Collagen type II solution extracted from supercritical carbon dioxide decellularized porcine cartilage: regenerative efficacy on post-traumatic osteoarthritis model

Srinivasan Periasamy , Yun-Ju Chen , Dur-Zong Hsu , Dar-Jen Hsieh

Bioresources and Bioprocessing ›› 2024, Vol. 11 ›› Issue (1) : 21

PDF
Bioresources and Bioprocessing ›› 2024, Vol. 11 ›› Issue (1) : 21 DOI: 10.1186/s40643-024-00731-1
Research

Collagen type II solution extracted from supercritical carbon dioxide decellularized porcine cartilage: regenerative efficacy on post-traumatic osteoarthritis model

Author information +
History +
PDF

Abstract

Osteoarthritis (OA) of the knee is a common degenerative articular disorder and is one of the main causes of pain and functional disability. Cartilage damage is frequently linked to elevated osteoarthritis incidence. Supercritical carbon dioxide (scCO2) decellularized cartilage graft produced from the porcine cartilage is an ideal candidate for cartilage tissue engineering. In the present study, we derived collagen type II (Col II) solution from the scCO2 decellularized porcine cartilage graft (dPCG) and compared its efficacy with hyaluronic acid (HA) in the surgical medial meniscectomy (MNX) induced post-traumatic osteoarthritis (PTOA) model. Dose-dependent attenuation of the OA (12.3 ± 0.8) progression was observed in the intra‐articular administration of Col II solution (7.3 ± 1.2) which significantly decreased the MNX-induced OA symptoms similar to HA. The pain of the OA group (37.4 ± 2.7) was attenuated dose-dependently by Col II solution (45.9 ± 4.1) similar to HA (43.1 ± 3.5) as evaluated by a capacitance meter. Micro‐CT depicted a dose-dependent attenuation of articular cartilage damage by the Col II solution similar to HA treatment. A significant (p < 0.001) dose-dependent elevation in the bone volume was also observed in Col II solution-treated OA animals. The protective competence of Col II solution on articular cartilage damage is due to its significant (p < 0.001) increase in the expression of type II collagen, aggrecan and SOX‐9 similar to HA. To conclude, intra‐articular administration of type II collagen solution and HA reestablished the injured cartilage and decreased osteoarthritis progression in the experimental PTOA model.

Keywords

Type II collagen solution / Supercritical carbon dioxide (scCO2) / Decellularized porcine cartilage graft (dPCG) / Medial meniscectomy (MNX) / Osteoarthritis (OA)

Cite this article

Download citation ▾
Srinivasan Periasamy, Yun-Ju Chen, Dur-Zong Hsu, Dar-Jen Hsieh. Collagen type II solution extracted from supercritical carbon dioxide decellularized porcine cartilage: regenerative efficacy on post-traumatic osteoarthritis model. Bioresources and Bioprocessing, 2024, 11(1): 21 DOI:10.1186/s40643-024-00731-1

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Amin AK, Simpson AHRW, Hall AC. Iatrogenic articular cartilage injury: the elephant in the operating theatre: the surgeons' role in chondroprotection. Bone Joint J, 2017, 99-B(12): 1555-1556.

[2]

Anonymous WHO. Chronic rheumatic conditions WHO, 2016, Geneva: World Health Organization, 1.

[3]

Antons J, Marascio MG, Aeberhard P, . Decellularised tissues obtained by a CO2-philic detergent and supercritical CO2. Eur Cells Mater, 2018, 36: 81-95.

[4]

Ashraf S, Mapp PI, Shahtaheri SM, Walsh DA. Effects of carrageenan induced synovitis on joint damage and pain in a rat model of knee osteoarthritis. Osteoarthr Cartil, 2018, 26(10): 1369-1378.

[5]

Bansal S, Miller LM, Patel JM, . Transection of the medial meniscus anterior horn results in cartilage degeneration and meniscus remodeling in a large animal model. J Orthop Res, 2020, 38(12): 2696-2708.

[6]

Barbour KE, Helmick CG, Boring M, Brady TJ. Vital signs: prevalence of doctor-diagnosed arthritis and arthritis-attributable activity limitation—United States, 2013–2015. MMWR Morb Mortal Wkly Rep, 2017, 66(9): 246-253.

[7]

Brown TD, Johnston RC, Saltzman CL, Marsh JL, Buckwalter JA. Posttraumatic osteoarthritis: a first estimate of incidence, prevalence, and burden of disease. J Orthop Trauma, 2006, 20(10): 739-744.

[8]

Chu JG, Dai MW, Wang Y, . Strontium ranelate causes osteophytes overgrowth in a model of early phase osteoarthritis. BMC Musculoskelet Disord, 2017, 18(1): 78.

[9]

Conduah AH, Baker CL. Managing joint pain in osteoarthritis: safety and efficacy of hylan G-F 20. J Pain Res, 2009, 2: 87-98.

[10]

Cox LG, van Rietbergen B, van Donkelaar CC, Ito K. Bone structural changes in osteoarthritis as a result of mechanoregulated bone adaptation: a modeling approach. Osteoarthr Cartil, 2011, 19: 676-682.

[11]

Crowley DC, Lau FC, Sharma P, . Safety and efficacy of undenatured type II collagen in the treatment of osteoarthritis of the knee: a clinical trial. Int J Med Sci, 2009, 6: 312-321.

[12]

Davis AM, Lohmander LS, Wong R, Venkataramanan V, Hawker GA. Evaluating the responsiveness of the ICOAP following hip or knee replacement. Osteoarthr Cartil, 2010, 18: 1043-1045.

[13]

Deparle LA, Gupta RC, Canerdy TD, . Efficacy and safety of glycosylated undenatured type-II (UC-II) collagen in therapy of arthritic dogs. J Vet Pharmacol Ther, 2005, 28: 385-390.

[14]

Dieppe PA, Lohmander LS. Pathogenesis and management of pain in osteoarthritis. Lancet, 2005, 365(9463): 965e73.

[15]

Duarte MM, Silva IV, Eisenhut AR, . Contributions of supercritical fluid technology for advancing decellularization and postprocessing of viable biological materials. Mater Horizons, 2022, 9(3): 864-891.

[16]

Gupta RC, Bagchi D, Skaggs P, . Therapeutic efficacy of undenatured type-II collagen (UC-II) in comparison to glucosamine and chondroitin in arthritic horses. J Vet Pharmacol Ther, 2009, 32: 577-584.

[17]

Han Y, Zhang B, Li J, . Preparation of extracellular matrix of fish swim bladders by decellularization with supercritical carbon dioxide. Bioresour Bioprocess, 2023, 10(1): 14.

[18]

Hawker, G (2016) Osteoarthritis: a serious disease Osteoarthris Research Society International 2016. https://www.oarsi.org/research/oa-serious-disease. https://oarsi.org/sites/oarsi/files/docs/2016/oarsi_white_paper_oa_serious_disease_121416_1.pdf. Accessed 3 April 2023

[19]

Hill CL, Hunter DJ, Niu J, . Synovitis detected on magnetic resonance imaging and its relation to pain and cartilage loss in knee osteoarthritis. Ann Rheum Dis, 2007, 66(12): 1599e603.

[20]

Hsieh DJ, Srinivasan P. Protocols for accelerated production and purification of collagen scaffold and atelocollagen from animal tissues. Biotechniques, 2020, 69(3): 220-225.

[21]

Hsu YH, Hsieh PP, Chang MS. Interleukin-19 blockade attenuates collagen-induced arthritis in rats. Rheumatology, 2012, 51: 434-442.

[22]

Huebner JL, Williams JM, Deberg M, Henrotin Y, Kraus VB. Collagen fibril disruption occurs early in primary guinea pig knee osteoarthritis. Osteoarthr Cartil, 2010, 18(3): 397-405.

[23]

Jordan JM, Helmick CG, Renner JB, . Prevalence of knee symptoms and radiographic and symptomatic knee osteoarthritis in African Americans and Caucasians: the Johnston County Osteoarthritis project. J Rheumatol, 2007, 34(1): 172.

[24]

Katz JN, Arant KR, Loeser RF. Diagnosis and treatment of hip and knee osteoarthritis: a review. JAMA, 2021, 325(6): 568-578.

[25]

Kiani C, Chen L, Wu YJ, Yee AJ, Yang BB. Structure and function of aggrecan. Cell Res, 2002, 12(1): 19-32.

[26]

Kim JE, Song DH, Kim SH, Jung Y, Kim SJ. Development and characterization of various osteoarthritis models for tissue engineering. PLoS ONE, 2018, 13(3): e0194288.

[27]

Kocak D, Annaswamy T, Chong S, Arora R. Development of systemic inflammatory polyarthritis after zygapophyseal joint injection with hylan G-F 20 (Synvisc-One). Am J Phys Med Rehabil, 2018, 97(2): 147-149.

[28]

Kroesen S, Schmid W, Theiler R. Induction of an acute attack of calcium pyrophosphate dihydrate arthritis by intra-articular injection of hylan G-F 20 (Synvisc). Clin Rheumatol, 2000, 19: 147-149.

[29]

Loeser RF, Goldring SR, Scanzello CR, Goldring MB. Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum, 2012, 64(6): 1697-1707.

[30]

Losina E, Weinstein AM, Reichmann WM, . Lifetime risk and age at diagnosis of symptomatic knee osteoarthritis in the US. Arthritis Care Res, 2013, 65(5): 703-711.

[31]

Malfait AM, Little CB, McDougall JJ. A commentary on modelling osteoarthritis pain in small animals. Osteoarthr Cartil, 2013, 21: 1316-1326.

[32]

Mannelli LDC, Micheli L, Zanardelli M, Ghelardini C. Low dose native type II collagen prevents pain in a rat osteoarthritis model. BMC Musculoskelet Disord, 2013, 14: 228.

[33]

Mapp PI, Avery PS, McWilliams DF, . Angiogenesis in two animal models of osteoarthritis. Osteoarthr Cartil, 2008, 16(1): 61e9.

[34]

Mapp PI, Sagar DR, Ashraf S, . Differences in structural and pain phenotypes in the sodium monoiodoacetate and meniscal transection models of osteoarthritis. Osteoarthr Cartil, 2013, 21(9): 1336-1345.

[35]

Michou L, Job-Deslandre C, de Pinieux G, Kahan A. Granulomatous synovitis after intraarticular hylan GF-20. A report of two cases. Joint Bone Spine, 2004, 71: 438-440.

[36]

Migliore A, Giovannangeli F, Granata M, Laganà B. Hylan g-f 20: review of its safety and efficacy in the management of joint pain in osteoarthritis. Clin Med Insights Arthritis Musculoskelet Disord, 2010, 3: 55-68.

[37]

Nees TA, Rosshirt N, Zhang JA, . Synovial cytokines significantly correlate with osteoarthritis-related knee pain and disability: inflammatory mediators of potential clinical relevance. J Clin Med, 2019, 8(9): 1343.

[38]

Neogi T, Guermazi A, Roemer F, . Association of joint inflammation with pain sensitization in knee osteoarthritis: the multicenter osteoarthritis study. Arthritis Rheumatol, 2016, 68: 654e61.

[39]

O'Brien MS, McDougall JJ. Neurophysiological assessment of joint nociceptors in the rat medial meniscus transection model of post-traumatic osteoarthritis. Osteoarthr Cartil, 2020, 28: 1255-1264.

[40]

Orfanidou T, Iliopoulos D, Malizos KN, Tsezou A. Involvement of SOX-9 and FGF-23 in RUNX-2 regulation in osteoarthritic chondrocytes. J Cell Mol Med, 2009, 13(9B): 3186-3194.

[41]

Ouyang Y, Wang W, Tu B, Zhu Y, Fan C, Li Y. Overexpression of SOX9 alleviates the progression of human osteoarthritis in vitro and in vivo. Drug Des Devel Ther, 2019, 13: 2833-2842.

[42]

Philpott HT, O’Brien M, McDougall JJ. Attenuation of early phase inflammation by cannabidiol prevents pain and nerve damage in rat osteoarthritis. Pain, 2017, 158: 2442-2451.

[43]

Proffen BL, Sieker JT, Murray MM, . Extracellular matrix-blood composite injection reduces post-traumatic osteoarthritis after anterior cruciate ligament injury in the rat. J Orthop Res, 2016, 34(6): 995-1003.

[44]

Pucha KA, McKinney JM, Fuller JM, Willett NJ. Characterization of OA development between sexes in the rat medial meniscal transection model. Osteoarthr Cartil Open, 2020, 2(3): 100066.

[45]

Ross JR, Larson CM, Bedi A. Indications for Hip Arthroscopy. Sports. Health, 2017, 9(5): 402-413.

[46]

Roughley PJ, Mort JS. The role of aggrecan in normal and osteoarthritic cartilage. J Exp Orthop, 2014, 1(1): 8.

[47]

Sambamurthy N, Zhou C, Nguyen V, . Deficiency of the pattern-recognition receptor CD14 protects against joint pathology and functional decline in a murine model of osteoarthritis. PLoS ONE, 2018, 13(11): 1-25.

[48]

Scanzello CR, Goldring SR. The role of synovitis in osteoarthritis pathogenesis. Bone, 2012, 51: 249-257.

[49]

Srikanth VK, Fryer JL, Zhai G, Winzenberg TM, Hosmer D, Jones G. A metaanalysis of sex differences prevalence, incidence and severity of osteoarthritis. Osteoarthr Cartil, 2005, 413(9): 769-781.

[50]

Sung SY, Lin YW, Wu CC, . Supercritical carbon dioxide-decellularized arteries exhibit physiologic-like vessel regeneration following xenotransplantation in rats. Biomater Sci, 2023, 11(7): 2566-2580.

[51]

Suri S, Gill SE, Massena de Camin S, Wilson D, McWilliams DF, Walsh DA. Neurovascular invasion at the osteochondral junction and in osteophytes in osteoarthritis. Ann Rheum Dis, 2007, 66(11): 1423e8.

[52]

Tawonsawatruk T, Sriwatananukulkit O, Himakhun W, Hemstapat W. Comparison of pain behaviour and osteoarthritis progression between anterior cruciate ligament transection and osteochondral injury in rat models. Bone Joint Res, 2018, 7(3): 244-251.

[53]

Walsh DA, Yousef A, McWilliams DF, Hill R, Hargin E, Wilson D. Evaluation of a photographic chondropathy score (PCS) for pathological samples in a study of inflammation in tibiofemoral osteoarthritis. Osteoarthr Cartil, 2009, 17: 304-312.

[54]

Wang X, Hunter DJ, Jin X, Ding C. The importance of synovial inflammation in osteoarthritis: current evidence from imaging assessments and clinical trials. Osteoarthr Cartil, 2018, 26: 165e74.

[55]

Wei W, Zhang LL, Xu JH, . A multicenter, double-blind, randomized, controlled phase III Clinical trial of chicken type II collagen in rheumatoid arthritis. Arthritis Res Ther, 2009, 11: 180.

[56]

Wu CC, Tarng YW, Hsu DZ, . Supercritical carbon dioxide decellularized porcine cartilage graft with PRP attenuated OA progression and regenerated articular cartilage in ACLT-induced OA rats. J Tissue Eng Regen Med, 2021, 15: 1118-1130.

[57]

Wysocka-Skurska I, Sierakowska M, Kułak W. Evaluation of quality of life in chronic, progressing rheumatic diseases based on the example of osteoarthritis and rheumatoid arthritis. Clin Interv Aging, 2016, 11: 1741-1750.

[58]

Xu Y, Dai GJ, Liu Q, Liu ZL, Song ZQ, Li L, Chen WH, Lin N. Sanmiao formula inhibits chondrocyte apoptosis and cartilage matrix degradation in a rat model of osteoarthritis. Exp Ther Med, 2014, 8(4): 1065-1074.

[59]

Yan Z, Qi W, Zhan J, . Activating Nrf2 signalling alleviates osteoarthritis development by inhibiting inflammasome activation. J Cell Mol Med, 2020, 24(22): 13046-13057.

[60]

You L, Weikang X, Lifeng Y, . In vivo immunogenicity of bovine bone removed by a novel decellularization protocol based on supercritical carbon dioxide. Artif Cells Nanomed Biotechnol, 2018, 46(sup2): 334-344.

[61]

Yu DG, Ding HF, Mao YQ, . Strontium ranelate reduces cartilage degeneration and subchondral bone remodeling in a rat osteoarthritis model. Acta Pharmacol Sin, 2013, 34: 393-402.

[62]

Zhang W, Nuki G, Moskowitz RW, . OARSI recommendations for the management of hip and knee osteoarthritis Part III: changes in evidence following systematic cumulative update of research published through January 2009. Osteoarthr Cartil, 2010, 18(4): 476-499.

AI Summary AI Mindmap
PDF

173

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/