Remodeling of articular cartilage and subchondral zone of the tibia in exo‑prosthetics of the limb

Introduction Exo-prosthetics of limbs through osseointegration opens up new possibilities in prosthetics. Modern prostheses are becoming more high-tech, which requires deep understanding of the anatomical and functional features of the bone-joint system.
Aim To identify features of structural reorganization of articular cartilage and subchondral zone of the tibia in lower leg prosthetics using an implant with calcium phosphate coating and an implant without additional coating.
Materials and methods The study was performed on 5 intact (control) and 6 experimental dogs (age 1.8 ± 0.5 years, weight 19 ± 1.2 kg). A tibial stump was modeled in the animals at the border of the middle and  upper third of the diaphysis. After 2.5 months a PressFit type implant was installed. Depending on  the  Press‑Fit type, the animals were divided into groups: group 1 made of Ti6Al4V alloy (n = 3); group 2 of Ti6Al4V alloy with calcium phosphate coating (n = 3). Duration of the experiment was 180 days after prosthesis fitting. Histomorphometric study of the articular cartilage and subchondral zone was performed on paraffin sections using an AxioScope.A1 microscope supplied with AxioCam camera and Zenblue software (CarlZeissMicroImagingGmbH, Germany).
Results Bone tissue remodeling was expressed by thinning of the subchondral bone plate, osteolysis, changes in the architecture of bone trabeculae in the subchondral trabecular bone, and a decrease in bone tissue mineralization. These signs were more intense in group 1. Signs of reparative osteogenesis with osteoblasts on the surface of bone trabeculae were noted in group 2. Subchondral bone plate thickness reduced twofold in  group  1, and by 1.5 times in group 2 relative to the control. The values of the parameter of trabecular area were reduced in group 1 by 17 % and in group 2 by 10 %. Statistically significant decrease in the values of  articular cartilage thickness was recorded in group 1 and was accompanied by a higher (by 1.8 times) frequency of vessels been found in the deep zone of cartilage compared to group 2.
Discussion The identified changes in the subchondral zone corresponded to stage 0 (according to the O‑M classification. Aho et al., 2017): very early signs of osteoarthritis, when subchondral sclerosis is not pronounced, the subchondral bone plate is thin. Structural changes in articular cartilage corresponded to  grade  0–1 according to the histological classification of the International Society for the Study of Osteoarthritis OARSI.
Conclusion Histomorphometric changes in the osteochondral component of the tibial plateau during lower leg prosthetics (thinning of the subchondral bone plate, rarefaction of the subchondral trabecular bone, penetration of vessels into non-calcified cartilage) are predictors of arthrosis. The use of implants made of Ti6Al4V alloy coated with a calcium phosphate provides reduction of bone resoption intensity and activates reparative osteogenesis.

1. Li Y, Lindeque B. Percutaneous Osseointegrated Prostheses for Transfemoral Amputations. Orthopedics. 2018;41(2):75‑80. doi: 10.3928/01477447-20180227-03.

2. Ontario Health (Quality). Osseointegrated Prosthetic Implants for People With Lower-Limb Amputation: A Health Technology Assessment. Ont Health Technol Assess Ser. 2019;19(7):1-126.

3. Hoellwarth JS, Tetsworth K, Rozbruch SR, et al. Osseointegration for Amputees: Current Implants, Techniques, and Future Directions. JBJS Rev. 2020;8(3):e0043. doi: 10.2106/JBJS.RVW.19.00043.

4. Bates TJ, Fergason JR, Pierrie SN. Technological Advances in Prosthesis Design and Rehabilitation Following Upper Extremity Limb Loss. Curr Rev Musculoskelet Med. 2020;13(4):485-493. doi: 10.1007/s12178-020-09656-6.

5. Raschke SU. Limb Prostheses: Industry 1.0 to 4.0: Perspectives on Technological Advances in Prosthetic Care. Front Rehabil Sci. 2022;3:854404. doi: 10.3389/fresc.2022.854404.

6. Varaganti P, Seo S. Recent Advances in Biomimetics for the Development of Bio-Inspired Prosthetic Limbs. Biomimetics (Basel). 2024;9(5):273. doi: 10.3390/biomimetics9050273.

7. Kuznetsov VP, Emanov AA, Gorbach EN, Gorgots VG. Implants for one-stage osteointegration with mechanobiological stimulation of bone formation. Materials. Technologies. Design. 2021;3(5):23-30. (In Russ.) doi: 10.54708/26587572_2021_33523.

8. Stupina TA, Emanov AA, Kuznetsov VP, Ovchinnikov EN. Assessment of knee osteoarthritis risk following canine tibial prosthetics (pilot experimental morphological study). Genij Ortopedii. 2021;27(6):795-799. doi: 10.18019/1028-4427-2021-27-6-795-799.

9. Li G, Yin J, Gao J, et al. Subchondral bone in osteoarthritis: insight into risk factors and microstructural changes. Arthritis Res Ther. 2013;15:223. doi: 10.1186/ar4405.

10. Stupina TA, Stepanov MA, Teplen’kii MP. Role of subchondral bone in the restoration of articular cartilage. Bulletin of Experimental Biology and Medicine. 2015;158(6): 820-823. doi: 10.1007/s10517-015-2870-4.

11. Kotelnikov GP, Lartsev YV, Kudashev DS, et al. Pathogenetic and clinical aspects of osteoarthritis and osteoarthritisassociated defects of the cartilage of the knee joint from the standpoint of understanding the role of the subchondral bone. N.N. Priorov Journal of Traumatology and Orthopedics. 2023;30(2):219-231. doi: 10.17816/vto346679.

12. Nagira K, Ikuta Y, Shinohara M, et al. Histological scoring system for subchondral bone changes in murine models of joint aging and osteoarthritis. Sci Rep. 2020;10(1):10077. doi: 10.1038/s41598-020-66979-7.

13. Dudaric L, Dumic-Cule I, Divjak E, et al. Bone Remodeling in Osteoarthritis-Biological and Radiological Aspects. Medicina (Kaunas). 2023;59(9):1613. doi: 10.3390/medicina59091613.

14. Zhang YY, Zhu Y, Lu DZ, et al. Evaluation of osteogenic and antibacterial properties of strontium/silver-containing porous TiO2 coatings prepared by micro-arc oxidation. J Biomed Mater Res B Appl Biomater. 2021;109(4):505-516. doi: 10.1002/jbm.b.34719.

15. Wang YR, Yang NY, Sun H, et al. The effect of strontium content on physicochemical and osteogenic property of Sr/Ag-containing TiO2 microporous coatings. J Biomed Mater Res B Appl Biomater. 2023;111(4):846-857. doi: 10.1002/jbm.b.35195.

16. Drevet R, Fauré J, Benhayoune H. Bioactive calcium phosphate coatings for bone implant applications: a review. Coatings. 2023;13(6):1091. doi: 10.3390/coatings13061091.

17. Stogov MV, Emanov AA, Kuznetsov VP, et al. The effect of zinc-containing calcium phosphate coating on the osseointegration of transcutaneous implants for limb prosthetics. Genij Ortopedii. 2024;30(5):677-686. doi: 10.18019/1028-4427-2024-30-5-677-686.

18. Ivashenka SV, Astapovich AA, Jamal A. Experimental substantiation of the use of drug magnetophoresis to improve the osseointegration of dental implants. Modern dentistry. 2021;1:27-31. (In Russ.)

19. Kuznetsov VP, Gorgots VG, Anikeev AV, et al. Tubular bone stump implant. Patent RF, no. 194912, 2019. Available at: https:// www.fips.ru/registers-doc-view/fips_servlet?DB=RUPM&DocNumber=194912&TypeFile=html. Accessed May 28, 2025. (In Russ.)

20. Kuznetsov VP, Gubin AV, Gorgots VG, et al. Device for osseointegration of the implant into the bone of the stump of the lower limb. Patent RF, no. 185647, 2018. Available at: https://www.fips.ru/registers-doc-view/fips_servlet?DB=RU PM&DocNumber=185647&TypeFile=html. Accessed May 28, 2025. (In Russ.)

21. Stupina TA, Chtchoudlo MM. A technique for quantitative evaluation of articular cartilage condition at different levels of structural organization. Genij Ortopedii. 2009;(1):55-57. (In Russ.)

22. Susliaev VG, Shcherbina KK, Smirnova LM, et al. Early prosthetic and orthopedic assistance in medical rehabilitation of children with congenital and amputation defects of the lower limbs. Genij Ortopedii. 2020;26(2):198-205. doi: 10.18019/1028-4427-2020-26-2-198-205.

23. Makarov MA, Makarov SA, Pavlov VP, Vardikova GN. Stress bone remodeling after endoprosthetic replacement of large joints and its conservative correction. Modern Rheumatology Journal. 2009;3(1):62-67. (In Russ.) doi: 10.14412/1996-7012-2009-526.

24. Emanov AA, Stupina TA, Borzunov DYu, Shastov AL. The features of structural reorganization of the knee articular cartilage and synovial membrane in the process of filling a postresection defect of leg bones under transosseous osteosynthesis with the Ilizarov fixator experimentally. International Journal of Applied and Fundamental Research. 2015;12(7):1228-1232. (In Russ.)

25. Stupina TA, Emanov AA, Antonov NI. Bone union and structural changes in the articular cartilage of the knee joint after immediate and delayed antegrade locked intramedullary nailing of femoral shaft fractures. Experimental findings. Genij Ortopedii. 2016;(4):76-80. doi: 10.18019/1028-4427-2016-4-76-80.

26. Aho O-M, Finnila M, Thevenot J, et al. Subchondral bone histology and grading in osteoarthritis. PLoS One. 2017;12(3):e0173726. doi: 10.1371/journal.pone.0173726.

27. Klementeva VI, Chernisheva TV, Korochina KV, Korochina IE. Laboratory and instrumntal study of knee joints in patients with early gonarthrosis: search for relationship. Medical academic journal. 2020;20(3):99-106. (In Russ.) doi: 10.17816/MAJ43455.

28. Burr DB, Gallant MA. Bone remodelling in osteoarthritis. Nat Rev Rheumatol. 2012;8(11):665-673. doi: 10.1038/nrrheum.2012.130.

29. Hu Y, Chen X, Wang S, Jing Y, Su J. Subchondral bone microenvironment in osteoarthritis and pain. Bone Res. 2021;9(1):20. doi: 10.1038/s41413-021-00147-z.

30. Pavlova VN, Pavlov GG, Shostak NA, Slutsky LI. Joint: Morphology, clinic, diagnosis, treatment. Moscow: Medical Information Agency Publ.; 2011:552. (In Russ.).

31. Madry H, Orth P, Cucchiarini M. Role of the Subchondral Bone in Articular Cartilage Degeneration and Repair. J Am Acad Orthop Surg. 2016;24(4):e45-e46. doi: 10.5435/JAAOS-D-16-00096.

32. Imhof H, Sulzbacher I, Grampp S, et al. Subchondral bone and cartilage disease: a rediscovered functional unit. Invest Radiol. 2000;35(10):581-588. doi: 10.1097/00004424-200010000-00004.

33. Bäuerle T, Roemer FW. Dynamic contrast-enhanced MRI for assessment of subchondral bone marrow vascularization in an experimental osteoarthritis model: a major step towards clinical translation? Osteoarthritis Cartilage. 2021;29(5):603-606. doi: 10.1016/j.joca.2021.03.001.

34. Dorraki M, Muratovic D, Fouladzadeh A, et al. Hip osteoarthritis: A novel network analysis of subchondral trabecular bone structures. PNAS Nexus. 2022;1(5):pgac258. doi: 10.1093/pnasnexus/pgac258.

35. Pritzker KP, Gay S, Jimenez SA, et al. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage. 2006;14(1):13-29. doi: 10.1016/j.joca.2005.07.014.