Cartilage collagen damage in hip osteoarthritis similar to that seen in knee osteoarthritis; a case–control study of relationship between collagen, glycosaminoglycan and cartilage swelling

BMC Musculoskeletal Disorders

Leif E Dahlberg¹  Lisbeth R Lindberg¹  Shahrzad Hosseininia¹ 

[1]Department of Orthopaedics, Lund University, Skåne University Hospital, Malmö SE-205 02, Sweden

关键词: Hydration;    Glycosaminoglycan;    Collagen;    Osteoarthritis;    Hip;    Cartilage;   

Others  :  1134212
DOI  :  10.1186/1471-2474-14-18

 received in 2012-05-08, accepted in 2013-01-05,  发布年份 2013

【 摘 要 】

Background

It remains to be shown whether OA shares molecular similarities between different joints in humans. This study provides evidence for similarities in cartilage molecular damage in osteoarthritic (OA) joints.

Methods

Articular cartilage from osteoarthritic hip joints were analysed and compared to non-OA controls regarding collagen, glycosaminoglycan and water content. Femoral heads from 16 osteoarthritic (OA) and 20 reference patients were obtained from hip replacement surgery due to OA and femoral neck fracture, respectively. Cartilage histological changes were assessed by Mankin grading and denatured collagen type II immunostaining and cartilage was extracted by α-chymotrypsin. Hydroxyproline and Alcian blue binding assays were used to measure collagen and glycosaminoglycan (GAG) content, respectively.

Results

Mankin and immunohistology scores were significantly higher in hip OA samples than in reference samples. Cartilage water content was 6% higher in OA samples than in references. 2.5 times more collagen was extracted from OA than from reference samples. There was a positive association between water content and percentage of extractable collagen pool (ECP) in both groups. The amounts of collagen per wet and dry weights did not differ statistically between OA and reference cartilage. % Extractable collagen was not related to collagen per dry weight in either group. However when collagen was expressed by wet weight there was a negative correlation between % extractable and collagen in OA cartilage. The amount of GAG per wet weight was similar in both groups but the amount of GAG per dry weight was higher in OA samples compared to reference samples, which suggests a capacity for GAG biosynthesis in hip OA cartilage. Neither of the studied parameters was related to age in either group.

Conclusions

Increased collagen extractability and water content in human hip cartilage is associated with OA pathology and can be observed at early stages of the degenerative hip OA process. Our results suggest a common degradative pathway of collagen in articular cartilage of different joints. Furthermore, the study suggests that biochemical changes precede more overt OA changes and that chondrocytes may have a capability to compensate molecular loss in the early phase of OA.

【 授权许可】

   
2013 Hosseininia et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Roos H, Lauren M, Adalberth T, Roos EM, Jonsson K, Lohmander LS: Knee osteoarthritis after meniscectomy: prevalence of radiographic changes after twenty-one years, compared with matched controls. Arthritis Rheum 1998, 41:687-693.
• [2]Felson DT, Lawrence RC, Dieppe PA, Hirsch R, Helmick CG, Jordan JM, Kington RS, Lane NE, Nevitt MC, Zhang Y, et al.: Osteoarthritis: new insights. Part 1: the disease and its risk factors. Ann Intern Med 2000, 133:635-646.
• [3]Thorstensson CA, Petersson IF, Jacobsson LT, Boegard TL, Roos EM: Reduced functional performance in the lower extremity predicted radiographic knee osteoarthritis five years later. Ann Rheum Dis 2004, 63:402-407.
• [4]Jacobsen S, Sonne-Holm S: Hip dysplasia: a significant risk factor for the development of hip osteoarthritis. A cross-sectional survey. Rheumatology (Oxford) 2005, 44:211-218.
• [5]Vingard E, Alfredsson L, Goldie I, Hogstedt C: Occupation and osteoarthrosis of the hip and knee: a register-based cohort study. Int J Epidemiol 1991, 20:1025-1031.
• [6]Brandt KD, Dieppe P, Radin E: Etiopathogenesis of osteoarthritis. Med Clin North Am 2009, 93:1-24. xv
• [7]Oliveria SA, Felson DT, Reed JI, Cirillo PA, Walker AM: Incidence of symptomatic hand, hip, and knee osteoarthritis among patients in a health maintenance organization. Arthritis Rheum 1995, 38:1134-1141.
• [8]Eyre DR, Weis MA, Wu JJ: Articular cartilage collagen: an irreplaceable framework? Eur Cell Mater 2006, 12:57-63.
• [9]Venn M, Maroudas A: Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. I. Chemical composition. Ann Rheum Dis 1977, 36:121-129.
• [10]Tiderius CJ, Olsson LE, Leander P, Ekberg O, Dahlberg L: Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis. Magn Reson Med 2003, 49:488-492.
• [11]Ericsson YB, Tjornstrand J, Tiderius CJ, Dahlberg LE: Relationship between cartilage glycosaminoglycan content (assessed with dGEMRIC) and OA risk factors in meniscectomized patients. Osteoarthritis Cartilage 2009, 17:565-570.
• [12]Poole AR: Cartilage in health and disease. In Arthritis and allied conditions. A textbook of rheumatology. Edited by Koopman W. Baltimore: Williams and Wilkins; 2000:226-284.
• [13]Nelson F, Dahlberg L, Laverty S, Reiner A, Pidoux I, Ionescu M, Fraser GL, Brooks E, Tanzer M, Rosenberg LC, et al.: Evidence for altered synthesis of type II collagen in patients with osteoarthritis. J Clin Invest 1998, 102:2115-2125.
• [14]Heathfield TF, Onnerfjord P, Dahlberg L, Heinegard D: Cleavage of fibromodulin in cartilage explants involves removal of the N-terminal tyrosine sulfate-rich region by proteolysis at a site that is sensitive to matrix metalloproteinase-13. J Biol Chem 2004, 279:6286-6295.
• [15]Woessner JF Jr: The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 1961, 93:440-447.
• [16]Bank RA, Krikken M, Beekman B, Stoop R, Maroudas A, Lafeber FP, te Koppele JM: A simplified measurement of degraded collagen in tissues: application in healthy, fibrillated and osteoarthritic cartilage. Matrix Biol 1997, 16:233-243.
• [17]Riley GP, Curry V, DeGroot J, van El B, Verzijl N, Hazleman BL, Bank RA: Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology. Matrix Biol 2002, 21:185-195.
• [18]Hollander AP, Heathfield TF, Webber C, Iwata Y, Bourne R, Rorabeck C, Poole AR: Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay. J Clin Invest 1994, 93:1722-1732.
• [19]Hollander AP, Pidoux I, Reiner A, Rorabeck C, Bourne R, Poole AR: Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration. J Clin Invest 1995, 96:2859-2869.
• [20]Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorabeck C, Mitchell P, Hambor J, Diekmann O, Tschesche H, et al.: Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest 1997, 99:1534-1545.
• [21]Mankin HJ, Dorfman H, Lippiello L, Zarins A: Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 1971, 53:523-537.
• [22]Stegemann H, Stalder K: Determination of hydroxyproline. Clin Chim Acta 1967, 18:267-273.
• [23]Poole AR, Nelson F, Dahlberg L, Tchetina E, Kobayashi M, Yasuda T, Laverty S, Squires G, Kojima T, Wu W, et al.: Proteolysis of the collagen fibril in osteoarthritis. Biochem Soc Symp 2003, 70:115-123.
• [24]Theocharis AD, Karamanos NK, Papageorgakopoulou N, Tsiganos CP, Theocharis DA: Isolation and characterization of matrix proteoglycans from human nasal cartilage. Compositional and structural comparison between normal and scoliotic tissues. Biochim Biophys Acta 2002, 1569:117-126.
• [25]Bjornsson S: Simultaneous preparation and quantitation of proteoglycans by precipitation with alcian blue. Anal Biochem 1993, 210:282-291.
• [26]Rizkalla G, Reiner A, Bogoch E, Poole AR: Studies of the articular cartilage proteoglycan aggrecan in health and osteoarthritis. Evidence for molecular heterogeneity and extensive molecular changes in disease. J Clin Invest 1992, 90:2268-2277.
• [27]Basser PJ, Schneiderman R, Bank RA, Wachtel E, Maroudas A: Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. Arch Biochem Biophys 1998, 351:207-219.
• [28]Calvo E, Palacios I, Delgado E, Ruiz-Cabello J, Hernandez P, Sanchez-Pernaute O, Egido J, Herrero-Beaumont G: High-resolution MRI detects cartilage swelling at the early stages of experimental osteoarthritis. Osteoarthritis Cartilage 2001, 9:463-472.
• [29]McDevitt C, Gilbertson E, Muir H: An experimental model of osteoarthritis; early morphological and biochemical changes. J Bone Joint Surg Br 1977, 59:24-35.
• [30]Bank RA, Soudry M, Maroudas A, Mizrahi J, TeKoppele JM: The increased swelling and instantaneous deformation of osteoarthritic cartilage is highly correlated with collagen degradation. Arthritis Rheum 2000, 43:2202-2210.
• [31]Hollander AP, Heathfield TF, Liu JJ, Pidoux I, Roughley PJ, Mort JS, Poole AR: Enhanced denaturation of the alpha (II) chains of type-II collagen in normal adult human intervertebral discs compared with femoral articular cartilage. J Orthop Res 1996, 14:61-66.
• [32]Eyre DR, McDevitt CA, Billingham ME, Muir H: Biosynthesis of collagen and other matrix proteins by articular cartilage in experimental osteoarthrosis. Biochem J 1980, 188:823-837.
• [33]Vignon E, Arlot M, Hartmann D, Moyen B, Ville G: Hypertrophic repair of articular cartilage in experimental osteoarthrosis. Ann Rheum Dis 1983, 42:82-88.
• [34]Adams ME, Brandt KD: Hypertrophic repair of canine articular cartilage in osteoarthritis after anterior cruciate ligament transection. J Rheumatol 1991, 18:428-435.
• [35]Johnson LC: Kinetics of osteoarthritis. Lab Invest 1959, 8:1223-1241.
• [36]Braunstein EM, Brandt KD, Albrecht M: MRI demonstration of hypertrophic articular cartilage repair in osteoarthritis. Skeletal Radiol 1990, 19:335-339.
• [37]Le Graverand MP, Buck RJ, Wyman BT, Vignon E, Mazzuca SA, Brandt KD, Piperno M, Charles HC, Hudelmaier M, Hunter DJ, et al.: Change in regional cartilage morphology and joint space width in osteoarthritis participants versus healthy controls: a multicentre study using 3.0 Tesla MRI and Lyon-Schuss radiography. Ann Rheum Dis 2010, 69:155-162.
• [38]Nelson F, Billinghurst RC, Pidoux I, Reiner A, Langworthy M, McDermott M, Malogne T, Sitler DF, Kilambi NR, Lenczner E, et al.: Early post-traumatic osteoarthritis-like changes in human articular cartilage following rupture of the anterior cruciate ligament. Osteoarthritis Cartilage 2006, 14:114-119.
• [39]Tiderius CJ, Svensson J, Leander P, Ola T, Dahlberg L: dGEMRIC (delayed gadolinium-enhanced MRI of cartilage) indicates adaptive capacity of human knee cartilage. Magn Reson Med 2004, 51:286-290.
• [40]Grushko G, Schneiderman R, Maroudas A: Some biochemical and biophysical parameters for the study of the pathogenesis of osteoarthritis: a comparison between the processes of ageing and degeneration in human hip cartilage. Connect Tissue Res 1989, 19:149-176.
• [41]Aigner T, Rose J, Martin J, Buckwalter J: Aging theories of primary osteoarthritis: from epidemiology to molecular biology. Rejuvenation Res 2004, 7:134-145.
• [42]van der Kraan PM, van den Berg WB: Osteoarthritis in the context of ageing and evolution. Loss of chondrocyte differentiation block during ageing. Ageing Res Rev 2008, 7:106-113.
• [43]Hudelmaier M, Glaser C, Hohe J, Englmeier KH, Reiser M, Putz R, Eckstein F: Age-related changes in the morphology and deformational behavior of knee joint cartilage. Arthritis Rheum 2001, 44:2556-2561.
• [44]Howell DS: Aging in Osteoarthritis: Osteoarthrosis or Degenerative Joint Disease. In Aging, Immunity and Arthritic Disease. Edited by Kay MMB, Galpin J, Makinodan T. New York: Raven Press; 1980:135-150.
• [45]Brandt KD, Fife RS: Ageing in relation to the pathogenesis of osteoarthritis. Clin Rheum Dis 1986, 12:117-130.
• [46]Burkhardt D, Michel BA, Baici A, Kissling R, Theiler R: Comparison of chondroitin sulphate composition of femoral head articular cartilage from patients with femoral neck fractures and osteoarthritis and controls. Rheumatol Int 1995, 14:235-241.
• [47]Maroudas A, Evans H, Almeida L: Cartilage of the hip joint. Topographical variation of glycosaminoglycan content in normal and fibrillated tissue. Ann Rheum Dis 1973, 32:1-9.