The Human Microbiome and Its Role in Musculoskeletal Disorders
Abstract
:1. Introduction
2. Human Microbiome
3. Microbiome in Health and Disease
Metabolites | Functions |
---|---|
Polyamines, e.g., putrescine, spermidine, and spermine [74,75,76,77,78] |
|
Vitamins, e.g., thiamine (B1), riboflavin (B2), pantothenic acid (B5), niacin (B3), pyridoxine (B6), folate (B11–B9) biotin (B7), cobalamin (B12), and menaquinone (K2) [79,80] |
|
Phenolic derivatives, e.g., 4-OH phenyl acetic acid, equol, urolithins, enterolactone, enterodiol, 8-prenylnaringenin, 2-(3,4-dihydroxyphenyl) acetic acid, 3-(4-hydroxyphenyl) propionic acid, and 5-(3,4-dihydroxyphenyl) valeric acid [81,82,83] |
|
Choline metabolites, e.g., betaine and choline, and trimethylamine N-oxide (TMAO) [84,85] |
|
Bile acid metabolites, e.g., lithocholic acid (LCA) and deoxycholic acid (DCA) [86] |
|
Indole derivatives, e.g., indole, indoxyl sulfate, and indole-3-propionic acid (IPA) [87,88,89] |
|
Short-chain fatty acids (SCFAs), e.g., acetate, butyrate, propionate, hexanoate, and valerate [89,90,91] |
|
4. Microbiome and Musculoskeletal Development
5. Gut Microbiota and Bone Health
6. Osteoporosis
7. Rheumatoid Arthritis
8. Sarcopenia
9. Osteoarthritis
10. Intervertebral Disc Degeneration
11. Modic Changes
12. Scoliosis
13. Microbiome and Inflammatory Conditions
13.1. Septic Arthritis
13.2. Osteomyelitis
13.3. Post-Operative Infection
13.4. Discitis
13.5. Ankylosing Spondylitis
13.6. Fibromyalgia and Chronic Pain
14. Potential Therapeutics Related to the Microbiome
15. Future Directions
16. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Arumugam, M.; Raes, J.; Pelletier, E.; Le Paslier, D.; Yamada, T.; Mende, D.R.; Fernandes, G.R.; Tap, J.; Bruls, T.; Batto, J.M.; et al. Enterotypes of the human gut microbiome. Nature 2011, 473, 174–180. [Google Scholar] [CrossRef]
- Sender, R.; Fuchs, S.; Milo, R. Are We Really Vastly Outnumbered? Revisiting the Ratio of Bacterial to Host Cells in Humans. Cell 2016, 164, 337–340. [Google Scholar] [CrossRef]
- Locey, K.J.; Lennon, J.T. Scaling laws predict global microbial diversity. Proc. Natl. Acad. Sci. USA 2016, 113, 5970–5975. [Google Scholar] [CrossRef]
- Wang, B.; Yao, M.; Lv, L.; Ling, Z.; Li, L. The Human Microbiota in Health and Disease. Engineering 2017, 3, 71–82. [Google Scholar] [CrossRef]
- Zheng, P.; Zeng, B.; Zhou, C.; Liu, M.; Fang, Z.; Xu, X.; Zeng, L.; Chen, J.; Fan, S.; Du, X.; et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism. Mol. Psychiatry 2016, 21, 786–796. [Google Scholar] [CrossRef]
- Conlon, M.A.; Bird, A.R. The impact of diet and lifestyle on gut microbiota and human health. Nutrients 2014, 7, 17–44. [Google Scholar] [CrossRef]
- Sonnenburg, E.D.; Sonnenburg, J.L. The ancestral and industrialized gut microbiota and implications for human health. Nat. Rev. Microbiol. 2019, 17, 383–390. [Google Scholar] [CrossRef]
- Blaser, M.J. Antibiotic use and its consequences for the normal microbiome. Science 2016, 352, 544–545. [Google Scholar] [CrossRef]
- Bello, M.G.D.; Knight, R.; Gilbert, J.A.; Blaser, M.J. Preserving microbial diversity. Science 2018, 362, 33–34. [Google Scholar] [CrossRef]
- Costello, M.E.; Robinson, P.C.; Benham, H.; Brown, M.A. The intestinal microbiome in human disease and how it relates to arthritis and spondyloarthritis. Best Pract. Res. Clin. Rheumatol. 2015, 29, 202–212. [Google Scholar] [CrossRef]
- Goodrich, J.K.; Di Rienzi, S.C.; Poole, A.C.; Koren, O.; Walters, W.A.; Caporaso, J.G.; Knight, R.; Ley, R.E. Conducting a microbiome study. Cell 2014, 158, 250–262. [Google Scholar] [CrossRef]
- Sharpton, T.J. An introduction to the analysis of shotgun metagenomic data. Front. Plant Sci. 2014, 5, 209. [Google Scholar] [CrossRef]
- Hiergeist, A.; Gläsner, J.; Reischl, U.; Gessner, A. Analyses of Intestinal Microbiota: Culture versus Sequencing. ILAR J. 2015, 56, 228–240. [Google Scholar] [CrossRef]
- Coit, P.; Sawalha, A.H. The human microbiome in rheumatic autoimmune diseases: A comprehensive review. Clin. Immunol. 2016, 170, 70–79. [Google Scholar] [CrossRef]
- Scher, J.U.; Littman, D.R.; Abramson, S.B. Microbiome in Inflammatory Arthritis and Human Rheumatic Diseases. Arthritis Rheumatol. 2016, 68, 35–45. [Google Scholar] [CrossRef]
- Caminer, A.C.; Haberman, R.; Scher, J.U. Human microbiome, infections, and rheumatic disease. Clin. Rheumatol. 2017, 36, 2645–2653. [Google Scholar] [CrossRef]
- Das, M.; Cronin, O.; Keohane, D.M.; Cormac, E.M.; Nugent, H.; Nugent, M.; Molloy, C.; O’Toole, P.W.; Shanahan, F.; Molloy, M.G.; et al. Gut microbiota alterations associated with reduced bone mineral density in older adults. Rheumatology 2019, 58, 2295–2304. [Google Scholar] [CrossRef]
- Nilsson, A.G.; Sundh, D.; Bäckhed, 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, 307–317. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Liu, C.; Cheung, W.H.; Li, J.; Chow, S.K.; Yu, J.; Wong, S.H.; Ip, M.; Sung, J.J.Y.; Wong, R.M.Y. Understanding the gut microbiota and sarcopenia: A systematic review. J. Cachexia Sarcopenia Muscle 2021, 12, 1393–1407. [Google Scholar] [CrossRef]
- Coulson, S.; Butt, H.; Vecchio, P.; Gramotnev, H.; Vitetta, L. Green-lipped mussel extract (Perna canaliculus) and glucosamine sulphate in patients with knee osteoarthritis: Therapeutic efficacy and effects on gastrointestinal microbiota profiles. Inflammopharmacology 2013, 21, 79–90. [Google Scholar] [CrossRef]
- Cardoso, J.; Ribeiro, I.; Araújo, T.; Carvalho, F.; Reis, E. Prevalência de dor musculoesquelética em professores. Rev. Bras. De Epidemiol. 2009, 12, 604–614. [Google Scholar] [CrossRef]
- Cardoneanu, A.; Cozma, S.; Rezus, C.; Petrariu, F.; Burlui, A.M.; Rezus, E. Characteristics of the intestinal microbiome in ankylosing spondylitis. Exp. Ther. Med. 2021, 22, 676. [Google Scholar] [CrossRef]
- Fritzell, P.; Welinder-Olsson, C.; Jonsson, B.; Melhus, A.; Andersson, S.G.E.; Bergstrom, T.; Tropp, H.; Gerdhem, P.; Hagg, O.; Laestander, H.; et al. Bacteria: Back pain, leg pain and Modic sign-a surgical multicentre comparative study. Eur. Spine J. 2019, 28, 2981–2989. [Google Scholar] [CrossRef]
- Rajasekaran, S.; Tangavel, C.; Aiyer, S.N.; Nayagam, S.M.; Raveendran, M.; Demonte, N.L.; Subbaiah, P.; Kanna, R.; Shetty, A.P.; Dharmalingam, K. ISSLS PRIZE IN CLINICAL SCIENCE 2017: Is infection the possible initiator of disc disease? An insight from proteomic analysis. Eur. Spine J. 2017, 26, 1384–1400. [Google Scholar] [CrossRef]
- Rajasekaran, S.; Soundararajan, D.C.R.; Tangavel, C.; Muthurajan, R.; Sri Vijay Anand, K.S.; Matchado, M.S.; Nayagam, S.M.; Shetty, A.P.; Kanna, R.M.; Dharmalingam, K. Human intervertebral discs harbour a unique microbiome and dysbiosis determines health and disease. Eur. Spine J. 2020, 29, 1621–1640. [Google Scholar] [CrossRef]
- Rajasekaran, S.; Tangavel, C.; Sri Vijay Anand, K.S.; Soundararajan, D.C.R.; Nayagam, S.M.; Matchado, M.S.; Raveendran, M.; Shetty, A.P.; Kanna, R.M.; Dharmalingam, K. Inflammaging determines health and disease in lumbar discs-evidence from differing proteomic signatures of healthy, aging, and degenerating discs. Spine J. 2020, 20, 48–59. [Google Scholar] [CrossRef]
- Rao, P.J.; Maharaj, M.; Chau, C.; Taylor, P.; Phan, K.; Choy, W.J.; Scherman, D.; Mews, P.; Scholsem, M.; Coughlan, M.; et al. Degenerate-disc infection study with contaminant control (DISC): A multicenter prospective case-control trial. Spine J. 2020, 20, 1544–1553. [Google Scholar] [CrossRef]
- Rettedal, E.A.; Ilesanmi-Oyelere, B.L.; Roy, N.C.; Coad, J.; Kruger, M.C. The Gut Microbiome Is Altered in Postmenopausal Women With Osteoporosis and Osteopenia. JBMR Plus 2020, 5, e10452. [Google Scholar] [CrossRef]
- Scher, J.U.; Sczesnak, A.; Longman, R.S.; Segata, N.; Ubeda, C.; Bielski, C.; Rostron, T.; Cerundolo, V.; Pamer, E.G.; Abramson, S.B.; et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife 2013, 2, e01202. [Google Scholar] [CrossRef]
- Guss, J.D.; Taylor, E.; Rouse, Z.; Roubert, S.; Higgins, C.H.; Thomas, C.J.; Baker, S.P.; Vashishth, D.; Donnelly, E.; Shea, M.K.; et al. The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength. Bone 2019, 127, 146–154. [Google Scholar] [CrossRef] [PubMed]
- Hernandez, C.J.; Yang, X.; Ji, G.; Niu, Y.; Sethuraman, A.S.; Koressel, J.; Shirley, M.; Fields, M.W.; Chyou, S.; Li, T.M.; et al. Disruption of the Gut Microbiome Increases the Risk of Periprosthetic Joint Infection in Mice. Clin. Orthop. Relat. Res. 2019, 477, 2588–2598. [Google Scholar] [CrossRef] [PubMed]
- Li, J.Y.; Chassaing, B.; Tyagi, A.M.; Vaccaro, C.; Luo, T.; Adams, J.; Darby, T.M.; Weitzmann, M.N.; Mulle, J.G.; Gewirtz, A.T.; et al. Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J. Clin. Investig. 2016, 126, 2049–2063. [Google Scholar] [CrossRef] [PubMed]
- Sjögren, K.; Engdahl, C.; Henning, P.; Lerner, U.H.; Tremaroli, V.; Lagerquist, M.K.; Ohlsson, C. The gut microbiota regulates bone mass in mice. J. Bone Miner. Res. 2012, 27, 1357–1367. [Google Scholar] [CrossRef]
- Wang, Z.; Wu, H.; Chen, Y.; Chen, H.; Wang, X.; Yuan, W. Lactobacillus paracasei S16 Alleviates Lumbar Disc Herniation by Modulating Inflammation Response and Gut Microbiota. Front. Nutr. 2021, 8, 701644. [Google Scholar] [CrossRef]
- Yan, J.; Herzog, J.W.; Tsang, K.; Brennan, C.A.; Bower, M.A.; Garrett, W.S.; Sartor, B.R.; Aliprantis, A.O.; Charles, J.F. Gut microbiota induce IGF-1 and promote bone formation and growth. Proc. Natl. Acad. Sci. USA 2016, 113, E7554–E7563. [Google Scholar] [CrossRef]
- Reis Ferreira, M.; Andreyev, H.J.N.; Mohammed, K.; Truelove, L.; Gowan, S.M.; Li, J.; Gulliford, S.L.; Marchesi, J.R.; Dearnaley, D.P. Microbiota- and Radiotherapy-Induced Gastrointestinal Side-Effects (MARS) Study: A Large Pilot Study of the Microbiome in Acute and Late-Radiation Enteropathy. Clin. Cancer Res. 2019, 25, 6487–6500. [Google Scholar] [CrossRef]
- Turnbaugh, P.J.; Ley, R.E.; Hamady, M.; Fraser-Liggett, C.M.; Knight, R.; Gordon, J.I. The human microbiome project. Nature 2007, 449, 804–810. [Google Scholar] [CrossRef]
- Peterson, J.; Garges, S.; Giovanni, M.; McInnes, P.; Wang, L.; Schloss, J.A.; Bonazzi, V.; McEwen, J.E.; Wetterstrand, K.A.; Deal, C.; et al. The NIH Human Microbiome Project. Genome Res. 2009, 19, 2317–2323. [Google Scholar] [CrossRef]
- Qin, J.; Li, R.; Raes, J.; Arumugam, M.; Burgdorf, K.S.; 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, 59–65. [Google Scholar] [CrossRef] [PubMed]
- Gilbert, J.; Quinn, R.; Debelius, J.; Xu, Z.; Morton, J.; Garg, N.; Jansson, J.; Dorrestein, P.; Knight, R. Microbiome-wide association studies link dynamic microbial consortia to disease. Nature 2016, 535, 94–103. [Google Scholar] [CrossRef] [PubMed]
- Gilbert, J.A.; Blaser, M.J.; Caporaso, J.G.; Jansson, J.K.; Lynch, S.V.; Knight, R. Current understanding of the human microbiome. Nat. Med. 2018, 24, 392–400. [Google Scholar] [CrossRef]
- Voreades, N.; Kozil, A.; Weir, T.L. Diet and the development of the human intestinal microbiome. Front. Microbiol. 2014, 5, 494. [Google Scholar] [CrossRef] [PubMed]
- Quigley, E.M. Gut bacteria in health and disease. Gastroenterol. Hepatol. 2013, 9, 560–569. [Google Scholar]
- Debré, P. Challenges set by the microbiota. Biol. Aujourdhui 2017, 211, 19–28. [Google Scholar] [CrossRef] [PubMed]
- Sekirov, I.; Russell, S.L.; Antunes, L.C.; Finlay, B.B. Gut microbiota in health and disease. Physiol. Rev. 2010, 90, 859–904. [Google Scholar] [CrossRef]
- Cryan, J.F.; O’Mahony, S.M. The microbiome-gut-brain axis: From bowel to behavior. Neurogastroenterol. Motil. 2011, 23, 187–192. [Google Scholar] [CrossRef]
- Flint, H.J.; Scott, K.P.; Duncan, S.H.; Louis, P.; Forano, E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012, 3, 289–306. [Google Scholar] [CrossRef]
- Lynch, S.V.; Pedersen, O. The Human Intestinal Microbiome in Health and Disease. N. Engl. J. Med. 2016, 375, 2369–2379. [Google Scholar] [CrossRef]
- Eckburg, P.B.; Bik, E.M.; Bernstein, C.N.; Purdom, E.; Dethlefsen, L.; Sargent, M.; Gill, S.R.; Nelson, K.E.; Relman, D.A. Diversity of the human intestinal microbial flora. Science 2005, 308, 1635–1638. [Google Scholar] [CrossRef] [PubMed]
- Reyes, A.; Haynes, M.; Hanson, N.; Angly, F.E.; Heath, A.C.; Rohwer, F.; Gordon, J.I. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 2010, 466, 334–338. [Google Scholar] [CrossRef] [PubMed]
- Pérez-Cobas, A.E.; Gosalbes, M.J.; Friedrichs, A.; Knecht, H.; Artacho, A.; Eismann, K.; Otto, W.; Rojo, D.; Bargiela, R.; von Bergen, M.; et al. Gut microbiota disturbance during antibiotic therapy: A multi-omic approach. Gut 2013, 62, 1591–1601. [Google Scholar] [CrossRef] [PubMed]
- Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P.; et al. Human gut microbiome viewed across age and geography. Nature 2012, 486, 222–227. [Google Scholar] [CrossRef] [PubMed]
- Koren, O.; Goodrich, J.K.; Cullender, T.C.; Spor, A.; Laitinen, K.; Bäckhed, H.K.; Gonzalez, A.; Werner, J.J.; Angenent, L.T.; Knight, R.; et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012, 150, 470–480. [Google Scholar] [CrossRef]
- David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A.; et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563. [Google Scholar] [CrossRef]
- He, Y.; Wu, W.; Zheng, H.M.; Li, P.; McDonald, D.; Sheng, H.F.; Chen, M.X.; Chen, Z.H.; Ji, G.Y.; Zheng, Z.D.; et al. Author Correction: Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat. Med. 2018, 24, 1940. [Google Scholar] [CrossRef]
- Deschasaux, M.; Bouter, K.E.; Prodan, A.; Levin, E.; Groen, A.K.; Herrema, H.; Tremaroli, V.; Bakker, G.J.; Attaye, I.; Pinto-Sietsma, S.J.; et al. Depicting the composition of gut microbiota in a population with varied ethnic origins but shared geography. Nat. Med. 2018, 24, 1526–1531. [Google Scholar] [CrossRef]
- Fasano, A.; Shea-Donohue, T. Mechanisms of disease: The role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat. Clin. Pract. Gastroenterol. Hepatol. 2005, 2, 416–422. [Google Scholar] [CrossRef]
- Nougayrède, J.P.; Homburg, S.; Taieb, F.; Boury, M.; Brzuszkiewicz, E.; Gottschalk, G.; Buchrieser, C.; Hacker, J.; Dobrindt, U.; Oswald, E. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 2006, 313, 848–851. [Google Scholar] [CrossRef]
- Serban, D.E. Microbiota in Inflammatory Bowel Disease Pathogenesis and Therapy: Is It All About Diet? Nutr. Clin. Pract. 2015, 30, 760–779. [Google Scholar] [CrossRef] [PubMed]
- Dabke, K.; Hendrick, G.; Devkota, S. The gut microbiome and metabolic syndrome. J. Clin. Investig. 2019, 129, 4050–4057. [Google Scholar] [CrossRef] [PubMed]
- Vallianou, N.; Christodoulatos, G.S.; Karampela, I.; Tsilingiris, D.; Magkos, F.; Stratigou, T.; Kounatidis, D.; Dalamaga, M. Understanding the Role of the Gut Microbiome and Microbial Metabolites in Non-Alcoholic Fatty Liver Disease: Current Evidence and Perspectives. Biomolecules 2021, 12, 56. [Google Scholar] [CrossRef]
- Singh, B.; Qin, N.; Reid, G. Microbiome Regulation of Autoimmune, Gut and Liver Associated Diseases. Inflamm. Allergy Drug Targets 2015, 14, 84–93. [Google Scholar] [CrossRef]
- Gioia, C.; Lucchino, B.; Tarsitano, M.G.; Iannuccelli, C.; Di Franco, M. Dietary Habits and Nutrition in Rheumatoid Arthritis: Can. Diet. Influence Disease Development and Clinical Manifestations? Nutrients 2020, 12, 1456. [Google Scholar] [CrossRef] [PubMed]
- Mowry, E.M.; Glenn, J.D. The Dynamics of the Gut Microbiome in Multiple Sclerosis in Relation to Disease. Neurol. Clin. 2018, 36, 185–196. [Google Scholar] [CrossRef] [PubMed]
- Wei, Y.; Li, Y.; Yan, L.; Sun, C.; Miao, Q.; Wang, Q.; Xiao, X.; Lian, M.; Li, B.; Chen, Y.; et al. Alterations of gut microbiome in autoimmune hepatitis. Gut 2020, 69, 569–577. [Google Scholar] [CrossRef]
- Manasson, J.; Shen, N.; Garcia Ferrer, H.R.; Ubeda, C.; Iraheta, I.; Heguy, A.; Von Feldt, J.M.; Espinoza, L.R.; Garcia Kutzbach, A.; Segal, L.N.; et al. Gut Microbiota Perturbations in Reactive Arthritis and Postinfectious Spondyloarthritis. Arthritis Rheumatol. 2018, 70, 242–254. [Google Scholar] [CrossRef]
- Bibbò, S.; Dore, M.P.; Pes, G.M.; Delitala, G.; Delitala, A.P. Is there a role for gut microbiota in type 1 diabetes pathogenesis? Ann. Med. 2017, 49, 11–22. [Google Scholar] [CrossRef]
- Vitetta, L.; Coulson, S.; Linnane, A.W.; Butt, H. The gastrointestinal microbiome and musculoskeletal diseases: A beneficial role for probiotics and prebiotics. Pathogens 2013, 2, 606–626. [Google Scholar] [CrossRef]
- Brial, F.; Le Lay, A.; Dumas, M.E.; Gauguier, D. Implication of gut microbiota metabolites in cardiovascular and metabolic diseases. Cell. Mol. Life Sci. 2018, 75, 3977–3990. [Google Scholar] [CrossRef]
- Bennett, B.J.; de Aguiar Vallim, T.Q.; Wang, Z.; Shih, D.M.; Meng, Y.; Gregory, J.; Allayee, H.; Lee, R.; Graham, M.; Crooke, R.; et al. Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. Cell Metab. 2013, 17, 49–60. [Google Scholar] [CrossRef] [PubMed]
- Kho, Z.Y.; Lal, S.K. The Human Gut Microbiome—A Potential Controller of Wellness and Disease. Front. Microbiol. 2018, 9, 1835. [Google Scholar] [CrossRef] [PubMed]
- Guo, X.; Rao, J.N.; Liu, L.; Zou, T.T.; Turner, D.J.; Bass, B.L.; Wang, J.Y. Regulation of adherens junctions and epithelial paracellular permeability: A novel function for polyamines. Am. J. Physiol. Cell Physiol. 2003, 285, C1174–C1187. [Google Scholar] [CrossRef] [PubMed]
- Guo, X.; Rao, J.N.; Liu, L.; Zou, T.; Keledjian, K.M.; Boneva, D.; Marasa, B.S.; Wang, J.Y. Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288, G1159–G1169. [Google Scholar] [CrossRef]
- Pérez-Cano, F.J.; González-Castro, A.; Castellote, C.; Franch, A.; Castell, M. Influence of breast milk polyamines on suckling rat immune system maturation. Dev. Comp. Immunol. 2010, 34, 210–218. [Google Scholar] [CrossRef]
- Johnson, C.H.; Dejea, C.M.; Edler, D.; Hoang, L.T.; Santidrian, A.F.; Felding, B.H.; Ivanisevic, J.; Cho, K.; Wick, E.C.; Hechenbleikner, E.M.; et al. Metabolism links bacterial biofilms and colon carcinogenesis. Cell Metab. 2015, 21, 891–897. [Google Scholar] [CrossRef]
- Rooks, M.G.; Garrett, W.S. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 2016, 16, 341–352. [Google Scholar] [CrossRef]
- Nicholson, J.K.; Holmes, E.; Kinross, J.; Burcelin, R.; Gibson, G.; Jia, W.; Pettersson, S. Host-gut microbiota metabolic interactions. Science 2012, 336, 1262–1267. [Google Scholar] [CrossRef]
- Lerner, A.; Neidhöfer, S.; Matthias, T. The Gut Microbiome Feelings of the Brain: A Perspective for Non-Microbiologists. Microorganisms 2017, 5, 66. [Google Scholar] [CrossRef]
- Selma, M.V.; Espín, J.C.; Tomás-Barberán, F.A. Interaction between phenolics and gut microbiota: Role in human health. J. Agric. Food Chem. 2009, 57, 6485–6501. [Google Scholar] [CrossRef] [PubMed]
- Larrosa, M.; González-Sarrías, A.; García-Conesa, M.T.; Tomás-Barberán, F.A.; Espín, J.C. Urolithins, ellagic acid-derived metabolites produced by human colonic microflora, exhibit estrogenic and antiestrogenic activities. J. Agric. Food Chem. 2006, 54, 1611–1620. [Google Scholar] [CrossRef] [PubMed]
- Larrosa, M.; González-Sarrías, A.; Yáñez-Gascón, M.J.; Selma, M.V.; Azorín-Ortuño, M.; Toti, S.; Tomás-Barberán, F.; Dolara, P.; Espín, J.C. Anti-inflammatory properties of a pomegranate extract and its metabolite urolithin-A in a colitis rat model and the effect of colon inflammation on phenolic metabolism. J. Nutr. Biochem. 2010, 21, 717–725. [Google Scholar] [CrossRef] [PubMed]
- Dumas, M.E.; Barton, R.H.; Toye, A.; Cloarec, O.; Blancher, C.; Rothwell, A.; Fearnside, J.; Tatoud, R.; Blanc, V.; Lindon, J.C.; et al. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc. Natl. Acad. Sci. USA 2006, 103, 12511–12516. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Klipfell, E.; Bennett, B.J.; Koeth, R.; Levison, B.S.; Dugar, B.; Feldstein, A.E.; Britt, E.B.; Fu, X.; Chung, Y.M.; et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011, 472, 57–63. [Google Scholar] [CrossRef] [PubMed]
- Hylemon, P.B.; Zhou, H.; Pandak, W.M.; Ren, S.; Gil, G.; Dent, P. Bile acids as regulatory molecules. J. Lipid Res. 2009, 50, 1509–1520. [Google Scholar] [CrossRef]
- Deguchi, T.; Ohtsuki, S.; Otagiri, M.; Takanaga, H.; Asaba, H.; Mori, S.; Terasaki, T. Major role of organic anion transporter 3 in the transport of indoxyl sulfate in the kidney. Kidney Int. 2002, 61, 1760–1768. [Google Scholar] [CrossRef]
- Wikoff, W.R.; Anfora, A.T.; Liu, J.; Schultz, P.G.; Lesley, S.A.; Peters, E.C.; Siuzdak, G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl. Acad. Sci. USA 2009, 106, 3698–3703. [Google Scholar] [CrossRef]
- Venkatesh, M.; Mukherjee, S.; Wang, H.; Li, H.; Sun, K.; Benechet, A.P.; Qiu, Z.; Maher, L.; Redinbo, M.R.; Phillips, R.S.; et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity 2014, 41, 296–310. [Google Scholar] [CrossRef]
- Tolhurst, G.; Heffron, H.; Lam, Y.S.; Parker, H.E.; Habib, A.M.; Diakogiannaki, E.; Cameron, J.; Grosse, J.; Reimann, F.; Gribble, F.M. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 2012, 61, 364–371. [Google Scholar] [CrossRef]
- Galus, M.; Jeyaranjaan, J.; Smith, E.; Li, H.; Metcalfe, C.; Wilson, J.Y. Chronic effects of exposure to a pharmaceutical mixture and municipal wastewater in zebrafish. Aquat. Toxicol. 2013, 132, 212–222. [Google Scholar] [CrossRef]
- Steves, C.J.; Bird, S.; Williams, F.M.; Spector, T.D. The Microbiome and Musculoskeletal Conditions of Aging: A Review of Evidence for Impact and Potential Therapeutics. J. Bone Miner. Res. 2016, 31, 261–269. [Google Scholar] [CrossRef] [PubMed]
- Derrien, M.; Alvarez, A.-S.; de Vos, W.M. The Gut Microbiota in the First Decade of Life. Trends Microbiol. 2019, 27, 997–1010. [Google Scholar] [CrossRef]
- Matamoros, S.; Gras-Leguen, C.; Le Vacon, F.; Potel, G.; de La Cochetiere, M.F. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol. 2013, 21, 167–173. [Google Scholar] [CrossRef] [PubMed]
- Jansson, P.-A.; Curiac, D.; Ahrén, I.; Hansson, F.; Martinsson Niskanen, T.; Sjögren, K.; Ohlsson, C. Probiotic treatment using a mix of three Lactobacillus strains for lumbar spine bone loss in postmenopausal women: A randomised, double-blind, placebo-controlled, multicentre trial. Lancet Rheumatol. 2019, 1, e154–e162. [Google Scholar] [CrossRef]
- Martin-Millan, M.; Almeida, M.; Ambrogini, E.; Han, L.; Zhao, H.; Weinstein, R.S.; Jilka, R.L.; O’Brien, C.A.; Manolagas, S.C. The estrogen receptor-α in osteoclasts mediates the protective effects of estrogens on cancellous but not cortical bone. Mol. Endocrinol. 2010, 24, 323–334. [Google Scholar] [CrossRef] [PubMed]
- Nakamura, T.; Imai, Y.; Matsumoto, T.; Sato, S.; Takeuchi, K.; Igarashi, K.; Harada, Y.; Azuma, Y.; Krust, A.; Yamamoto, Y.; et al. Estrogen prevents bone loss via estrogen receptor α and induction of Fas ligand in osteoclasts. Cell 2007, 130, 811–823. [Google Scholar] [CrossRef]
- 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, 2673–2682. [Google Scholar] [CrossRef]
- Takayanagi, H.; Ogasawara, K.; Hida, S.; Chiba, T.; Murata, S.; Sato, K.; Takaoka, A.; Yokochi, T.; Oda, H.; Tanaka, K.; et al. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-γ. Nature 2000, 408, 600–605. [Google Scholar] [CrossRef]
- Yu, M.; Malik Tyagi, A.; Li, J.Y.; Adams, J.; Denning, T.L.; Weitzmann, M.N.; Jones, R.M.; Pacifici, R. PTH induces bone loss via microbial-dependent expansion of intestinal TNF+ T cells and Th17 cells. Nat. Commun. 2020, 11, 468. [Google Scholar] [CrossRef]
- Lorentzon, M.; Cummings, S.R. Osteoporosis: The evolution of a diagnosis. J. Intern. Med. 2015, 277, 650–661. [Google Scholar] [CrossRef] [PubMed]
- Pasco, J.A.; Kotowicz, M.A.; Henry, M.J.; Nicholson, G.C.; Spilsbury, H.J.; Box, J.D.; Schneider, H.G. High-sensitivity C-reactive protein and fracture risk in elderly women. JAMA 2006, 296, 1353–1355. [Google Scholar] [CrossRef] [PubMed]
- Ding, C.; Parameswaran, V.; Udayan, R.; Burgess, J.; Jones, G. Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: A longitudinal study. J. Clin. Endocrinol. Metab. 2008, 93, 1952–1958. [Google Scholar] [CrossRef]
- Schett, G.; Kiechl, S.; Weger, S.; Pederiva, A.; Mayr, A.; Petrangeli, M.; Oberhollenzer, F.; Lorenzini, R.; Redlich, K.; Axmann, R.; et al. High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch. Intern. Med. 2006, 166, 2495–2501. [Google Scholar] [CrossRef]
- Koh, J.M.; Khang, Y.H.; Jung, C.H.; Bae, S.; Kim, D.J.; Chung, Y.E.; Kim, G.S. Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre- and postmenopausal women: Evidence for a link between systemic inflammation and osteoporosis. Osteoporos. Int. 2005, 16, 1263–1271. [Google Scholar] [CrossRef] [PubMed]
- Hienz, S.A.; Paliwal, S.; Ivanovski, S. Mechanisms of Bone Resorption in Periodontitis. J. Immunol. Res. 2015, 2015, 615486. [Google Scholar] [CrossRef]
- Griffin, I.J.; Davila, P.M.; Abrams, S.A. Non-digestible oligosaccharides and calcium absorption in girls with adequate calcium intakes. Br. J. Nutr. 2002, 87 (Suppl. S2), S187–S191. [Google Scholar] [CrossRef]
- van den Heuvel, E.G.; Muys, T.; van Dokkum, W.; Schaafsma, G. Oligofructose stimulates calcium absorption in adolescents. Am. J. Clin. Nutr. 1999, 69, 544–548. [Google Scholar] [CrossRef]
- Whisner, C.M.; Castillo, L.F. Prebiotics, Bone and Mineral Metabolism. Calcif. Tissue Int. 2018, 102, 443–479. [Google Scholar] [CrossRef]
- Costa, G.; Vasconcelos, Q.; Abreu, G.; Albuquerque, A.; Vilarejo, J.; Aragao, G. Changes in nutrient absorption in children and adolescents caused by fructans, especially fructooligosaccharides and inulin. Arch. Pediatr. 2020, 27, 166–169. [Google Scholar] [CrossRef]
- Ohlsson, C.; Sjogren, K. Effects of the gut microbiota on bone mass. Trends Endocrinol. Metab. 2015, 26, 69–74. [Google Scholar] [CrossRef]
- Abrams, S.A.; Griffin, I.J.; Hawthorne, K.M.; Liang, L.; Gunn, S.K.; Darlington, G.; Ellis, K.J. A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am. J. Clin. Nutr. 2005, 82, 471–476. [Google Scholar] [CrossRef] [PubMed]
- Whisner, C.M.; Martin, B.R.; Nakatsu, C.H.; McCabe, G.P.; McCabe, L.D.; Peacock, M.; Weaver, C.M. Soluble maize fibre affects short-term calcium absorption in adolescent boys and girls: A randomised controlled trial using dual stable isotopic tracers. Br. J. Nutr. 2014, 112, 446–456. [Google Scholar] [CrossRef] [PubMed]
- Mangnus, L.; van Steenbergen, H.W.; Lindqvist, E.; Brouwer, E.; Reijnierse, M.; Huizinga, T.W.; Gregersen, P.K.; Berglin, E.; Rantapaa-Dahlqvist, S.; van der Heijde, D.; et al. Studies on ageing and the severity of radiographic joint damage in rheumatoid arthritis. Arthritis Res. Ther. 2015, 17, 222. [Google Scholar] [CrossRef] [PubMed]
- Ivanov, I.I.; Atarashi, K.; Manel, N.; Brodie, E.L.; Shima, T.; Karaoz, U.; Wei, D.; Goldfarb, K.C.; Santee, C.A.; Lynch, S.V.; et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139, 485–498. [Google Scholar] [CrossRef]
- McLean, M.H.; Dieguez, D.; Jr Miller, L.M.; Young, H.A. Does the microbiota play a role in the pathogenesis of autoimmune diseases? Gut 2015, 64, 332–341. [Google Scholar] [CrossRef]
- Biagi, E.; Candela, M.; Fairweather-Tait, S.; Franceschi, C.; Brigidi, P. Aging of the human metaorganism: The microbial counterpart. Age (Dordr) 2012, 34, 247–267. [Google Scholar] [CrossRef]
- de Aquino, S.G.; Abdollahi-Roodsaz, S.; Koenders, M.I.; van de Loo, F.A.; Pruijn, G.J.; Marijnissen, R.J.; Walgreen, B.; Helsen, M.M.; van den Bersselaar, L.A.; de Molon, R.S.; et al. Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1-driven Th17 response. J. Immunol. 2014, 192, 4103–4111. [Google Scholar] [CrossRef]
- Marchesan, J.T.; Gerow, E.A.; Schaff, R.; Taut, A.D.; Shin, S.Y.; Sugai, J.; Brand, D.; Burberry, A.; Jorns, J.; Lundy, S.K.; et al. Porphyromonas gingivalis oral infection exacerbates the development and severity of collagen-induced arthritis. Arthritis Res. Ther. 2013, 15, R186. [Google Scholar] [CrossRef]
- Wells, P.M.; Adebayo, A.S.; Bowyer, R.C.E.; Freidin, M.B.; Finckh, A.; Strowig, T.; Lesker, T.R.; Alpizar-Rodriguez, D.; Gilbert, B.; Kirkham, B.; et al. Associations between gut microbiota and genetic risk for rheumatoid arthritis in the absence of disease: A cross-sectional study. Lancet Rheumatol. 2020, 2, e418–e427. [Google Scholar] [CrossRef]
- Lopez-Oliva, I.; Paropkari, A.D.; Saraswat, S.; Serban, S.; Yonel, Z.; Sharma, P.; de Pablo, P.; Raza, K.; Filer, A.; Chapple, I.; et al. Dysbiotic Subgingival Microbial Communities in Periodontally Healthy Patients With Rheumatoid Arthritis. Arthritis Rheumatol. 2018, 70, 1008–1013. [Google Scholar] [CrossRef] [PubMed]
- 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, 107. [Google Scholar] [CrossRef] [PubMed]
- Santilli, V.; Bernetti, A.; Mangone, M.; Paoloni, M. Clinical definition of sarcopenia. Clin. Cases Miner. Bone Metab. 2014, 11, 177–180. [Google Scholar] [CrossRef] [PubMed]
- Cruz-Jentoft, A.J.; Baeyens, J.P.; Bauer, J.M.; Boirie, Y.; Cederholm, T.; Landi, F.; Martin, F.C.; Michel, J.P.; Rolland, Y.; Schneider, S.M.; 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. [Google Scholar] [CrossRef]
- Bindels, L.B.; Delzenne, N.M. Muscle wasting: The gut microbiota as a new therapeutic target? Int. J. Biochem. Cell. Biol. 2013, 45, 2186–2190. [Google Scholar] [CrossRef]
- Schaap, L.A.; Pluijm, S.M.; Deeg, D.J.; Visser, M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am. J. Med. 2006, 119, 526.e9–526.e17. [Google Scholar] [CrossRef]
- 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, 4628. [Google Scholar] [CrossRef]
- Inglis, J.E.; Ilich, J.Z. The Microbiome and Osteosarcopenic Obesity in Older Individuals in Long-Term Care Facilities. Curr. Osteoporos. Rep. 2015, 13, 358–362. [Google Scholar] [CrossRef]
- Goldring, M.B.; Otero, M. Inflammation in osteoarthritis. Curr. Opin. Rheumatol. 2011, 23, 471–478. [Google Scholar] [CrossRef]
- Benito, M.J.; Veale, D.J.; FitzGerald, O.; van den Berg, W.B.; Bresnihan, B. Synovial tissue inflammation in early and late osteoarthritis. Ann. Rheum. Dis. 2005, 64, 1263–1267. [Google Scholar] [CrossRef]
- Boer, C.G.; Radjabzadeh, D.; Medina-Gomez, C.; Garmaeva, S.; Schiphof, D.; Arp, P.; Koet, T.; Kurilshikov, A.; Fu, J.; Ikram, M.A.; et al. Intestinal microbiome composition and its relation to joint pain and inflammation. Nat. Commun. 2019, 10, 4881. [Google Scholar] [CrossRef] [PubMed]
- Siala, M.; Gdoura, R.; Fourati, H.; Rihl, M.; Jaulhac, B.; Younes, M.; Sibilia, J.; Baklouti, S.; Bargaoui, N.; Sellami, S.; et al. Broad-range PCR, cloning and sequencing of the full 16S rRNA gene for detection of bacterial DNA in synovial fluid samples of Tunisian patients with reactive and undifferentiated arthritis. Arthritis Res. Ther. 2009, 11, R102. [Google Scholar] [CrossRef] [PubMed]
- Olmez, N.; Wang, G.F.; Li, Y.; Zhang, H.; Schumacher, H.R. Chlamydial nucleic acids in synovium in osteoarthritis: What are the implications? J. Rheumatol. 2001, 28, 1874–1880. [Google Scholar] [PubMed]
- Diseases, G.B.D.; Injuries, C. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: A systematic analysis for the Global Burden of Disease Study 2019. Lancet 2020, 396, 1204–1222. [Google Scholar] [CrossRef]
- Chou, D.; Samartzis, D.; Bellabarba, C.; Patel, A.; Luk, K.D.; Kisser, J.M.; Skelly, A.C. Degenerative magnetic resonance imaging changes in patients with chronic low back pain: A systematic review. Spine 2011, 36 (Suppl. S21), S43–S53. [Google Scholar] [CrossRef]
- Mallow, G.M.; Zepeda, D.; Kuzel, T.G.; Barajas, J.N.; Aboushaala, K.; Nolte, M.T.; Espinoza-Orias, A.; Oh, C.; Colman, M.; Kogan, M.; et al. ISSLS PRIZE in Clinical Science 2022: Epidemiology, risk factors and clinical impact of juvenile Modic changes in paediatric patients with low back pain. Eur. Spine J. 2022, 31, 1069–1079. [Google Scholar] [CrossRef]
- Rudisill, S.S.; Hornung, A.L.; Kia, C.; Mallow, G.M.; Aboushaala, K.; Lim, P.; Martin, J.; Wong, A.Y.L.; Toro, S.; Kozaki, T.; et al. Obesity in children with low back pain: Implications with imaging phenotypes and opioid use. Spine J. 2023, 23, 945–953. [Google Scholar] [CrossRef]
- Wan, Z.Y.; Zhang, J.; Shan, H.; Liu, T.F.; Song, F.; Samartzis, D.; Wang, H.Q. Epidemiology of Lumbar Degenerative Phenotypes of Children and Adolescents: A Large-Scale Imaging Study. Glob. Spine J. 2023, 13, 599–608. [Google Scholar] [CrossRef]
- Zehra, U.; Tryfonidou, M.; Iatridis, J.C.; Illien-Junger, S.; Mwale, F.; Samartzis, D. Mechanisms and clinical implications of intervertebral disc calcification. Nat. Rev. Rheumatol. 2022, 18, 352–362. [Google Scholar] [CrossRef]
- Sadowska, A.; Touli, E.; Hitzl, W.; Greutert, H.; Ferguson, S.J.; Wuertz-Kozak, K.; Hausmann, O.N. Inflammaging in cervical and lumbar degenerated intervertebral discs: Analysis of proinflammatory cytokine and TRP channel expression. Eur. Spine J. 2018, 27, 564–577. [Google Scholar] [CrossRef]
- Capoor, M.N.; Birkenmaier, C.; Wang, J.C.; McDowell, A.; Ahmed, F.S.; Bruggemann, H.; Coscia, E.; Davies, D.G.; Ohrt-Nissen, S.; Raz, A.; et al. A review of microscopy-based evidence for the association of Propionibacterium acnes biofilms in degenerative disc disease and other diseased human tissue. Eur. Spine J. 2019, 28, 2951–2971. [Google Scholar] [CrossRef] [PubMed]
- Ohrt-Nissen, S.; Fritz, B.G.; Walbom, J.; Kragh, K.N.; Bjarnsholt, T.; Dahl, B.; Manniche, C. Bacterial biofilms: A possible mechanism for chronic infection in patients with lumbar disc herniation—A prospective proof-of-concept study using fluorescence in situ hybridization. APMIS 2018, 126, 440–447. [Google Scholar] [CrossRef] [PubMed]
- Urquhart, D.M.; Zheng, Y.; Cheng, A.C.; Rosenfeld, J.V.; Chan, P.; Liew, S.; Hussain, S.M.; Cicuttini, F.M. Could low grade bacterial infection contribute to low back pain? A systematic review. BMC Med. 2015, 13, 13. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.; Tang, G.; Jiao, Y.; Yuan, Y.; Zheng, Y.; Chen, Y.; Xiao, J.; Li, C.; Chen, Z.; Cao, P. Propionibacterium acnes Induces Intervertebral Disc Degeneration by Promoting iNOS/NO and COX-2/PGE(2) Activation via the ROS-Dependent NF-kappaB Pathway. Oxid. Med. Cell. Longev. 2018, 2018, 3692752. [Google Scholar] [CrossRef] [PubMed]
- De la Fuente, M. The Role of the Microbiota-Gut-Brain Axis in the Health and Illness Condition: A Focus on Alzheimer’s Disease. J. Alzheimers Dis. 2021, 81, 1345–1360. [Google Scholar] [CrossRef] [PubMed]
- Dekker Nitert, M.; Mousa, A.; Barrett, H.L.; Naderpoor, N.; de Courten, B. Altered Gut Microbiota Composition Is Associated With Back Pain in Overweight and Obese Individuals. Front. Endocrinol. 2020, 11, 605. [Google Scholar] [CrossRef]
- Tamai, H.; Teraguchi, M.; Hashizume, H.; Oka, H.; Cheung, J.P.Y.; Samartzis, D.; Muraki, S.; Akune, T.; Kawaguchi, H.; Nakamura, K.; et al. A Prospective, 3-year Longitudinal Study of Modic Changes of the Lumbar Spine in a Population-based Cohort: The Wakayama Spine Study. Spine 2022, 47, 490–497. [Google Scholar] [CrossRef]
- Teraguchi, M.; Hashizume, H.; Oka, H.; Cheung, J.P.Y.; Samartzis, D.; Tamai, H.; Muraki, S.; Akune, T.; Tanaka, S.; Yoshida, M.; et al. Detailed Subphenotyping of Lumbar Modic Changes and Their Association with Low Back Pain in a Large Population-Based Study: The Wakayama Spine Study. Pain Ther. 2022, 11, 57–71. [Google Scholar] [CrossRef]
- Udby, P.M.; Modic, M.; Elmose, S.; Carreon, L.Y.; Andersen, M.O.; Karppinen, J.; Samartzis, D. The Clinical Significance of the Modic Changes Grading Score. Glob. Spine J. 2022, 21925682221123012. [Google Scholar] [CrossRef]
- Udby, P.M.; Samartzis, D.; Carreon, L.Y.; Andersen, M.O.; Karppinen, J.; Modic, M. A definition and clinical grading of Modic changes. J. Orthop. Res. 2022, 40, 301–307. [Google Scholar] [CrossRef]
- McGrath, S.; Zhao, X.; Steele, R.; Thombs, B.D.; Benedetti, A.; Collaboration, D.E.S.D. Estimating the sample mean and standard deviation from commonly reported quantiles in meta-analysis. Stat. Methods Med. Res. 2020, 29, 2520–2537. [Google Scholar] [CrossRef]
- Riley, R.D.; Higgins, J.P.; Deeks, J.J. Interpretation of random effects meta-analyses. BMJ 2011, 342, d549. [Google Scholar] [CrossRef] [PubMed]
- Higgins, J.P.; Thompson, S.G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 2002, 21, 1539–1558. [Google Scholar] [CrossRef] [PubMed]
- Mok, F.P.; Samartzis, D.; Karppinen, J.; Fong, D.Y.; Luk, K.D.; Cheung, K.M. Modic changes of the lumbar spine: Prevalence, risk factors, and association with disc degeneration and low back pain in a large-scale population-based cohort. Spine J. 2016, 16, 32–41. [Google Scholar] [CrossRef] [PubMed]
- Grant, R.; Lovecchio, F.; Samartzis, D.; Louie, P.K.; Germscheid, N.; An, H.S.; Cheung, J.P.Y.; Chutkan, N.; Mallow, G.M.; Neva, M.H.; et al. Telemedicine in spine surgery: Global perspectives and practices. Glob. Spine J. 2023, 13, 1200–1211. [Google Scholar]
- Storheim, K.; Espeland, A.; Grovle, L.; Skouen, J.S.; Assmus, J.; Anke, A.; Froholdt, A.; Pedersen, L.M.; Haugen, A.J.; Fors, T.; et al. Antibiotic treatment In patients with chronic low back pain and Modic changes (the AIM study): Study protocol for a randomised controlled trial. Trials 2017, 18, 596. [Google Scholar] [CrossRef]
- Saukkonen, J.; Maatta, J.; Oura, P.; Kyllonen, E.; Tervonen, O.; Niinimaki, J.; Auvinen, J.; Karppinen, J. Association Between Modic Changes and Low Back Pain in Middle Age: A Northern Finland Birth Cohort Study. Spine 2020, 45, 1360–1367. [Google Scholar] [CrossRef]
- Määttä, J.H.; Wadge, S.; MacGregor, A.; Karppinen, J.; Williams, F.M. ISSLS Prize Winner: Vertebral Endplate (Modic) Change is an Independent Risk Factor for Episodes of Severe and Disabling Low Back Pain. Spine 2015, 40, 1187–1193. [Google Scholar] [CrossRef]
- Capoor, M.N.; Ruzicka, F.; Schmitz, J.E.; James, G.A.; Machackova, T.; Jancalek, R.; Smrcka, M.; Lipina, R.; Ahmed, F.S.; Alamin, T.F.; et al. Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. PLoS ONE 2017, 12, e0174518. [Google Scholar] [CrossRef]
- Chen, Z.; Zheng, Y.; Yuan, Y.; Jiao, Y.; Xiao, J.; Zhou, Z.; Cao, P. Modic Changes and Disc Degeneration Caused by Inoculation of Propionibacterium acnes inside Intervertebral Discs of Rabbits: A Pilot Study. Biomed. Res. Int. 2016, 2016, 9612437. [Google Scholar] [CrossRef]
- Dudli, S.; Liebenberg, E.; Magnitsky, S.; Miller, S.; Demir-Deviren, S.; Lotz, J.C. Propionibacterium acnes infected intervertebral discs cause vertebral bone marrow lesions consistent with Modic changes. J. Orthop. Res. 2016, 34, 1447–1455. [Google Scholar] [CrossRef]
- Albert, H.B.; Sorensen, J.S.; Christensen, B.S.; Manniche, C. Antibiotic treatment in patients with chronic low back pain and vertebral bone edema (Modic type 1 changes): A double-blind randomized clinical controlled trial of efficacy. Eur. Spine J. 2013, 22, 697–707. [Google Scholar] [CrossRef]
- Farrar, M.D.; Ingham, E. Acne: Inflammation. Clin. Dermatol. 2004, 22, 380–384. [Google Scholar] [CrossRef] [PubMed]
- Albert, H.B.; Manniche, C.; Sorensen, J.S.; Deleuran, B.W. Antibiotic treatment in patients with low-back pain associated with Modic changes Type 1 (bone oedema): A pilot study. Br. J. Sports Med. 2008, 42, 969–973. [Google Scholar] [CrossRef] [PubMed]
- Braten, L.C.H.; Gjefsen, E.; Gervin, K.; Pripp, A.H.; Skouen, J.S.; Schistad, E.; Pedersen, L.M.; Wigemyr, M.; Selmer, K.K.; Aass, H.C.D.; et al. Cytokine Patterns as Predictors of Antibiotic Treatment Effect in Chronic Low Back Pain with Modic Changes: Subgroup Analyses of a Randomized Trial (AIM Study). J. Pain Res. 2023, 16, 1713–1724. [Google Scholar] [CrossRef]
- Braten, L.C.H.; Rolfsen, M.P.; Espeland, A.; Wigemyr, M.; Assmus, J.; Froholdt, A.; Haugen, A.J.; Marchand, G.H.; Kristoffersen, P.M.; Lutro, O.; et al. Efficacy of antibiotic treatment in patients with chronic low back pain and Modic changes (the AIM study): Double blind, randomised, placebo controlled, multicentre trial. BMJ 2019, 367, l5654. [Google Scholar] [CrossRef]
- Cheng, J.C.; Castelein, R.M.; Chu, W.C.; Danielsson, A.J.; Dobbs, M.B.; Grivas, T.B.; Gurnett, C.A.; Luk, K.D.; Moreau, A.; Newton, P.O.; et al. Adolescent idiopathic scoliosis. Nat. Rev. Dis. Primers 2015, 1, 15030. [Google Scholar] [CrossRef] [PubMed]
- Weinstein, S.L.; Dolan, L.A.; Spratt, K.F.; Peterson, K.K.; Spoonamore, M.J.; Ponseti, I.V. Health and function of patients with untreated idiopathic scoliosis: A 50-year natural history study. JAMA 2003, 289, 559–567. [Google Scholar] [CrossRef]
- Lau, K.K.L.; Law, K.K.P.; Kwan, K.Y.H.; Cheung, J.P.Y.; Cheung, K.M.C.; Wong, A.Y.L. Timely Revisit of Proprioceptive Deficits in Adolescent Idiopathic Scoliosis: A Systematic Review and Meta-Analysis. Glob. Spine J. 2022, 12, 1852–1861. [Google Scholar] [CrossRef]
- Wang, W.J.; Yeung, H.Y.; Chu, W.C.; Tang, N.L.; Lee, K.M.; Qiu, Y.; Burwell, R.G.; Cheng, J.C. Top theories for the etiopathogenesis of adolescent idiopathic scoliosis. J. Pediatr. Orthop. 2011, 31 (Suppl. S1), S14–S27. [Google Scholar] [CrossRef]
- Sun, Z.J.; Jia, H.M.; Qiu, G.X.; Zhou, C.; Guo, S.; Zhang, J.G.; Shen, J.X.; Zhao, Y.; Zou, Z.M. Identification of candidate diagnostic biomarkers for adolescent idiopathic scoliosis using UPLC/QTOF-MS analysis: A first report of lipid metabolism profiles. Sci. Rep. 2016, 6, 22274. [Google Scholar] [CrossRef]
- Lombardi, G.; Akoume, M.Y.; Colombini, A.; Moreau, A.; Banfi, G. Biochemistry of adolescent idiopathic scoliosis. Adv. Clin. Chem. 2011, 54, 165–182. [Google Scholar] [CrossRef]
- Wang, Y.J.; Yu, H.G.; Zhou, Z.H.; Guo, Q.; Wang, L.J.; Zhang, H.Q. Leptin Receptor Metabolism Disorder in Primary Chondrocytes from Adolescent Idiopathic Scoliosis Girls. Int. J. Mol. Sci. 2016, 17, 1160. [Google Scholar] [CrossRef]
- Yan, J.; Charles, J.F. Gut Microbiome and Bone: To Build, Destroy, or Both? Curr. Osteoporos. Rep. 2017, 15, 376–384. [Google Scholar] [CrossRef]
- Shen, N.; Chen, N.; Zhou, X.; Zhao, B.; Huang, R.; Liang, J.; Yang, X.; Chen, M.; Song, Y.; Du, Q. Alterations of the gut microbiome and plasma proteome in Chinese patients with adolescent idiopathic scoliosis. Bone 2019, 120, 364–370. [Google Scholar] [CrossRef] [PubMed]
- Goldenberg, D.L. Septic arthritis. Lancet 1998, 351, 197–202. [Google Scholar] [CrossRef] [PubMed]
- Ross, J.J.; Davidson, L. Methicillin-resistant Staphylococcus aureus septic arthritis: An emerging clinical syndrome. Rheumatology 2005, 44, 1197–1198. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Hatcher, J.D. Gonococcal Arthritis; StatPearls: Treasure Island, FL, USA, 2022. [Google Scholar]
- Antimicrobial Resistance, C. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet 2022, 399, 629–655. [Google Scholar] [CrossRef]
- Bonnal, C.; Birgand, G.; Lolom, I.; Diamantis, S.; Dumortier, C.; L’Heriteau, F.; Armand-Lefevre, L.; Lucet, J.C. Staphylococcus aureus healthcare associated bacteraemia: An indicator of catheter related infections. Med. Mal. Infect. 2015, 45, 84–88. [Google Scholar] [CrossRef]
- Ferry, T.; Perpoint, T.; Vandenesch, F.; Etienne, J. Virulence determinants in Staphylococcus aureus and their involvement in clinical syndromes. Curr. Infect. Dis. Rep. 2005, 7, 420–428. [Google Scholar] [CrossRef] [PubMed]
- Peterson, T.C.; Pearson, C.; Zekaj, M.; Hudson, I.; Fakhouri, G.; Vaidya, R. Septic arthritis in intravenous drug abusers: A historical comparison of habits and pathogens. J. Emerg. Med. 2014, 47, 723–728. [Google Scholar] [CrossRef]
- Vardakas, K.Z.; Kontopidis, I.; Gkegkes, I.D.; Rafailidis, P.I.; Falagas, M.E. Incidence, characteristics, and outcomes of patients with bone and joint infections due to community-associated methicillin-resistant Staphylococcus aureus: A systematic review. Eur. J. Clin. Microbiol. Infect. Dis. 2013, 32, 711–721. [Google Scholar] [CrossRef] [PubMed]
- Helito, C.P.; Zanon, B.B.; Miyahara Hde, S.; Pecora, J.R.; Lima, A.L.; Oliveira, P.R.; Vicente, J.R.; Demange, M.K.; Camanho, G.L. Clinical and epidemiological differences between septic arthritis of the knee and hip caused by oxacillin-sensitive and -resistant S. aureus. Clinics 2015, 70, 30–33. [Google Scholar] [CrossRef] [PubMed]
- Mohanty, N.; Misra, S.; Sahoo, S.; Mishra, S.; Vasudevan, V.; Subramanian, K. Rhinomaxillary Mucormycosis Masquerading as Chronic Osteomyelitis: A Series of Four Rare Cases with Review of Literature. J. Indian Acad. Oral Med. Radiol. 2012, 24, 315–323. [Google Scholar] [CrossRef]
- Kremers, H.M.; Nwojo, M.E.; Ransom, J.E.; Wood-Wentz, C.M.; Melton, L.J., 3rd; Huddleston, P.M., 3rd. Trends in the epidemiology of osteomyelitis: A population-based study, 1969 to 2009. J. Bone Jt. Surgery. Am. 2015, 97, 837–845. [Google Scholar] [CrossRef]
- Cunha, B. Osteomyelitis in Elderly Patients. Clin. Infect. Dis. 2002, 35, 287–293. [Google Scholar] [CrossRef]
- Romanò, C.L.; Logoluso, N.; Elia, A.; Romanò, D. Osteomyelitis in elderly patients. BMC Geriatr. 2010, 10, L15. [Google Scholar] [CrossRef]
- Rana, A.; Rabbani, N.U.A.; Wood, S.; McCorkle, C.; Gilkerson, C. A Complicated Case of Vertebral Osteomyelitis by Serratia Marcescens. Cureus 2020, 12, e9002. [Google Scholar] [CrossRef]
- Mauffrey, C.; Bailey, J.R.; Bowles, R.J.; Price, C.; Hasson, D.; Hak, D.J.; Stahel, P.F. Acute management of open fractures: Proposal of a new multidisciplinary algorithm. Orthopedics 2012, 35, 877–881. [Google Scholar] [CrossRef]
- Zeus, M.; Janssen, S.; Laws, H.J.; Fischer, U.; Borkhardt, A.; Oommen, P.T. Results from a pilot study on the oral microbiome in children and adolescents with chronic nonbacterial osteomyelitis. Z. Für Rheumatol. 2023, 82, 123–133. [Google Scholar] [CrossRef]
- Johani, K.; Fritz, B.G.; Bjarnsholt, T.; Lipsky, B.A.; Jensen, S.O.; Yang, M.; Dean, A.; Hu, H.; Vickery, K.; Malone, M. Understanding the microbiome of diabetic foot osteomyelitis: Insights from molecular and microscopic approaches. Clin. Microbiol. Infect. 2019, 25, 332–339. [Google Scholar] [CrossRef] [PubMed]
- Meng, J.; Zhu, Y.; Li, Y.; Sun, T.; Zhang, F.; Qin, S.; Zhao, H. Incidence and risk factors for surgical site infection following elective foot and ankle surgery: A retrospective study. J. Orthop. Surg. Res. 2020, 15, 449. [Google Scholar] [CrossRef] [PubMed]
- Deng, H.; Chan, A.K.; Ammanuel, S.; Chan, A.Y.; Oh, T.; Skrehot, H.C.; Edwards, S.; Kondapavulur, S.; Nichols, A.D.; Liu, C.; et al. Risk factors for deep surgical site infection following thoracolumbar spinal surgery. J. Neurosurg. Spine 2019, 32, 292–301. [Google Scholar] [CrossRef] [PubMed]
- Gernaat-van der Sluis, A.J.; Hoogenboom-Verdegaal, A.M.; Edixhoven, P.J.; Spies-van Rooijen, N.H. Prophylactic mupirocin could reduce orthopedic wound infections. 1,044 patients treated with mupirocin compared with 1,260 historical controls. Acta Orthop. Scand. 1998, 69, 412–414. [Google Scholar] [CrossRef]
- Kalmeijer, M.D.; van Nieuwland-Bollen, E.; Bogaers-Hofman, D.; de Baere, G.A. Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery. Infect. Control Hosp. Epidemiol. 2000, 21, 319–323. [Google Scholar] [CrossRef]
- Nakamura, M.; Shimakawa, T.; Nakano, S.; Chikawa, T.; Yoshioka, S.; Kashima, M.; Toki, S.; Sairyo, K. Screening for nasal carriage of Staphylococcus aureus among patients scheduled to undergo orthopedic surgery: Incidence of surgical site infection by nasal carriage. J. Orthop. Sci. 2017, 22, 778–782. [Google Scholar] [CrossRef]
- Kapsalaki, E.; Gatselis, N.; Stefos, A.; Makaritsis, K.; Vassiou, A.; Fezoulidis, I.; Dalekos, G.N. Spontaneous spondylodiscitis: Presentation, risk factors, diagnosis, management, and outcome. Int. J. Infect. Dis. 2009, 13, 564–569. [Google Scholar] [CrossRef]
- Kim, C.J.; Song, K.H.; Jeon, J.H.; Park, W.B.; Park, S.W.; Kim, H.B.; Oh, M.D.; Choe, K.W.; Kim, N.J. A comparative study of pyogenic and tuberculous spondylodiscitis. Spine 2010, 35, E1096–E1100. [Google Scholar] [CrossRef]
- Tali, E.T. Spinal infections. Eur. J. Radiol. 2004, 50, 120–133. [Google Scholar] [CrossRef]
- Cottle, L.; Riordan, T. Infectious spondylodiscitis. J. Infect. 2008, 56, 401–412. [Google Scholar] [CrossRef]
- Jimenez-Mejias, M.E.; de Dios Colmenero, J.; Sanchez-Lora, F.J.; Palomino-Nicas, J.; Reguera, J.M.; Garcia de la Heras, J.; Garcia-Ordonez, M.A.; Pachon, J. Postoperative spondylodiskitis: Etiology, clinical findings, prognosis, and comparison with nonoperative pyogenic spondylodiskitis. Clin. Infect. Dis. 1999, 29, 339–345. [Google Scholar] [CrossRef] [PubMed]
- Hopkinson, N.; Stevenson, J.; Benjamin, S. A case ascertainment study of septic discitis: Clinical, microbiological and radiological features. QJM 2001, 94, 465–470. [Google Scholar] [CrossRef] [PubMed]
- Boody, B.S.; Jenkins, T.J.; Maslak, J.; Hsu, W.K.; Patel, A.A. Vertebral Osteomyelitis and Spinal Epidural Abscess: An Evidence-based Review. J. Spinal Disord. Tech. 2015, 28, E316–E327. [Google Scholar] [CrossRef]
- Gouliouris, T.; Aliyu, S.H.; Brown, N.M. Spondylodiscitis: Update on diagnosis and management. J. Antimicrob. Chemother. 2010, 65 (Suppl. S3), iii11–iii24. [Google Scholar] [CrossRef] [PubMed]
- Al-Nammari, S.S.; Lucas, J.D.; Lam, K.S. Hematogenous methicillin-resistant Staphylococcus aureus spondylodiscitis. Spine 2007, 32, 2480–2486. [Google Scholar] [CrossRef]
- Hadjipavlou, A.G.; Mader, J.T.; Necessary, J.T.; Muffoletto, A.J. Hematogenous pyogenic spinal infections and their surgical management. Spine 2000, 25, 1668–1679. [Google Scholar] [CrossRef]
- Di Martino, A.; Papapietro, N.; Lanotte, A.; Russo, F.; Vadala, G.; Denaro, V. Spondylodiscitis: Standards of current treatment. Curr. Med. Res. Opin. 2012, 28, 689–699. [Google Scholar] [CrossRef]
- D’Agostino, C.; Scorzolini, L.; Massetti, A.P.; Carnevalini, M.; d’Ettorre, G.; Venditti, M.; Vullo, V.; Orsi, G.B. A seven-year prospective study on spondylodiscitis: Epidemiological and microbiological features. Infection 2010, 38, 102–107. [Google Scholar] [CrossRef]
- Zhou, C.; Zhao, H.; Xiao, X.-Y.; Chen, B.-D.; Guo, R.-J.; Wang, Q.; Chen, H.; Zhao, L.-D.; Zhang, C.-C.; Jiao, Y.-H.; et al. Metagenomic profiling of the pro-inflammatory gut microbiota in ankylosing spondylitis. J. Autoimmun. 2020, 107, 102360. [Google Scholar] [CrossRef]
- Zhang, L.; Hu, Y.; Xu, Y.; Li, P.; Ma, H.; Li, X.; Li, M. The correlation between intestinal dysbiosis and the development of ankylosing spondylitis. Microb. Pathog. 2019, 132, 188–192. [Google Scholar] [CrossRef]
- Turner, M.J.; Sowders, D.P.; DeLay, M.L.; Mohapatra, R.; Bai, S.; Smith, J.A.; Brandewie, J.R.; Taurog, J.D.; Colbert, R.A. HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response. J. Immunol. 2005, 175, 2438–2448. [Google Scholar] [CrossRef] [PubMed]
- Ciccia, F.; Accardo-Palumbo, A.; Rizzo, A.; Guggino, G.; Raimondo, S.; Giardina, A.; Cannizzaro, A.; Colbert, R.A.; Alessandro, R.; Triolo, G. Evidence that autophagy, but not the unfolded protein response, regulates the expression of IL-23 in the gut of patients with ankylosing spondylitis and subclinical gut inflammation. Ann. Rheum. Dis. 2014, 73, 1566–1574. [Google Scholar] [CrossRef] [PubMed]
- Ciccia, F.; Rizzo, A.; Triolo, G. Subclinical gut inflammation in ankylosing spondylitis. Curr. Opin. Rheumatol. 2016, 28, 89–96. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Zheng, X.; Wu, X.; Wu, J.; Li, X.; Wei, Q.; Zhang, X.; Fang, L.; Jin, O.; Gu, J. Adalimumab Therapy Restores the Gut Microbiota in Patients With Ankylosing Spondylitis. Front. Immunol. 2021, 12, 700570. [Google Scholar] [CrossRef] [PubMed]
- Minerbi, A.; Gonzalez, E.; Brereton, N.J.B.; Anjarkouchian, A.; Dewar, K.; Fitzcharles, M.-A.; Chevalier, S.; Shir, Y. Altered microbiome composition in individuals with fibromyalgia. Pain 2019, 160, 2589–2602. [Google Scholar] [CrossRef] [PubMed]
- Cassisi, G.; Sarzi-Puttini, P.; Cazzola, M. Chronic widespread pain and fibromyalgia: Could there be some relationships with infections and vaccinations? Clin. Exp. Rheumatol. 2011, 29 (Suppl. S69), S118–S126. [Google Scholar]
- Giacomelli, C.; Sernissi, F.; Rossi, A.; Bombardieri, S.; Bazzichi, L. Biomarkers in fibromyalgia: A review. Curr. Biomark. Find. 2014, 4, 35. [Google Scholar] [CrossRef]
- Albrecht, D.S.; Forsberg, A.; Sandström, A.; Bergan, C.; Kadetoff, D.; Protsenko, E.; Lampa, J.; Lee, Y.C.; Höglund, C.O.; Catana, C.; et al. Brain glial activation in fibromyalgia—A multi-site positron emission tomography investigation. Brain Behav. Immun. 2019, 75, 72–83. [Google Scholar] [CrossRef]
- Kendler, K.S.; Rosmalen, J.G.M.; Ohlsson, H.; Sundquist, J.; Sundquist, K. A distinctive profile of family genetic risk scores in a Swedish national sample of cases of fibromyalgia, irritable bowel syndrome, and chronic fatigue syndrome compared to rheumatoid arthritis and major depression. Psychol. Med. 2022, 53, 3879–3886. [Google Scholar] [CrossRef]
- Clos-Garcia, M.; Andres-Marin, N.; Fernandez-Eulate, G.; Abecia, L.; Lavin, J.L.; van Liempd, S.; Cabrera, D.; Royo, F.; Valero, A.; Errazquin, N.; et al. Gut microbiome and serum metabolome analyses identify molecular biomarkers and altered glutamate metabolism in fibromyalgia. EBioMedicine 2019, 46, 499–511. [Google Scholar] [CrossRef]
- Wang, Y.; Wei, J.; Zhang, W.; Doherty, M.; Zhang, Y.; Xie, H.; Li, W.; Wang, N.; Lei, G.; Zeng, C. Gut dysbiosis in rheumatic diseases: A systematic review and meta-analysis of 92 observational studies. EBioMedicine 2022, 80, 104055. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Z.; Hui, E.S.; Kranz, G.S.; Chang, J.R.; de Luca, K.; Pinto, S.M.; Chan, W.W.; Yau, S.Y.; Chau, B.K.; Samartzis, D.; et al. Potential mechanisms underlying the accelerated cognitive decline in people with chronic low back pain: A scoping review. Ageing Res. Rev. 2022, 82, 101767. [Google Scholar] [CrossRef] [PubMed]
- Stecher, B.; Maier, L.; Hardt, W.-D. ‘Blooming’ in the gut: How dysbiosis might contribute to pathogen evolution. Nat. Rev. Microbiol. 2013, 11, 277–284. [Google Scholar] [CrossRef]
- Clayton, T.A.; Baker, D.; Lindon, J.C.; Everett, J.R.; Nicholson, J.K. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc. Natl. Acad. Sci. USA 2009, 106, 14728–14733. [Google Scholar] [CrossRef] [PubMed]
- Zhang, G.; Qin, L.; Shi, Y. Epimedium-derived phytoestrogen flavonoids exert beneficial effect on preventing bone loss in late postmenopausal women: A 24-month randomized, double-blind and placebo-controlled trial. J. Bone Miner. Res. 2007, 22, 1072–1079. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Ma, Y.H.; Zhou, Z.; Chen, Y.; Wang, Y.; Gao, X. Intestinal Absorption and Metabolism of Epimedium Flavonoids in Osteoporosis Rats. Drug Metab. Dispos. 2015, 43, 1590–1600. [Google Scholar] [CrossRef] [PubMed]
- Zhu, H.M.; Qin, L.; Garnero, P.; Genant, H.K.; Zhang, G.; Dai, K.; Yao, X.; Gu, G.; Hao, Y.; Li, Z.; et al. The first multicenter and randomized clinical trial of herbal Fufang for treatment of postmenopausal osteoporosis. Osteoporos. Int. 2012, 23, 1317–1327. [Google Scholar] [CrossRef]
- Höllriegl, V.; Röhmuss, M.; Oeh, U.; Roth, P. Strontium biokinetics in humans: Influence of alginate on the uptake of ingested strontium. Health Phys. 2004, 86, 193–196. [Google Scholar] [CrossRef]
- Kalyan, S.; Wang, J.; Quabius, E.S.; Huck, J.; Wiltfang, J.; Baines, J.F.; Kabelitz, D. Systemic immunity shapes the oral microbiome and susceptibility to bisphosphonate-associated osteonecrosis of the jaw. J. Transl. Med. 2015, 13, 212. [Google Scholar] [CrossRef]
Author | Population Size | Population Characteristics | Males:Females | Microbe | Musculoskeletal Disorder | Findings |
---|---|---|---|---|---|---|
Cardoneanu et al. (2021) [24] | 60 | 32 healthy controls, 28 ankylosing spondylitis | 29:31 | Several microbes | Ankylosing Spondylitis | Decreased intestinal bacterial diversity ankylosing spondylitis patients compared to control |
Das et al. (2019) [17] | 181 | Older adults | 13:17 | Several microbes | Osteoporosis | Different gut microbiota profiles were found to be associated with osteopenic, osteoporotic, and normal bone mass density |
Fritzell et al. (2019) [25] | 60 | 40 adults with lumbar disc herniation/lower back pain, 20 control patients with scoliosis | 30:30 | Cutibacterium acnes | Degenerative disc | C. acnes found in discs and vertebrae during surgery for disc herniation |
Nilsson et al. (2018) [18] | 90 | Elderly women between the ages of 75 and 80 who have diminished bone mineral density | 0:90 | Lactobacillus reuteri | Osteoporosis | L. reuteri reduces total bone mass density compared to the placebo |
Rajasekaran et al. (2017) [26] | 22 | 15-disc herniations, 5- degenerate, 2-normal in MRI | 15:7 | Propionibacterium acnes | Proteome in intervertebral discs | Specific bacterial and host defense proteins were present in intervertebral discs |
Rajasekaran et al. (2019) [27] | 6 control discs, 5 degenerated discs | Group A (young 2nd–4th decades), Group B (aging. 5th–7th decade), Group C (degenerative discs) | 4:7 | --- | Degenerative Disc | Unique proteome signatures of bacteria in discs of young, aging, and degenerative discs |
Rajasekaran et al. (2020) [28] | 24 | 8- brain-dead but living organ donors had healthy MRI discs, 8 had herniated discs, 8-disc degeneration | 15:9 | Several microbes | Degenerative disc | Distinct microbiome profiles in patients with healthy disc, disc herniations, and degenerative disc |
Rao et al. (2020) [29] | 812 | NA | NA | Cutibacterium acnes | Degenerative disc | The research did not reveal any distinction in actual infection rates between the groups with non-degenerative and degenerative discs |
Rettedal et al. (2020) [30] | 86 | All postmenopausal women: 18 osteoporosis, 42 osteopenia, 26 healthy controls | 0:86 | Bacteroides | Osteoporosis | Bacteroides taxa were more abundant in both osteopenia and osteoporosis |
Scher et al. (2013) [31] | 114 | Rheumatoid Arthritis | 11:33 | Prevotella copri | Rheumatoid Arthritis | P. copri in stool is correlated with new onset untreated. rheumatoid arthritis |
Scher et al. (2016) [15] | 58 | Rheumatoid Arthritis, Sarcoidosis, Control | 43:25 | Pseudonocardia | Rheumatoid Arthritis, Sarcoidosis | The composition of gut microbiota in individuals with rheumatoid arthritis and sarcoidosis was significantly decreased and is less varied in comparison to individuals without health issues |
Wang et al. (2017) [19] | 18 | 6 adults with primary osteoporosis, 6 with primary osteopenia, and 6 normal controls | 3:15 | Firmicutes and Bacteroidetes | Osteoporosis | Osteoporosis individuals contained an increased proportion of Firmicutes phyla but decreased proportion of Bacteroidetes compared to the control |
Xu et al. (2020) [20] | 96 | 48 primary osteoporosis patients and 48 healthy | 37:59 | Faecalibacterium and dialister | Osteoporosis | Increase in abundance of Faecalibacterium and dialister in patients with primary Osteoporosis |
Author | Sample Size | Intervention | MSK Disorder | Result |
---|---|---|---|---|
Guss et al. (2019) [32] | 6–7 mice per group, 2 groups | Oral antibiotics vs. untreated | Osteoporosis | The decrease in microbiota synthesized vitamin K from the antibiotics led to a decrease in bone matrix quality |
Guss et al. (2019) [32] | 10–11 mice group 2 groups | Toll-le mceptor-5 deficient mice | Osteoarthritis | Gut microbiome may influence cartilage pathology |
Hemandez et al. (2019) [33] | 82 (40 modified microbiome, 42 untreated) | A tibial implant made of titanium, along with the introduction of Staphylococcus aureus in the synovial space. | Periprosthetic joint infection | Gut microbiota may influence susceptibility to periprosthetic joint infection The composition of gut microbiota could impact one’s vulnerability to periprosthetic joint infection |
Li et al. (2016) [34] | 10 mice per group 2 groups | Control vs. Probiotics | Osteoporosis | The microbiota within the gut lumen and heightened gut permeability contribute to the initiation of inflammatory pathways that are essential in causing bone loss in mice lacking sex steroids |
Sjogren et al. (2012) [35] | 485 mice | Germ free mice vs conventionally raised mice | Osteoporosis | In mice, the gut microbiota manages bone density by decreasing the production of inflammatory cytokines in both bone and bone marrow. |
Wang et al. (2021) [36] | 12 mice per group, 4 groups | Control, Control + L. paracasei S16 probiotic, Lumbar Doc Herniation (LDH), LDH+ L. paracasei S16 probiotics | Lumbar Disc Herniation (Low Back Pain) | L. paracasei S16 has the potential to alleviate LDH symptoms through the reduction of inflammation, modifications in gut microbiota, and alterations in serum metabolite |
Yan et al. (2016) [37] | 6 mice | Control vs. Antibiotics | Osteoporosis | The gut microbiota negatively impacts bone health, likely through IGF-1 mediation, causing a net anabolic deficit |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Aboushaala, K.; Wong, A.Y.L.; Barajas, J.N.; Lim, P.; Al-Harthi, L.; Chee, A.; Forsyth, C.B.; Oh, C.-d.; Toro, S.J.; Williams, F.M.K.; et al. The Human Microbiome and Its Role in Musculoskeletal Disorders. Genes 2023, 14, 1937. https://doi.org/10.3390/genes14101937
Aboushaala K, Wong AYL, Barajas JN, Lim P, Al-Harthi L, Chee A, Forsyth CB, Oh C-d, Toro SJ, Williams FMK, et al. The Human Microbiome and Its Role in Musculoskeletal Disorders. Genes. 2023; 14(10):1937. https://doi.org/10.3390/genes14101937
Chicago/Turabian StyleAboushaala, Khaled, Arnold Y. L. Wong, Juan Nicolas Barajas, Perry Lim, Lena Al-Harthi, Ana Chee, Christopher B. Forsyth, Chun-do Oh, Sheila J. Toro, Frances M. K. Williams, and et al. 2023. "The Human Microbiome and Its Role in Musculoskeletal Disorders" Genes 14, no. 10: 1937. https://doi.org/10.3390/genes14101937
APA StyleAboushaala, K., Wong, A. Y. L., Barajas, J. N., Lim, P., Al-Harthi, L., Chee, A., Forsyth, C. B., Oh, C. -d., Toro, S. J., Williams, F. M. K., An, H. S., & Samartzis, D. (2023). The Human Microbiome and Its Role in Musculoskeletal Disorders. Genes, 14(10), 1937. https://doi.org/10.3390/genes14101937