Comparison of Three Imaging Methods for the Evaluation of Osteoarthritis Induced by Cranial Cruciate Ligament Transection in Rabbits

Giovanna Cristina Brombini, Sheila Canevese Rahal, Ivan Felismino Charas dos Santos, Maria Jaqueline Mamprim, Miriam Tsunemi, Jeana Pereira da Silva, Danuta Pulz Doiche, Jean Guilherme Fernandes Joaquim

Abstract


Background:Osteoarthritis is a degenerative joint disease that affects specially cartilage, meniscus, and tendons. Ligaments, muscles, subchondral bone and synovium. This pathology is a common condition limiting the quality of life of patients. Imaging modalities have also been used for evaluation the progression of the osteoarthritis, or degenerative processes induced by acute injury. In order to use more accessible imaging modalities for experimentation, this study aimed to compare radiographic, computed tomography, and ultrasound findings in the evaluation of osteoarthritis induced by the cranial cruciate ligament transection model in rabbits.

Materials, Methods & Results:Twenty-four male Norfolk rabbits aged approximately 5 months old were used. All rabbits were submitted to cranial cruciate ligament transection of the left stifle and evaluated 45 days after the surgery. The radiographic findings were subchondral bone sclerosis (33.33%); joint space narrowing (66%); presence of osteophytes at medial femoral condyle (4.16%), lateral femoral condyle (4.16%), medial fabela (20.83%), lateral fabela (8.33%) and sesamoid of the popliteal muscle (4.16%). No osteophytes were seen at medial and lateral tibial condyles. The tomographic computed findings were joint space narrowing (62.5%); presence of osteophytes at medial femoral condyle (75%), lateral femoral condyle (54.16%), medial fabela (66.66%), lateral fabela (37.5%), medial tibial condyle (75%), lateral tibial condyle (20.83%) and sesamoid of the popliteal muscle (37.5%). The ultrasound findings were synovial hypertrophy (95.83%); effusion in the suprapatellar recess (75%), distal tibial recess (16.66%) and cranial joint space (75%); changes (hyperechogenic foci and heterogeneity) of the lateral meniscus (50%) and medial meniscus (25%); increased thickness of the medial condyle (54.16%) and lateral condyle (45.83%); irregularity of the medial condyle (66.66%) and lateral condyle (58.33%); alterations of the patellar tendon (12.5%) and extensor ligament (effusion and increased echogenicity) (20.83%).

Discussion: Osteoarthritis is a degenerative joint disease and is common condition which limiting the quality of life of patients. Many studies performed in rabbits have evaluated the development of osteoarthritis through post-mortem macroscopic or microscopic assessments. Imaging modalities have also been used for evaluation the progression of the osteoarthritis, or degenerative processes induced by acute injury. High quality radiographs are accurate in identifying structural changes resulted from osteoarthritis, but computed tomography allows earlier identification in relation to conventional radiography. The three imaging modalities were helpful to identify the osteoarthritis, but the findings were different and compatible with each analysis method. The computed tomographic detected a higher number of osteophytes than plain radiographs. Also, osteophytes did not visualized by radiographic examination, such as medial tibial condyle and lateral tibial condyle, were identified by computed tomography. In turn, the ultrasound examination enabled identification of lesions did not seen on radiographic and computed tomography examinations. Synovial hypertrophy and joint effusion had the highest percentage. In human patients, ultrasound examination has been used to assess hypertrophy and inflammation of the synovium due to osteoarthritis. In conclusion, computerized tomography images provided more information than plain X-ray images and can be complemented by ultrasound examination to identify osteoarthritis induced by cranial cruciate ligament transection in rabbits.

Comparison of Three Imaging Methods for the Evaluation of Osteoarthritis Induced by Cranial Cruciate Ligament Transection in Rabbits

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References


Abramoff B. & Caldera F.E. 2020. Osteoarthritis: Pathology, Diagnosis, and Treatment Options. The Medical clinics of North America. 104: 293-311. doi: 10.1016/j.mcna.2019.10.007

Ahmad N., Ansari M.Y. & Haqqi T.M. 2020. Role of iNOS in osteoarthritis: Pathological and therapeutic aspects. Journal of Cellular Physiology. 235: 6366-6376. doi: 10.1002/jcp.29607

Albano M.B., Vidigal L., Oliveira M.Z., Namba M.M., Silva J.L., Pereira Filho F.A., Barbosa M.A. & Silva E.M. 2015. Macroscopic analyses of the effects of hyaluronates and corticosteroids on induced osteoarthritis in rabbits' knees. Revista Brasileira de Ortopedia. 45: 273-278. doi: 10.1016/S2255-4971(15)30368-2

Ayhan E., Kesmezacar H. & Akgun I. 2014. Intraarticular injections (corticosteroid, hyaluronic acid, platelet rich plasma) for the knee osteoarthritis. World Journal of Orthopedics. 5: 351-361.

Batiste D.L., Kirkley A., Laverty S., Thain L.M., Spouge A.R., Gati J.S., Foster P.J. & Holdsworth D.W. 2004. High-resolution MRI and micro-CT in an ex vivo rabbit anterior cruciate ligament transection model of osteoarthritis. Osteoarthritis and Cartilage. 12: 614-626. doi: 10.5312/wjo.v5.i3.351

Bouchgua M., Alexander K., d'Anjou M.A., Girard C.A., Carmel E.N., Beauchamp G., Richard H. & Laverty S. 2009. Use of routine clinical multimodality imaging in a rabbit model of osteoarthritis--part I. Osteoarthritis and cartilage 17: 188-196. doi: 10.1016/j.joca.2008.06.017

Boulocher C., Duclos M.E., Arnault F., Roualdes O., Fau D., Hartmann D.J., Roger T., Vignon E. & Viguier E. 2008. Knee joint ultrasonography of the ACLT rabbit experimental model of osteoarthritis: relevance and effectiveness in detecting meniscal lesions. Osteoarthritis and Cartilage. 16: 470-479. doi: 10.1016/j.joca.2007.07.012

Boulocher C.B., Viguier E.R., Cararo R., Fau D.J., Arnault F., Collard F., Maitre P.A., Roualdes O., Duclos M.E., Vignon E.P. & Roger T.W. 2010. Radiographic assessment of the femorotibial joint of the CCLT rabbit experimental model of osteoarthritis. BMC Medical Imaging 10: 1-10. doi: 10.1186/1471-2342-10-3

Butler M., Colombo C., Hickman L., O'Byrne E., Steele R., Steinetz B., Quintavalla J. & Yokoyama N. 1983. A new model of osteoarthritis in rabbits. III. Evaluation of anti-osteoarthritic effects of selected drugs administered intraarticularly. Arthritis and Rheumatism 26: 1380-1386. doi: 10.1002/art.1780261111

Campos W.N.S., Souza M.A., Ruiz T., Peres T.P., Néspoli P.B., Marques A.T.C., Colodel E.M. & Souza R.L. 2013. Experimental osteoarthritis in rabbits: lesion progression. Pesquisa Veterinária Brasileira. 33: 279-285

Casper-Taylor M.E., Barr A.J., Williams S., Wilcox R.K. & Conaghan P.G. 2020. Initiating factors for the onset of OA: A systematic review of animal bone and cartilage pathology in OA. Journal of Orthopaedic Research. 38: 1810-1818. doi: 10.1590/S0100-736X2013000300001

Chang D.G., Iverson E.P., Schinagl R.M., Sonoda M., Amiel D., Coutts R.D. & Sah R.L. 1997. Quantitation and localization of cartilage degeneration following the induction of osteoarthritis in the rabbit knee. Osteoarthritis and Cartilage. 5: 357-372. doi: 10.1016/s1063-4584(97)80039-8

Colombo C., Butler M., O'Byrne E., Hickman L., Swartzendruber D., Selwyn M. & Steinetz B. 1983. A new model of osteoarthritis in rabbits. I. Development of knee joint pathology following lateral meniscectomy and section of the fibular collateral and sesamoid ligaments. Arthritis and Rheumatism. 26: 875-886. doi: 10.1002/art.1780260709

Cucchiarini M., Girolamo L., Filardo G., Oliveira J.M., Orth P., Pape D. & Reboul P. 2016. Basic science of osteoarthritis. Journal of Experimental Orthopaedics. 3: 1-18. doi: 10.1186/s40634-016-0060-6

Dawson J., Gustard, S. & Beckmann N. 1999. High-resolution three-dimensional magnetic resonance imaging for the investigation of knee joint damage during the time course of antigen-induced arthritis in rabbits. Arthritis and Rheumatism. 42: 119-128. doi: 10.1002/1529-0131(199901)

Florea C., Malo M.K., Rautiainen J., Mäkelä J.T., Fick J.M., Nieminen M.T., Jurvelin J.S., Davidescu A. & Korhonen R.K. 2015. Alterations in subchondral bone plate, trabecular bone and articular cartilage properties of rabbit femoral condyles at 4 weeks after anterior cruciate ligament transection. Osteoarthritis and Cartilage. 23: 414-422. doi:10.1016/j.joca.2014.11.023

Goldring M.B. & Goldring S.R. 2010. Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Annals of the New York Academy of Sciences. 1192: 230-237. doi: 10.1111/j.1749-6632.2009.05240.x

Gupta R.C., Lall R., Srivastava A. & Sinha A. 2019. Hyaluronic Acid: Molecular Mechanisms and Therapeutic Trajectory. Frontiers in Veterinary Science. 6: 1-24. doi: 10.3389/fvets.2019.00192

Graverand M.P.H., Vignon E., Otterness I.G. & Hart D.A. 2001. Early changes in lapine menisci during osteoarthritis development: Part I: cellular and matrix alterations. Osteoarthritis and Cartilage. 9: 56-64. doi: 10.1053/joca.2000.0350

Hsu H. & Siwiec R.M. 2020. Knee Osteoarthritis. In: StatPearls. Treasure Island (FL): StatPearls Publishing. Available from: https://www.ncbi.nlm.nih.gov/books/NBK507884

Hulth A., Lindberg L. & Telhag H. 1970. Experimental osteoarthritis in rabbits. Preliminary report. Acta Orthopaedica Scandinavica. 41: 522-530

Kaderli S., Viguier E., Watrelot-Virieux D., Roger T., Gurny R., Scapozza L., Möller M., Boulocher C. & Jordan O. 2015. Efficacy study of two novel hyaluronic acid-based formulations for viscosupplementation therapy in an early osteoarthrosic rabbit model. European Journal of Pharmaceutics and Biopharmaceutics. 96: 388-395. doi: 10.1016/j.ejpb.2015.09.005

Manoto S.L., Maepa M.J. & Motaung S.K. 2018. Medical ozone therapy as a potential treatment modality for regeneration of damaged articular cartilage in osteoarthritis. Saudi Journal of Biological Sciences. 25: 672-679. doi: 10.1016/j.sjbs.2016.02.002

Mihara M., Higo S., Uchiyama Y., Tanabe K. & Saito K. 2007. Different effects of high molecular weight sodium hyaluronate and NSAID on the progression of the cartilage degeneration in rabbit OA model. Osteoarthritis and Cartilage. 15: 543-549. doi: 10.1016/j.joca.2006.11.001

Moskowitz R.W., Davis W., Sammarco J., Martens M., Baker J., Mayor M., Burstein A.H. & Frankel V.H. 1973. Experimentally induced degenerative joint lesions following partial meniscectomy in the rabbit. Arthritis and Rheumatism. 16: 397-405.

Paukkonen K., Jurvelin J. & Helminen H.J. 1986. Effects of immobilization on the articular cartilage in young rabbits. A quantitative light microscopic stereological study. Clinical Orthopaedics and Related Research. 206: 270-280. PMID: 3708985.

Rahmati M., Mobasheri A. & Mozafari M. 2016. Inflammatory mediators in osteoarthritis: A critical review of the state-of-the-art, current prospects, and future challenges. Bone. 85: 81-90. doi: 10.1016/j.bone.2016.01.019

Seyam O., Smith N.L., Reid I., Gandhi J., Jiang W. & Khan S.A. 2018. Clinical utility of ozone therapy for musculoskeletal disorders. Medical Gas Research. 8: 103-110. doi: 10.4103/2045-9912.241075

Shapiro F. & Glimcher M.J. 1980. Induction of osteoarthrosis in the rabbit knee joint. Clinical Orthopaedics and Related Research. 147: 287-295. PMID: 6154558.

Torelli S.R., Rahal S.C., Volpi R.S., Yamashita S., Mamprim M.J. & Crocci A.J. 2004. Radiography, computed tomography and magnetic resonance imaging at 0.5 Tesla of mechanically induced osteoarthritis in rabbit knees. Brazilian Journal of Medical and Biological Research. 37: 493-501. doi: 10.1590/S0100-879X2004000400006

Wachsmuth L., Keiffer R., Juretschke H.P., Raiss R.X., Kimmig N. & Lindhorst E. 2003. In vivo contrast-enhanced micro MR-imaging of experimental osteoarthritis in the rabbit knee joint at 7.1T1. Osteoarthritis and Cartilage. 11: 891-902. doi: 10.1016/j.joca.2003.08.008

Yoshioka M., Coutts R.D., Amiel D. & Hacker S.A. 1996. Characterization of a model of osteoarthritis in the rabbit knee. Osteoarthritis and Cartilage. 4: 87-98. doi: 10.1016/s1063-4584(05)80318-8




DOI: https://doi.org/10.22456/1679-9216.107645

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