Inflammation and Fibrosis Induced by Joint Remobilization, and Relevance to Progression of Arthrogenic Joint Contracture: A Narrative Review

. 2022 Aug 31 ; 71 (4) : 447-488. [epub] 20220630

Jazyk angličtina Země Česko Médium print-electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid35770468

Joint immobilization is frequently administered after fractures and ligament injuries and can cause joint contracture as a side effect. The structures responsible for immobilization-induced joint contracture can be roughly divided into muscular and articular. During remobilization, although myogenic contracture recovers spontaneously, arthrogenic contracture is irreversible or deteriorates further. Immediately after remobilization, an inflammatory response is observed, characterized by joint swelling, deposit formation in the joint space, edema, inflammatory cell infiltration, and the upregulation of genes encoding proinflammatory cytokines in the joint capsule. Subsequently, fibrosis in the joint capsule develops, in parallel with progressing arthrogenic contracture. The triggers of remobilization-induced joint inflammation are not fully understood, but two potential mechanisms are proposed: 1) micro-damage induced by mechanical stress in the joint capsule, and 2) nitric oxide (NO) production via NO synthase 2. Some interventions can modulate remobilization-induced inflammatory and subsequent fibrotic reactions. Anti-inflammatory treatments, such as steroidal anti-inflammatory drugs and low-level laser therapy, can attenuate joint capsule fibrosis and the progression of arthrogenic contracture in remobilized joints. Antiproliferative treatment using the cell-proliferation inhibitor mitomycin C can also attenuate joint capsule fibrosis by inhibiting fibroblast proliferation without suppressing inflammation. Conversely, aggressive exercise during the early remobilization phases is counterproductive, because it facilitates inflammatory and then fibrotic reactions in the joint. However, the adverse effects of aggressive exercise on remobilization-induced inflammation and fibrosis are offset by anti-inflammatory treatment. To prevent the progression of arthrogenic contracture during remobilization, therefore, care should be taken to control inflammatory and fibrotic reactions in the joints.

Zobrazit více v PubMed

Kannus P, Jarvinen M. Nonoperative treatment of acute knee ligament injuries. A review with special reference to indications and methods. Sports Med. 1990;9:244–260. PubMed

Moseley AM, Herbert RD, Nightingale EJ, Taylor DA, Evans TM, Robertson GJ, Gupta SK, Penn J. Passive stretching does not enhance outcomes in patients with plantarflexion contracture after cast immobilization for ankle fracture: A randomized controlled trial. Arch Phys Med Rehabil. 2005;86:1118–1126. doi: 10.1016/j.apmr.2004.11.017. PubMed DOI

Stevens JE, Pathare NC, Tillman SM, Scarborough MT, Gibbs CP, Shah P, Jayaraman A, Walter GA, Vandenborne K. Relative contributions of muscle activation and muscle size to plantarflexor torque during rehabilitation after immobilization. J Orthop Res. 2006;24:1729–1736. doi: 10.1002/jor.20153. PubMed DOI

Stevens JE, Walter GA, Okereke E, Scarborough MT, Esterhai JL, George SZ, Kelley MJ, Tillman SM, Gibbs JD, Elliott MA, Frimel TN, Gibbs CP, Vandenborne K. Muscle adaptations with immobilization and rehabilitation after ankle fracture. Med Sci Sports Exerc. 2004;36:1695–1701. doi: 10.1249/01.mss.0000142407.25188.05. PubMed DOI

Vandenborne K, Elliott MA, Walter GA, Abdus S, Okereke E, Shaffer M, Tahernia D, Esterhai JL. Longitudinal study of skeletal muscle adaptations during immobilization and rehabilitation. Muscle Nerve. 1998;21:1006–1012. doi: 10.1002/(sici)1097-4598(199808)21:8<1006::aid-mus4>3.0.co;2-c. PubMed DOI

Hudelmaier M, Glaser C, Hausschild A, Burgkart R, Eckstein F. Effects of joint unloading and reloading on human cartilage morphology and function, muscle cross-sectional areas, and bone density - a quantitative case report. J Musculoskelet Neuronal Interact. 2006;6:284–290. PubMed

Born CT, Gil JA, Goodman AD. Joint contractures resulting from prolonged immobilization: Etiology, prevention, and management. J Am Acad Orthop Surg. 2017;25:110–116. doi: 10.5435/JAAOS-D-15-00697. PubMed DOI

Chimoto E, Hagiwara Y, Ando A, Itoi E. Progression of an arthrogenic motion restriction after immobilization in a rat experimental knee model. Ups J Med Sci. 2007;112:347–355. PubMed

Goto K, Sakamoto J, Nakano J, Kataoka H, Honda Y, Sasabe R, Origuchi T, Okita M. Development and progression of immobilization-induced skin fibrosis through overexpression of transforming growth factor-ss1 and hypoxic conditions in a rat knee joint contracture model. Connect Tissue Res. 2017;58:586–596. doi: 10.1080/03008207.2017.1284823. PubMed DOI

Hagiwara Y, Ando A, Onoda Y, Matsui H, Chimoto E, Suda H, Itoi E. Expression patterns of collagen types i and iii in the capsule of a rat knee contracture model. J Orthop Res. 2010;28:315–321. doi: 10.1002/jor.20997. PubMed DOI

Kaneguchi A, Ozawa J, Minamimoto K, Yamaoka K. Morphological and biomechanical adaptations of skeletal muscle in the recovery phase after immobilization in a rat. Clin Biomech (Bristol, Avon) 2020;75:104992. doi: 10.1016/j.clinbiomech.2020.104992. PubMed DOI

Nagai M, Aoyama T, Ito A, Iijima H, Yamaguchi S, Tajino J, Zhang X, Akiyama H, Kuroki H. Contributions of biarticular myogenic components to the limitation of the range of motion after immobilization of rat knee joint. BMC Musculoskelet Disord. 2014;15:224. doi: 10.1186/1471-2474-15-224. PubMed DOI PMC

Ozawa J, Kaneguchi A, Minamimoto K, Tanaka R, Kito N, Moriyama H. Accumulation of advanced-glycation end products (ages) accelerates arthrogenic joint contracture in immobilized rat knee. J Orthop Res. 2017;36:854–863. doi: 10.1002/jor.23719. PubMed DOI

Ozawa J, Kaneguchi A, Tanaka R, Kito N, Moriyama H. Cyclooxygenase-2 inhibitor celecoxib attenuates joint contracture following immobilization in rat knees. BMC Musculoskelet Disord. 2016;17:446. doi: 10.1186/s12891-016-1303-5. PubMed DOI PMC

Sasabe R, Sakamoto J, Goto K, Honda Y, Kataoka H, Nakano J, Origuchi T, Endo D, Koji T, Okita M. Effects of joint immobilization on changes in myofibroblasts and collagen in the rat knee contracture model. J Orthop Res. 2017;35:1998–2006. doi: 10.1002/jor.23498. PubMed DOI

Trudel G, Laneuville O, Coletta E, Goudreau L, Uhthoff HK. Quantitative and temporal differential recovery of articular and muscular limitations of knee joint contractures; results in a rat model. J Appl Physiol (1985) 2014;117:730–737. doi: 10.1152/japplphysiol.00409.2014. PubMed DOI

Trudel G, Uhthoff HK. Contractures secondary to immobility: Is the restriction articular or muscular? An experimental longitudinal study in the rat knee. Arch Phys Med Rehabil. 2000;81:6–13. doi: 10.1016/s0003-9993(00)90213-2. PubMed DOI

Trudel G, Uhthoff HK, Brown M. Extent and direction of joint motion limitation after prolonged immobility: An experimental study in the rat. Arch Phys Med Rehabil. 1999;80:1542–1547. PubMed

Ando A, Suda H, Hagiwara Y, Onoda Y, Chimoto E, Itoi E. Remobilization does not restore immobilization-induced adhesion of capsule and restricted joint motion in rat knee joints. Tohoku J Exp Med. 2012;227:13–22. doi: 10.1620/tjem.227.13. PubMed DOI

Trudel G, Zhou J, Uhthoff HK, Laneuville O. Four weeks of mobility after 8 weeks of immobility fails to restore normal motion: A preliminary study. Clin Orthop Relat Res. 2008;466:1239–1244. doi: 10.1007/s11999-008-0181-z. PubMed DOI PMC

Kaneguchi A, Ozawa J. The preventive effects of low-level laser therapy on arthrogenic contracture progression in remobilized rat knee (in japanese) Japanese Journal of Electrophysical Agents. 2017;24:47–51.

Kaneguchi A, Ozawa J, Kawamata S, Yamaoka K. Development of arthrogenic joint contracture as a result of pathological changes in remobilized rat knees. J Orthop Res. 2017;35:1414–1423. doi: 10.1002/jor.23419. PubMed DOI

Kaneguchi A, Ozawa J, Minamimoto K, Yamaoka K. Active exercise on immobilization-induced contractured rat knees develops arthrogenic joint contracture with pathological changes. J Appl Physiol (1985) 2018;124:291–301. doi: 10.1152/japplphysiol.00438.2017. PubMed DOI

Kaneguchi A, Ozawa J, Minamimoto K, Yamaoka K. Low-level laser therapy prevents treadmill exercise-induced progression of arthrogenic joint contracture via attenuation of inflammation and fibrosis in remobilized rat knees. Inflammation. 2019;42:857–873. doi: 10.1007/s10753-018-0941-1. PubMed DOI

Kaneguchi A, Ozawa J, Yamaoka K. Anti-inflammatory drug dexamethasone treatment during the remobilization period improves range of motion in a rat knee model of joint contracture. Inflammation. 2018;41:1409–1423. doi: 10.1007/s10753-018-0788-5. PubMed DOI

Kaneguchi A, Ozawa J, Yamaoka K. Intra-articular injection of mitomycin c prevents progression of immobilization-induced arthrogenic contracture in the remobilized rat knee. Physiol Res. 2020;69:145–156. doi: 10.33549/physiolres.934149. PubMed DOI PMC

Cho CH, Lho YM, Hwang I, Kim DH. Role of matrix metalloproteinases 2 and 9 in the development of frozen shoulder: Human data and experimental analysis in a rat contracture model. J Shoulder Elbow Surg. 2019;28:1265–1272. doi: 10.1016/j.jse.2018.11.072. PubMed DOI

Kim DH, Lee KH, Lho YM, Ha E, Hwang I, Song KS, Cho CH. Characterization of a frozen shoulder model using immobilization in rats. J Orthop Surg Res. 2016;11:160. doi: 10.1186/s13018-016-0493-8. PubMed DOI PMC

Yabe Y, Hagiwara Y, Suda H, Ando A, Onoda Y, Tsuchiya M, Hatori K, Itoi E. Joint immobilization induced hypoxic and inflammatory conditions in rat knee joints. Connect Tissue Res. 2013;54:210–217. doi: 10.3109/03008207.2013.786056. PubMed DOI

Kaneguchi A, Ozawa J, Minamimoto K, Yamaoka K. Nitric oxide synthase inhibitor l-ng-nitroarginine methyl ester (l-name) attenuates remobilization-induced joint inflammation. Nitric Oxide. 2020;96:13–19. doi: 10.1016/j.niox.2020.01.003. PubMed DOI

Michelsson JE, Hunneyball IM. Inflammatory involvement in rabbit knee following immobilization and resulting in osteoarthritis. Scand J Rheumatol. 1984;13:273–281. PubMed

Dixon D, Coates J, del Carpio Pons A, Horabin J, Walker A, Abdul N, Kalson NS, Brewster NT, Weir DJ, Deehan DJ, Mann DA, Borthwick LA. A potential mode of action for anakinra in patients with arthrofibrosis following total knee arthroplasty. Sci Rep. 2015;5:16466. doi: 10.1038/srep16466. PubMed DOI PMC

Lee WS, Lim JH, Sung MS, Lee EG, Oh YJ, Yoo WH. Ethyl acetate fraction from angelica sinensis inhibits il-1beta-induced rheumatoid synovial fibroblast proliferation and cox-2, pge2, and mmps production. Biol Res. 2014;47:41. doi: 10.1186/0717-6287-47-41. PubMed DOI PMC

Biernacka A, Dobaczewski M, Frangogiannis NG. TGF-βeta signaling in fibrosis. Growth Factors. 2011;29:196–202. doi: 10.3109/08977194.2011.595714. PubMed DOI PMC

Fukui N, Fukuda A, Kojima K, Nakajima K, Oda H, Nakamura K. Suppression of fibrous adhesion by proteoglycan decorin. J Orthop Res. 2001;19:456–462. doi: 10.1016/S0736-0266(00)90016-0. PubMed DOI

Fukui N, Tashiro T, Hiraoka H, Oda H, Nakamura K. Adhesion formation can be reduced by the suppression of transforming growth factor-beta1 activity. J Orthop Res. 2000;18:212–219. doi: 10.1002/jor.1100180208. PubMed DOI

Zhang Y, Lu S, Fan S, Xu L, Jiang X, Wang K, Cai B. Macrophage migration inhibitory factor activates the inflammatory response in joint capsule fibroblasts following post-traumatic joint contracture. Aging (Albany NY) 2021;13:5804–5823. doi: 10.18632/aging.202505. PubMed DOI PMC

Nesterenko S, Morrey ME, Abdel MP, An KN, Steinmann SP, Morrey BF, Sanchez-Sotelo J. New rabbit knee model of posttraumatic joint contracture: Indirect capsular damage induces a severe contracture. J Orthop Res. 2009;27:1028–1032. doi: 10.1002/jor.20845. PubMed DOI

Ando A, Hagiwara Y, Onoda Y, Hatori K, Suda H, Chimoto E, Itoi E. Distribution of type a and b synoviocytes in the adhesive and shortened synovial membrane during immobilization of the knee joint in rats. Tohoku J Exp Med. 2010;221:161–168. doi: 10.1620/tjem.221.161. PubMed DOI

Trudel G, Seki M, Uhthoff HK. Synovial adhesions are more important than pannus proliferation in the pathogenesis of knee joint contracture after immobilization: An experimental investigation in the rat. J Rheumatol. 2000;27:351–357. PubMed

Kaneguchi A, Ozawa J, Minamimoto K, Yamaoka K. Three-week joint immobilization increases anterior-posterior laxity without alterations in mechanical properties of the anterior cruciate ligament in the rat knee. Clin Biomech (Bristol, Avon) 2020;75:104993. doi: 10.1016/j.clinbiomech.2020.104993. PubMed DOI

Evans EB, Eggers GWN, Butler JK, Blumel J. Experimental immobilization and remobilization of rat knee joints. JBJS. 1960;42:737–758.

Michelsson JE, Riska EB. The effect of temporary exercising of a joint during an immobilization period: An experimental study on rabbits. Clin Orthop Relat Res. 1979:321–325. PubMed

Cuzzocrea S. Role of nitric oxide and reactive oxygen species in arthritis. Curr Pharm Des. 2006;12:3551–3570. PubMed

Chenevier-Gobeaux C, Simonneau C, Lemarechal H, Bonnefont-Rousselot D, Poiraudeau S, Rannou F, Ekindjian OG, Anract P, Borderie D. Effect of hypoxia/reoxygenation on the cytokine-induced production of nitric oxide and superoxide anion in cultured osteoarthritic synoviocytes. Osteoarthritis Cartilage. 2013;21:874–881. doi: 10.1016/j.joca.2013.03.010. PubMed DOI

Sotobayashi D, Kawahata H, Anada N, Ogihara T, Morishita R, Aoki M. Therapeutic effect of intra-articular injection of ribbon-type decoy oligonucleotides for hypoxia inducible factor-1 on joint contracture in an immobilized knee animal model. J Gene Med. 2016;18:180–192. doi: 10.1002/jgm.2891. PubMed DOI

dos Santos G, Kutuzov MA, Ridge KM. The inflammasome in lung diseases. Am J Physiol Lung Cell Mol Physiol. 2012;303:L627–633. doi: 10.1152/ajplung.00225.2012. PubMed DOI PMC

Morrey ME, Abdel MP, Riester SM, Dudakovic A, van Wijnen AJ, Morrey BF, Sanchez-Sotelo J. Molecular landscape of arthrofibrosis: Microarray and bioinformatic analysis of the temporal expression of 380 genes during contracture genesis. Gene. 2017;610:15–23. doi: 10.1016/j.gene.2017.01.025. PubMed DOI

Schacke H, Docke WD, Asadullah K. Mechanisms involved in the side effects of glucocorticoids. Pharmacol Ther. 2002;96:23–43. doi: 10.1016/s0163-7258(02)00297-8. PubMed DOI

Yamaura M, Yao M, Yaroslavsky I, Cohen R, Smotrich M, Kochevar IE. Low level light effects on inflammatory cytokine production by rheumatoid arthritis synoviocytes. Lasers Surg Med. 2009;41:282–290. doi: 10.1002/lsm.20766. PubMed DOI

Kaneguchi A, Ozawa J, Minamimoto K, Yamaoka K. Low-level laser therapy attenuates arthrogenic contracture induced by anterior cruciate ligament reconstruction surgery in rats. Physiol Res. In press. PubMed PMC

Lee Y, Kim H, Hong N, Ahn JC, Kang HW. Combined treatment of low-level laser therapy and phloroglucinol for inhibition of fibrosis. Lasers Surg Med. 2020;52:276–285. doi: 10.1002/lsm.23131. PubMed DOI

Cheuy VA, Foran JRH, Paxton RJ, Bade MJ, Zeni JA, Stevens-Lapsley JE. Arthrofibrosis associated with total knee arthroplasty. J Arthroplasty. 2017;32:2604–2611. doi: 10.1016/j.arth.2017.02.005. PubMed DOI

Usher KM, Zhu S, Mavropalias G, Carrino JA, Zhao J, Xu J. Pathological mechanisms and therapeutic outlooks for arthrofibrosis. Bone Res. 2019;7:9. doi: 10.1038/s41413-019-0047-x. PubMed DOI PMC

Abdul N, Dixon D, Walker A, Horabin J, Smith N, Weir DJ, Brewster NT, Deehan DJ, Mann DA, Borthwick LA. Fibrosis is a common outcome following total knee arthroplasty. Sci Rep. 2015;5:16469. doi: 10.1038/srep16469. PubMed DOI PMC

Kendall RT, Feghali-Bostwick CA. Fibroblasts in fibrosis: Novel roles and mediators. Front Pharmacol. 2014;5:123. doi: 10.3389/fphar.2014.00123. PubMed DOI PMC

Volpe A, Racioppi M, D’Agostino D, Cappa E, Filianoti A, Bassi PF. Mitomycin c for the treatment of bladder cancer. Minerva Urol Nefrol. 2010;62:133–144. PubMed

Chen N, Zhang J, Xu M, Wang YL, Pei YH. Inhibitory effect of mitomycin c on proliferation of primary cultured fibroblasts from human airway granulation tissues. Respiration. 2013;85:500–504. doi: 10.1159/000346648. PubMed DOI

Li X, Yan L, Wang J, Sun Y, Wang Q, Lu Z, Wang Q, Liu Z, Hu J. Comparison of the effects of mitomycin c and 10-hydroxycamptothecin on an experimental intraarticular adhesion model in rabbits. Eur J Pharmacol. 2013;703:42–45. doi: 10.1016/j.ejphar.2013.02.001. PubMed DOI

Wang J, Yan L, Sun Y, Wang D, Dai S, Yu T, Gu J, Jiang B, Feng X, Hu H, Wang Q, Yin B, Lv G. A comparative study of the preventive effects of mitomycin c and chitosan on intraarticular adhesion after knee surgery in rabbits. Cell Biochem Biophys. 2012;62:101–105. doi: 10.1007/s12013-011-9266-5. PubMed DOI

DeGroot J, Verzijl N, Bank RA, Lafeber FP, Bijlsma JW, TeKoppele JM. Age-related decrease in proteoglycan synthesis of human articular chondrocytes: The role of nonenzymatic glycation. Arthritis Rheum. 1999;42:1003–1009. doi: 10.1002/1529-0131(199905)42:5<1003::AID-ANR20>3.0.CO;2-K. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...