Gut permeability and osteoarthritis, towards a mechanistic understanding of the pathogenesis: a systematic review

References

• Glyn-Jones S, et al. Osteoarthritis. Lancet. 2015;386(9991):376-387.
   Google Scholar
• Martel-Pelletier J, Barr AJ, Cicuttini FM, et al. Osteoarthritis. Nat Rev Dis Primers. 2016;2:16072.
   PubMed Web of Science ®Google Scholar
• Guilak F. Biomechanical factors in osteoarthritis. Best Practice and Research: Clinical Rheumatology. 2011;25(6):815–823.
   PubMed Web of Science ®Google Scholar
• Panoutsopoulou K, Zeggini E. Advances in osteoarthritis genetics. J Med Genet. 2013;50(11):715–724.
   PubMed Web of Science ®Google Scholar
• Boer CG, Radjabzadeh D, Medina-Gomez C, et al. Intestinal microbiome composition and its relation to joint pain and inflammation. Nat Commun. 2019;10:4881.
   Google Scholar
• Rinninella E, Raoul P, Cintoni M, et al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 2019;7(1):14.
   PubMed Web of Science ®Google Scholar
• Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180.
   PubMed Web of Science ®Google Scholar
• Frank DN, St. Amand AL, Feldman RA, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007;104(34):13780–13785.
   PubMed Web of Science ®Google Scholar
• Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125(3):926–938.
   PubMed Web of Science ®Google Scholar
• Manfredo Vieira S, Hiltensperger M, Kumar V, et al. Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science. 2018;359(6380):1156–1161.
   PubMed Web of Science ®Google Scholar
• Carnevale R, Sciarretta S, Valenti V, et al. Low-grade endotoxaemia enhances artery thrombus growth via toll-like receptor 4: implication for myocardial infarction. Eur Heart J. 2020;41(33):3156–3165.
   PubMed Web of Science ®Google Scholar
• Ruff WE, Greiling TM, Kriegel MA. Host–microbiota interactions in immune-mediated diseases. Nat Rev Microbiol. 2020;18(9):521–538.
   PubMed Web of Science ®Google Scholar
• Manfredo Vieira S, Hiltensperger M, Kumar V, et al. Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science. 2018;359(6380):1156–1161.
   PubMed Web of Science ®Google Scholar
• Pesesse L, Sanchez C, Henrotin Y. Osteochondral plate angiogenesis: a new treatment target in osteoarthritis. Joint Bone Spine. 2011;78(2):144–149.
   PubMed Web of Science ®Google Scholar
• Hongyi Zhu TY, Jin H, Zhang C. Intestinal methicillin-resistant Staphylococcus aureus causes periprosthetic infection via trojan horse mechanism: Evidence from a rat model. Bone and Joint Res. 2020;9(4):152–161.
   PubMed Web of Science ®Google Scholar
• Krezalek MA, Hyoju S, Zaborin A, et al. Can methicillin-resistant Staphylococcus aureus silently travel from the gut to the wound and cause postoperative infection? Modeling the “Trojan Horse Hypothesis”. Ann Surg. 2018;267(4):749–758.
   PubMed Web of Science ®Google Scholar
• Richards RL, et al. Persistent Staphylococcus aureus isolates from two independent cases of bacteremia display increased bacterial fitness and novel immune evasion phenotypes. Infect Immun. 2015;83(8):3311–3324.
   Google Scholar
• Collins KH, Paul HA, Reimer RA, et al. Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model. Osteoarthr Cartil. 2015;23(11):1989–1998.
   PubMed Web of Science ®Google Scholar
• Cuevas-Sierra A, Ramos-Lopez O, Riezu-Boj JI, et al. Diet, gut microbiota, and obesity: links with host genetics and epigenetics and potential applications. 2019;10(suppl_1):S17-S30.
   Google Scholar
• Dunn CM, Velasco C, Rivas A, et al. Identification of cartilage microbial DNA signatures and associations with knee and hip osteoarthritis. Arthritis Rheumatol. 2020;72(7):1111–1122.
   PubMed Web of Science ®Google Scholar
• Huang ZY, Stabler T, Pei FX, et al. Both systemic and local lipopolysaccharide (LPS) burden are associated with knee OA severity and inflammation. Osteoarthr Cartil. 2016;24(10):1769–1775.
   PubMed Web of Science ®Google Scholar
• Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
   PubMed Web of Science ®Google Scholar
• Richardson WS, Wilson MC, Nishikawa J, et al. The well-built clinical question: a key to evidence-based decisions. ACP Journal Club. 1995;;123(3):A12-A13.
   Google Scholar
• Sterne JA, Hernán MA, Reeves BC, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919.
   PubMed Web of Science ®Google Scholar
• Hooijmans CR, Rovers MM, de Vries RB, et al. SYRCLE's risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14(1):43.
   PubMed Web of Science ®Google Scholar
• Guyatt GH, Oxman AD, Schünemann HJ, et al. GRADE guidelines: a new series of articles in the journal of clinical Epidemiology. J Clin Epidemiol. 2011;64(4):380–382.
   PubMed Web of Science ®Google Scholar
• Landis SC, Amara SG, Asadullah K, et al. A call for transparent reporting to optimize the predictive value of preclinical research. Nature. 2012;490(7419):187–191.
   PubMed Web of Science ®Google Scholar
• Macleod MR, O'Collins T, Howells DW, et al. Pooling of animal experimental data reveals influence of study design and publication bias. Stroke. 2004;35(5):1203–1208.
   PubMed Web of Science ®Google Scholar
• Huang ZYu, Chen J, Li BLei, et al. Faecal microbiota transplantation from metabolically compromised human donors accelerates osteoarthritis in mice. Ann Rheum Dis. 2020;79(5):646–656.
   PubMed Web of Science ®Google Scholar
• Tan C, Zhang J, Chen W, et al. Inflammatory cytokines via up-regulation of aquaporins deteriorated the pathogenesis of early osteoarthritis. PLOS One. 2019;14(8):e0220846.
   PubMed Web of Science ®Google Scholar
• Lee MC, et al. CCL17 blockade as a therapy for osteoarthritis pain and disease. Arthritis Res Ther. 2018;20(1):62.
   Web of Science ®Google Scholar
• Raghu H, Lepus CM, Wang Q, et al. CCL2/CCR2, but not CCL5/CCR5, mediates monocyte recruitment, inflammation and cartilage destruction in osteoarthritis. Ann Rheum Dis. 2017;76(5):914–922.
   PubMed Web of Science ®Google Scholar
• Miotla Zarebska J, Chanalaris A, Driscoll C, et al. CCL2 and CCR2 regulate pain-related behaviour and early gene expression in post-traumatic murine osteoarthritis but contribute little to chondropathy. Osteoarthr Cartil . 2017;25(3):406–412.
   PubMed Web of Science ®Google Scholar
• Rios JL, Bomhof MR, Reimer RA, et al. Protective effect of prebiotic and exercise intervention on knee health in a rat model of diet-induced obesity. Sci Rep. 2019;9(1):3893.
   Web of Science ®Google Scholar
• Schott EM, Farnsworth CW, Grier A, et al. Targeting the gut microbiome to treat the osteoarthritis of obesity. JCI Insight. 2018;;3(8):e95997.
   PubMed Web of Science ®Google Scholar
• Panicker S, Borgia J, Fhied C, et al. Oral glucosamine modulates the response of the liver and lymphocytes of the mesenteric lymph nodes in a papain-induced model of joint damage and repair. Osteoarthr Cartil. 2009;17(8):1014–1021.
   PubMed Web of Science ®Google Scholar
• So J-S, Song M-K, Kwon H-K, et al. Lactobacillus casei enhances type II collagen/glucosamine-mediated suppression of inflammatory responses in experimental osteoarthritis. Life Sci. 2011;88(7–8):358–366.
   PubMed Web of Science ®Google Scholar
• Ulici V, Kelley KL, Azcarate-Peril MA, et al. Osteoarthritis induced by destabilization of the medial meniscus is reduced in germ-free mice. Osteoarthr Cartil. 2018;26(8):1098–1109.
   PubMed Web of Science ®Google Scholar
• Joosten LAB, van de Loo FAJ, Lubberts E, et al. An IFN-γ-Independent proinflammatory role of IL-18 in murine streptococcal cell wall arthritis. J Immunol. 2000;165(11):6553–6558.
   PubMed Web of Science ®Google Scholar
• Joosten LAB, Helsen MMA, Van Den Berg WB. Blockade of endogenous interleukin 12 results in suppression of murine streptococcal cell wall arthritis by enhancement of interleukin 10 and interleukin 1 Ra. Ann Rheum Dis. 2000;59(3):196–205.
   PubMed Web of Science ®Google Scholar
• Zhao X, Gu M, Xu X, et al. CCL3/CCR1 mediates CD14 + CD16− circulating monocyte recruitment in knee osteoarthritis progression. Osteoarthr Cartil. 2020;28(5):613–625.
   PubMed Web of Science ®Google Scholar
• Yang P, Tan J, Yuan Z, et al. Expression profile of cytokines and chemokines in osteoarthritis patients: proinflammatory roles for CXCL8 and CXCL11 to chondrocytes. Int Immunopharmacol. 2016;40:16–23.
   PubMed Web of Science ®Google Scholar
• Ren G, Whittaker JL, Leonard C, et al. CCL22 is a biomarker of cartilage injury and plays a functional role in chondrocyte apoptosis. Cytokine. 2019;115:32–44.
   PubMed Web of Science ®Google Scholar
• Griffin TM, Huebner JL, Kraus VB, et al. Induction of osteoarthritis and metabolic inflammation by a very high-fat diet in mice: effects of short-term exercise. Arthritis Rheum. 2012;64(2):443–453.
   PubMed Web of Science ®Google Scholar
• Xu Z, Li J, Yang H, et al. Association of CCL2 gene variants with osteoarthritis. Arch Med Res. 2019;50(3):86–90.
   PubMed Web of Science ®Google Scholar
• Metcalfe D, Harte AL, Aletrari MO, et al. Does endotoxaemia contribute to osteoarthritis in obese patients? Clin Sci. 2012;123(11):627–634.
   Web of Science ®Google Scholar
• Kolasinski SL, et al. 2019 American college of rheumatology/arthritis foundation guideline for the management of osteoarthritis of the hand, hip, and knee. Arthritis Rheum. 2020;72(2):220–233.
   Web of Science ®Google Scholar
• Messier SP, et al. Intentional weight loss in overweight and obese patients with knee osteoarthritis: is more better? Arthritis Care Res. 2018.;70(11):1569-1575.
   Web of Science ®Google Scholar
• Goh S-L, Persson MSM, Stocks J, et al. Relative efficacy of different exercises for pain, function, performance and quality of life in knee and hip osteoarthritis: systematic review and network meta-analysis. Sports Med. 2019;49(5):743–761.
   PubMed Web of Science ®Google Scholar
• Coulson S, Butt H, Vecchio P, et al. Green-lipped mussel extract (perna canaliculus) and glucosamine sulphate in patients with knee osteoarthritis: therapeutic efficacy and effects on gastrointestinal microbiota profiles. Inflammopharmacol. 2013;21(1):79–90.
   PubMed Web of Science ®Google Scholar
• Ruff WE, Kriegel MA. Autoimmune host-microbiota interactions at barrier sites and beyond. Trends Mol Med. 2015;21(4):233–244.
   PubMed Web of Science ®Google Scholar
• Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science. 2010;330(6012):1768–1773.
   PubMed Web of Science ®Google Scholar
• Chakaroun RM, Massier L, Kovacs P. Gut microbiome, intestinal permeability, and tissue bacteria in metabolic disease: perpetrators or bystanders? Nutrients. 2020;12(4):1082.
   PubMed Web of Science ®Google Scholar
• Lamprecht M, Bogner S, Schippinger G, et al. Probiotic supplementation affects markers of intestinal barrier, oxidation, and inflammation in trained men; a randomized, double-blinded, placebo-controlled trial. J Int Soc Sports Nutr. 2012; ;9(1):45.
   PubMed Web of Science ®Google Scholar
• Aleksandrova K, Romero-Mosquera B, Hernandez V. Diet, gut microbiome and epigenetics: emerging links with inflammatory bowel diseases and prospects for management and prevention. Nutrients. 2017;9(9):962.
   PubMed Web of Science ®Google Scholar
• Saltiel AR, Olefsky JM. Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest. 2017;127(1):1–4.
   PubMed Web of Science ®Google Scholar
• Rohr MW, Narasimhulu CA, Rudeski-Rohr TA, et al. Negative effects of a high-fat diet on intestinal permeability: a review. Adv Nutrition. 2019;11(1):77–91.
   Web of Science ®Google Scholar
• Johnson AMF, Costanzo A, Gareau MG, et al. High fat diet causes depletion of intestinal eosinophils associated with intestinal permeability. PLOS One. 2015;10(4):e0122195.
   PubMed Web of Science ®Google Scholar
• Araújo JR, Tomas J, Brenner C, et al. Impact of high-fat diet on the intestinal microbiota and small intestinal physiology before and after the onset of obesity. Biochimie. 2017;141:97–106.
   PubMed Web of Science ®Google Scholar
• Araújo JR, Tomas J, Brenner C, et al. Impact of high-fat diet on the intestinal microbiota and small intestinal physiology before and after the onset of obesity. Biochimie. 2017;141:97–106.
   PubMed Web of Science ®Google Scholar
• Chelakkot C, Ghim J, Ryu SH. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med. 2018;50(8):1–9.
   PubMed Web of Science ®Google Scholar
• Groschwitz KR, Hogan SP. Intestinal barrier function: molecular regulation and disease pathogenesis. J Allergy Clin Immunol. 2009;124(1):3–20.
   PubMed Web of Science ®Google Scholar
• Awad WA, Hess C, Hess M. Enteric pathogens and their toxin-induced disruption of the intestinal barrier through alteration of tight junctions in chickens. Toxins. 2017;9(2):60.
   PubMed Web of Science ®Google Scholar
• Fasano A. All disease begins in the (leaky) gut: role of zonulin-mediated gut permeability in the pathogenesis of some chronic inflammatory diseases. F1000Res. 2020;9:69.
   Google Scholar
• Sturgeon C, Fasano A. Zonulin, a regulator of epithelial and endothelial barrier functions, and its involvement in chronic inflammatory diseases. Tissue Barriers. 2016;4(4):e1251384.
   PubMed Web of Science ®Google Scholar
• Stevens BR, Goel R, Seungbum K, et al. Increased human intestinal barrier permeability plasma biomarkers zonulin and FABP2 correlated with plasma LPS and altered gut microbiome in anxiety or depression. Gut. 2018;67(8):1555.2–1557.
   Web of Science ®Google Scholar
• Pedersen SJ, Maksymowych WP. The pathogenesis of ankylosing spondylitis: an update. Curr Rheumatol Rep. 2019 ;21(10):58.
   PubMed Web of Science ®Google Scholar
• Camara-Lemarroy CR, Silva C, Greenfield J, et al. Biomarkers of intestinal barrier function in multiple sclerosis are associated with disease activity. Mult Scler. 2020;26(11):1340–1350.
   PubMed Web of Science ®Google Scholar
• Fasano A. All disease begins in the (leaky) gut: role of zonulin-mediated gut permeability in the pathogenesis of some chronic inflammatory diseases. F1000Res. 2020;9:69.
   Google Scholar
• Honda K, Littman DR. The microbiome in infectious disease and inflammation. Annu Rev Immunol. 2012;30(1):759–795.
   PubMed Web of Science ®Google Scholar
• Tajik N, Frech M, Schulz O, et al. Targeting zonulin and intestinal epithelial barrier function to prevent onset of arthritis. Nat Commun. 2020;;11(1):1995.
   Web of Science ®Google Scholar
• Fachi JL, Felipe J. D S, Pral LP, et al. Butyrate protects mice from clostridium difficile-induced colitis through an HIF-1-Dependent mechanism. Cell Rep. 2019;27(3):750–761.e7.
   PubMed Web of Science ®Google Scholar
• Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol. 2011;11(11):750–761.
   PubMed Web of Science ®Google Scholar
• Daghestani HN, Pieper CF, Kraus VB. Soluble macrophage biomarkers indicate inflammatory phenotypes in patients with knee osteoarthritis. Arthritis and Rheumatology. 2015;67(4):956–65.
   PubMed Web of Science ®Google Scholar
• Miller RJ, Malfait AM, Miller RE. The innate immune response as a mediator of osteoarthritis pain. Osteoarthritis Cartilage. 2020;28(5):562–571.
   PubMed Web of Science ®Google Scholar
• Culemann S, Grüneboom A, Nicolás-Ávila JÁ, et al. Locally renewing resident synovial macrophages provide a protective barrier for the joint. Nature. 2019;572(7771):670–675.
   PubMed Web of Science ®Google Scholar
• Zhang H, Cai D, Bai X. Macrophages regulate the progression of osteoarthritis. Osteoarthr Cartil. 2020;28(5):555–561.
   PubMed Web of Science ®Google Scholar
• Tan C, Zhang J, Chen W, et al. Inflammatory cytokines via up-regulation of aquaporins deteriorated the pathogenesis of early osteoarthritis. PLOS One. 2019;14(8):e0220846.
   PubMed Web of Science ®Google Scholar
• Vujkovic-Cvijin I, Sklar J, Jiang L, et al. Host variables confound gut microbiota studies of human disease. Nature. 2020;587(7834):448–454.
   PubMed Web of Science ®Google Scholar
• Pasolli E, Asnicar F, Manara S, et al. Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle. Cell. 2019;176(3):649–662.e20.
   PubMed Web of Science ®Google Scholar
• Chakaroun RM, Massier L, Kovacs P. Gut microbiome, intestinal permeability, and tissue bacteria in metabolic disease: perpetrators or bystanders? Nutrients. 2020;12(4):1082.
   PubMed Web of Science ®Google Scholar
• Alverdy JC, Hyman N, Gilbert J. Re-examining causes of surgical site infections following elective surgery in the era of asepsis. Lancet Infect Dis. 2020;20(3):e38–e43.
   PubMed Web of Science ®Google Scholar
• Thwaites GE, Gant V. Are bloodstream leukocytes trojan horses for the metastasis of Staphylococcus aureus? Nat Rev Microbiol. 2011;9(3):215–222.
   PubMed Web of Science ®Google Scholar
• Miller RJ, Malfait AM, Miller RE. The innate immune response as a mediator of osteoarthritis pain. Osteoarthr Cartil. 2020;28(5):562–571.
   PubMed Web of Science ®Google Scholar
• Muraille E, Leo O, Moser M. Th1/Th2 paradigm extended: macrophage polarization as an unappreciated pathogen-driven escape mechanism? Front Immunol. 2014;;5:603.
   Web of Science ®Google Scholar
• Thwaites GE, Gant V. Are bloodstream leukocytes trojan horses for the metastasis of Staphylococcus aureus? Nat Rev Microbiol. 2011;9(3):215–222.
   PubMed Web of Science ®Google Scholar
• Alverdy JC, Hyman N, Gilbert J. Re-examining causes of surgical site infections following elective surgery in the era of asepsis. Lancet Infect Dis. 2020;20(3):e38–e43.
   PubMed Web of Science ®Google Scholar
• Païssé S, Valle C, Servant F, et al. Comprehensive description of blood microbiome from healthy donors assessed by 16S targeted metagenomic sequencing. Transfusion. 2016;56(5):1138–1147.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Chen B, Li S, et al. Detection and characterization of bacterial nucleic acids in culture-negative synovial tissue and fluid samples from rheumatoid arthritis or osteoarthritis patients. Sci Rep.2018;8(1):14305.
   Google Scholar
• Walsh DA, Bonnet CS, Turner EL, et al. Angiogenesis in the synovium and at the osteochondral junction in osteoarthritis. Osteoarthr Cartil. 2007;15(7):743–751.
   PubMed Web of Science ®Google Scholar
• Moravcová S, Pačesová D, Melkes B, et al. The day/night difference in the circadian clock’s response to acute lipopolysaccharide and the rhythmic Stat3 expression in the rat suprachiasmatic nucleus. PLoS One. 2018;13(9):e0199405.
   PubMed Web of Science ®Google Scholar
• Vatanen T, Kostic AD, d’Hennezel E, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016;165(6):1551.
   PubMed Web of Science ®Google Scholar
• Wu H-J, Ivanov II, Darce J, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010;32(6):815–827.
   PubMed Web of Science ®Google Scholar
• Kolasinski SL, et al. 2019 American college of rheumatology/arthritis foundation guideline for the management of osteoarthritis of the hand, hip, and knee. Arthritis Rheumatol. 2020;72(2):220–233.
   PubMed Web of Science ®Google Scholar