Targeting the synovial angiogenesis as a novel treatment approach to osteoarthritis

Therapeutic Advances in Musculoskeletal Disease

Volumn 6, Issue 1, 2014, Pages 20-34

  Henrotin, Yves ^a   Pesesse, Laurence ^a   Lambert, Cecile ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

angiogenesis; arthritis; synovium; vascularization

Indexed keywords

ANGIOPOIETIN; ANGIOSTATIN; CHEMOKINE; CHONDROITIN SULFATE; DIACEREIN; ENDOSTATIN; ENDOTHELIAL CELL GROWTH FACTOR; HYALURONIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLIXIMAB; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; METALLOPROTEINASE; METHIONYL AMINOPEPTIDASE 2; NERVE GROWTH FACTOR; NONSTEROID ANTIINFLAMMATORY AGENT; PIASCLEDINE; PROTEINASE; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; ARTHROPATHY; BIOLOGICAL THERAPY; BLOOD VESSEL; CARTILAGE DEGENERATION; CELLULAR IMMUNITY; CRYSTAL; DOPPLER FLOWMETRY; HUMAN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; JOINT SWELLING; MICROARRAY ANALYSIS; NONHUMAN; OSTEOARTHRITIS; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; SPONDYLOSIS; SYNOVIOCYTE; SYNOVITIS; SYNOVIUM; T LYMPHOCYTE; UNSPECIFIED SIDE EFFECT; VASCULARIZATION;

EID: 84892867619     PISSN: 1759720X     EISSN: 17597218     Source Type: Journal    
DOI: 10.1177/1759720X13514669     Document Type: Review

References (96)

1. Altinel L. Saritas Z. Kose K. Pamuk K. Aksoy Y. Serteser M. (2007) Treatment with unsaponifiable extracts of avocado and soybean increases TGF-β1 and TGF-β2 levels in canine joint fluid. Tohoku J Exp Med 211: 181–186.
2. Alvarez-Soria M. Herrero-Beaumont G. Sanchez-Pernaute O. Bellido M. Largo R. (2008) Diacerein has a weak effect on the catabolic pathway of human osteoarthritis synovial fibroblast–comparison to its effects on osteoarthritic chondrocytes. Rheumatology 47: 627–633.
3. Ammazzalorso A. de Filippis B. Giampietro L. Amoroso R. (2013) Blocking the peroxisome proliferator-activated receptor (PPAR): an overview. ChemMedChem. Epub ahead of print 12 August 2013. doi: 10.1002/cmdc.201300250.
4. Ashraf S. Mapp P. Walsh D. (2011) Contributions of angiogenesis to inflammation, joint damage, and pain in a rat model of osteoarthritis. Arthritis Rheum 63: 2700–2710.
5. Au R. Al-Talib T. Au A. Phan P. Frondoza C. (2007) Avocado soybean unsaponifiables (ASU) suppress TNF-α, IL-1β, COX-2, INOS gene expression, and prostaglandin E 2 and nitric oxide production in articular chondrocytes and monocyte/macrophages. Osteoarthritis Cartilage 15: 1249–1255.
6. Ayral X. Mayoux-Benhamou A. Dougados M. (1996) Proposed scoring system for assessing synovial membrane abnormalities at arthroscopy in knee osteoarthritis. Br J Rheumatol 35(Suppl. 3): 14–17.
7. Ayral X. Pickering E. Woodworth T. Mackillop N. Dougados M. (2005) Synovitis: a potential predictive factor of structural progression of medial tibiofemoral knee osteoarthritis – results of a 1 year longitudinal arthroscopic study in 422 patients. Osteoarthritis Cartilage 13: 361–367.
8. Bainbridge J. Madden L. Essex D. Binks M. Malhotra R. Paleolog E. (2007) Methionine aminopeptidase-2 blockade reduces chronic collagen-induced arthritis: potential role for angiogenesis inhibition. Arthritis Res Ther 9: R127.
9. Berenbaum F. (2013) Osteoarthritis as an inflammatory disease (osteoarthritis is not osteoarthrosis!). Osteoarthritis Cartilage 21: 16–21.
10. Boileau C. Martel-Pelletier J. Caron J. Msika P. Guillou G. Baudouin C. et al. (2009) Protective effects of total fraction of avocado/soybean unsaponifiables on the structural changes in experimental dog osteoarthritis: inhibition of nitric oxide synthase and matrix metalloproteinase-13. Arthritis Res Ther 11: R41.
11. Bonnet C. Walsh D. (2005) Osteoarthritis, angiogenesis and inflammation. Rheumatology 44: 7–16.
12. Boumediene K. Felisaz N. Bogdanowicz P. Galera P. Guillou G. Pujol J. (1999) Avocado/soya unsaponifiables enhance the expression of transforming growth factor β1 and β2 in cultured articular chondrocytes. Arthritis Rheum 42: 148–156.
13. Calamia V. Lourido L. Fernandez-Puente P. Mateos J. Rocha B. Montell E. et al. (2012) Secretome analysis of chondroitin sulfate-treated chondrocytes reveals anti-angiogenic, anti-inflammatory and anti-catabolic properties. Arthritis Res Ther 14: R202.
14. Campo G. Avenoso A. D'Ascola A. Scuruchi M. Prestipino V. Calatroni A. et al. (2012 a) 6-Mer hyaluronan oligosaccharides increase IL-18 and IL-33 production in mouse synovial fibroblasts subjected to collagen-induced arthritis. Innate Immun 18: 675–684.
15. Campo G. Avenoso A. D'Aascola A. Scuruchi M. Prestipino V. Nastasi G. et al. (2012 b) The inhibition of hyaluronan degradation reduced pro-inflammatory cytokines in mouse synovial fibroblasts subjected to collagen-induced arthritis. J Cell Biochem 113: 1852–1867.
16. Campo G. Avenoso A. Nastasi G. Micali A. Prestipino V. Vaccaro M. et al. (2011) Hyaluronan reduces inflammation in experimental arthritis by modulating TLR-2 and TLR-4 cartilage expression. Biochim Biophys Acta 1812: 1170–1181.
17. Chevalier X. Giraudeau B. Conrozier T. Marliere J. Kiefer P. Goupille P. (2005) Safety study of intraarticular injection of interleukin 1 receptor antagonist in patients with painful knee osteoarthritis: a multicenter study. J Rheumatol 32: 1317–1323.
18. Cho S. Sim J. Jeong C. Chang S. Choi D. Toida T. et al. (2004) Effects of low molecular weight chondroitin sulfate on type II collagen-induced arthritis in DBA/1J mice. Biol Pharm Bull 27: 47–51.
19. Christensen R. Bartels E. Astrup A. Bliddal H. (2008) Symptomatic efficacy of avocado-soybean unsaponifiables (ASU) in osteoarthritis (OA) patients: a meta-analysis of randomized controlled trials. Osteoarthritis Cartilage 16: 399–408.
20. Csaki C. Mobasheri A. Shakibaei M. (2009) Synergistic chondroprotective effects of curcumin and resveratrol in human articular chondrocytes: inhibition of IL-1β-induced NF-kappab-mediated inflammation and apoptosis. Arthritis Res Ther 11: R165.
21. Cui X. Xu H. Zhou S. Zhao T. Liu A. Guo X. et al. (2009) Evaluation of angiogenic activities of hyaluronan oligosaccharides of defined minimum size. Life Sci 85: 573–577.
22. Deberg M. Labasse A. Christgau S. Cloos P. Bang Henriksen D. Chapelle J. et al. (2005) New serum biochemical markers (Coll 2–1 and Coll 2–1 NO2) for studying oxidative-related type II collagen network degradation in patients with osteoarthritis and rheumatoid arthritis. Osteoarthritis Cartilage 13: 258–265.
23. de Boer T. van Spil W. Huisman A. Polak A. Bijlsma J. Lafeber F. et al. (2012) Serum adipokines in osteoarthritis; comparison with controls and relationship with local parameters of synovial inflammation and cartilage damage. Osteoarthritis Cartilage 20: 846–853.
24. de Lange-Brokaar B. Ioan-Facsinay A. van Osch G. Zuurmond A. Schoones J. Toes R. et al. (2012) Synovial inflammation, immune cells and their cytokines in osteoarthritis: a review. Osteoarthritis Cartilage 20: 1484–1499.
25. Fernand V. Losso J. Truax R. Villar E. Bwambok D. Fakayode S. et al. (2011) Rhein inhibits angiogenesis and the viability of hormone-dependent and -independent cancer cells under normoxic or hypoxic conditions in vitro. Chem Biol Interact 192: 220–232.
26. Gao W. Sweeney C. Walsh C. Rooney P. Mccormick J. Veale D. et al. (2013) Notch signalling pathways mediate synovial angiogenesis in response to vascular endothelial growth factor and angiopoietin 2. Ann Rheum Dis 72: 1080–1088.
27. Giatromanolaki A. Sivridis E. Maltezos E. Athanassou N. Papazoglou D. Gatter K. et al. (2003) Upregulated hypoxia inducible factor-1α and -2α pathway in rheumatoid arthritis and osteoarthritis. Arthritis Res Ther 5: R193–R201
28. Gok M. Erdem H. Gogus F. Yilmaz S. Karadag O. Simsek I. et al. (2013) Relationship of Ultrasonographic findings with synovial angiogenesis modulators in different forms of knee arthritides. Rheumatol Int 33: 879–885.
29. Goldring M. Otero M. Plumb D. Dragomir C. Favero M. El Hachem K. et al. (2011) Roles of inflammatory and anabolic cytokines in cartilage metabolism: signals and multiple effectors converge upon MMP-13 regulation in osteoarthritis. Eur Cell Mater 21: 202–220.
30. Gonzalez-Alvaro I. Ortiz A. Alvaro-Gracia J. Castaneda S. Diaz-Sanchez B. Carvajal I. et al. (2011) Interleukin 15 levels in serum may predict a severe disease course in patients with early arthritis. PloS ONE 6: e29492.
31. Griffith E. Su Z. Turk B. Chen S. Chang Y. Wu Z. et al. (1997) Methionine aminopeptidase (type 2) is the common target for angiogenesis inhibitors AGM-1470 and ovalicin. Chem Biol 4: 461–471.
32. Grosios K. Wood J. Esser R. Raychaudhuri A. Dawson J. (2004) Angiogenesis inhibition by the novel VEGF receptor tyrosine kinase inhibitor, PTK787/ZK222584, causes significant anti-arthritic effects in models of rheumatoid arthritis. Inflamm Res 53: 133–142.
33. Gullo F. de Bari C. (2013) Prospective purification of a subpopulation of human synovial mesenchymal stem cells with enhanced chondro-osteogenic potency. Rheumatology 52: 1758–68.
34. Henrotin Y. Lambert C. Couchourel D. Ripoll C. Chiotelli E. (2011) Nutraceuticals: Do they represent a new era in the management of osteoarthritis? A narrative review from the lessons taken with five products. Osteoarthritis Cartilage 19: 1–21.
35. Henrotin Y. Mathy M. Sanchez C. Lambert C. (2010) Chondroitin sulfate in the treatment of osteoarthritis: from in vitro studies to clinical recommendations. Ther Adv Musculoskelet Dis 2: 335–348.
36. Henrotin Y. Mobasheri A. Marty M. (2012) Is there any scientific evidence for the use of glucosamine in the management of human osteoarthritis? Arthritis Res Ther 14: 201.
37. Henrotin Y. Priem F. Mobasheri A. (2013) Curcumin: a new paradigm and therapeutic opportunity for the treatment of osteoarthritis: curcumin for osteoarthritis management. Springerplus 2: 56.
38. Hochberg M. Altman R. April K. Benkhalti M. Guyatt G. Mcgowan J. et al. (2012) American College of Rheumatology 2012 recommendations for the use of nonpharmacologic and pharmacologic therapies in osteoarthritis of the hand, hip, and knee. Arthritis Care Res 64: 465–474.
39. Honorati M. Bovara M. Cattini L. Piacentini A. Facchini A. (2002) Contribution of interleukin 17 to human cartilage degradation and synovial inflammation in osteoarthritis. Osteoarthritis Cartilage 10: 799–807.
40. Honorati M. Cattini L. Facchini A. (2007) VEGF production by osteoarthritic chondrocytes cultured in micromass and stimulated by IL-17 and TNF-Alpha. Connect Tissue Res 48: 239–245.
41. Hsieh J. Shen P. Shiau A. Jou I. Lee C. Wang C. et al. (2010) Intra-articular gene transfer of thrombospondin-1 suppresses the disease progression of experimental osteoarthritis. J Orthop Res 28: 1300–1306.
42. Kaspiris A. Mikelis C. Heroult M. Khaldi L. Grivas T. Kouvaras I. et al. (2013) Expression of the growth factor pleiotrophin and its receptor protein tyrosine phosphatase beta/zeta in the serum, cartilage and subchondral bone of patients with osteoarthritis. Joint Bone Spine:
43. Kennedy A. Ng C. Biniecka M. Saber T. Taylor C. O'sullivan J. et al. (2010) Angiogenesis and blood vessel stability in inflammatory arthritis. Arthritis Rheum 62: 711–721.
44. Kim H. Kim W. Cho M. Lee S. Youn J. Kim S. et al. (1999) Enhanced T cell proliferative response to type II collagen and synthetic peptide CII (255–274) in patients with rheumatoid arthritis. Arthritis Rheum 42: 2085–2093.
45. Kjaer B. Struve C. Friis T. Engel A. Beyer N. Hojrup P. et al. (2010) Synthesis and anti-angiogenic effect of conjugates between serum albumin and non-steroidal anti-inflammatory drugs. Protein Pept Lett 17: 121–130.
46. Kosinska M. Liebisch G. Lochnit G. Wilhelm J. Klein H. Kaesser U. et al. (2013) A lipidomic study of phospholipid classes and species in human synovial fluid. Arthritis Rheum:
47. Krenn V. Morawietz L. Burmester G. Kinne R. Mueller-Ladner U. Muller B. et al. (2006) Synovitis score: discrimination between chronic low-grade and high-grade synovitis. Histopathology 49: 358–364.
48. Kut-Lasserre C. Miller C. Ejeil A. Gogly B. Dridi M. Piccardi N. et al. (2001) Effect of Avocado and soybean unsaponifiables on gelatinase A (MMP-2), stromelysin 1 (MMP-3), and tissue inhibitors of matrix metalloproteinase (TIMP-1 and TIMP-2) secretion by human fibroblasts in culture. J Periodontol 72: 1685–1694.
49. Lainer-Carr D. Brahn E. (2007) Angiogenesis Inhibition as a therapeutic approach for inflammatory synovitis. Nat Clin Pract Rheumatol 3: 434–442.
50. Lambert C. Mathy-Hartert M. Dubuc J. Montell E. Verges J. Munaut C. et al. (2012) Characterization of synovial angiogenesis in osteoarthritis patients and its modulation by chondroitin sulfate. Arthritis Res Ther 14: R58.
51. Lazarus D. Doyle E. Bernier S. Rogers A. Labenski M. Wakefield J. et al. (2008) An inhibitor of methionine aminopeptidase type-2, PPI-2458, ameliorates the pathophysiological disease processes of rheumatoid arthritis. Inflamm Res 57: 18–27.
52. Lee J. Huh J. Jeon G. Yang H. Woo H. Choi D. et al. (2009) Flavonol-rich RVHxR from Rhus verniciflua Stokes and its major compound fisetin inhibits inflammation-related cytokines and angiogenic factor in rheumatoid arthritic fibroblast-like synovial cells and in vivo models. Int Immunopharmacol 9: 268–276.
53. Lee H. Magesh V. Nam D. Lee E. Ahn K. Jung M. et al. (2008) Shikonin, acetylshikonin, and isobutyroylshikonin inhibit VEGF-induced angiogenesis and suppress tumor growth in Lewis lung carcinoma-bearing mice. Yakugaku Zasshi 128: 1681–1688.
54. Lin Y. Huang Y. Fong Y. Tsai C. Chou M. Tang C. (2012) Hepatocyte growth factor increases vascular endothelial growth factor-A production in human synovial fibroblasts through C-met receptor pathway. PloS ONE 7: e50924.
55. Lu M. Chen P. Shih Y. Chang Y. Huang E. Liu C. et al. (2010) Alpha-chaconine inhibits angiogenesis in vitro by reducing matrix metalloproteinase-2. Biol Pharm Bull 33: 622–630.
56. Ludwig T. Mcallister J. Lun V. Wiley J. Schmidt T. (2012) Diminished cartilage-lubricating ability of human osteoarthritic synovial fluid deficient in proteoglycan 4: restoration through proteoglycan 4 supplementation. Arthritis Rheum 64: 3963–3971.
57. Magnano M. Chakravarty E. Broudy C. Chung L. Kelman A. Hillygus J. et al. (2007) A Pilot study of tumor necrosis factor inhibition in erosive/inflammatory osteoarthritis of the hands. J Rheumatol 34: 1323–1327.
58. Manley P. Martiny-Baron G. Schlaeppi J. Wood J. (2002) Therapies directed at vascular endothelial growth factor. Expert Opin Invest Drugs 11: 1715–1736.
59. Matou-Nasri S. Gaffney J. Kumar S. Slevin M. (2009) Oligosaccharides of hyaluronan induce angiogenesis through distinct CD 44 and rhamm-mediated signalling pathways involving CDC 2 and gamma-adducin. Int J Oncol 35: 761–773.
60. McNulty A. Rothfusz N. Leddy H. Guilak F. (2013) Synovial fluid concentrations and relative potency of interleukin-1 α and β in cartilage and meniscus degradation. J Orthop Res 31: 1039–1045.
61. Menendez-Gutierrez M. Roszer T. Ricote M. (2012) Biology and therapeutic applications of peroxisome proliferator-activated receptors. Curr Top Med Chem 12: 548–584.
62. Nakahara H. Song J. Sugimoto M. Hagihara K. Kishimoto T. Yoshizaki K. et al. (2003) Anti-interleukin-6 receptor antibody therapy reduces vascular endothelial growth factor production in rheumatoid arthritis. Arthritis Rheum 48: 1521–1529.
63. Omata T. Itokazu Y. Inoue N. Segawa Y. (2000) Effects of chondroitin sulfate-C on articular cartilage destruction in murine collagen-induced arthritis. Arzneimittelforschung 50: 148–153.
64. Pakneshan P. Birsner A. Adini I. Becker C. D'Amato R. (2008) Differential suppression of vascular permeability and corneal angiogenesis by nonsteroidal anti-inflammatory drugs. Invest Ophthalmol Vis Sci 49: 3909–3913.
65. Park D. Kim Y. Kim H. Kim K. Lee Y. Choe J. et al. (2012) Hyaluronic acid promotes angiogenesis by inducing RHAMM-TGFβ receptor interaction via CD44-PKCdelta. Mol Cells 33: 563–574.
66. Park Y. Kang Y. Butterfield J. Detmar M. Goronzy J. Weyand C. (2004) Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in rheumatoid arthritis. Am J Pathol 165: 2087–2098.
67. Pelletier J. Mineau F. Fernandes J. Duval N. Martel-Pelletier J. (1998) Diacerhein and rhein reduce the interleukin 1β stimulated inducible nitric oxide synthesis level and activity while stimulating cyclooxygenase-2 synthesis in human osteoarthritic chondrocytes. J Rheumatol 25: 2417–2424.
68. Pessler F. Dai L. Diaz-Torne C. Gomez-Vaquero C. Paessler M. Zheng D. et al. (2008) The synovitis of ‘non-inflammatory’ orthopaedic arthropathies: a quantitative histological and immunohistochemical analysis. Ann Rheum Dis 67: 1184–1187.
69. Rhee D. Marcelino J. Baker M. Gong Y. Smits P. Lefebvre V. et al. (2005) The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J Clin Invest 115: 622–631.
70. Riente L. Delle Sedie A. Filippucci E. Scire C. Iagnocco A. Gutierrez M. et al. (2010) Ultrasound imaging for the rheumatologist XXVII. Sonographic assessment of the knee in patients with rheumatoid arthritis. Clin Exp Rheumatol 28: 300–303.
71. Ritter S. Subbaiah R. Bebek G. Crish J. Scanzello C. Krastins B. et al. (2013) Proteomic analysis of synovial fluid from the osteoarthritic knee: comparison with transcriptome analyses of joint tissues. Arthritis Rheum 65: 981–992.
72. Salvado M. Alfranca A. Haeggstrom J. Redondo J. (2012) Prostanoids in tumor angiogenesis: therapeutic intervention beyond COX-2. Trends Mol Med 18: 233–243.
73. Sanchez C. Mathy-Hartert M. Deberg M. Ficheux H. Reginster J. Henrotin Y. (2003) Effects of rhein on human articular chondrocytes in alginate beads. Biochem Pharmacol 65: 377–388.
74. Scanzello C. Umoh E. Pessler F. Diaz-Torne C. Miles T. Dicarlo E. et al. (2009) Local Cytokine profiles in knee osteoarthritis: elevated synovial fluid interleukin-15 differentiates early from end-stage disease. Osteoarthritis Cartilage 17:1040–1048.
75. Sellam J. Berenbaum F. (2010) The Role of synovitis in pathophysiology and clinical symptoms of osteoarthritis. Nat Rev Rheumatol 6: 625–635.
76. Shakibaei M. John T. Seifarth C. Mobasheri A. (2007) Resveratrol inhibits IL-1β induced stimulation of caspase-3 and cleavage of PARP in human articular chondrocytes in vitro. Ann NY Acad Sci 1095: 554–563.
77. Shibakawa A. Aoki H. Masuko-Hongo K. Kato T. Tanaka M. Nishioka K. et al. (2003) Presence of pannus-like tissue on osteoarthritic cartilage and its histological character. Osteoarthritis Cartilage 11: 133–140.
78. Silver K. Desormaux A. Freeman L. Lillich J. (2012) Expression of pleiotrophin, an important regulator of cell migration, is inhibited in intestinal epithelial cells by treatment with non-steroidal anti-inflammatory drugs. Growth Factors 30: 258–266.
79. Slansky E. Li J. Haupl T. Morawietz L. Krenn V. Pessler F. (2010) Quantitative determination of the diagnostic accuracy of the synovitis score and its components. Histopathology 57: 436–443.
80. Sokolove J. Lepus C. (2013) Role of Inflammation in the pathogenesis of osteoarthritis: latest findings and interpretations. Ther Adv Musculoskelet Dis 5: 77–94.
81. Staikos C. Ververidis A. Drosos G. Manolopoulos V. Verettas D. Tavridou A. (2013) The association of adipokine levels in plasma and synovial fluid with the severity of knee osteoarthritis. Rheumatology 52: 1077–1083.
82. Stannus O. Jones G. Blizzard L. Cicuttini F. Ding C. (2013) Associations between serum levels of inflammatory markers and change in knee pain over 5 years in older adults: a prospective cohort study. Ann Rheum Dis 72: 535–540.
83. Szekanecz Z. Besenyei T. Paragh G. Koch A. (2010) New insights in synovial angiogenesis. Joint Bone Spine 77: 13–19.
84. Szekanecz Z. Koch A. (2001) Chemokines and angiogenesis. Curr Opin Rheumatol 13: 202–208.
85. Szekanecz Z. Koch A. (2008 a) Targeting angiogenesis in rheumatoid arthritis. Curr Rheumatol Rev 4: 298–303.
86. Szekanecz Z. Koch A. (2008 b) Vascular involvement in rheumatic diseases: ‘vascular rheumatology’. Arthritis Res Ther 10: 224.
87. Takeshita M. Nakamura J. Ohtori S. Inoue G. Orita S. Miyagi M. et al. (2012) Sensory innervation and inflammatory cytokines in hypertrophic synovia associated with pain transmission in osteoarthritis of the hip: a case-control study. Rheumatology 51: 1790–1795.
88. Tong Q. Qing Y. Shu D. He Y. Zhao Y. Li Y. et al. (2011) Deltonin, a steroidal saponin, inhibits colon cancer cell growth in vitro and tumor growth in vivo via induction of apoptosis and anti-angiogenesis. Cell Physiol Biochem 27: 233–242.
89. Vergunst C. van de Sande M. Lebre M. Tak P. (2005) The role of chemokines in rheumatoid arthritis and osteoarthritis. Scand J Rheumatol 34: 415–425.
90. Xi W. Zhou Y. Lv S. Gao Q. Bu G. Wang Y. et al. (2010) Plasma hyaluronan and collateral development in patients with coronary artery disease. Coron Artery Dis 21: 228–232.
91. Yanni S. Clark M. Yang R. Bingaman D. Penn J. (2010) The effects of nepafenac and amfenac on retinal angiogenesis. Brain Res Bull 81: 310–319.
92. Yaron M. Shirazi I. Yaron I. (1999) Anti-interleukin-1 effects of diacerein and rhein in human osteoarthritic synovial tissue and cartilage cultures. Osteoarthritis Cartilage 7: 272–280.
93. Zhang W. Doherty M. Arden N. Bannwarth B. Bijlsma J. Gunther K. et al. (2005) EULAR evidence based recommendations for the management of hip osteoarthritis: report of a task force of the EULAR Standing Committee for International Clinical Studies Including Therapeutics (ESCISIT). Ann Rheum Dis 64: 669–681.
94. Zhang W. Doherty M. Leeb B. Alekseeva L. Arden N. Bijlsma J. et al. (2007) EULAR evidence based recommendations for the management of hand osteoarthritis: report of a task force of the EULAR Standing Committee for International Clinical Studies Including Therapeutics (ESCISIT). Ann Rheum Dis 66: 377–388.
95. Zhang W. Doherty M. Peat G. Bierma-Zeinstra M. Arden N. Bresnihan B. et al. (2010) EULAR evidence-based recommendations for the diagnosis of knee osteoarthritis. Ann Rheum Dis 69: 483–489.
96. Zhang W. Moskowitz R. Nuki G. Abramson S. Altman R. Arden N. et al. (2008) OARSI recommendations for the management of hip and knee osteoarthritis, part II: OARSI evidence-based, expert consensus guidelines. Osteoarthritis Cartilage 16: 137–162.