Independent and combined effects of obesity and traumatic joint injury to the structure and composition of rat knee cartilage

References

• Bijlsma JWJ, Berenbaum F, Lafeber FPJG. Osteoarthritis: an update with relevance for clinical practice. Lancet. 2011;377(9783):2115–2126. doi:10.1016/S0140-6736(11)60243-2.
   PubMed Web of Science ®Google Scholar
• Zhuo Q, Yang W, Chen J, Wang Y. Metabolic syndrome meets osteoarthritis. Nat Rev Rheumatol. 2012;8(12):729–737. doi:10.1038/nrrheum.2012.135.
   PubMed Web of Science ®Google Scholar
• Glyn-Jones S, Palmer AJR, Agricola R, Price AJ, Vincent TL, Weinans H, Carr AJ, et al. Osteoarthritis. Lancet. 2015;386(9991):376–387. doi:10.1016/S0140-6736(14)60802-3.
   PubMed Web of Science ®Google Scholar
• Guilak F. Biomechanical factors in osteoarthritis. Best Pract Res Clin Rheumatol. 2011;25(6):815–823. doi:10.1016/j.berh.2011.11.013.
   PubMed Web of Science ®Google Scholar
• Bhosale AM, Richardson JB. Articular cartilage: structure, injuries and review of management. Br Med Bull. 2008;87(1):77–95. doi:10.1093/bmb/ldn025.
   PubMed Web of Science ®Google Scholar
• Buckwalter JA. Mechanical injuries of articular cartilage. Iowa Orthop J. 1992;12:50.
   Google Scholar
• Borrelli J, Ricci WM. Acute effects of cartilage impact. Clin Orthop Relat Res. 2004;423(423):33–39. doi:10.1097/01.blo.0000132627.13539.02.
   Google Scholar
• Teeple E, Elsaid KA, Fleming BC. Coefficients of friction, lubricin, and cartilage damage in the anterior cruciate ligament-deficient guinea pig knee. J Orthop Res. 2008;26(2):231–237. doi:10.1002/jor.20492.
   PubMed Web of Science ®Google Scholar
• Roemhildt ML, Beynnon BD, Gauthier AE, Gardner-Morse M, Ertem F, Badger GJ, et al. Chronic in vivo load alteration induces degenerative changes in the rat tibiofemoral joint. Osteoarthr Cartil. 2013;21(2):346–357. doi:10.1016/j.joca.2012.10.014.
   PubMed Web of Science ®Google Scholar
• Mäkelä JTA, Rezaeian ZS, Mikkonen S, Madden R, Han S-K, Jurvelin JS, Herzog W, Korhonen RK, et al. Site-dependent changes in structure and function of lapine articular cartilage 4 weeks after anterior cruciate ligament transection. Osteoarthr Cartil. 2014;22(6):869–878. doi:10.1016/j.joca.2014.04.010.
   PubMed Web of Science ®Google Scholar
• Ojanen SP, Finnilä MAJ, Mäkelä JTA, Saarela K, Happonen E, Herzog W, Saarakkala S, Korhonen RK, et al. Anterior cruciate ligament transection of rabbits alters composition, structure and biomechanics of articular cartilage and chondrocyte deformation 2 weeks post-surgery in a site-specific manner. J Biomech. 2020;98:0–11.
   Web of Science ®Google Scholar
• Kapoor M, Martel-Pelletier J, Lajeunesse D, Pelletier J-P, Fahmi H, et al. Role of proinflammatory cytokines in the pathophysiology of osteoarthritis. Nat Rev Rheumatol. 2011;7(1):33–42. doi:10.1038/nrrheum.2010.196.
   PubMed Web of Science ®Google Scholar
• Collins AT, Hu G, Newman H, Reinsvold MH, Goldsmith MR, Twomey-Kozak JN, Leddy HA, Sharma D, Shen L, DeFrate LE, Karner CM, et al. Obesity alters the collagen organization and mechanical properties of murine cartilage. Sci Rep. 2021;11(1):1–10. doi:10.1038/s41598-020-80599-1.
   PubMedGoogle Scholar
• Collins KH, Lenz KL, Pollitt EN. Adipose tissue is a critical regulator of osteoarthritis. Proc Natl Acad Sci U S A. 2020;118(1):1–12. doi:10.1073/pnas.2021096118.
   Web of Science ®Google Scholar
• Goldring MB, Otero M. Inflammation in osteoarthritis. Curr Opin Rheumatol. 2011;23(5):471–478. doi:10.1097/BOR.0b013e328349c2b1.
   PubMed Web of Science ®Google Scholar
• Wang X, Hunter D, Xu J, Ding C. Metabolic triggered inflammation in osteoarthritis. Osteoarthr Cartil. 2015;23(1):22–30. doi:10.1016/j.joca.2014.10.002.
   PubMed Web of Science ®Google Scholar
• Berenbaum F. Osteoarthritis as an inflammatory disease (osteoarthritis is not osteoarthrosis!). Osteoarthr Cartil. 2013;21(1):16–21. doi:10.1016/j.joca.2012.11.012.
   PubMed Web of Science ®Google Scholar
• Daghestani HN, Kraus VB. Inflammatory biomarkers in osteoarthritis. Osteoarthr Cartil. 2015;23(11):1890–1896. doi:10.1016/j.joca.2015.02.009.
   PubMed Web of Science ®Google Scholar
• Mitchell NS, Catenacci VA, Wyatt HR, Hill JO. Obesity: overview of an epidemic. Psychiatr Clin North Am. 2011;34(4):717–732. doi:10.1016/j.psc.2011.08.005.
   PubMed Web of Science ®Google Scholar
• Messier SP, Pater M, Beavers DP, Legault C, Loeser RF, Hunter DJ, DeVita P, et al. Influences of alignment and obesity on knee joint loading in osteoarthritic gait. Osteoarthr Cartil. 2014;22(7):912–917. doi:10.1016/j.joca.2014.05.013.
   PubMed Web of Science ®Google Scholar
• Sokolove J, Lepus CM. Role of inflammation in the pathogenesis of osteoarthritis: latest findings and interpretations. Ther Adv Musculoskelet Dis. 2013;5(2):77–94. doi:10.1177/1759720X12467868.
   PubMedGoogle Scholar
• Janney CA, Jakicic JM. The influence of exercise and BMI on injuries and illnesses in overweight and obese individuals: a randomized control trial. Int J Behav Nutr Phys Act. 2010;7(1):1–11. doi:10.1186/1479-5868-7-1.
   PubMedGoogle Scholar
• Richmond SA, Nettel-Aguirre A, Doyle-Baker PK, Macpherson A, Emery CA, et al. Examining measures of weight as risk factors for sport-related injury in adolescents. J Sports Med. 2016;2016:1–5.
   Google Scholar
• Pfeifer CE, Beattie PF, Sacko RS, Hand A. Risk factors associated with non-contact anterior cruciate ligament injury: a systematic review. Int J Sports Phys Ther. 2018;13(4):575–587. doi:10.26603/ijspt20180575.
   PubMedGoogle Scholar
• Moo EK, Ebrahimi M, Sibole SC. The intrinsic quality of proteoglycans, but not collagen fibres, degrades in osteoarthritic cartilage. Acta Biomater. 2022;153:178–189.
   PubMed Web of Science ®Google Scholar
• Thijssen E, Van Caam A, Van Der Kraan PM. Obesity and osteoarthritis, more than just wear and tear: pivotal roles for inflamed adipose tissue and dyslipidaemia in obesity-induced osteoarthritis. Rheumatology. 2014;54(4):588–600. doi:10.1093/rheumatology/keu464.
   PubMed Web of Science ®Google Scholar
• Blaker CL, Clarke EC, Little CB. Adding insult to injury: synergistic effect of combining risk-factors in models of post-traumatic osteoarthritis. Osteoarthr Cartil. 2019;27(12):1731–1734. doi:10.1016/j.joca.2019.06.010.
   PubMed Web of Science ®Google Scholar
• Collins KH, Reimer RA, Seerattan RA, Leonard TR, Herzog W, et al. Using diet-induced obesity to understand a metabolic subtype of osteoarthritis in rats. Osteoarthr Cartil. 2015;23(6):957–965. doi:10.1016/j.joca.2015.01.015.
   PubMed Web of Science ®Google Scholar
• Kiraly K, Lapveteläinen T, Arokoski J, Törrönen K, Modis L, Kiviranta HJHI, Helminen HJ. Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry. Histochem J. 1996;28(8):577–590. doi:10.1007/BF02331378.
   PubMedGoogle Scholar
• Kiviranta I, Jurvelin J, Säämänen AM, Helminen HJ. Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O. Histochemistry. 1985;82(3):249–255. doi:10.1007/BF00501401.
   PubMedGoogle Scholar
• Rieppo J, Hallikainen J, Jurvelin JS, Kiviranta I, Helminen HJ, Hyttinen MM, et al. Practical considerations in the use of polarized light microscopy in the analysis of the collagen network in articular cartilage. Microsc Res Tech. 2008;71(4):279–287. doi:10.1002/jemt.20551.
   PubMed Web of Science ®Google Scholar
• Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with imageJ. Biophotonics Int. 2004;11(7):36–41.
   Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–675. doi:10.1038/nmeth.2089.
   PubMed Web of Science ®Google Scholar
• Karjalainen K, Tanska P, Sibole SC. Effect of cells on spatial quantification of proteoglycans in articular cartilage of small animals. Connect Tissue Res. 2022;63(6):603–614. doi:10.1080/03008207.2022.2048827.
   PubMed Web of Science ®Google Scholar
• Rieppo J, Hyttinen MM, Halmesmaki E, Ruotsalainen H, Vasara A, Kiviranta I, Jurvelin JS, Helminen HJ, et al. Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation. Osteoarthr Cartil. 2009;17(4):448–455. doi:10.1016/j.joca.2008.09.004.
   PubMed Web of Science ®Google Scholar
• Panula HE, Hyttinen MM, Arokoski JPA, Langsjo TK, Pelttari A, Kiviranta I, Helminen HJ, et al. Articular cartilage superficial zone collagen birefringence reduced and cartilage thickness increased before surface fibrillation in experimental osteoarthritis. Ann Rheum Dis. 1998;57(4):237–245. doi:10.1136/ard.57.4.237.
   PubMed Web of Science ®Google Scholar
• Guilak F, Ratcliffe A, Lane N. Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis. J Orthop Res. 1994;12(4):474–484. doi:10.1002/jor.1100120404.
   PubMed Web of Science ®Google Scholar
• Rios JL, Bomhof MR, Reimer RA, Hart DA, Collins KH, Herzog W, 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):1–10. doi:10.1038/s41598-019-40601-x.
   PubMedGoogle Scholar
• Collins KH, Paul HA, Hart DA. A high-fat high-sucrose diet rapidly alters muscle integrity, inflammation and gut microbiota in male rats. Sci Rep. 2016;6(1):1–10. doi:10.1038/srep37278.
   PubMedGoogle Scholar
• Griffin TM, Fermor B, Huebner JL, Kraus VB, Rodriguiz RM, Wetsel WC, Cao L, Setton LA, Guilak F, et al. Diet-induced obesity differentially regulates behavioral, biomechanical, and molecular risk factors for osteoarthritis in mice. Arthritis Res Ther. 2010;12(4):R130. doi:10.1186/ar3068.
   PubMed Web of Science ®Google Scholar
• Collins KH, Paul HA, Reimer RA, Seerattan RA, Hart DA, Herzog W, et al. Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model. Osteoarthr Cartil. 2015;23(11):1989–1998. doi:10.1016/j.joca.2015.03.014.
   PubMed Web of Science ®Google Scholar
• Mooney RA, Sampson ER, Lerea J, Rosier RN, Zuscik MJ, et al. High-fat diet accelerates progression of osteoarthritis after meniscal/ligamentous injury. Arthritis Res Ther. 2011;13(6):R198. doi:10.1186/ar3529.
   PubMed Web of Science ®Google Scholar
• Louer CR, Furman BD, Huebner JL, Kraus VB, Olson SA, Guilak F, et al. Diet-induced obesity significantly increases the severity of posttraumatic arthritis in mice. Arthritis Rheumatism. 2012;64(10):3220–3230. doi:10.1002/art.34533.
   PubMedGoogle Scholar
• Vincent TL. Il-1 in osteoarthritis: time for a critical review of the literature. F1000Res. 2019;8:934–939. doi:10.12688/f1000research.18831.1.
   Google Scholar
• McNulty AL, Rothfusz NE, Leddy HA, Guilak F. Synovial fluid concentrations and relative potency of interleukin-1 alpha and beta in cartilage and meniscus degradation. J Orthop Res. 2013;31(7):1039–1045. doi:10.1002/jor.22334.
   PubMed Web of Science ®Google Scholar
• Roughley PJ. The structure and function of cartilage proteoglycans. Eur Cell Mater. 2006;12:92–101. doi:10.22203/eCM.v012a11.
   PubMed Web of Science ®Google Scholar
• Furman BD, Kent CL, Huebner JL, Kraus VB, McNulty AL, Guilak F, Olson SA. CXCL10 is upregulated in synovium and cartilage following articular fracture. J Orthop Res. 2018;36(4):1220–1227. doi:10.1002/jor.23735.
   PubMed Web of Science ®Google Scholar
• Dumond H, Presle N, Terlain B, Mainard D, Loeuille D, Netter P, Pottie P, et al. Evidence for a key role of leptin in osteoarthritis. Arthritis Rheumatism. 2003;48(11):3118–3129. doi:10.1002/art.11303.
   PubMed Web of Science ®Google Scholar
• Donnenfield JI, Karamchedu NP, Fleming BC. Articular cartilage and synovium may be important sources of post-surgical synovial fluid inflammatory mediators. Am J Transl Res. 2022;14(3):1640–1651.
   PubMed Web of Science ®Google Scholar
• Catterall JB, Stabler TV, Flannery CR, Kraus VB. Changes in serum and synovial fluid biomarkers after acute injury (NCT00332254). Arthritis Res Ther. 2010;12(6):R229. doi:10.1186/ar3216.
   PubMed Web of Science ®Google Scholar
• Kloefkorn HE, Jacobs BY, Loye AM, Allen KD. Spatiotemporal gait compensations following medial collateral ligament and medial meniscus injury in the rat: correlating gait patterns to joint damage. Arthritis Res Ther. 2015;17(1):1–15. doi:10.1186/s13075-015-0791-2.
   PubMedGoogle Scholar
• Christiansen BA, Guilak F, Lockwood KA, Olson SA, Pitsillides AA, Sandell LJ, Silva MJ, van der Meulen MCH, Haudenschild DR, et al. Non-invasive mouse models of post-traumatic osteoarthritis. Osteoarthr Cartil. 2015;23(10):1627–1638. doi:10.1016/j.joca.2015.05.009.
   PubMed Web of Science ®Google Scholar
• Maerz T, Kurdziel MD, Davidson AA, Baker KC, Anderson K, Matthew HWT, et al. Biomechanical characterization of a model of noninvasive, traumatic anterior cruciate ligament injury in the rat. Ann Biomed Eng. 2015;43(10):2467–2476. doi:10.1007/s10439-015-1292-9.
   PubMed Web of Science ®Google Scholar
• Christiansen BA, Anderson MJ, Lee CA, Williams JC, Yik JHN, Haudenschild DR, et al. Musculoskeletal changes following non-invasive knee injury using a novel mouse model of post-traumatic osteoarthritis. Osteoarthr Cartil. 2012;20(7):773–782. doi:10.1016/j.joca.2012.04.014.
   PubMed Web of Science ®Google Scholar
• Brown SB, Hornyak JA, Jungels RR. Characterization of post-traumatic osteoarthritis in rats following anterior cruciate ligament rupture by non-invasive knee injury (NIKI). J Orthop Res. 2020;38(2):356–367. doi:10.1002/jor.24470.
   PubMed Web of Science ®Google Scholar
• Furman BD, Strand J, Hembree WC. Joint degeneration following closed intraarticular fracture in the mouse knee: a Model of posttraumatic arthritis. J Orthop Res. 2007;25(5):578–592. doi:10.1002/jor.20331.
   PubMed Web of Science ®Google Scholar
• Poulet B, Hamilton RW, Shefelbine S, Pitsillides AA. Characterizing a novel and adjustable noninvasive murine joint loading model. Arthritis Rheumatism. 2011;63(1):137–147. doi:10.1002/art.27765.
   PubMedGoogle Scholar
• Froimson MI, Ratcliffe A, Gardner TR, Mow VC. Differences in patellofemoral joint cartilage material properties and their significance to the etiology of cartilage surface fibrillation. Osteoarthr Cartil. 1997;5(6):377–386. doi:10.1016/S1063-4584(97)80042-8.
   PubMed Web of Science ®Google Scholar
• Arokoski MEA, Tiitu V, Jurvelin JS. Topographical investigation of changes in depth-wise proteoglycan distribution in rabbit femoral articular cartilage at 4 weeks after transection of the anterior cruciate ligament. J Orthop Res. 2015;33(9):1278–1286. doi:10.1002/jor.22906.
   PubMed Web of Science ®Google Scholar
• Li G, Sang EP, DeFrate LE. The cartilage thickness distribution in the tibiofemoral joint and its correlation with cartilage-to-cartilage contact. Clin Biomech. 2005;20(7):736–744. doi:10.1016/j.clinbiomech.2005.04.001.
   PubMed Web of Science ®Google Scholar
• Glasson SS, Blanchet TJ, Morris EA. The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthr Cartil. 2007;15(9):1061–1069. doi:10.1016/j.joca.2007.03.006.
   PubMed Web of Science ®Google Scholar
• Warmink K, Kozijn AE, Bobeldijk I, Stoop R, Weinans H, Korthagen NM, et al. High-fat feeding primes the mouse knee joint to develop osteoarthritis and pathologic infrapatellar fat pad changes after surgically induced injury. Osteoarthr Cartil. 2020;28(5):593–602. doi:10.1016/j.joca.2020.03.008.
   PubMed Web of Science ®Google Scholar
• Afzali MF, Radakovich LB, Sykes MM, Campbell MA, Patton KM, Sanford JL, Vigon N, Ek R, Narez GE, Marolf AJ, Sikes KJ, Haut Donahue TL, Santangelo KS, et al. Early removal of the infrapatellar fat pad/synovium complex beneficially alters the pathogenesis of moderate stage idiopathic knee osteoarthritis in male Dunkin Hartley guinea pigs. Arthritis Res Ther. 2022;24(1):1–19. doi:10.1186/s13075-022-02971-y.
   PubMed Web of Science ®Google Scholar
• Clockaerts S, Bastiaansen-Jenniskens YM, Runhaar J, Van Osch GJVM, Van Offel JF, Verhaar JAN, De Clerck LS, Somville J, et al. The infrapatellar fat pad should be considered as an active osteoarthritic joint tissue: a narrative review. Osteoarthr Cartil. 2010;18(7):876–882. doi:10.1016/j.joca.2010.03.014.
   PubMed Web of Science ®Google Scholar
• Zhou S, Maleitzke T, Geissler S. Source and hub of inflammation: the infrapatellar fat pad and its interactions with articular tissues during knee osteoarthritis. J Orthop Res. 2022;40(7):1492–1504. doi:10.1002/jor.25347.
   PubMed Web of Science ®Google Scholar
• Turunen SM, Han SK, Herzog W, Korhonen RK. Cell deformation behavior in mechanically loaded rabbit articular cartilage 4 weeks after anterior cruciate ligament transection. Osteoarthr Cartil. 2013;21(3):505–513. doi:10.1016/j.joca.2012.12.001.
   PubMed Web of Science ®Google Scholar
• Huebner JL, Williams JM, Deberg M, Henrotin Y, Kraus VB, et al. Collagen fibril disruption occurs early in primary guinea pig knee osteoarthritis. Osteoarthr Cartil. 2010;18(3):397–405. doi:10.1016/j.joca.2009.09.011.
   PubMed Web of Science ®Google Scholar
• Saarakkala S, Julkunen P, Kiviranta P, Mäkitalo J, Jurvelin JS, Korhonen RK, et al. Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics. Osteoarthr Cartil. 2010;18(1):73–81. doi:10.1016/j.joca.2009.08.003.
   PubMed Web of Science ®Google Scholar
• Sibole SC, Moo EK, Federico S, Herzog W. The protective function of directed asymmetry in the pericellular matrix enveloping chondrocytes. Ann Biomed Eng. 2022;50(1):39–55. doi:10.1007/s10439-021-02900-1.
   PubMed Web of Science ®Google Scholar
• Ojanen SP, Finnilä MAJ, Reunamo AE, Ronkainen AP, Mikkonen S, Herzog W, Saarakkala S, Korhonen RK, et al. Site-specific glycosaminoglycan content is better maintained in the pericellular matrix than the extracellular matrix in early post-traumatic osteoarthritis. PloS ONE. 2018;13(4):1–19. doi:10.1371/journal.pone.0196203.
   Web of Science ®Google Scholar
• Moo EK, Sibole SC, Han SK, Herzog W. Three-dimensional micro-scale strain mapping in living biological soft tissues. Acta Biomater. 2018;70:260–269. doi:10.1016/j.actbio.2018.01.048.
   PubMed Web of Science ®Google Scholar
• Guilak F, Nims RJ, Dicks A. Osteoarthritis as a disease of the cartilage pericellular matrix. Matrix Biol. 2018;71–72:40–50.
   PubMed Web of Science ®Google Scholar
• Leipzig ND, Athanasiou KA. Static compression of single chondrocytes catabolically modifies single-cell gene Expression. Biophys J. 2008;94(6):2412–2422. doi:10.1529/biophysj.107.114207.
   PubMed Web of Science ®Google Scholar
• Jones WR, Ping Ting-Beall H, Lee GM, Kelley SS, Hochmuth RM, Guilak F, et al. Alterations in the Young’s modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. J Biomech. 1999;32(2):119–127. doi:10.1016/S0021-9290(98)00166-3.
   PubMed Web of Science ®Google Scholar
• Fan M, Wang C, Kwok B, Kahle ER, He L, Lucas Lu X, Mauck RL, Han L, et al. Impacts of aging on murine cartilage biomechanics and chondrocyte in situ calcium signaling. J Biomech. 2022;144:111336.
   PubMed Web of Science ®Google Scholar
• Moo EK, Han SK, Federico S, Sibole SC, Jinha A, Abu Osman NA, Pingguan-Murphy B, Herzog W, et al. Extracellular matrix integrity affects the mechanical behaviour of in-situ chondrocytes under compression. J Biomech. 2014;47(5):1004–1013. doi:10.1016/j.jbiomech.2014.01.003.
   PubMed Web of Science ®Google Scholar
• Moo EK, Amrein M, Epstein M, Duvall M, Abu Osman N, Pingguan-Murphy B, Herzog W, et al. The properties of chondrocyte membrane reservoirs and their role in impact-induced cell death. Biophys J. 2013;105(7):1590–1600. doi:10.1016/j.bpj.2013.08.035.
   PubMed Web of Science ®Google Scholar
• Moo EK, Herzog W. Unfolding of membrane ruffles of in situ chondrocytes under compressive loads. J Orthop Res. 2017;35(2):304–310. doi:10.1002/jor.23260.
   PubMed Web of Science ®Google Scholar
• Moo EK, Sibole SC, Federico S. Microscale investigation of the anisotropic swelling of cartilage tissue and cells in response to hypo-osmotic challenges. J Orthop Res. 2023;42(1):54–65. doi:10.1002/jor.25657.
   PubMed Web of Science ®Google Scholar