Advanced search
Publication Cover
Gut Microbes Volume 15, 2023 - Issue 2
Submit an article Journal homepage
2,605
Views
2
CrossRef citations to date
0
Altmetric
Review

Progress of linking gut microbiota and musculoskeletal health: casualty, mechanisms, and translational values

Yu Wanga Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, ChinaView further author information
,
Yusheng Lib Department of Orthopedics, Xiangya Hospital, Central South University, Changsha, China;c National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, ChinaView further author information
,
Lin Bod Department of Rheumatology, The Second Affiliated Hospital of Soochow University, Suzhou, Jiangsu, ChinaView further author information
,
Enyuan Zhoua Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, ChinaView further author information
,
Yanyan Chena Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, ChinaView further author information
,
Shinen Naranmandakhe School of Arts and Sciences, National University of Mongolia, Ulaanbaatar, MongoliaView further author information
,
Wenqing Xieb Department of Orthopedics, Xiangya Hospital, Central South University, Changsha, China;c National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, ChinaView further author information
,
Qin Rua Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-2169-7471View further author information
ORCID Icon,
Lin Chena Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-1005-1202View further author information
ORCID Icon,
Zhaohua Zhuf Clinical Research Centre, Orthopedic Centre, Zhujiang Hospital, Southern Medical University, Guangzhou, ChinaCorrespondence[email protected]
View further author information
,
Changhai Dingf Clinical Research Centre, Orthopedic Centre, Zhujiang Hospital, Southern Medical University, Guangzhou, China;g Department of Rheumatology, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology, Guangzhou, China;h Department of Orthopaedics, Affiliated Hospital of Youjiang Medical University for Nationalities, Baise, China;i Menzies Institute for Medical Research, University of Tasmania, Hobart, AustraliaView further author information
&
Yuxiang Wua Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-9041-4471View further author information
ORCID Icon show all
Article: 2263207 | Received 21 May 2023, Accepted 21 Sep 2023, Published online: 06 Oct 2023

References

  • Petermann-Rocha F, Balntzi V, Gray SR, Lara J, Ho FK, Pell JP, Celis‐Morales C. Global prevalence of sarcopenia and severe sarcopenia: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle. 2022;13(1):86–35. doi:10.1002/jcsm.12783.
  • Ayers C, Kansagara D, Lazur B, Fu R, Kwon A, Harrod C. Effectiveness and safety of treatments to prevent fractures in people with low bone mass or primary osteoporosis: a living systematic review and network meta-analysis for the American college of physicians. Ann Intern Med. 2023;176(2):182–195. doi:10.7326/M22-0684.
  • Wei J, Zhang Y, Hunter D, Zeng C, Lei G. The gut microbiome-joint axis in osteoarthritis. Sci Bull (Beijing). 2023;68(8):759–762. doi:10.1016/j.scib.2023.03.024.
  • Dey P, Chaudhuri SR, Efferth T, Pal S. The intestinal 3M (microbiota, metabolism, metabolome) zeitgeist - from fundamentals to future challenges. Free Radic Biol Med. 2021;176:265–285. doi:10.1016/j.freeradbiomed.2021.09.026.
  • Gilbert JA, Blaser MJ, Caporaso JG, Jansson JK, Lynch SV, Knight R. Current understanding of the human microbiome. Nat Med. 2018;24(4):392–400. doi:10.1038/nm.4517.
  • Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449(7164):804–810. doi:10.1038/nature06244.
  • Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19(1):55–71. doi:10.1038/s41579-020-0433-9.
  • Delzenne NM, Neyrinck AM, Backhed F, Cani PD. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol. 2011;7(11):639–646. doi:10.1038/nrendo.2011.126.
  • Ma Q, Li Y, Li P, Wang M, Wang J, Tang Z, Wang T, Luo L, Wang C, Wang T, et al. Research progress in the relationship between type 2 diabetes mellitus and intestinal flora. Biomed Pharmacother. 2019;117:109138. doi:10.1016/j.biopha.2019.109138.
  • Lynch SV, Pedersen O, Phimister EG. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375(24):2369–2379. doi:10.1056/NEJMra1600266.
  • Ridaura V, Belkaid Y. Gut microbiota: the link to your second brain. Cell. 2015;161(2):193–194. doi:10.1016/j.cell.2015.03.033.
  • Chen Y, Zhou J, Wang L. Role and mechanism of gut microbiota in human disease. Front Cell Infect Microbiol. 2021;11:625913. doi:10.3389/fcimb.2021.625913.
  • Dinan TG, Cryan JF. Brain-gut-microbiota axis and mental health. Psychosom Med. 2017;79(8):920–926. doi:10.1097/PSY.0000000000000519.
  • Hu X, Wang T, Jin F. Alzheimer’s disease and gut microbiota. Sci China Life Sci. 2016;59(10):1006–1023. doi:10.1007/s11427-016-5083-9.
  • Witkowski M, Weeks TL, Hazen SL. Gut microbiota and cardiovascular disease. Circ Res. 2020;127(4):553–570. doi:10.1161/CIRCRESAHA.120.316242.
  • Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60. doi:10.1038/nature11450.
  • Moludi J, Maleki V, Jafari-Vayghyan H, Vaghef-Mehrabany E, Alizadeh M. Metabolic endotoxemia and cardiovascular disease: a systematic review about potential roles of prebiotics and probiotics. Clin Exp Pharmacol Physiol. 2020;47(6):927–939. doi:10.1111/1440-1681.13250.
  • Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–1345. doi:10.1016/j.cell.2016.05.041.
  • Bana B, Cabreiro F. The microbiome and aging. Annu Rev Genet. 2019;53(1):239–261. doi:10.1146/annurev-genet-112618-043650.
  • Strasser B, Wolters M, Weyh C, Kruger K, Ticinesi A. The effects of lifestyle and diet on gut microbiota composition, inflammation and muscle performance in our aging society. Nutrients. 2021;13(6):2045. doi:10.3390/nu13062045.
  • Ticinesi A, Lauretani F, Milani C, Nouvenne A, Tana C, Del Rio D, Maggio M, Ventura M, Meschi T. Aging gut microbiota at the cross-road between Nutrition, physical frailty, and sarcopenia: is there a gut–muscle axis? Nutrients. 2017;9(12):1303. doi:10.3390/nu9121303.
  • Zaiss MM, Jones RM, Schett G, Pacifici R. The gut-bone axis: how bacterial metabolites bridge the distance. J Clin Invest. 2019;129(8):3018–3028. doi:10.1172/JCI128521.
  • Giron M, Thomas M, Dardevet D, Chassard C, Savary-Auzeloux I. Gut microbes and muscle function: can probiotics make our muscles stronger? J Cachexia Sarcopenia Muscle. 2022;13(3):1460–1476. doi:10.1002/jcsm.12964.
  • Behera J, Ison J, Tyagi SC, Tyagi N. The role of gut microbiota in bone homeostasis. Bone. 2020;135:115317. doi:10.1016/j.bone.2020.115317.
  • Biver E, Berenbaum F, Valdes AM, Araujo de Carvalho I, Bindels LB, Brandi ML, Calder PC, Castronovo V, Cavalier E, Cherubini A, et al. Gut microbiota and osteoarthritis management: an expert consensus of the European society for clinical and economic aspects of osteoporosis, osteoarthritis and musculoskeletal diseases (ESCEO). Ageing Res Rev. 2019;55:100946. doi:10.1016/j.arr.2019.100946.
  • Lahiri S, Kim H, Garcia-Perez I, Reza MM, Martin KA, Kundu P, Cox LM, Selkrig J, Posma JM, Zhang H, et al. The gut microbiota influences skeletal muscle mass and function in mice. Sci Transl Med. 2019;11(502):11. doi:10.1126/scitranslmed.aan5662.
  • Tintignac LA, Lagirand J, Batonnet S, Sirri V, Leibovitch MP, Leibovitch SA. Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem. 2005;280(4):2847–2856. doi:10.1074/jbc.M411346200.
  • Yoshida T, Delafontaine P. Mechanisms of IGF-1-Mediated regulation of skeletal muscle hypertrophy and atrophy. Cells. 2020;9(9):1970. doi:10.3390/cells9091970.
  • Waddell DS, Baehr LM, van den Brandt J, Johnsen SA, Reichardt HM, Furlow JD, Bodine SC. The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab. 2008;295(4):E785–97. doi:10.1152/ajpendo.00646.2007.
  • Woldt E, Sebti Y, Solt LA, Duhem C, Lancel S, Eeckhoute J, Hesselink MKC, Paquet C, Delhaye S, Shin Y, et al. Rev-erb-α modulates skeletal muscle oxidative capacity by regulating mitochondrial biogenesis and autophagy. Nat Med. 2013;19(8):1039–1046. doi:10.1038/nm.3213.
  • Goodpaster BH, Sparks LM. Metabolic flexibility in health and disease. Cell Metab. 2017;25(5):1027–1036. doi:10.1016/j.cmet.2017.04.015.
  • Jope RS, Jenden DJ. The utilization of choline and acetyl coenzyme a for the synthesis of acetylcholine. J Neurochem. 1980;35(2):318–325. doi:10.1111/j.1471-4159.1980.tb06267.x.
  • Fambrough DM. Control of acetylcholine receptors in skeletal muscle. Physiol Rev. 1979;59(1):165–227. doi:10.1152/physrev.1979.59.1.165.
  • Gomes AV, Potter JD, Szczesna-Cordary D. The role of troponins in muscle contraction. IUBMB Life (Int Union Biochem Mol Biol: Life). 2002;54(6):323–333. doi:10.1080/15216540216037.
  • Ohlsson C, Sjogren K. Effects of the gut microbiota on bone mass. Trends Endocrinol Metab. 2015;26(2):69–74. doi:10.1016/j.tem.2014.11.004.
  • Evans L. Bone: gut immune status affects bone mass in mice. Nat Rev Endocrinol. 2012;8(6):318. doi:10.1038/nrendo.2012.51.
  • Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Bäckhed F, Ohlsson C. The gut microbiota regulates bone mass in mice. J Bone Miner Res. 2012;27(6):1357–1367. doi:10.1002/jbmr.1588.
  • Quach D, Collins F, Parameswaran N, McCabe L, Britton RA, Ellermeier CD. Microbiota reconstitution does not cause bone loss in germ-free mice. mSphere. 2018;3(1):3. doi:10.1128/mSphereDirect.00545-17.
  • Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, Martino ME, Balmand S, Hudcovic T, Heddi A, et al. Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Sci. 2016;351(6275):854–857. doi:10.1126/science.aad8588.
  • Yan J, Herzog JW, Tsang K, Brennan CA, Bower MA, Garrett WS, Sartor BR, Aliprantis AO, Charles JF. Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci U S A. 2016;113(47):E7554–E63. doi:10.1073/pnas.1607235113.
  • Holick MF. Vitamin D deficiency. N Engl J Med. 2007;357(3):266–281. doi:10.1056/NEJMra070553.
  • Bora SA, Kennett MJ, Smith PB, Patterson AD, Cantorna MT. The gut microbiota regulates endocrine vitamin D metabolism through fibroblast growth factor 23. Front Immunol. 2018;9:408. doi:10.3389/fimmu.2018.00408.
  • Liu JH, Chen CY, Liu ZZ, Luo ZW, Rao SS, Jin L, Wan T-F, Yue T, Tan Y-J, Yin H, et al. Extracellular vesicles from child gut microbiota enter into bone to preserve bone mass and strength. Adv Sci. 2021;8(9):2004831. doi:10.1002/advs.202004831.
  • Liu H, Zhang H, Han Y, Hu Y, Geng Z, Su J. Bacterial extracellular vesicles-based therapeutic strategies for bone and soft tissue tumors therapy. Theranostics. 2022;12(15):6576–6594. doi:10.7150/thno.78034.
  • Huang Z, Chen J, Li B, Zeng B, Chou CH, Zheng X, Xie J, Li H, Hao Y, Chen G, et al. Faecal microbiota transplantation from metabolically compromised human donors accelerates osteoarthritis in mice. Ann Rheum Dis. 2020;79(5):646–656. doi:10.1136/annrheumdis-2019-216471.
  • Abdollahi-Roodsaz S, Joosten LA, Roelofs MF, Radstake TR, Matera G, Popa C, van der Meer JWM, Netea MG, van den Berg WB. Inhibition of Toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis. Arthritis & Rheumatism. 2007;56(9):2957–2967. doi:10.1002/art.22848.
  • van den Berg WB, van Lent PL, Joosten LA, Abdollahi-Roodsaz S, Koenders MI. Amplifying elements of arthritis and joint destruction. Ann Rheum Dis. 2007;66(Suppl 3):iii45–8. doi:10.1136/ard.2007.079830.
  • Ulici V, Kelley KL, Azcarate-Peril MA, Cleveland RJ, Sartor RB, Schwartz TA, Loeser RF. Osteoarthritis induced by destabilization of the medial meniscus is reduced in germ-free mice. Osteoarthritis Cartilage. 2018;26(8):1098–1109. doi:10.1016/j.joca.2018.05.016.
  • Levy M, Kolodziejczyk AA, Thaiss CA, Elinav E. Dysbiosis and the immune system. Nat Rev Immunol. 2017;17(4):219–232. doi:10.1038/nri.2017.7.
  • Haran JP, Bucci V, Dutta P, Ward D, McCormick B. The nursing home elder microbiome stability and associations with age, frailty, nutrition and physical location. J Med Microbiol. 2018;67(1):40–51. doi:10.1099/jmm.0.000640.
  • Gupta SS, Mohammed MH, Ghosh TS, Kanungo S, Nair GB, Mande SS. Metagenome of the gut of a malnourished child. Gut Pathog. 2011;3(1):7. doi:10.1186/1757-4749-3-7.
  • Genton L, Mareschal J, Charretier Y, Lazarevic V, Bindels LB, Schrenzel J. Targeting the gut microbiota to treat cachexia. Front Cell Infect Microbiol. 2019;9:305. doi:10.3389/fcimb.2019.00305.
  • Jackson MA, Jeffery IB, Beaumont M, Bell JT, Clark AG, Ley RE, O’Toole PW, Spector TD, Steves CJ. Signatures of early frailty in the gut microbiota. Genome Med. 2016;8(1):8. doi:10.1186/s13073-016-0262-7.
  • Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HMB, Coakley M, Lakshminarayanan B, O’Sullivan O, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488(7410):178–184. doi:10.1038/nature11319.
  • Zhang L, Liao J, Chen Q, Chen M, Kuang Y, Chen L, He W. Characterization of the gut microbiota in frail elderly patients. Aging Clin Exp Res. 2020;32(10):2001–2011. doi:10.1007/s40520-019-01385-2.
  • Illiano P, Brambilla R, Parolini C. The mutual interplay of gut microbiota, diet and human disease. FEBS J. 2020;287(5):833–855. doi:10.1111/febs.15217.
  • Nardone OM, de Sire R, Petito V, Testa A, Villani G, Scaldaferri F, Castiglione F. Inflammatory bowel diseases and sarcopenia: the role of inflammation and gut microbiota in the development of muscle failure. Front Immunol. 2021;12:694217. doi:10.3389/fimmu.2021.694217.
  • Grosicki GJ, Fielding RA, Lustgarten MS. Gut microbiota contribute to age-related changes in skeletal muscle size, composition, and function: biological basis for a gut-muscle axis. Calcif Tissue Int. 2018;102(4):433–442. doi:10.1007/s00223-017-0345-5.
  • Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214.
  • Wang H, Wang G, Banerjee N, Liang Y, Du X, Boor PJ, Hoffman KL, Khan MF. Aberrant gut microbiome contributes to intestinal oxidative stress, barrier dysfunction, inflammation and systemic autoimmune responses in MRL/lpr mice. Front Immunol. 2021;12:651191. doi:10.3389/fimmu.2021.651191.
  • Callahan LA, Supinski GS. Sepsis-induced myopathy. Crit Care Med. 2009;37:S354–67. doi:10.1097/CCM.0b013e3181b6e439.
  • Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008;88(4):1243–1276. doi:10.1152/physrev.00031.2007.
  • Saul D, Kosinsky RL. Dextran Sodium Sulfate-induced colitis as a model for sarcopenia in mice. Inflamm Bowel Dis. 2020;26(1):56–65. doi:10.1093/ibd/izz127.
  • Kishimoto Y, Zhu W, Hosoda W, Sen JM, Mattson MP. Chronic mild gut inflammation accelerates brain neuropathology and motor dysfunction in α-synuclein mutant mice. Neuromolecular Med. 2019;21(3):239–249. doi:10.1007/s12017-019-08539-5.
  • Puleo F, Meirelles K, Navaratnarajah M, Fitzpatrick L, Shumate ML, Cooney RN, Lang CH. Skeletal muscle catabolism in trinitrobenzene sulfonic acid–induced murine colitis. Metabolism. 2010;59(11):1680–1690. doi:10.1016/j.metabol.2010.03.021.
  • Ryan E, McNicholas D, Creavin B, Kelly ME, Walsh T, Beddy D. Sarcopenia and inflammatory bowel disease: a systematic review. Inflamm Bowel Dis. 2019;25(1):67–73. doi:10.1093/ibd/izy212.
  • Scaldaferri F, Pizzoferrato M, Lopetuso LR, Musca T, Ingravalle F, Sicignano LL, Mentella M, Miggiano G, Mele MC, Gaetani E, et al. Nutrition and IBD: malnutrition and/or sarcopenia? A practical guide. Gastroenterology Research And Practice. 2017;2017:1–11. doi:10.1155/2017/8646495.
  • Pizzoferrato M, de Sire R, Ingravalle F, Mentella MC, Petito V, Martone AM, Landi F, Miggiano GAD, Mele MC, Lopetuso LR, et al. Characterization of sarcopenia in an IBD population attending an Italian gastroenterology tertiary center. Nutrients. 2019;11(10):11. doi:10.3390/nu11102281.
  • de Sire R, Rizzatti G, Ingravalle F, Pizzoferrato M, Petito V, Lopetuso L, Graziani C, de Sire A, Mentella MC, Mele MC, et al. Skeletal muscle-gut axis: emerging mechanisms of sarcopenia for intestinal and extra intestinal diseases. Minerva Gastroenterol Dietol. 2018;64(4):351–362. doi:10.23736/S1121-421X.18.02511-4.
  • Maffei VJ, Kim S, Blanchard E, Luo M, Jazwinski SM, Taylor CM, Welsh DA. Biological aging and the human gut microbiota. J Gerontol A Biol Sci Med Sci. 2017;72(11):1474–1482. doi:10.1093/gerona/glx042.
  • Ticinesi A, Nouvenne A, Cerundolo N, Catania P, Prati B, Tana C, Meschi T. Gut microbiota, muscle mass and function in aging: a focus on physical frailty and sarcopenia. Nutrients. 2019;11(7):11. doi:10.3390/nu11071633.
  • Thevaranjan N, Puchta A, Schulz C, Naidoo A, Szamosi JC, Verschoor CP, Loukov D, Schenck LP, Jury J, Foley KP, et al. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host & Microbe. 2017;21(4):455–466.e4. doi:10.1016/j.chom.2017.03.002.
  • Ghosh S, Lertwattanarak R, Garduno Jde J, Galeana JJ, Li J, Zamarripa F, Lancaster JL, Mohan S, Hussey S, Musi N, et al. Elevated muscle TLR4 expression and metabolic endotoxemia in human aging. J Gerontol A Biol Sci Med Sci. 2015;70(2):232–246. doi:10.1093/gerona/glu067.
  • Cevenini E, Caruso C, Candore G, Capri M, Nuzzo D, Duro G, Rizzo C, Colonna-Romano G, Lio D, Carlo D, et al. Age-related inflammation: the contribution of different organs, tissues and systems. How to face it for therapeutic approaches. Curr Pharm Des. 2010;16(6):609–618. doi:10.2174/138161210790883840.
  • Jensen GL. Inflammation: roles in aging and sarcopenia. JPEN J Parenter Enteral Nutr. 2008;32(6):656–659. doi:10.1177/0148607108324585.
  • Li YP, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB. TNF-α acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 2005;19(3):362–370. doi:10.1096/fj.04-2364com.
  • Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 2005;19(3):422–424. doi:10.1096/fj.04-2640fje.
  • Patel HP, Al-Shanti N, Davies LC, Barton SJ, Grounds MD, Tellam RL, Stewart CE, Cooper C, Sayer AA. Lean mass, muscle strength and gene expression in community dwelling older men: findings from the Hertfordshire Sarcopenia Study (HSS). Calcif Tissue Int. 2014;95(4):308–316. doi:10.1007/s00223-014-9894-z.
  • Giannos P, Prokopidis K, Isanejad M, Wright HL. Markers of immune dysregulation in response to the ageing gut: insights from aged murine gut microbiota transplants. BMC Gastroenterol. 2022;22(1):533. doi:10.1186/s12876-022-02613-2.
  • De Spiegeleer A, Wynendaele E, Descamps A, Debunne N, Braeckman BP, De Mey M, Coudenys J, Crombez L, Verbeke F, Janssens Y, et al. The bacterial quorum sensing peptide iAM373 is a novel inducer of sarcopenia. Clin Transl Med. 2022;12(10):e1053. doi:10.1002/ctm2.1053.
  • Ticinesi A, Mancabelli L, Tagliaferri S, Nouvenne A, Milani C, Del Rio D, Lauretani F, Maggio MG, Ventura M, Meschi T, et al. The gut-muscle axis in older Subjects with low muscle mass and performance: a proof of concept study exploring fecal microbiota composition and function with shotgun metagenomics sequencing. Int J Mol Sci. 2020;21(23):21. doi:10.3390/ijms21238946.
  • Kang L, Li P, Wang D, Wang T, Hao D, Qu X. Alterations in intestinal microbiota diversity, composition, and function in patients with sarcopenia. Sci Rep. 2021;11(1):4628. doi:10.1038/s41598-021-84031-0.
  • Mancin L, Wu GD, Paoli A. Gut microbiota–bile acid–skeletal muscle axis. Trends Microbiol. 2022;31(3):322. doi:10.1016/j.tim.2023.01.003.
  • Zmora N, Suez J, Elinav E. You are what you eat: diet, health and the gut microbiota. Nat Rev Gastroenterol Hepatol. 2019;16(1):35–56. doi:10.1038/s41575-018-0061-2.
  • Charles JF, Ermann J, Aliprantis AO. The intestinal microbiome and skeletal fitness: connecting bugs and bones. Clin Immunol. 2015;159(2):163–169. doi:10.1016/j.clim.2015.03.019.
  • Chen Y, Wang X, Zhang C, Liu Z, Li C, Ren Z. Gut microbiota and bone diseases: a growing partnership. Front Microbiol. 2022;13:877776. doi:10.3389/fmicb.2022.877776.
  • Guss JD, Horsfield MW, Fontenele FF, Sandoval TN, Luna M, Apoorva F, Lima SF, Bicalho RC, Singh A, Ley RE, et al. Alterations to the gut microbiome impair bone strength and tissue material properties. J Bone Miner Res. 2017;32(6):1343–1353. doi:10.1002/jbmr.3114.
  • Guss JD, Taylor E, Rouse Z, Roubert S, Higgins CH, Thomas CJ, Baker SP, Vashishth D, Donnelly E, Shea MK, et al. The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength. Bone. 2019;127:146–154. doi:10.1016/j.bone.2019.06.010.
  • Yu M, Pal S, Paterson CW, Li JY, Tyagi AM, Adams J, Coopersmith CM, Weitzmann MN, Pacifici R. Ovariectomy induces bone loss via microbial-dependent trafficking of intestinal TNF+ T cells and Th17 cells. J Clin Invest. 2021;131(4):131. doi:10.1172/JCI143137.
  • Cheng S, Qi X, Ma M, Zhang L, Cheng B, Liang C, Liu L, Li P, Kafle OP, Wen Y, et al. Assessing the relationship between gut microbiota and bone mineral density. Front Genet. 2020;11:6. doi:10.3389/fgene.2020.00006.
  • Ni JJ, Yang XL, Zhang H, Xu Q, Wei XT, Feng GJ, Zhao M, Pei Y-F, Zhang L. Assessing causal relationship from gut microbiota to heel bone mineral density. Bone. 2021;143:115652. doi:10.1016/j.bone.2020.115652.
  • Mitsui T, Shimaoka K, Takagi C, Goto Y, Kagami H, Ito A. Small bowel bacterial overgrowth may not affect bone mineral density in older people. Clin Nutr. 2005;24(6):920–924. doi:10.1016/j.clnu.2005.05.022.
  • Compston JE, Judd D, Crawley EO, Evans WD, Evans C, Church HA, Reid EM, Rhodes J. Osteoporosis in patients with inflammatory bowel disease. Gut. 1987;28(4):410–415. doi:10.1136/gut.28.4.410.
  • Semeao EJ, Jawad AF, Stouffer NO, Zemel BS, Piccoli DA, Stallings VA. Risk factors for low bone mineral density in children and young adults with Crohn’s disease. J Pediatr. 1999;135(5):593–600. doi:10.1016/S0022-3476(99)70058-2.
  • Li C, Huang Q, Yang R, Dai Y, Zeng Y, Tao L, Li X, Zeng J, Wang Q. Gut microbiota composition and bone mineral loss—epidemiologic evidence from individuals in Wuhan, China. Osteoporos Int. 2019;30(5):1003–1013. doi:10.1007/s00198-019-04855-5.
  • Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65. doi:10.1038/nature08821.
  • Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Sci. 2005;308(5728):1635–1638. doi:10.1126/science.1110591.
  • Wang J, Wang Y, Gao W, Wang B, Zhao H, Zeng Y, Ji Y, Hao D. Diversity analysis of gut microbiota in osteoporosis and osteopenia patients. PeerJ. 2017;5:e3450. doi:10.7717/peerj.3450.
  • Das M, Cronin O, Keohane DM, Cormac EM, Nugent H, Nugent M, Molloy C, O’Toole PW, Shanahan F, Molloy MG, et al. Gut microbiota alterations associated with reduced bone mineral density in older adults. Rheumatology (Oxford). 2019;58(12):2295–2304. doi:10.1093/rheumatology/kez302.
  • Xu Z, Xie Z, Sun J, Huang S, Chen Y, Li C, Sun X, Xia B, Tian L, Guo C, et al. Gut microbiome reveals specific dysbiosis in primary osteoporosis. Front Cell Infect Microbiol. 2020;10:160. doi:10.3389/fcimb.2020.00160.
  • DeLuca HF. Evolution of our understanding of vitamin D. Nutr Rev. 2008;66:S73–87. doi:10.1111/j.1753-4887.2008.00105.x.
  • Yatsonsky Ii D, Pan K, Shendge VB, Liu J, Ebraheim NA. Linkage of microbiota and osteoporosis: a mini literature review. World J Orthop. 2019;10(3):123–127. doi:10.5312/wjo.v10.i3.123.
  • Smith BJ, Lerner MR, Bu SY, Lucas EA, Hanas JS, Lightfoot SA, Postier RG, Bronze MS, Brackett DJ. Systemic bone loss and induction of coronary vessel disease in a rat model of chronic inflammation. Bone. 2006;38(3):378–386. doi:10.1016/j.bone.2005.09.008.
  • Chongwatpol P, Rendina-Ruedy E, Stoecker BJ, Clarke SL, Lucas EA, Smith BJ. Implications of compromised zinc status on bone loss associated with chronic inflammation in C57BL/6 mice. J Inflamm Res. 2015;8:117–128. doi:10.2147/JIR.S82261.
  • Quach D, Britton RA. Gut microbiota and Bone Health. Adv Exp Med Biol. 2017;1033:47–58.
  • Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–141. doi:10.1016/j.cell.2014.03.011.
  • Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, McCabe S, et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature. 1999;402(6759):304–309. doi:10.1038/46303.
  • D’Amelio P, Grimaldi A, Di Bella S, Brianza SZM, Cristofaro MA, Tamone C, Giribaldi G, Ulliers D, Pescarmona GP, Isaia G, et al. Estrogen deficiency increases osteoclastogenesis up-regulating T cells activity: a key mechanism in osteoporosis. Bone. 2008;43(1):92–100. doi:10.1016/j.bone.2008.02.017.
  • Ibanez L, Abou-Ezzi G, Ciucci T, Amiot V, Belaid N, Obino D, Mansour A, Rouleau M, Wakkach A, Blin-Wakkach C, et al. Inflammatory osteoclasts prime TNFα-producing CD4+T cells and express CX 3 CR1. J Bone Miner Res. 2016;31(10):1899–1908. doi:10.1002/jbmr.2868.
  • Tyagi AM, Yu M, Darby TM, Vaccaro C, Li JY, Owens JA, Hsu E, Adams J, Weitzmann MN, Jones RM, et al. The microbial metabolite butyrate stimulates bone formation via T regulatory cell-mediated regulation of WNT10B expression. Immunity. 2018;49(6):1116–1131.e7. doi:10.1016/j.immuni.2018.10.013.
  • Pawlak D, Domaniewski T, Znorko B, Oksztulska-Kolanek E, Lipowicz P, Doroszko M, Karbowska M, Pawlak K. The impact of peripheral serotonin on leptin-brain serotonin axis, bone metabolism and strength in growing rats with experimental chronic kidney disease. Bone. 2017;105:1–10. doi:10.1016/j.bone.2017.08.004.
  • Shen S, Prame Kumar K, Wen SW, Shim R, Wanrooy BJ, Stanley D, Moore RJ, Van TTH, Robert R, Hickey MJ, et al. Deficiency of dietary fiber modulates gut microbiota composition, neutrophil recruitment and worsens experimental colitis. Front Immunol. 2021;12:619366. doi:10.3389/fimmu.2021.619366.
  • Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen-gut microbiome axis: physiological and clinical implications. Maturitas. 2017;103:45–53. doi:10.1016/j.maturitas.2017.06.025.
  • Guan Z, Jia J, Zhang C, Sun T, Zhang W, Yuan W, Leng H, Song C. Gut microbiome dysbiosis alleviates the progression of osteoarthritis in mice. Clin Sci (Lond). 2020;134(23):3159–3174. doi:10.1042/CS20201224.
  • Jackson MA, Verdi S, Maxan ME, Shin CM, Zierer J, Bowyer RCE, Martin T, Williams FMK, Menni C, Bell JT, et al. Gut microbiota associations with common diseases and prescription medications in a population-based cohort. Nat Commun. 2018;9(1):2655. doi:10.1038/s41467-018-05184-7.
  • Boer CG, Radjabzadeh D, Medina-Gomez C, Garmaeva S, Schiphof D, Arp P, Koet T, Kurilshikov A, Fu J, Ikram MA, et al. Intestinal microbiome composition and its relation to joint pain and inflammation. Nat Commun. 2019;10(1):4881. doi:10.1038/s41467-019-12873-4.
  • Sanchez Romero EA, Melendez Oliva E, Alonso Perez JL, Martin Perez S, Turroni S, Marchese L, Villafañe JH. Relationship between the gut microbiome and osteoarthritis pain: review of the literature. Nutrients. 2021;13(3):716. doi:10.3390/nu13030716.
  • Santoro A, Ostan R, Candela M, Biagi E, Brigidi P, Capri M, Franceschi C. Gut microbiota changes in the extreme decades of human life: a focus on centenarians. Cell Mol Life Sci. 2018;75(1):129–148. doi:10.1007/s00018-017-2674-y.
  • Kayama H, Okumura R, Takeda K. Interaction between the microbiota, Epithelia, and immune cells in the intestine. Annu Rev Immunol. 2020;38(1):23–48. doi:10.1146/annurev-immunol-070119-115104.
  • Van de Wiele T, Van Praet JT, Marzorati M, Drennan MB, Elewaut D. How the microbiota shapes rheumatic diseases. Nat Rev Rheumatol. 2016;12(7):398–411. doi:10.1038/nrrheum.2016.85.
  • Boutagy NE, McMillan RP, Frisard MI, Hulver MW. Metabolic endotoxemia with obesity: is it real and is it relevant? Biochimie. 2016;124:11–20. doi:10.1016/j.biochi.2015.06.020.
  • Huang Z, Kraus VB. Does lipopolysaccharide-mediated inflammation have a role in OA? Nat Rev Rheumatol. 2016;12(2):123–129. doi:10.1038/nrrheum.2015.158.
  • Tanoue T, Atarashi K, Honda K. Development and maintenance of intestinal regulatory T cells. Nat Rev Immunol. 2016;16(5):295–309. doi:10.1038/nri.2016.36.
  • Opazo MC, Ortega-Rocha EM, Coronado-Arrazola I, Bonifaz LC, Boudin H, Neunlist M, Bueno SM, Kalergis AM, Riedel CA. Intestinal microbiota influences non-intestinal related autoimmune diseases. Front Microbiol. 2018;9:432. doi:10.3389/fmicb.2018.00432.
  • Zaiss MM, Joyce Wu HJ, Mauro D, Schett G, Ciccia F. The gut–joint axis in rheumatoid arthritis. Nat Rev Rheumatol. 2021;17(4):224–237. doi:10.1038/s41584-021-00585-3.
  • Liu X, Zou Q, Zeng B, Fang Y, Wei H. Analysis of fecal Lactobacillus community structure in patients with early rheumatoid arthritis. Curr Microbiol. 2013;67(2):170–176. doi:10.1007/s00284-013-0338-1.
  • Picchianti-Diamanti A, Panebianco C, Salemi S, Sorgi ML, Di Rosa R, Tropea A, Sgrulletti M, Salerno G, Terracciano F, D’Amelio R, et al. Analysis of gut microbiota in rheumatoid arthritis patients: disease-related dysbiosis and modifications induced by Etanercept. Int J Mol Sci. 2018;19(10):2938. doi:10.3390/ijms19102938.
  • Liu X, Zeng B, Zhang J, Li W, Mou F, Wang H, Zou Q, Zhong B, Wu L, Wei H, et al. Role of the gut microbiome in modulating arthritis progression in mice. Sci Rep. 2016;6(1):30594. doi:10.1038/srep30594.
  • Alipour B, Homayouni-Rad A, Vaghef-Mehrabany E, Sharif SK, Vaghef-Mehrabany L, Asghari-Jafarabadi M, Nakhjavani MR, Mohtadi‐Nia J. Effects of Lactobacillus casei supplementation on disease activity and inflammatory cytokines in rheumatoid arthritis patients: a randomized double-blind clinical trial. Int J Rheum Dis. 2014;17(5):519–527. doi:10.1111/1756-185X.12333.
  • Kalinkovich A, Livshits G. A cross talk between dysbiosis and gut-associated immune system governs the development of inflammatory arthropathies. Semin Arthritis Rheum. 2019;49(3):474–484. doi:10.1016/j.semarthrit.2019.05.007.
  • Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, Tanaka S, Kodama T, Akira S, Iwakura Y, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006;203(12):2673–2682. doi:10.1084/jem.20061775.
  • Suez J, Zmora N, Segal E, Elinav E. The pros, cons, and many unknowns of probiotics. Nat Med. 2019;25(5):716–729. doi:10.1038/s41591-019-0439-x.
  • Varian BJ, Gourishetti S, Poutahidis T, Lakritz JR, Levkovich T, Kwok C, Teliousis K, Ibrahim YM, Mirabal S, Erdman SE, et al. Beneficial bacteria inhibit cachexia. Oncotarget. 2016;7(11):11803–11816. doi:10.18632/oncotarget.7730.
  • Lee K, Kim J, Park SD, Shim JJ, Lee JL. Lactobacillus plantarum HY7715 ameliorates sarcopenia by improving skeletal muscle mass and function in aged Balb/c mice. Int J Mol Sci. 2021;22(18):22. doi:10.3390/ijms221810023.
  • Chen YM, Wei L, Chiu YS, Hsu YJ, Tsai TY, Wang MF, Huang C-C. Lactobacillus plantarum TWK10 supplementation improves exercise performance and increases muscle mass in mice. Nutrients. 2016;8(4):205. doi:10.3390/nu8040205.
  • Chen LH, Huang SY, Huang KC, Hsu CC, Yang KC, Li LA, Chan C-H, Huang H-Y. Lactobacillus paracasei PS23 decelerated age-related muscle loss by ensuring mitochondrial function in SAMP8 mice. Aging (Albany NY). 2019;11(2):756–770. doi:10.18632/aging.101782.
  • Bindels LB, Beck R, Schakman O, Martin JC, De Backer F, Sohet FM, Dewulf EM, Pachikian BD, Neyrinck AM, Thissen J-P, et al. Restoring specific lactobacilli levels decreases inflammation and muscle atrophy markers in an acute leukemia mouse model. PloS One. 2012;7(6):e37971. doi:10.1371/journal.pone.0037971.
  • Ni Y, Yang X, Zheng L, Wang Z, Wu L, Jiang J, Yang T, Ma L, Fu Z. Lactobacillus and Bifidobacterium improves physiological function and cognitive ability in aged mice by the regulation of gut microbiota. Mol Nutr Food Res. 2019;63(22):e1900603. doi:10.1002/mnfr.201900603.
  • Liu C, Cheung WH, Li J, Chow SK, Yu J, Wong SH, Ip M, Sung JJY, Wong RMY. Understanding the gut microbiota and sarcopenia: a systematic review. J Cachexia Sarcopenia Muscle. 2021;12(6):1393–1407. doi:10.1002/jcsm.12784.
  • Daily JW, Park S. Sarcopenia is a cause and consequence of metabolic dysregulation in aging humans: effects of gut dysbiosis, glucose dysregulation, diet and lifestyle. Cells. 2022;11(3):11. doi:10.3390/cells11030338.
  • Huang WC, Hsu YJ, Li H, Kan NW, Chen YM, Lin JS, Hsu, TK, Tsai, TY, Chiu, YS, Huang, CC. Effect of Lactobacillus plantarum TWK10 on improving endurance performance in humans. Chin J Physiol. 2018;61(3):163–170. doi:10.4077/CJP.2018.BAH587.
  • Huang WC, Lee MC, Lee CC, Ng KS, Hsu YJ, Tsai TY, Young S-L, Lin J-S, Huang C-C. Effect of Lactobacillus plantarum TWK10 on exercise physiological adaptation, performance, and body composition in healthy humans. Nutrients. 2019;11(11):11. doi:10.3390/nu11112836.
  • Neto JV, de Melo CM, Ribeiro SM. Effects of three-month intake of synbiotic on inflammation and body composition in the elderly: a pilot study. Nutrients. 2013;5(4):1276–1286. doi:10.3390/nu5041276.
  • Prokopidis K, Giannos P, Kirwan R, Ispoglou T, Galli F, Witard OC, Triantafyllidis KK, Kechagias KS, Morwani‐Mangnani J, Ticinesi A, et al. Impact of probiotics on muscle mass, muscle strength and lean mass: a systematic review and meta-analysis of randomized controlled trials. J Cachexia Sarcopenia Muscle. 2023;14(1):30–44. doi:10.1002/jcsm.13132.
  • Hsu YJ, Huang WC, Lin JS, Chen YM, Ho ST, Huang CC, Tung Y-T. Kefir supplementation modifies gut microbiota composition, reduces physical fatigue, and improves exercise performance in mice. Nutrients. 2018;10(7):10. doi:10.3390/nu10070862.
  • Sagar S, Morgan ME, Chen S, Vos AP, Garssen J, van Bergenhenegouwen J, Boon L, Georgiou NA, Kraneveld AD, Folkerts G, et al. Bifidobacterium breve and Lactobacillus rhamnosus treatment is as effective as budesonide at reducing inflammation in a murine model for chronic asthma. Respir Res. 2014;15(1):46. doi:10.1186/1465-9921-15-46.
  • Bindels LB, Neyrinck AM, Claus SP, Le Roy CI, Grangette C, Pot B, Martinez I, Walter J, Cani PD, Delzenne NM, et al. Synbiotic approach restores intestinal homeostasis and prolongs survival in leukaemic mice with cachexia. ISME J. 2016;10(6):1456–1470. doi:10.1038/ismej.2015.209.
  • Maathuis AJ, Keller D, Farmer S. Survival and metabolic activity of the GanedenBC30 strain of Bacillus coagulans in a dynamic in vitro model of the stomach and small intestine. Benef Microbes. 2010;1(1):31–36. doi:10.3920/BM2009.0009.
  • Krautkramer KA, Fan J, Backhed F. Gut microbial metabolites as multi-kingdom intermediates. Nat Rev Microbiol. 2021;19(2):77–94. doi:10.1038/s41579-020-0438-4.
  • 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(9):840–848. doi:10.1038/s42255-020-0188-7.
  • McCarville JL, Chen GY, Cuevas VD, Troha K, Ayres JS. Microbiota metabolites in health and disease. Annu Rev Immunol. 2020;38(1):147–170. doi:10.1146/annurev-immunol-071219-125715.
  • Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28(10):1221–1227. doi:10.1136/gut.28.10.1221.
  • Wang Y, Dilidaxi D, Wu Y, Sailike J, Sun X, Nabi XH. Composite probiotics alleviate type 2 diabetes by regulating intestinal microbiota and inducing GLP-1 secretion in db/db mice. Biomed Pharmacother. 2020;125:109914. doi:10.1016/j.biopha.2020.109914.
  • Markowiak-Kopec P, Slizewska K. The effect of probiotics on the production of Short-chain fatty acids by human intestinal microbiome. Nutrients. 2020;12(4):12. doi:10.3390/nu12041107.
  • Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11(10):577–591. doi:10.1038/nrendo.2015.128.
  • Walsh ME, Bhattacharya A, Sataranatarajan K, Qaisar R, Sloane L, Rahman MM, Kinter M, Van Remmen H. The histone deacetylase inhibitor butyrate improves metabolism and reduces muscle atrophy during aging. Aging Cell. 2015;14(6):957–970. doi:10.1111/acel.12387.
  • Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58(7):1509–1517. doi:10.2337/db08-1637.
  • Al-Harbi NO, Nadeem A, Ahmad SF, Alotaibi MR, AlAsmari AF, Alanazi WA, Al-Harbi MM, El-Sherbeeny AM, Ibrahim KE. Short chain fatty acid, acetate ameliorates sepsis-induced acute kidney injury by inhibition of NADPH oxidase signaling in T cells. Int Immunopharmacol. 2018;58:24–31. doi:10.1016/j.intimp.2018.02.023.
  • Liu L, Fu C, Li F. Acetate affects the process of lipid metabolism in rabbit liver, skeletal muscle and adipose tissue. Anim (Basel). 2019;9(10):9. doi:10.3390/ani9100799.
  • Gizard F, Fernandez A, De Vadder F. Interactions between gut microbiota and skeletal muscle. Nutr Metab Insights. 2020;13:1178638820980490. doi:10.1177/1178638820980490.
  • Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host & Microbe. 2018;23(6):716–724. doi:10.1016/j.chom.2018.05.003.
  • Alexeev EE, Lanis JM, Kao DJ, Campbell EL, Kelly CJ, Battista KD, Gerich ME, Jenkins BR, Walk ST, Kominsky DJ, et al. Microbiota-derived indole metabolites promote human and murine intestinal homeostasis through regulation of Interleukin-10 receptor. Am J Pathol. 2018;188(5):1183–1194. doi:10.1016/j.ajpath.2018.01.011.
  • Wlodarska M, Luo C, Kolde R, d’Hennezel E, Annand JW, Heim CE, Krastel P, Schmitt EK, Omar AS, Creasey EA, et al. Indoleacrylic acid produced by commensal peptostreptococcus species suppresses inflammation. Cell Host & Microbe. 2017;22(1):25–37.e6. doi:10.1016/j.chom.2017.06.007.
  • de Aguiar Vallim TQ, Tarling EJ, Edwards PA. Pleiotropic roles of bile acids in metabolism. Cell Metab. 2013;17(5):657–669. doi:10.1016/j.cmet.2013.03.013.
  • Ridlon JM, Kang DJ, Hylemon PB, Bajaj JS. Bile acids and the gut microbiome. Curr Opin Gastroenterol. 2014;30(3):332–338. doi:10.1097/MOG.0000000000000057.
  • Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. The controversial role of human gut Lachnospiraceae. Microorganisms. 2020;8(4):8. doi:10.3390/microorganisms8040573.
  • Arora T, Backhed F. The gut microbiota and metabolic disease: current understanding and future perspectives. J Intern Med. 2016;280(4):339–349. doi:10.1111/joim.12508.
  • Qiu Y, Yu J, Li Y, Yang F, Yu H, Xue M, Zhang F, Jiang X, Ji X, Bao Z, et al. Depletion of gut microbiota induces skeletal muscle atrophy by FXR-FGF15/19 signalling. Ann Med. 2021;53(1):508–522. doi:10.1080/07853890.2021.1900593.
  • Kobayashi Y, Hara N, Sugimoto R, Mifuji-Moroka R, Tanaka H, Eguchi A, Iwasa M, Hasegawa H, Iwata K, Takei Y, et al. The associations between circulating bile acids and the muscle volume in patients with Non-Alcoholic Fatty Liver Disease (NAFLD). Intern Med. 2017;56(7):755–762. doi:10.2169/internalmedicine.56.7796.
  • LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24(2):160–168. doi:10.1016/j.copbio.2012.08.005.
  • Piquereau J, Boitard SE, Ventura-Clapier R, Mericskay M. Metabolic therapy of heart failure: is there a future for B vitamins? Int J Mol Sci. 2021;23(1):23. doi:10.3390/ijms23010030.
  • Mithal A, Bonjour JP, Boonen S, Burckhardt P, Degens H, El Hajj Fuleihan G, Josse R, Lips P, Morales Torres J, Rizzoli R, et al. Impact of nutrition on muscle mass, strength, and performance in older adults. Osteoporos Int. 2013;24(5):1555–1566. doi:10.1007/s00198-012-2236-y.
  • Schepper JD, Irwin R, Kang J, Dagenais K, Lemon T, Shinouskis A, Parameswaran N, McCabe, LR. Probiotics in gut-bone signaling. Adv Exp Med Biol. 2017;1033:225–247.
  • Zhao X, Ai J, Mao H, Gao X. Effects of Eclipta prostrata on gut microbiota of SAMP6 mice with osteoporosis. J Med Microbiol. 2019;68(3):402–416. doi:10.1099/jmm.0.000936.
  • Schepper JD, Collins FL, Rios-Arce ND, Raehtz S, Schaefer L, Gardinier JD, Britton RA, Parameswaran N, McCabe LR. Probiotic Lactobacillus reuteri prevents postantibiotic bone loss by reducing intestinal dysbiosis and preventing barrier disruption. J Bone Miner Res. 2019;34(4):681–698. doi:10.1002/jbmr.3635.
  • Nilsson AG, Sundh D, Backhed F, Lorentzon M. Lactobacillus reuteri reduces bone loss in older women with low bone mineral density: a randomized, placebo-controlled, double-blind, clinical trial. J Intern Med. 2018;284(3):307–317. doi:10.1111/joim.12805.
  • Yuan S, Shen J. Bacteroides vulgatus diminishes colonic microbiota dysbiosis ameliorating lumbar bone loss in ovariectomized mice. Bone. 2021;142:115710. doi:10.1016/j.bone.2020.115710.
  • Dar HY, Shukla P, Mishra PK, Anupam R, Mondal RK, Tomar GB, Sharma V, Srivastava RK. Lactobacillus acidophilus inhibits bone loss and increases bone heterogeneity in osteoporotic mice via modulating Treg-Th17 cell balance. Bone Rep. 2018;8:46–56. doi:10.1016/j.bonr.2018.02.001.
  • Dar HY, Pal S, Shukla P, Mishra PK, Tomar GB, Chattopadhyay N, Srivastava RK. Bacillus clausii inhibits bone loss by skewing Treg-Th17 cell equilibrium in postmenopausal osteoporotic mice model. Nutrition. 2018;54:118–128. doi:10.1016/j.nut.2018.02.013.
  • Parvaneh K, Ebrahimi M, Sabran MR, Karimi G, Hwei AN, Abdul-Majeed S, Ahmad Z, Ibrahim Z, Jamaluddin R. Probiotics (Bifidobacterium longum) increase bone mass density and upregulate sparc and bmp-2 genes in rats with bone loss resulting from Ovariectomy. Biomed Res IntBiomed Res Int. 2015;2015:1–10. doi:10.1155/2015/897639.
  • Rodrigues FC, Castro AS, Rodrigues VC, Fernandes SA, Fontes EA, de Oliveira TT, Martino HSD, de Luces Fortes Ferreira CL. Yacon flour and Bifidobacterium longum modulate bone health in rats. J Med Food. 2012;15(7):664–670. doi:10.1089/jmf.2011.0296.
  • Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, Parameswaran N, McCabe LR. Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol. 2014;229(11):1822–1830. doi:10.1002/jcp.24636.
  • Lucas S, Omata Y, Hofmann J, Bottcher M, Iljazovic A, Sarter K, Albrecht O, Schulz O, Krishnacoumar B, Krönke G, et al. Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss. Nat Commun. 2018;9(1):55. doi:10.1038/s41467-017-02490-4.
  • Tang X, Ma S, Li Y, Sun Y, Zhang K, Zhou Q, Yu R. Evaluating the activity of sodium butyrate to prevent osteoporosis in rats by promoting osteal GSK-3β/Nrf2 signaling and mitochondrial function. J Agric Food Chem. 2020;68(24):6588–6603. doi:10.1021/acs.jafc.0c01820.
  • Metz R, Smith C, DuHadaway JB, Chandler P, Baban B, Merlo LM, Pigott E, Keough MP, Rust S, Mellor AL, et al. IDO2 is critical for IDO1-mediated T-cell regulation and exerts a non-redundant function in inflammation. Int Immunol. 2014;26(7):357–367. doi:10.1093/intimm/dxt073.
  • Kim BJ, Hamrick MW, Yoo HJ, Lee SH, Kim SJ, Koh JM, Isales CM. The detrimental effects of Kynurenine, a tryptophan metabolite, on human bone metabolism. J Clin Endocrinol Metab. 2019;104(6):2334–2342. doi:10.1210/jc.2018-02481.
  • Refaey ME, McGee-Lawrence ME, Fulzele S, Kennedy EJ, Bollag WB, Elsalanty M, Zhong Q, Ding K-H, Bendzunas NG, Shi X-M, et al. Kynurenine, a tryptophan metabolite that accumulates with age, induces bone loss. J Bone Miner Res. 2017;32(11):2182–2193. doi:10.1002/jbmr.3224.
  • Kim GS, Kim CH, Park JY, Lee KU, Park CS. Effects of vitamin B12 on cell proliferation and cellular alkaline phosphatase activity in human bone marrow stromal osteoprogenitor cells and UMR106 osteoblastic cells. Metabolism. 1996;45(12):1443–1446. doi:10.1016/S0026-0495(96)90171-7.
  • Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients. 2013;5(4):1417–1435. doi:10.3390/nu5041417.
  • Al-Harbi NO, Imam F, Nadeem A, Al-Harbi MM, Iqbal M, Ahmad SF. Carbon tetrachloride-induced hepatotoxicity in rat is reversed by treatment with riboflavin. Int Immunopharmacol. 2014;21(2):383–388. doi:10.1016/j.intimp.2014.05.014.
  • LeBlanc JG, Levit R, Savoy de Giori G, de Moreno de LeBlanc A. Application of vitamin-producing lactic acid bacteria to treat intestinal inflammatory diseases. Appl Microbiol Biotechnol. 2020;104(8):3331–3337. doi:10.1007/s00253-020-10487-1.
  • Dehkordi EH, Sattari F, Khoshdel A, Kasiri K. Effect of folic acid and metformin on insulin resistance and inflammatory factors of obese children and adolescents. J Res Med Sci. 2016;21(1):71. doi:10.4103/1735-1995.189669.
  • Wallace TC, Marzorati M, Spence L, Weaver CM, Williamson PS. New frontiers in fibers: innovative and emerging research on the gut microbiome and bone health. J Am Coll Nutr. 2017;36(3):218–222. doi:10.1080/07315724.2016.1257961.
  • Cho SW, An JH, Park H, Yang JY, Choi HJ, Kim SW, Park YJ, Kim SY, Yim M, Baek W-Y, et al. Positive regulation of osteogenesis by bile acid through FXR. J Bone Miner Res. 2013;28(10):2109–2121. doi:10.1002/jbmr.1961.
  • Sandoval DA, D’Alessio DA. Physiology of proglucagon peptides: role of glucagon and GLP-1 in health and disease. Physiol Rev. 2015;95(2):513–548. doi:10.1152/physrev.00013.2014.
  • Kwon JY, Lee SH, Jhun J, Choi J, Jung K, Cho KH, Kim SJ, Yang CW, Park S-H, Cho M-L, et al. The combination of probiotic complex, Rosavin, and zinc improves pain and cartilage destruction in an osteoarthritis rat model. J Med Food. 2018;21(4):364–371. doi:10.1089/jmf.2017.4034.
  • Lei M, Guo C, Wang D, Zhang C, Hua L. The effect of probiotic Lactobacillus casei Shirota on knee osteoarthritis: a randomised double-blind, placebo-controlled clinical trial. Benef Microbes. 2017;8(5):697–703. doi:10.3920/BM2016.0207.
  • Lyu JL, Wang TM, Chen YH, Chang ST, Wu MS, Lin YH, Lin Y-H, Kuan C-M. Oral intake of Streptococcus thermophil us improves knee osteoarthritis degeneration: a randomized, double-blind, placebo-controlled clinical study. Heliyon. 2020;6(4):e03757. doi:10.1016/j.heliyon.2020.e03757.
  • Sim BY, Choi HJ, Kim MG, Jeong DG, Lee DG, Yoon JM, Kang D-J, Park S, Ji J-G, Joo I-H, et al. Effects of ID-CBT5101 in preventing and alleviating osteoarthritis symptoms in a monosodium Iodoacetate-induced rat model. J Microbiol Biotechnol. 2018;28(7):1199–1208. doi:10.4014/jmb.1803.03032.
  • Amdekar S, Singh V, Singh R, Sharma P, Keshav P, Kumar A. Lactobacillus casei reduces the inflammatory joint damage associated with collagen-induced arthritis (CIA) by reducing the pro-inflammatory cytokines: lactobacillus casei: COX-2 inhibitor. J Clin Immunol. 2011;31(2):147–154. doi:10.1007/s10875-010-9457-7.
  • Pan H, Guo R, Ju Y, Wang Q, Zhu J, Xie Y, Zheng Y, Li T, Liu Z, Lu L, et al. A single bacterium restores the microbiome dysbiosis to protect bones from destruction in a rat model of rheumatoid arthritis. Microbiome. 2019;7(1):107. doi:10.1186/s40168-019-0719-1.
  • Dourado E, Ferro M, Sousa Guerreiro C, Fonseca JE. Diet as a modulator of intestinal microbiota in rheumatoid arthritis. Nutrients. 2020;12(11):12. doi:10.3390/nu12113504.
  • Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Sci. 2013;341(6145):569–573. doi:10.1126/science.1241165.
  • Cho KH, Na HS, Jhun J, Woo JS, Lee AR, Lee SY, Lee JS, Um IG, Kim SJ, Park S-H, et al. Lactobacillus (LA-1) and butyrate inhibit osteoarthritis by controlling autophagy and inflammatory cell death of chondrocytes. Front Immunol. 2022;13:930511. doi:10.3389/fimmu.2022.930511.
  • Lee S, Koh J, Chang Y, Kim HY, Chung DH. Invariant NKT cells functionally link microbiota-induced butyrate production and joint inflammation. J Immunol. 2019;203(12):3199–3208. doi:10.4049/jimmunol.1801314.
  • Lee MC, Hsu YJ, Chuang HL, Hsieh PS, Ho HH, Chen WL, Chiu Y-S, Huang C-C. In vivo ergogenic properties of the Bifidobacterium longum OLP-01 isolated from a weightlifting gold medalist. Nutrients. 2019;11(9):11. doi:10.3390/nu11092003.
  • Huang WC, Wei CC, Huang CC, Chen WL, Huang HY. The beneficial effects of Lactobacillus plantarum PS128 on high-intensity, exercise-induced oxidative stress, inflammation, and performance in triathletes. Nutrients. 2019;11(2):11. doi:10.3390/nu11020353.
  • Lee MC, Hsu YJ, Ho HH, Hsieh SH, Kuo YW, Sung HC, Huang C-C. Lactobacillus salivarius subspecies salicinius SA-03 is a new probiotic capable of enhancing exercise performance and decreasing fatigue. Microorganisms. 2020;8(4):8. doi:10.3390/microorganisms8040545.
  • Toda K, Yamauchi Y, Tanaka A, Kuhara T, Odamaki T, Yoshimoto S, Xiao J-Z. Heat-killed Bifidobacterium breve B-3 enhances muscle functions: possible involvement of increases in muscle mass and mitochondrial biogenesis. Nutrients. 2020;12(1):12. doi:10.3390/nu12010219.
  • Zhang J, Motyl KJ, Irwin R, MacDougald OA, Britton RA, McCabe LR. Loss of bone and Wnt10b expression in male type 1 diabetic mice is blocked by the probiotic Lactobacillus reuteri. Endocrinology. 2015;156(9):3169–3182. doi:10.1210/EN.2015-1308.
  • Li JY, Chassaing B, Tyagi AM, Vaccaro C, Luo T, Adams J, Darby TM, Weitzmann MN, Mulle JG, Gewirtz AT, et al. Sex steroid deficiency–associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest. 2016;126(6):2049–2063. doi:10.1172/JCI86062.
  • Parvaneh M, Karimi G, Jamaluddin R, Ng MH, Zuriati I, Muhammad SI. Lactobacillus helveticus (ATCC 27558) upregulates Runx2 and Bmp2 and modulates bone mineral density in ovariectomy-induced bone loss rats. Clin Interv Aging. 2018;13:1555–1564. doi:10.2147/CIA.S169223.
  • Davani-Davari D, Negahdaripour M, Karimzadeh I, Seifan M, Mohkam M, Masoumi SJ, Berenjian A, Ghasemi Y. Prebiotics: definition, types, sources, mechanisms, and clinical applications. Foods. 2019;8(3):92. doi:10.3390/foods8030092.
  • Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58(8):1091–1103. doi:10.1136/gut.2008.165886.
  • Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, Possemiers S, Van Holle A, François P, de Vos WM, et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes. 2011;60(11):2775–2786. doi:10.2337/db11-0227.
  • Li R, Boer CG, Oei L, Medina-Gomez C. The gut microbiome: a new frontier in musculoskeletal research. Curr Osteoporos Rep. 2021;19(3):347–357. doi:10.1007/s11914-021-00675-x.
  • Farre R, Fiorani M, Abdu Rahiman S, Matteoli G. Intestinal permeability, inflammation and the role of Nutrients. Nutrients. 2020;12(4):12. doi:10.3390/nu12041185.
  • Jamshidi S, Masoumi SJ, Abiri B, Vafa M. The effects of synbiotic and/or vitamin D supplementation on gut-muscle axis in overweight and obese women: a study protocol for a double-blind, randomized, placebo-controlled trial. Trials. 2022;23(1):631. doi:10.1186/s13063-022-06598-x.
  • Sigmundsdottir H, Pan J, Debes GF, Alt C, Habtezion A, Soler D, Butcher, E C. Dcs metabolize sunlight-induced vitamin D3 to ‘program’ T cell attraction to the epidermal chemokine CCL27. Nat Immunol. 2007;8(3):285–293. doi:10.1038/ni1433.
  • Elias KM, Laurence A, Davidson TS, Stephens G, Kanno Y, Shevach EM, O’Shea JJ. Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a stat-3/Stat-5 independent signaling pathway. Blood. 2008;111(3):1013–1020. doi:10.1182/blood-2007-06-096438.
  • Singh P, Rawat A, Alwakeel M, Sharif E, Al Khodor S. The potential role of vitamin D supplementation as a gut microbiota modifier in healthy individuals. Sci Rep. 2020;10(1):21641. doi:10.1038/s41598-020-77806-4.
  • Cantorna MT, Snyder L, Arora J. Vitamin a and vitamin D regulate the microbial complexity, barrier function, and the mucosal immune responses to ensure intestinal homeostasis. Crit Rev Biochem Mol Biol. 2019;54(2):184–192. doi:10.1080/10409238.2019.1611734.
  • Prokopidis K, Giannos P, Katsikas Triantafyllidis K, Kechagias KS, Mesinovic J, Witard OC, Scott D. Effect of vitamin D monotherapy on indices of sarcopenia in community-dwelling older adults: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle. 2022;13(3):1642–1652. doi:10.1002/jcsm.12976.
  • Chaplin A, Parra P, Laraichi S, Serra F, Palou A. Calcium supplementation modulates gut microbiota in a prebiotic manner in dietary obese mice. Mol Nutr Food Res. 2016;60(2):468–480. doi:10.1002/mnfr.201500480.
  • Nadeem Aslam M, Bassis CM, Zhang L, Zaidi S, Varani J, Bergin IL, Pazienza V. Calcium reduces liver injury in mice on a high-fat diet: alterations in microbial and bile acid profiles. PloS One. 2016;11(11):e0166178. doi:10.1371/journal.pone.0166178.
  • Shanahan F, van Sinderen D, O’Toole PW, Stanton C. Feeding the microbiota: transducer of nutrient signals for the host. Gut. 2017;66(9):1709–1717. doi:10.1136/gutjnl-2017-313872.
  • Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Sci. 2011;334(6052):105–108. doi:10.1126/science.1208344.
  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. doi:10.1038/nature12820.
  • Simpson HL, Campbell BJ. Review article: dietary fibre-microbiota interactions. Aliment Pharmacol Ther. 2015;42(2):158–179. doi:10.1111/apt.13248.
  • Ni Lochlainn M, Bowyer RCE, Steves CJ. Dietary protein and muscle in aging people: the potential role of the gut microbiome. Nutrients. 2018;10(7):929.
  • Clarke SF, Murphy EF, O’Sullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, O’Reilly M, Jeffery IB, Wood-Martin R, et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63(12):1913–1920. doi:10.1136/gutjnl-2013-306541.
  • Moreno-Perez D, Bressa C, Bailen M, Hamed-Bousdar S, Naclerio F, Carmona M, Pérez M, González-Soltero R, Montalvo-Lominchar M, Carabaña C, et al. Effect of a protein supplement on the gut microbiota of endurance athletes: a randomized, controlled, double-blind Pilot study. Nutrients. 2018;10(3):10. doi:10.3390/nu10030337.
  • Karlund A, Gomez-Gallego C, Turpeinen AM, Palo-Oja OM, El-Nezami H, Kolehmainen M. Protein supplements and their relation with Nutrition, microbiota composition and health: is more protein always better for sportspeople? Nutrients. 2019;11(4):11. doi:10.3390/nu11040829.
  • Gulhane M, Murray L, Lourie R, Tong H, Sheng YH, Wang R, Kang A, Schreiber V, Wong KY, Magor G, et al. High fat diets induce colonic epithelial cell stress and inflammation that is reversed by IL-22. Sci Rep. 2016;6(1):28990. doi:10.1038/srep28990.
  • Guo S, Al-Sadi R, Said HM, Ma TY. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. Am J Pathol. 2013;182(2):375–387. doi:10.1016/j.ajpath.2012.10.014.
  • Maurizi G, Della Guardia L, Maurizi A, Poloni A. Adipocytes properties and crosstalk with immune system in obesity-related inflammation. J Cell Physiol. 2018;233(1):88–97. doi:10.1002/jcp.25855.
  • Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, Mujagic Z, Vila AV, Falony G, Vieira-Silva S, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Sci. 2016;352(6285):565–569. doi:10.1126/science.aad3369.
  • Liu J, He Z, Ma N, Chen ZY. Beneficial effects of dietary polyphenols on high-fat diet-induced obesity Linking with modulation of gut microbiota. J Agric Food Chem. 2020;68(1):33–47. doi:10.1021/acs.jafc.9b06817.
  • Beaudart C, Dawson A, Shaw SC, Harvey NC, Kanis JA, Binkley N, Reginster JY, Chapurlat R, Chan DC, Bruyère O, et al. Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review. Osteoporos Int. 2017;28(6):1817–1833. doi:10.1007/s00198-017-3980-9.
  • Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR. American college of Sports M. American college of sports medicine position stand: physical activity and bone health. Med Sci Sports Exerc. 2004;36(11):1985–1996. doi:10.1249/01.MSS.0000142662.21767.58.
  • Regnaux JP, Lefevre-Colau MM, Trinquart L, Nguyen C, Boutron I, Brosseau L, Ravaud P. High-intensity versus low-intensity physical activity or exercise in people with hip or knee osteoarthritis. Cochrane Database Of Systematic Reviews. 2015;2015(10):CD010203. doi:10.1002/14651858.CD010203.pub2.
  • Denou E, Marcinko K, Surette MG, Steinberg GR, Schertzer JD. High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity. Am J Physiol Endocrinol Metab. 2016;310(11):E982–93. doi:10.1152/ajpendo.00537.2015.
  • Welly RJ, Liu TW, Zidon TM, Rowles JL 3rd, Park YM, Smith TN, SWANSON KS, PADILLA J, VIEIRA-POTTER VJ. Comparison of diet versus exercise on metabolic function and gut microbiota in obese rats. Med Sci Sports Exerc. 2016;48(9):1688–1698. doi:10.1249/MSS.0000000000000964.
  • O’Sullivan O, Cronin O, Clarke SF, Murphy EF, Molloy MG, Shanahan F, Cotter PD. Exercise and the microbiota. Gut Microbes. 2015;6(2):131–136. doi:10.1080/19490976.2015.1011875.
  • Scheiman J, Luber JM, Chavkin TA, MacDonald T, Tung A, Pham LD, Wibowo MC, Wurth RC, Punthambaker S, Tierney BT, et al. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med. 2019;25(7):1104–1109. doi:10.1038/s41591-019-0485-4.
  • Allen JM, Mailing LJ, Niemiro GM, Moore R, Cook MD, White BA, HOLSCHER HD, WOODS JA. Exercise alters gut microbiota composition and function in lean and obese humans. Med Sci Sports Exerc. 2018;50(4):747–757. doi:10.1249/MSS.0000000000001495.
  • Morita E, Yokoyama H, Imai D, Takeda R, Ota A, Kawai E, Hisada T, Emoto M, Suzuki Y, Okazaki K. Aerobic exercise training with brisk walking increases intestinal Bacteroides in healthy elderly women. Nutrients. 2019;11(4):11. doi:10.3390/nu11040868.
  • de Sire A, de Sire R, Petito V, Masi L, Cisari C, Gasbarrini A, Scaldaferri F, Invernizzi M. Gut–joint axis: the role of physical exercise on gut microbiota modulation in older people with osteoarthritis. Nutrients. 2020;12(2):12. doi:10.3390/nu12020574.
  • Hao X, Shang X, Liu J, Chi R, Zhang J, Xu T. The gut microbiota in osteoarthritis: where do we stand and what can we do? Arthritis Res Ther. 2021;23(1):42. doi:10.1186/s13075-021-02427-9.
  • Rios JL, Bomhof MR, Reimer RA, Hart DA, Collins KH, Herzog W. Protective effect of prebiotic and exercise intervention on knee health in a rat model of diet-induced obesity. Sci Rep. 2019;9(1):3893. doi:10.1038/s41598-019-40601-x.
  • Rios JL, Hart DA, Reimer RA, Herzog W. Prebiotic and exercise do not alter knee osteoarthritis in a rat model of established obesity. Cartilage. 2021;13(2_suppl):1456S–1466S. doi:10.1177/1947603520959399.
  • Przewlocka K, Folwarski M, Kazmierczak-Siedlecka K, Skonieczna-Zydecka K, Kaczor JJ. Gut-muscle AxisExists and May affect skeletal muscle adaptation to training. Nutrients. 2020;12(5):12. doi:10.3390/nu12051451.
  • Hearris MA, Hammond KM, Fell JM, Morton JP. Regulation of muscle glycogen metabolism during exercise: implications for endurance performance and training adaptations. Nutrients. 2018;10(3):10. doi:10.3390/nu10030298.
  • Sohail MU, Yassine HM, Sohail A, Thani AAA. Impact of physical exercise on gut microbiome, inflammation, and the pathobiology of metabolic disorders. Rev Diabet Stud. 2019;15(1):35–48. doi:10.1900/RDS.2019.15.35.
  • Karl JP, Margolis LM, Madslien EH, Murphy NE, Castellani JW, Gundersen Y, Hoke AV, Levangie MW, Kumar R, Chakraborty N, et al. Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress. Am J Physiol Gastrointest Liver Physiol. 2017;312(6):G559–G571. doi:10.1152/ajpgi.00066.2017.
  • Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533. doi:10.1371/journal.pbio.1002533.
  • Sinha T, Vich Vila A, Garmaeva S, Jankipersadsing SA, Imhann F, Collij V, Bonder MJ, Jiang X, Gurry T, Alm EJ, et al. Analysis of 1135 gut metagenomes identifies sex-specific resistome profiles. Gut Microbes. 2019;10(3):358–366. doi:10.1080/19490976.2018.1528822.
  • Yoon K, Kim N. Roles of sex hormones and gender in the gut microbiota. J Neurogastroenterol Motil. 2021;27(3):314–325. doi:10.5056/jnm20208.
  • Flores R, Shi J, Fuhrman B, Xu X, Veenstra TD, Gail MH, Gajer P, Ravel J, Goedert JJ. Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: a cross-sectional study. J Transl Med. 2012;10(1):253. doi:10.1186/1479-5876-10-253.
  • Morwani-Mangnani J, Giannos P, Belzer C, Beekman M, Eline Slagboom P, Prokopidis K. Gut microbiome changes due to sleep disruption in older and younger individuals: a case for sarcopenia? Sleep. 2022;45(12):zsac239. doi:10.1093/sleep/zsac239.
  • Stacchiotti A, Favero G, Rodella LF. Impact of melatonin on skeletal muscle and exercise. Cells. 2020;9(2):288. doi:10.3390/cells9020288.
  • Leonardo-Mendonca RC, Ocana-Wilhelmi J, de Haro T, de Teresa-Galvan C, Guerra-Hernandez E, Rusanova I, Fernández-Ortiz M, Sayed RKA, Escames G, Acuña-Castroviejo D, et al. The benefit of a supplement with the antioxidant melatonin on redox status and muscle damage in resistance-trained athletes. Appl Physiol Nutr Metab. 2017;42(7):700–707. doi:10.1139/apnm-2016-0677.
  • Rodriguez MI, Carretero M, Escames G, Lopez LC, Maldonado MD, Tan DX, Reiter RJ, Acuña-Castroviejo D. Chronic melatonin treatment prevents age-dependent cardiac mitochondrial dysfunction in senescence-accelerated mice. Free Radic Res. 2007;41(1):15–24. doi:10.1080/10715760600936359.
  • Obayashi K, Saeki K, Maegawa T, Iwamoto J, Sakai T, Otaki N, Kataoka H, Kurumatani N. Melatonin secretion and muscle strength in elderly individuals: a cross-sectional study of the HEIJO-KYO cohort. J Gerontol A Biol Sci Med Sci. 2016;71(9):1235–1240. doi:10.1093/gerona/glw030.
  • Gao T, Wang Z, Dong Y, Cao J, Lin R, Wang X, Yu Z, Chen Y. Role of melatonin in sleep deprivation-induced intestinal barrier dysfunction in mice. J Pineal Res. 2019;67(1):e12574. doi:10.1111/jpi.12574.
  • Yin J, Li Y, Han H, Chen S, Gao J, Liu G, Wu X, Deng J, Yu Q, Huang X, et al. Melatonin reprogramming of gut microbiota improves lipid dysmetabolism in high-fat diet-fed mice. J Pineal Res. 2018;65(4):e12524. doi:10.1111/jpi.12524.
  • Xu P, Wang J, Hong F, Wang S, Jin X, Xue T, Jia L, Zhai Y. Melatonin prevents obesity through modulation of gut microbiota in mice. J Pineal Res. 2017;62(4):62. doi:10.1111/jpi.12399.
  • She M, Deng X, Guo Z, Laudon M, Hu Z, Liao D, Hu X, Luo Y, Shen Q, Su Z, et al. NEU-P11, a novel melatonin agonist, inhibits weight gain and improves insulin sensitivity in high-fat/high-sucrose-fed rats. Pharmacol Res. 2009;59(4):248–253. doi:10.1016/j.phrs.2009.01.005.
  • Zhu X, Zhang Y, Yang H, He F, Lin J. Melatonin suppresses ti-particle-induced inflammatory osteolysis via activation of the Nrf2/Catalase signaling pathway. Int Immunopharmacol. 2020;88:106847. doi:10.1016/j.intimp.2020.106847.
  • Liebert A, Bicknell B, Johnstone DM, Gordon LC, Kiat H, Hamblin MR. “Photobiomics”: can light, including Photobiomodulation, alter the microbiome? Photobiomodul Photomed Laser Surg. 2019;37(11):681–693. doi:10.1089/photob.2019.4628.
  • Bicknell B, Liebert A, Johnstone D, Kiat H. Photobiomodulation of the microbiome: implications for metabolic and inflammatory diseases. Lasers Med Sci. 2019;34(2):317–327. doi:10.1007/s10103-018-2594-6.
  • Cui J, Fu Y, Yi Z, Dong C, Liu H. The beneficial effects of ultraviolet light supplementation on bone density are associated with the intestinal flora in rats. Appl Microbiol Biotechnol. 2021;105(9):3705–3715. doi:10.1007/s00253-021-11282-2.
  • Guo R, Du Y, Zhang S, Liu H, Fu Y. The effects of ultraviolet supplementation to the artificial lighting on rats’ bone metabolism, bone mineral density, and skin. J Photochem Photobiol B. 2018;188:12–18. doi:10.1016/j.jphotobiol.2018.08.020.
  • Gonzalez-Alvarez ME, Sanchez-Romero EA, Turroni S, Fernandez-Carnero J, Villafane JH. Correlation between the altered gut microbiome and lifestyle interventions in chronic widespread pain patients: a systematic review. Medicina (Kaunas). 2023;59(2):59. doi:10.3390/medicina59020256.
  • Wang K, Zhang Z, Hang J, Liu J, Guo F, Ding Y, Li M, Nie Q, Lin J, Zhuo Y, et al. Microbial-host-isozyme analyses reveal microbial DPP4 as a potential antidiabetic target. Sci. 2023;381(6657):eadd5787. doi:10.1126/science.add5787.
  • Wang Y, Zhang S, Borody TJ, Zhang F. Encyclopedia of fecal microbiota transplantation: a review of effectiveness in the treatment of 85 diseases. Chin Med J (Engl). 2022;135(16):1927–1939. doi:10.1097/CM9.0000000000002339.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.