Muscle strength is increased in mice that are colonized with microbiota from high-functioning older adults. Exp Gerontol. 2019;127:110722.
  • Buigues C, Fernandez-Garrido J, Pruimboom L, et al. Effect of a prebiotic formulation on frailty syndrome: a randomized, double-blind clinical trial. Int J Mol Sci. 2016;17.
  • Munukka E, Rintala A, Toivonen R, et al. Faecalibacterium prausnitzii treatment improves hepatic health and reduces adipose tissue inflammation in high-fat fed mice. ISME J. 2017;2017:24.
  • Lee MC, Hsu YJ, Ho HH, et al. Lactobacillus salivarius subspecies salicinius SA-03 is a new probiotic capable of enhancing exercise performance and decreasing fatigue. Microorganisms. 2020;8.
  • Lee MC, Hsu YJ, Chuang HL, et al. In vivo ergogenic properties of the bifidobacterium longum OLP-01 isolated from a weightlifting gold medalist. Nutrients. 2019;11.
  • Nay K, Jollet M, Goustard B, et al. bacteria are critical for optimal muscle function: a potential link with glucose homeostasis. Am J Physiol Endocrinol Metab. 2019;317:E158–E171.
  • Ragul K, Kandasamy S, Devi PB, Shetty PH. Evaluation of functional properties of potential probiotic isolates from fermented brine pickle. Food Chem. 2020;311:126057.
  • Ragul K, Syiem I, Sundar K, Shetty PH. Characterization of probiotic potential of Bacillus species isolated from a traditional brine pickle. J Food Sci Technol. 2017;54:4473–4483.
  • Kazmierczak-Siedlecka K, Folwarski M, Skonieczna-Zydecka K, Ruszkowski J, Makarewicz W. The use of Lactobacillus plantarum 299v (DSM 9843) in cancer patients receiving home enteral nutrition - study protocol for a randomized, double-blind, and placebo-controlled trial. Nutr J. 2020;19:98.
  • Huang WC, Lee MC, Lee CC, et al. Effect of Lactobacillus plantarum TWK10 on exercise physiological adaptation, performance, and body composition in healthy humans. Nutrients. 2019;11.
  • Sun L, Li J, Lan LL, Li XA. The effect of fecal microbiota transplantation on Hepatic myelopathy: a case report. Medicine (Baltimore). 2019;98:e16430.
  • Chen YM, Wei L, Chiu YS, et al. Lactobacillus plantarum TWK10 supplementation improves exercise performance and increases muscle mass in mice. Nutrients. 2016;8(4):205.
  • Marzetti E, Calvani R, Cesari M, et al. Mitochondrial dysfunction and sarcopenia of aging: from signaling pathways to clinical trials. Int J Biochem Cell Biol. 2013;45:2288–2301.
  • Joseph AM, Adhihetty PJ, Buford TW, et al. The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high- and low-functioning elderly individuals. Aging Cell. 2012;11:801–809.
  • Coen PM, Jubrias SA, Distefano G, et al. Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults. J Gerontol a Biol Sci Med Sci. 2013;68:447–455.
  • Leduc-Gaudet JP, Picard M, St-Jean PF, et al. Mitochondrial morphology is altered in atrophied skeletal muscle of aged mice. Oncotarget. 2015;6:17923–17937.
  • Short KR, Vittone JL, Bigelow ML, Proctor DN, Nair KS. Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am J Physiol Endocrinol Metab. 2004;286:E92–E101.
  • Kim Y, Triolo M, Hood DA. Impact of aging and exercise on mitochondrial quality control in skeletal muscle. Oxid Med Cell Longev. 2017;2017:3165396.
  • Franco-Obregon A, Gilbert JA. The microbiome-mitochondrion connection: common ancestries, common mechanisms, common goals. mSystems. 2017;2.
  • Lahiri S, Kim H, Garcia-Perez I, et al. gut microbiota influences skeletal muscle mass and function in mice. Sci Transl Med. 2019;11.
  • Barton-Davis ER, Shoturma DI, Musaro A, Rosenthal N, Sweeney HL. Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function. Proc Natl Acad Sci U S A. 1998;95:15603–15607.
  • Bosch-Marce M, Wee CD, Martinez TL, et al. 1 in muscle modulates the phenotype of severe SMA mice. Hum Mol Genet. 2011;20:1844–1853.
  • Brisson BK, Spinazzola J, Park S, Barton ER. Viral expression of insulin-like growth factor I E-peptides increases skeletal muscle mass but at the expense of strength. Am J Physiol Endocrinol Metab. 2014;306:E965–E974.
  • Abou-Samra M, Selvais CM, Boursereau R, Lecompte S, Noel L, Brichard SM. AdipoRon, a new therapeutic prospect for Duchenne muscular dystrophy. J Cachexia Sarcopenia Muscle. 2020.
  • Brunk UT, Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur J Biochem. 2002;269:1996–2002.
  • Ebner N, Anker SD, von Haehling S. Recent developments in the field of cachexia, sarcopenia, and muscle wasting: highlights from the 11th Cachexia Conference. J Cachexia Sarcopenia Muscle. 2019;10:218–225.
  • Wilson D, Jackson T, Sapey E, Lord JM. Frailty and sarcopenia: the potential role of an aged immune system. Ageing Res Rev. 2017;36:1–10.
  • Yoo JI, Ha YC, Choi H, et al. Malnutrition and chronic inflammation as risk factors for sarcopenia in elderly patients with hip fracture. Asia Pac J Clin Nutr. 2018;27:527–532.
  • Byun MK, Cho EN, Chang J, Ahn CM, Kim HJ. Sarcopenia correlates with systemic inflammation in COPD. Int J Chron Obstruct Pulmon Dis. 2017;12:669–675.
  • Abou-Samra M, Selvais CM, Boursereau R, Lecompte S, Noel L, Brichard SM. AdipoRon, a new therapeutic prospect for Duchenne muscular dystrophy. J Cachexia Sarcopenia Muscle. 2020.
  • Mentella MC, Scaldaferri F, Pizzoferrato M, et al. Nutrition, IBD and Gut Microbiota: a Review. Nutrients. 2020;12:4.
  • Graziani C, Talocco C, De Sire R, et al. Intestinal permeability in physiological and pathological conditions: major determinants and assessment modalities. Eur Rev Med Pharmacol Sci. 2019;23(2):795–810.
  • De Sire R, Talocco C, Petito V, et al. [Microbiota and inflammatory bowel disease: an update]. Recenti Prog Med. 2018;109(12):570–573. [Article in Italian].
  • Pizzoferrato M, de Sire R, Ingravalle F, et al. Characterization of Sarcopenia in an IBD population attending an Italian Gastroenterology Tertiary Center. Nutrients. 2019;11:10.
  • Scaldaferri F, Pizzoferrato M, Lopetuso LR, et al. Nutrition and IBD: malnutrition and/or sarcopenia? A practical guide. Gastroenterol Res Pract. 2017;2017:8646495.
  • de Sire R, Rizzatti G, Ingravalle F, et al. Skeletal muscle-gut axis: emerging mechanisms of sarcopenia for intestinal and extra intestinal diseases. Minerva Gastroenterol Dietol. 2018;64(4):351–362.
  • Picca A, Ponziani FR, Calvani R, et al. Gut microbial, inflammatory and metabolic signatures in older people with physical frailty and sarcopenia: results from the BIOSPHERE study. Nutrients. 2019;12.
  • Siddharth J, Chakrabarti A, Pannerec A, et al. Aging and sarcopenia associate with specific interactions between gut microbes, serum biomarkers and host physiology in rats. Aging (Albany NY). 2017;9:1698–1720.
  • Gophna U, Konikoff T, Nielsen HB. Oscillospira and related bacteria - From metagenomic species to metabolic features. Environ Microbiol. 2017;19:835–841.
  • Padoan A, Plebani M, Basso D. Inflammation and pancreatic cancer: focus on metabolism, cytokines, and immunity. Int J Mol Sci. 2019;20.
  • Tuomisto AE, Makinen MJ, Vayrynen JP. Systemic inflammation in colorectal cancer: underlying factors, effects, and prognostic significance. World J Gastroenterol. 2019;25:4383–4404.
  • Dev R, Wong A, Hui D, Bruera E. The evolving approach to management of cancer cachexia. Oncology (Williston Park). 2017;31:23–32.
  • Ali S, Garcia JM. Sarcopenia, cachexia and aging: diagnosis, mechanisms and therapeutic options - a mini-review. Gerontology. 2014;60:294–305.
  • Dunne RF, Loh KP, Williams GR, Jatoi A, Mustian KM, Mohile SG. Cachexia and sarcopenia in older adults with cancer: a comprehensive review. Cancers (Basel). 2019;11.
  • Bindels LB, Beck R, Schakman O, et al. Restoring specific lactobacilli levels decreases inflammation and muscle atrophy markers in an acute leukemia mouse model. PLoS One. 2012;7:e37971.
  • Bindels LB, Neyrinck AM, Claus SP, et al. Synbiotic approach restores intestinal homeostasis and prolongs survival in leukaemic mice with cachexia. Isme J. 2016;10:1456–1470.
  • Potgens SA, Brossel H, Sboarina M, et al. Klebsiella oxytoca expands in cancer cachexia and acts as a gut pathobiont contributing to intestinal dysfunction. Sci Rep. 2018;8:12321.
  • Cerda B, Perez M, Perez-Santiago JD, Tornero-Aguilera JF, Gonzalez-Soltero R, Larrosa M. Gut microbiota modification: another piece in the puzzle of the benefits of physical exercise in health? Front Physiol. 2016;7:51.
  • J Y R, H M C, H I Y, et al. Dysregulated autophagy mediates sarcopenic obesity and its complications via AMPK and PGC1alpha signaling pathways: potential involvement of gut dysbiosis as a pathological link. Int J Mol Sci. 2020;21:18.
  • Maltais ML, Ladouceur JP, Dionne IJ. The effect of resistance training and different sources of postexercise protein supplementation on muscle mass and physical capacity in sarcopenic elderly men. J Strength Cond Res. 2016;30:1680–1687.
  • Strasser B, Keinrad M, Haber P, Schobersberger W. Efficacy of systematic endurance and resistance training on muscle strength and endurance performance in elderly adults–a randomized controlled trial. Wien Klin Wochenschr. 2009;121:757–764.
  • Martone AM, Marzetti E, Calvani R, et al. Exercise and protein intake: a synergistic approach against sarcopenia. Biomed Res Int. 2017;2017:2672435.
  • Dhillon RJ, Hasni S. Pathogenesis and management of sarcopenia. Clin Geriatr Med. 2017;33:17–26.
  • Landi F, Calvani R, Tosato M, et al. Protein intake and muscle health in old age: from biological plausibility to clinical evidence. Nutrients. 2016;8:5.
  • Marshall RN, Smeuninx B, Morgan PT, et al. Nutritional strategies to offset disuse-induced skeletal muscle atrophy and anabolic resistance in older adults: from whole-foods to isolated ingredients. Nutrients. 2020;12:5.
  • Invernizzi M, de Sire A, D’Andrea F, et al. Effects of essential amino acid supplementation and rehabilitation on functioning in hip fracture patients: a pilot randomized controlled trial. Aging Clin Exp Res. 2019;31(10):1517–1524.
  • Beaudart C, Buckinx F, Rabenda V, et al. The effects of vitamin D on skeletal muscle strength, muscle mass, and muscle power: a systematic review and meta-analysis of randomized controlled trials. J Clin Endocrinol Metab. 2014;99(11):4336–4345.
  • Gimigliano F, Moretti A, de Sire A, et al. The combination of vitamin D deficiency and overweight affects muscle mass and function in older post-menopausal women. Aging Clin Exp Res. 2018;30(6):625–631.
  • Iolascon G, Moretti A, de Sire A, et al. Effectiveness of calcifediol in improving muscle function in post-menopausal women: a prospective cohort study. Adv Ther. 2017;34(3):744–752.
  • Avola M, Mangano G, Testa G, et al. Rehabilitation strategies for patients with femoral neck fractures in sarcopenia: a narrative review. J Clin Med. 2020;9:10.
  • Evans CC, LePard KJ, Kwak JW, et al. Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS One. 2014;9:e92193.
  • Zhao X, Zhang Z, Hu B, Huang W, Yuan C, Zou L. Response of gut microbiota to metabolite changes induced by endurance exercise. Front Microbiol. 2018;9:765.
  • Morita E, Yokoyama H, Imai D, et al. Aerobic exercise training with brisk walking increases intestinal bacteroides in healthy elderly women. Nutrients. 2019;11.
  • Tottey W, Feria-Gervasio D, Gaci N, et al. Colonic transit time is a driven force of the gut microbiota composition and metabolism: in vitro evidence. J Neurogastroenterol Motil. 2017;23:124–134.
  • Abbas A, Wilding GE, Sitrin MD. Does colonic transit time affect colonic pH?. J Gastroenterol Hepatol Res. 2014;3:1103–1107.
  • De Schryver AM, Keulemans YC, Peters HP, et al. Effects of regular physical activity on defecation pattern in middle-aged patients complaining of chronic constipation. Scand J Gastroenterol. 2005;40:422–429.
  • Matsumoto M, Inoue R, Tsukahara T, et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem. 2008;72:572–576.
  • Walker AW, Duncan SH, McWilliam LE, Child MW, Flint HJ. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol. 2005;71:3692–3700.
  • Vlasova AN, Kandasamy S, Chattha KS, Rajashekara G, Saif LJ. Comparison of probiotic lactobacilli and bifidobacteria effects, immune responses and rotavirus vaccines and infection in different host species. Vet Immunol Immunopathol. 2016;172:72–84.
  • Damanti S, Azzolino D, Roncaglione C, Arosio B, Rossi P, Cesari M. Efficacy of nutritional interventions as stand-alone or synergistic treatments with exercise for the management of sarcopenia. Nutrients. 2019;11.
  • Zhu Y, Lin X, Zhao F, et al. Erratum: meat, dairy and plant proteins alter bacterial composition of rat gut bacteria. Sci Rep. 2015;5:16546.
  • Ma N, Tian Y, Wu Y, Ma X. Contributions of the interaction between dietary protein and gut microbiota to intestinal health. Curr Protein Pept Sci. 2017;18:795–808.
  • Dai X, Karring H. A determination and comparison of urease activity in feces and fresh manure from pig and cattle in relation to ammonia production and pH changes. PLoS One. 2014;9:e110402.
  • Moreno-Perez D, Bressa C, Bailen M, et al. Effect of a Protein Supplement on the Gut Microbiota of Endurance Athletes: A Randomized, Controlled, Double-Blind Pilot Study[J]. Nutrients. 2018,10(3).
  • Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–227.
  • Moreno-Perez D, Bressa C, Bailen M, et al. Effect of a protein supplement on the gut microbiota of endurance athletes: a randomized, controlled, double-blind pilot study. Nutrients. 2018;10.
  • Blanton LV, Charbonneau MR, Salih T, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016;351.
  • Newsome SD, Feeser KL, Bradley CJ, Wolf C, Takacs-Vesbach C, Fogel ML. Isotopic and genetic methods reveal the role of the gut microbiome in mammalian host essential amino acid metabolism. Proc Biol Sci. 2020;287:20192995.
  • Wolfe RR. Branched-chain amino acids and muscle protein synthesis in humans: myth or reality? J Int Soc Sports Nutr. 2017;14:30.
  • Santos CS, Nascimento F. Isolated branched-chain amino acid intake and muscle protein synthesis in humans: a biochemical review. Einstein (Sao Paulo). 2019;17:B4898.
  • Okamoto T, Morino K, Ugi S, et al. Microbiome potentiates endurance exercise through intestinal acetate production. Am J Physiol Endocrinol Metab. 2019;316:E956–E966.
  • Frampton J, Murphy KG, Frost G, Chambers ES. Short-chain fatty acids as potential regulators of skeletal muscle metabolism and function. Nat Metab. 2020;2:840–848.
  • Hu J, Lin S, Zheng B, Cheung P. Short-chain fatty acids in control of energy metabolism. Crit Rev Food Sci Nutr. 2018;58:1243–1249.
  • Scheithauer TP, Dallinga-Thie GM, de Vos WM, Nieuwdorp M, van Raalte DH. Causality of small and large gut microbiota in weight regulation and insulin resistance. Mol Metab. 2016;5:759–770.
  • Lam YY, Ha CW, Hoffmann JM, et al. Effects of dietary fat profile on gut permeability and microbiota and their relationships with metabolic changes in mice. Obesity (Silver Spring). 2015;23:1429–1439.
  • Zou H, Wang D, Ren H, et al. Effect of caloric restriction on BMI, gut microbiota, and blood amino acid levels in non-obese adults. Nutrients. 2020;12.
  • Barger K, Langsetmo L, Orwoll ES, Lustgarten MS. Investigation of the diet-gut-muscle axis in the osteoporotic fractures in men study. J Nutr Health Aging. 2020;24:445–452.
  • Bjorkhaug ST, Aanes H, Neupane SP, et al. Characterization of gut microbiota composition and functions in patients with chronic alcohol overconsumption. Gut Microbes. 2019;10:663–675.
  • Zhang L, Xue X, Zhai R, et al. Timing of calorie restriction in mice impacts host metabolic phenotype with correlative changes in gut microbiota. mSystems. 2019;4:6. doi:10.1128/mSystems.00348-19.
  • Manickam R, Oh H, Tan CK, Paramalingam E, Wahli W. Metronidazole causes skeletal muscle atrophy and modulates muscle chronometabolism. Int J Mol Sci. 2018;19.
  • Huang C, Tomata Y, Kakizaki M, et al. High circulating adiponectin levels predict decreased muscle strength among older adults aged 70 years and over: a prospective cohort study. Nutr Metab Cardiovasc Dis. 2015;25:594–601.
  • Suriano F, Van Hul M, Cani PD. Gut microbiota and regulation of myokine-adipokine function. Curr Opin Pharmacol. 2020;52:9–17.
  • Harada N, Hanaoka R, Hanada K, Izawa T, Inui H, Yamaji R. Hypogonadism alters cecal and fecal microbiota in male mice. Gut Microbes. 2016;7:533–539.
  • Foley KP, Zlitni S, Duggan BM, et al. Gut microbiota impairs insulin clearance in obese mice. Mol Metab. 2020;42:101067.