Intra-articular hyaluronic acid: dependence of the effect on molecular weight
DOI: 10.32364/2587-6821-2021-5-3-156-161
Yu.S. Filatova, V.R. Gawert
Yaroslavl State Medical University, Yaroslavl, Russian Federation
The article discusses the patient management with knee osteoarthritis according to the ESCEO 2019 algorithm. The focus is on the second stage in the persistence of osteoarthritis signs. The article pays attention to the means based on hyaluronic acid for intra-articular injection. It also provides the study analysis that proved the anti-inflammatory mechanism of action of hyaluronic acid-based drugs during intra-articular administration, as well as the study results in which histology data indicated that hyaluronic acid prevents cartilage degradation and can promote its regeneration. These researches show that repeated injections of hyaluronic acid are not only effective, but also safe. In the literature, there is evidence that during treatment, the time to endoprosthesis increases, as well as the need for taking NSAIDs and opioids decreases. The article discusses the molecular weight of hyaluronic acid, providing research data confirming the greatest efficacy of hyaluronic ac id with medium and high molecular weight.
Keywords: osteoarthritis, knee joints, hyaluronic acid, intraarticular injection.
For citation: Filatova Yu.S., Gawert V.R. Intra-articular hyaluronic acid: dependence of the effect on molecular weight. Russian Medical Inquiry. 2021;5(3):156–161. DOI: 10.32364/2587-6821-2021-5-3-156-161.
Acknowledgement
Editorial Board is grateful to Sistema Plus JSC for the assistance in technical edition of this publication.
About the authors:
Yulia S. Filatova — Cand. of Sci. (Med.), Associate Professor of the Department of Therapy named after E.N. Dormidontov, Institute of Postgraduate Education, Yaroslavl State Medical University; 5, Revolyutsionnaya str., Yaroslavl, 150000, Russian Federation; ORCID iD 0000-0003-3024-9483.
Veronika R. Gawert — Cand. of Sci. (Med.), Assistant Professor of the Department of Therapy named after E.N. Dormidontov, Institute of Postgraduate Education, Yaroslavl State Medical University; 5, Revolyutsionnaya str., Yaroslavl, 150000, Russian Federation; ORCID iD 0000-0003-3024-9483.
Contact information: Yulia S. Filatova, e-mail: y.s.filatova@mail.ru.
Financial Disclosure: no authors have a financial or property interest in any material or method mentioned. There is no conflict of interests. Received 19.03.2021, revised 07.04.2021, accepted 22.04.2021.
References
1. Du Souich P. Absorption, distribution and mechanism of action of SYSADOAS. Pharmacol Ther. 2014;142(3):362–374. DOI: 10.1016/j.pharmthera.2014.01.002.
2. Мартынов А.И., Наумов А.В., Верткин А.Л. и др. Ведение больных с остеоартритом и коморбидностью в общей врачебной практике: мнение экспертов, основанное на доказательной медицине. Лечащий врач. 2015;04:39–46. [Martynov A.I., Naumov A.V., Vertkin A.L. et al. Management of patients with osteoarthritis and comorbidity in general medical practice: expert opinion based on evidence-based medicine. Lechashchiy vrach. 2015;04:39–46 (in Russ.)].
3. Hiligsmann M., Cooper C., Arden N. et al. Health economics in the field of osteoarthritis: an expert’s consensus paper from the European Society for Clinical and Economic Aspects of Osteoroporis and Osteoarthritis (ESCEO). Semin Arthritis Rheum. 2013;43(3):303–313. DOI: 10.1016/j.semarthrit.2013.
4. March L., Cross M., Lo C. et al. Osteoarthritis: A Serious Disease. Osteoarthritis Research Society International; 2016.
5. Bruyere O., Cooper C., Pelletier J.P. et al. An algorithm recommendation for the management of knee osteoarthritis in Europe and internationally: a report from a task force of the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO). Semin Arthritis Rheum. 2014;44(3):253–263. DOI: 10.1016/j.semarthrit.2014.05.014.
6. Bruyère O., Cooper C., Pelletier J.P. et al. A consensus statement on the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO) algorithm for the management of knee osteoarthritis-From evidence-based medicine to the real-life setting. Semin Arthritis Rheum. 2016;45(4 Suppl):S3–11. DOI: 10.1016/j.semarthrit.2015.11.010.
7. Bruyère O., Honvo G., Veronese N. et al. An updated algorithm recommendation for the management of knee osteoarthritis from the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO). Semin Arthritis Rheum. 2019;49(3):337–350. DOI: 10.1016/j.semarthrit.2019.04.008.
8. Chernos M., Grecov D., Kwok E. et al. Rheological study of hyaluronic acid derivatives. Biomed Eng Lett. 2017;7:17–24. DOI: 10.1007/s13534-017-0010-y.
9. Migliore А., Procopio S. Effectiveness and utility of hyaluronic acid in osteoarthritis. Clin Cases Miner Bone Metab. 2015;12:31–33. DOI: 10.11138/ccmbm/2015.12.1.031.
10. Moreland L.W. Intra-articular hyaluronan. (hyaluronic acid) and hyalans for the treatment of osteoarthritis: mechanism of action. Arthr Res Ther. 2003;5:54–67. DOI: 10.1186/ar623.
11. Bannuru R.R., Natov N.S., Dasi U.R. et al. Therapeutic trajectory following intra-articular hyaluronic acid injection in knee osteoarthritis-meta-analysis. Osteoarthr Cartil. 2011;19(6):611–619. DOI: 10.1016/j.joca.2010.09.014.
12. Liang J., Jiang D., Noble P.W. Hyaluronan as a therapeutic target in human diseases. Adv Drug Deliv Rev. 2016;97:186–203. DOI: 10.1016/j.addr.2015.10.017
13. Maheu E., Rannou F., Reginster J.Y. Efficacy and safety of hyaluronic acid in the management of osteoarthritis: evidence from real-life setting trials and surveys. Semin Arthritis Rheum. 2016;45(4 Suppl):S28–S33. DOI: 10.1016/j.semarthrit.2015.11.008.
14. Campo G.M., Avenoso A., Campo S. et al. Differential effect of molecular mass hyaluronan on lipopolysaccharide-induced damage in chondrocytes. Innate Immun. 2010;16:48–63. DOI: 10.1177/1753425909340419.
15. Jerosch J. Effects of glucosamine and chondroitin sulfate on cartilage metabolism in OA: outlook on other nutrient partners especially omega-3 fatty acids. Int J Rheumatol. 2011;2011:1–17. DOI: 10.1155/2011/969012.
16. Cooper C., Rannou F., Richette P. et al. Use of intraarticular hyaluronic acid in the Management of Knee Osteoarthritis in clinical practice. Arthritis Care Res (Hoboken). 2017;69(9):1287–1296. DOI: 10.1002/acr.23204.
17. Liu L., Ishijima M., Futami I. et al. Correlation between synovitis detected on enhanced-magnetic resonance imaging and a histological analysis with a patient-oriented outcome measure for Japanese patients with end-stage knee osteoarthritis receiving joint replacement surgery. Clin Rheumatol. 2010;16:1185–1190. DOI: 10.1007/s10067-010-1522-3.
18. Julovi S.M., Ito H., Nishitani K. et al. Hyaluronan inhibits matrix metalloproteinase-13 in human arthritic chondrocytes via CD44 and P38. J Orthop Res. 2011;16:258–264. DOI: 10.1002/jor.21216.
19. Goldberg V.M., Goldberg L. Intra-articular hyaluronans: the treatment of knee pain in osteoarthritis. J Pain Res. 2010;3:51–56. DOI: 10.2147/jpr.s4733.
20. Cook J.L., Hung C.T., Kuroki K. et al. Animal models of cartilage repair. Bone Joint Res. 2014;3(4):89–94. DOI:10.1302/2046–3758.34.2000238.
21. Carapeba G.O.L., Cavaleti P., Nicácio G.M. et al. Intra-articular hyaluronic acid compared to traditional conservative treatment in dogs with osteoarthritis associated with hip dysplasia. Evid-Based Compl Altern Med. 2016;2016:20726921. DOI: 10.1155/2016/2076921 256-259.
22. Petrella R.J., Wakeford С. Pain relief and improved physical function in knee osteoarthritis patients receiving ongoing hylan G-F 20, a high-molecular-weight hyaluronan, versus other treatment options: data from a large real-world longitudinal cohort in Canada. Drug Des Devel Ther. 2015;9:5633–5640. DOI: 10.2147/DDDT.S88473.
23. Jubb R.W., Piva S., Beinat L. et al. A one-year, randomized placebo. (saline). controlled clinical trial of 500–730 kDa sodium hyaluronate. (Hyalgan). on the radiological change in osteoarthritis of the knee. Int J Clin Pract. 2003;57:467–474. PMID: 12918884.
24. Brandt K.D. Efficacy and safety of intraarticular sodium hyaluronate in knee osteoarthritis. ORTHOVISC Study Group. Clin Orthop Relat Res. 2001;(385):130–143. DOI: 10.1097/00003086-200104000-00021.
25. Hatoum H.T., Fierlinger A.L., Lin S.J., Altman R.D. Cost-effectiveness analysis of intra-articular injections of a high molecular weight bioengineered hyaluronic acid for the treatment of osteoarthritis knee pain. J Med Econ. 2014;17(5):326–337. DOI: 10.3111/13696998.2014.902843.
26. Navarro-Sarabia F., Coronel P., Collantes E. et al. AMELIA study group. A 40-month multicentre, randomised placebo-controlled study to assess the efficacy and carry-over effect of repeated intra-articular injections of hyaluronic acid in knee osteoarthritis: the AMELIA project. Ann Rheum Dis. 2011;70(11):1957–1962. DOI: 10.1136/ard.2011.152017.
27. Berenbaum F., Grifka J., Cazzaniga S. et al. A randomized, double-blind, controlled trial comparing two intra-articular hyaluronic acid preparations differing by their molecular weight in symptomatic knee osteoarthritis. Ann Rheum Dis. 2012;71:1454–1460. DOI: 10.1136/annrheumdis-2011-200972.
28. Altman R.D., Bedi A., Karlsson J. et al. Product Differences in Intra-articular Hyaluronic Acids for Osteoarthritis of the Knee. Am J Sports Med. 2016;44(8):2158–2165. DOI: 10.1177/0363546515609599.
29. Asari A., Miyauchi S., Matsuzaka S. et al. Molecular weightdependent effects of hyaluronate on the arthritic synovium. Arch Hislol Cytol. 1998:61:125–135.
30. Ghosh P., Guidolin D. Potential mechanism of action of intra-articular hyaluronan therapy in osteoarthritis: are the effects molecular weight dependent? Semin Arthritis Rheum. 2002;32(1):10–37. DOI: 10.1053/sarh.2002.33720.
31. Maneiro E., de Andres M.C., Fernández-Sueiro J.L. et al. The biological action of hyaluronan on human osteoartritic articular chondrocytes: the importance of molecular weight. Clin Exp Rheumatol. 2004;22(3):307–312.
32. Mochizuki T., Ikari K., Yano K., Okazaki K. Comparison of patient-reported outcomes of treatment with low- and intermediate molecular weight hyaluronic acid in Japanese patients with symptomatic knee osteoarthritis: A prospective, randomized, single-blind trial. Asia-Pacific journal of sports medicine, arthroscopy, rehabilitation and technology. 2020;21:22–26. DOI: 10.1016/j.asmart.2020.04.001.
33. Iturriaga V., Vásquez B., Bornhardt T., Del Sol M. Effects of low and high molecular weight hyaluronic acid on the osteoarthritic temporomandibular joint in rabbit. Clin Oral Investig. 2021 Jan 3. DOI: 10.1007/s00784-020-03763-x. Online ahead of print.
34. Gotoh S., Onaya J., Abe M. et al. Effects of the molecular weight of hyaluronic acid and its action mechanisms on experimental joint pain in rats. Ann Rheurn Dis. 1993;52:817–822.
35. Bowman S., Awad M.E., Hamrick M.W. et al. Recent advances in hyaluronic acid based therapy for osteoarthritis. Clin Trans Med. 2018;7:6. DOI: 10.1186/s40169-017-0180-3.
36. Richette P. Hyaluronic acid: Still useful in knee osteoarthritis? Joint Bone Spine. 2017;84(6):655–656. DOI: 10.1016/j.jbspin.2017.05.002.
37. Hermans J., Reijman M., Goossens L.M. et al. A cost utility analysis of high molecular weight hyaluronic acid for knee osteoarthritis in everyday clinical care in patients in the working age. An economic evaluation of a randomized clinical trial. Arthritis Care Res (Hoboken). 2018;70(1):89–97. DOI: 10.1002/acr.23242.
38. Ishijima M., Nakamura T., Shimizu K. et al. Intra-articular hyaluronic acid injection versus oral non-steroidal anti-inflammatory drug for the treatment of knee osteoarthritis: a multi-center, randomized, open-label, non-inferiority trial. Arthritis Res Ther. 2014;16(1):R18. DOI: 10.1186/ar4446.
39. Стребкова Е.А., Алексеева Л.И. Эффективность внутрисуставной терапии препаратами гиалуроновой кислоты у больных остеоартритом. Современная ревматология. 2019;13(2):96–104. [Strebkova E.A., Alekseeva L.I. Efficiency of intra-articular hyaluronic acid therapy in patients with osteoarthritis. Sovremennaya Revmatologiya. 2019;13(2):96–104 (in Russ.)]. DOI: 10.14412/1996-7012-2019-2-96-104.
40. Campbell K.A., Erickson B.J., Saltzman B.M. et al. Is local viscosupplementation injection clinically superior to other therapies in the treatment of osteoarthritis of the knee: a systematic review of overlapping meta-analyses. Arthroscopy. 2015;31(10):2036–2045. DOI: 10.1016/j. arthro.2015.03.030. e14.
41. Xing D., Wang B., Liu Q. et al. Intra-articular hyaluronic acid in treating knee osteoarthritis: a PRISMA-compliant systematic review of overlapping meta-analysis. Sci Rep. 2016;6:32790. DOI:10.1038/srep32790.
42. Филатова Ю.С., Соловьев И.Н. Тактика ведения пациентов с остеоартритом: взгляд ревматолога и травматолога-ортопеда. Медицинский совет. 2020;19:89–97. [Filatova Yu.S., Solovyov I.N. Management tactics for patients with osteoarthritis: a joint view of a rheumatologist and an orthopedic traumatologist. Meditsinskiy sovet. 2020;19:89–97 (in Russ.)]. DOI: 10.21518/2079-701X-2020-19-89-97.
43. Concoff A., Sancheti P., Niazi F. et al. The efficacy of multiple versus single hyaluronic acid injections: a systematic review and meta-analysis. BMC Musculoskelet Disord. 2017;18(1):542. DOI: 10.1186/s12891-017-1897-2.
44. Altman R., Hackel J., Niazi F. et al. Efficacy and safety of repeated courses of hyaluronic acid injections for knee osteoarthritis: A systematic review. Semin Arthritis Rheum. 2018;48(2):168–175. DOI: 10.1016/j.semarthrit.2018.01.009.
45. Abbott T., Altman R.D., Dimef R. et al. Do hyaluronic acid injections delay total knee replacement surgery? Arthritis Rheum. 2013;65: S910–S911.
46. Михайлова А.С., Теплякова О.В., Соколова Л.А. Влияние локальной терапии гонартроза препаратами гиалуроновой кислоты различной молекулярной массы на динамику альгофункциональных показателей. Фарматека. 2011;19(232):74–78. [Mikhailova A.S., Teplyakova O.V., Sokolova L.A. Influence of local therapy of gonarthrosis with hyaluronic acid preparations of different molecular weight on the dynamics of algofuectional indicators. Farmateka. 2011;19(232):74–78 (in Russ.)].
47. Беляева Е.А., Авдеева О.С. Влияние вискосапплементарной терапии с использованием гиалуроната натрия на потребность в эндопротезировании коленных суставов при остеоартрозе. РМЖ. 2017;25:1898–1904. [Вelyaeva E.A., Avdeeva O.S. Effect of viscosupplementary therapy with sodium hyaluronate on the need for the knee replacement in osteoarthrosis. RMJ. 2017;25:1898–1904 (in Russ.)].
48. Попов В.П., Корощенко С.А., Ларин М.А. Оптимальное использование препаратов гиалуроновой кислоты при суставной патологии. РМЖ. Медицинское обозрение. 2017;1:12–14. [Popov V.P., Koroshchenko S.A., Larin M.A. Optimal use of hyaluronic acid for joint pathology treatment. RMJ. Medical review. 2017;1:12–14 (in Russ.)].
2. Мартынов А.И., Наумов А.В., Верткин А.Л. и др. Ведение больных с остеоартритом и коморбидностью в общей врачебной практике: мнение экспертов, основанное на доказательной медицине. Лечащий врач. 2015;04:39–46. [Martynov A.I., Naumov A.V., Vertkin A.L. et al. Management of patients with osteoarthritis and comorbidity in general medical practice: expert opinion based on evidence-based medicine. Lechashchiy vrach. 2015;04:39–46 (in Russ.)].
3. Hiligsmann M., Cooper C., Arden N. et al. Health economics in the field of osteoarthritis: an expert’s consensus paper from the European Society for Clinical and Economic Aspects of Osteoroporis and Osteoarthritis (ESCEO). Semin Arthritis Rheum. 2013;43(3):303–313. DOI: 10.1016/j.semarthrit.2013.
4. March L., Cross M., Lo C. et al. Osteoarthritis: A Serious Disease. Osteoarthritis Research Society International; 2016.
5. Bruyere O., Cooper C., Pelletier J.P. et al. An algorithm recommendation for the management of knee osteoarthritis in Europe and internationally: a report from a task force of the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO). Semin Arthritis Rheum. 2014;44(3):253–263. DOI: 10.1016/j.semarthrit.2014.05.014.
6. Bruyère O., Cooper C., Pelletier J.P. et al. A consensus statement on the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO) algorithm for the management of knee osteoarthritis-From evidence-based medicine to the real-life setting. Semin Arthritis Rheum. 2016;45(4 Suppl):S3–11. DOI: 10.1016/j.semarthrit.2015.11.010.
7. Bruyère O., Honvo G., Veronese N. et al. An updated algorithm recommendation for the management of knee osteoarthritis from the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO). Semin Arthritis Rheum. 2019;49(3):337–350. DOI: 10.1016/j.semarthrit.2019.04.008.
8. Chernos M., Grecov D., Kwok E. et al. Rheological study of hyaluronic acid derivatives. Biomed Eng Lett. 2017;7:17–24. DOI: 10.1007/s13534-017-0010-y.
9. Migliore А., Procopio S. Effectiveness and utility of hyaluronic acid in osteoarthritis. Clin Cases Miner Bone Metab. 2015;12:31–33. DOI: 10.11138/ccmbm/2015.12.1.031.
10. Moreland L.W. Intra-articular hyaluronan. (hyaluronic acid) and hyalans for the treatment of osteoarthritis: mechanism of action. Arthr Res Ther. 2003;5:54–67. DOI: 10.1186/ar623.
11. Bannuru R.R., Natov N.S., Dasi U.R. et al. Therapeutic trajectory following intra-articular hyaluronic acid injection in knee osteoarthritis-meta-analysis. Osteoarthr Cartil. 2011;19(6):611–619. DOI: 10.1016/j.joca.2010.09.014.
12. Liang J., Jiang D., Noble P.W. Hyaluronan as a therapeutic target in human diseases. Adv Drug Deliv Rev. 2016;97:186–203. DOI: 10.1016/j.addr.2015.10.017
13. Maheu E., Rannou F., Reginster J.Y. Efficacy and safety of hyaluronic acid in the management of osteoarthritis: evidence from real-life setting trials and surveys. Semin Arthritis Rheum. 2016;45(4 Suppl):S28–S33. DOI: 10.1016/j.semarthrit.2015.11.008.
14. Campo G.M., Avenoso A., Campo S. et al. Differential effect of molecular mass hyaluronan on lipopolysaccharide-induced damage in chondrocytes. Innate Immun. 2010;16:48–63. DOI: 10.1177/1753425909340419.
15. Jerosch J. Effects of glucosamine and chondroitin sulfate on cartilage metabolism in OA: outlook on other nutrient partners especially omega-3 fatty acids. Int J Rheumatol. 2011;2011:1–17. DOI: 10.1155/2011/969012.
16. Cooper C., Rannou F., Richette P. et al. Use of intraarticular hyaluronic acid in the Management of Knee Osteoarthritis in clinical practice. Arthritis Care Res (Hoboken). 2017;69(9):1287–1296. DOI: 10.1002/acr.23204.
17. Liu L., Ishijima M., Futami I. et al. Correlation between synovitis detected on enhanced-magnetic resonance imaging and a histological analysis with a patient-oriented outcome measure for Japanese patients with end-stage knee osteoarthritis receiving joint replacement surgery. Clin Rheumatol. 2010;16:1185–1190. DOI: 10.1007/s10067-010-1522-3.
18. Julovi S.M., Ito H., Nishitani K. et al. Hyaluronan inhibits matrix metalloproteinase-13 in human arthritic chondrocytes via CD44 and P38. J Orthop Res. 2011;16:258–264. DOI: 10.1002/jor.21216.
19. Goldberg V.M., Goldberg L. Intra-articular hyaluronans: the treatment of knee pain in osteoarthritis. J Pain Res. 2010;3:51–56. DOI: 10.2147/jpr.s4733.
20. Cook J.L., Hung C.T., Kuroki K. et al. Animal models of cartilage repair. Bone Joint Res. 2014;3(4):89–94. DOI:10.1302/2046–3758.34.2000238.
21. Carapeba G.O.L., Cavaleti P., Nicácio G.M. et al. Intra-articular hyaluronic acid compared to traditional conservative treatment in dogs with osteoarthritis associated with hip dysplasia. Evid-Based Compl Altern Med. 2016;2016:20726921. DOI: 10.1155/2016/2076921 256-259.
22. Petrella R.J., Wakeford С. Pain relief and improved physical function in knee osteoarthritis patients receiving ongoing hylan G-F 20, a high-molecular-weight hyaluronan, versus other treatment options: data from a large real-world longitudinal cohort in Canada. Drug Des Devel Ther. 2015;9:5633–5640. DOI: 10.2147/DDDT.S88473.
23. Jubb R.W., Piva S., Beinat L. et al. A one-year, randomized placebo. (saline). controlled clinical trial of 500–730 kDa sodium hyaluronate. (Hyalgan). on the radiological change in osteoarthritis of the knee. Int J Clin Pract. 2003;57:467–474. PMID: 12918884.
24. Brandt K.D. Efficacy and safety of intraarticular sodium hyaluronate in knee osteoarthritis. ORTHOVISC Study Group. Clin Orthop Relat Res. 2001;(385):130–143. DOI: 10.1097/00003086-200104000-00021.
25. Hatoum H.T., Fierlinger A.L., Lin S.J., Altman R.D. Cost-effectiveness analysis of intra-articular injections of a high molecular weight bioengineered hyaluronic acid for the treatment of osteoarthritis knee pain. J Med Econ. 2014;17(5):326–337. DOI: 10.3111/13696998.2014.902843.
26. Navarro-Sarabia F., Coronel P., Collantes E. et al. AMELIA study group. A 40-month multicentre, randomised placebo-controlled study to assess the efficacy and carry-over effect of repeated intra-articular injections of hyaluronic acid in knee osteoarthritis: the AMELIA project. Ann Rheum Dis. 2011;70(11):1957–1962. DOI: 10.1136/ard.2011.152017.
27. Berenbaum F., Grifka J., Cazzaniga S. et al. A randomized, double-blind, controlled trial comparing two intra-articular hyaluronic acid preparations differing by their molecular weight in symptomatic knee osteoarthritis. Ann Rheum Dis. 2012;71:1454–1460. DOI: 10.1136/annrheumdis-2011-200972.
28. Altman R.D., Bedi A., Karlsson J. et al. Product Differences in Intra-articular Hyaluronic Acids for Osteoarthritis of the Knee. Am J Sports Med. 2016;44(8):2158–2165. DOI: 10.1177/0363546515609599.
29. Asari A., Miyauchi S., Matsuzaka S. et al. Molecular weightdependent effects of hyaluronate on the arthritic synovium. Arch Hislol Cytol. 1998:61:125–135.
30. Ghosh P., Guidolin D. Potential mechanism of action of intra-articular hyaluronan therapy in osteoarthritis: are the effects molecular weight dependent? Semin Arthritis Rheum. 2002;32(1):10–37. DOI: 10.1053/sarh.2002.33720.
31. Maneiro E., de Andres M.C., Fernández-Sueiro J.L. et al. The biological action of hyaluronan on human osteoartritic articular chondrocytes: the importance of molecular weight. Clin Exp Rheumatol. 2004;22(3):307–312.
32. Mochizuki T., Ikari K., Yano K., Okazaki K. Comparison of patient-reported outcomes of treatment with low- and intermediate molecular weight hyaluronic acid in Japanese patients with symptomatic knee osteoarthritis: A prospective, randomized, single-blind trial. Asia-Pacific journal of sports medicine, arthroscopy, rehabilitation and technology. 2020;21:22–26. DOI: 10.1016/j.asmart.2020.04.001.
33. Iturriaga V., Vásquez B., Bornhardt T., Del Sol M. Effects of low and high molecular weight hyaluronic acid on the osteoarthritic temporomandibular joint in rabbit. Clin Oral Investig. 2021 Jan 3. DOI: 10.1007/s00784-020-03763-x. Online ahead of print.
34. Gotoh S., Onaya J., Abe M. et al. Effects of the molecular weight of hyaluronic acid and its action mechanisms on experimental joint pain in rats. Ann Rheurn Dis. 1993;52:817–822.
35. Bowman S., Awad M.E., Hamrick M.W. et al. Recent advances in hyaluronic acid based therapy for osteoarthritis. Clin Trans Med. 2018;7:6. DOI: 10.1186/s40169-017-0180-3.
36. Richette P. Hyaluronic acid: Still useful in knee osteoarthritis? Joint Bone Spine. 2017;84(6):655–656. DOI: 10.1016/j.jbspin.2017.05.002.
37. Hermans J., Reijman M., Goossens L.M. et al. A cost utility analysis of high molecular weight hyaluronic acid for knee osteoarthritis in everyday clinical care in patients in the working age. An economic evaluation of a randomized clinical trial. Arthritis Care Res (Hoboken). 2018;70(1):89–97. DOI: 10.1002/acr.23242.
38. Ishijima M., Nakamura T., Shimizu K. et al. Intra-articular hyaluronic acid injection versus oral non-steroidal anti-inflammatory drug for the treatment of knee osteoarthritis: a multi-center, randomized, open-label, non-inferiority trial. Arthritis Res Ther. 2014;16(1):R18. DOI: 10.1186/ar4446.
39. Стребкова Е.А., Алексеева Л.И. Эффективность внутрисуставной терапии препаратами гиалуроновой кислоты у больных остеоартритом. Современная ревматология. 2019;13(2):96–104. [Strebkova E.A., Alekseeva L.I. Efficiency of intra-articular hyaluronic acid therapy in patients with osteoarthritis. Sovremennaya Revmatologiya. 2019;13(2):96–104 (in Russ.)]. DOI: 10.14412/1996-7012-2019-2-96-104.
40. Campbell K.A., Erickson B.J., Saltzman B.M. et al. Is local viscosupplementation injection clinically superior to other therapies in the treatment of osteoarthritis of the knee: a systematic review of overlapping meta-analyses. Arthroscopy. 2015;31(10):2036–2045. DOI: 10.1016/j. arthro.2015.03.030. e14.
41. Xing D., Wang B., Liu Q. et al. Intra-articular hyaluronic acid in treating knee osteoarthritis: a PRISMA-compliant systematic review of overlapping meta-analysis. Sci Rep. 2016;6:32790. DOI:10.1038/srep32790.
42. Филатова Ю.С., Соловьев И.Н. Тактика ведения пациентов с остеоартритом: взгляд ревматолога и травматолога-ортопеда. Медицинский совет. 2020;19:89–97. [Filatova Yu.S., Solovyov I.N. Management tactics for patients with osteoarthritis: a joint view of a rheumatologist and an orthopedic traumatologist. Meditsinskiy sovet. 2020;19:89–97 (in Russ.)]. DOI: 10.21518/2079-701X-2020-19-89-97.
43. Concoff A., Sancheti P., Niazi F. et al. The efficacy of multiple versus single hyaluronic acid injections: a systematic review and meta-analysis. BMC Musculoskelet Disord. 2017;18(1):542. DOI: 10.1186/s12891-017-1897-2.
44. Altman R., Hackel J., Niazi F. et al. Efficacy and safety of repeated courses of hyaluronic acid injections for knee osteoarthritis: A systematic review. Semin Arthritis Rheum. 2018;48(2):168–175. DOI: 10.1016/j.semarthrit.2018.01.009.
45. Abbott T., Altman R.D., Dimef R. et al. Do hyaluronic acid injections delay total knee replacement surgery? Arthritis Rheum. 2013;65: S910–S911.
46. Михайлова А.С., Теплякова О.В., Соколова Л.А. Влияние локальной терапии гонартроза препаратами гиалуроновой кислоты различной молекулярной массы на динамику альгофункциональных показателей. Фарматека. 2011;19(232):74–78. [Mikhailova A.S., Teplyakova O.V., Sokolova L.A. Influence of local therapy of gonarthrosis with hyaluronic acid preparations of different molecular weight on the dynamics of algofuectional indicators. Farmateka. 2011;19(232):74–78 (in Russ.)].
47. Беляева Е.А., Авдеева О.С. Влияние вискосапплементарной терапии с использованием гиалуроната натрия на потребность в эндопротезировании коленных суставов при остеоартрозе. РМЖ. 2017;25:1898–1904. [Вelyaeva E.A., Avdeeva O.S. Effect of viscosupplementary therapy with sodium hyaluronate on the need for the knee replacement in osteoarthrosis. RMJ. 2017;25:1898–1904 (in Russ.)].
48. Попов В.П., Корощенко С.А., Ларин М.А. Оптимальное использование препаратов гиалуроновой кислоты при суставной патологии. РМЖ. Медицинское обозрение. 2017;1:12–14. [Popov V.P., Koroshchenko S.A., Larin M.A. Optimal use of hyaluronic acid for joint pathology treatment. RMJ. Medical review. 2017;1:12–14 (in Russ.)].
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