Effects of physical exercise on the cartilage of ovariectomized rats submitted to immobilization

José Martim Marques Simas, Regina Inês Kunz, Rose Meire Costa Brancalhão, Lucinéia de Fátima Chasko Ribeiro, Gladson Ricardo Flor Bertolini, José Martim Marques Simas, Regina Inês Kunz, Rose Meire Costa Brancalhão, Lucinéia de Fátima Chasko Ribeiro, Gladson Ricardo Flor Bertolini

Abstract

Objective: To analyze the effects of physical exercise on cartilage histomorphometry in osteoporosis-induced rats subjected to immobilization.

Methods: We used 36 Wistar rats that were separated into six groups: G1, G2 and G3 submitted to pseudo-oophorectomy, and G4, G5 and G6 submitted to oophorectomy. After 60 days at rest, G2, G3, G5 and G6 had the right hind limbs immobilized for 15 days, followed by the same period in remobilization, being free in the box to G2 and G5, and climb ladder to G3 and G6. At the end of the experiment, the rats were euthanized, their tibias bilaterally removed and submitted to histological routine.

Results: There was significant increase in thickness of the articular cartilage (F(5;29)=13.88; p<0.0001) and epiphyseal plate (F(5;29)=14.72; p<0.0001) as the number of chondrocytes (F(5;29)=5.11; p=0.0021) in ovariectomized rats, immobilized and submitted to exercise. In the morphological analysis, degeneration of articular cartilage with subchondral bone exposure, loss of cellular organization, discontinuity of tidemark, presence of cracks and flocculation in ovariectomized, immobilized and free remobilization rats were found. In ovariectomized and immobilized remobilization ladder rats, signs of repair of the cartilaginous structures in the presence of clones, pannus, subcortical blood vessel invasion in the calcified zone, increasing the amount of isogenous groups and thickness of the calcified zone were observed.

Conclusion: Exercise climb ladder was effective in cartilaginous tissue recovery process damaged by immobilization, in model of osteoporosis by ovariectomy in rats.

Conflict of interest statement

Conflict of interest: none.

Figures

Figure 1. Thickness of the upper articular…
Figure 1. Thickness of the upper articular cartilage of the tibia, compared between rats in the different study groups (G1, G2, G3, G4, G5 and G6), and between the right (target) and left (control) hind limbs. The same letter represents similarities and different letters represent significant differences between experimental groups, for the same side
Figure 2. Thickness of the tibial epiphyseal…
Figure 2. Thickness of the tibial epiphyseal plate e, compared between rats in the different study groups (G1, G2, G3, G4, G5 and G6), and between the right (target) and left (control) hind limbs. The same letter represents similarities and different letters represent significant differences between experimental groups, for the same side
Figure 3. Chondrocyte count in the upper…
Figure 3. Chondrocyte count in the upper articular cartilage of the tibia (unit), compared between rats in the different study groups (G1, G2, G3, G4, G5 and G6), and between the right (target) and left (control) hind limbs. The same letter represents similarities and different letters represent significant differences between experimental groups, for the same side
Figure 4. Photomicrographs of the upper articular…
Figure 4. Photomicrographs of the upper articular cartilage from the right tibia of female rats, G1 (A), G2 (B), G3 (C), G4 (D), G5 (E and F) and G6 (G and H); frontal cut; hematoxylin and eosin stain. (A) Panoramic view of the articular cartilage (AC), with evidence of the tidemark (TM), and partial view of the subchondral bone (SB); (B) presence of cracks (C), flocculation (Fl) and tissue disorganization; (C) increased articular cartilage thickness, hypercellularity and increased number of isogenous groups (IG); (D) decreased articular cartilage thickness and normal cellular organization; (E) loss of articular cartilage (♦) with subchondral bone exposure; (F) presence of flocculation (Fl) on the cartilage surface; (G) restoration of the articular cartilage (♦) with pannus formation and presence of clones; (H) increased articular cartilage thickness, hypercellularity and increased isogenous groups
Figura 1. Espessura da cartilagem articular superior…
Figura 1. Espessura da cartilagem articular superior da tíbia, comparando-se as ratas distribuídas entre os grupos de estudo (G1, G2, G3, G4, G5 e G6) e os membros posteriores direito (alvo) e esquerdo (controle). Letras iguais significam semelhanças e letras diferentes significam diferenças significativas entre os grupos experimentais, para o mesmo lado
Figura 2. Espessura da placa epifisária da…
Figura 2. Espessura da placa epifisária da tíbia, comparando-se as ratas distribuídas entre os grupos de estudo (G1, G2, G3, G4, G5 e G6) e os membros posteriores direito (alvo) e esquerdo (controle). Letras iguais significam semelhanças e letras diferentes significam diferenças significativas entre os grupos experimentais, para o mesmo lado
Figura 3. Números de condrócitos na cartilagem…
Figura 3. Números de condrócitos na cartilagem articular superior da tíbia (unidade), comparando-se as ratas distribuídas entre os grupos de estudo (G1, G2, G3, G4, G5 e G6) e os membros posteriores direito (alvo) e esquerdo (controle). Letras iguais significam semelhanças e letras diferentes significam diferenças significativas entre os grupos experimentais, para o mesmo lado
Figura 4. Fotomicrografias da cartilagem articular superior…
Figura 4. Fotomicrografias da cartilagem articular superior da tíbia direita de ratas, G1 (A), G2 (B), G3 (C), G4 (D), G5 (E e F) e G6 (G e H); corte frontal; coloração em hematoxilina e eosina. (A) Vista panorâmica da cartilagem articular (CA), com evidência para a tidemark (TM) e visualização de parte de osso subcondral (OS); (B) presença de fissuras (F), floculações (Fl) e desorganização tecidual; (C) aumento da espessura da cartilagem articular, hipercelularidade e aumento do número de grupos isógenos (GI); (D) diminuição da espessura da cartilagem articular e organização celular normal; (E) perda da cartilagem articular (♦) com exposição de osso subcondral; (F) presença de floculações na superfície da cartilagem (FI); (G) recuperação da cartilagem articular (♦) com formação de pannus e presença de clones; (H) aumento da espessura da cartilagem articular, hipercelularidade e aumento de grupos isógenos

References

    1. Claassen H, Schlüter M, Schünke M, Kurz B. Influence of 17beta-estradiol and insulin on type II collagen and protein synthesis of articular chondrocytes. Bone. 2006;39(2):310–317.
    1. The North American Menopause Society . The menopause guidebook. 7a. 2012. 89
    1. Li S, Luo Q, Huang L, Hu Y, Xia Q, He C. Effects of pulsed electromagnetic fields on cartilage apoptosis signalling pathways in ovariectomised rats. Int Orthop. 2011;35(12):1875–1882.
    1. Høegh-Andersen P, Tankó LB, Andersen TL, Lundberg CV, Mo JA, Heegaard AM, et al. Ovariectomized rats as a model of postmenopausal osteoarthritis: validation and application. Arthritis Res Ther. 2004;6(2):R169–R180.
    1. Sniekers YH, Weinans H, Bierma-Zeinstra SM, van Leeuwen JP, van Osch GJ. Animal models for osteoarthritis: the effect of ovariectomy and estrogen treatment - a systematic approach. Osteartrites Cartilage. 2008;16(5):533–541. Review.
    1. Talwar R, Wong B, Svoboda K, Harper R. Effects of estrogen on chondrocyte proliferation and collagen synthesis in skeletally mature articular cartilage. J Oral Maxillofac Surg. 2006;64(4):600–609.
    1. Kunz RI, Coradini JG, Silva LI, Bertolini GR, Brancalhão RM, Ribeiro LF. Effects of immobilization and remobilization on the ankle joint in Wistar rats. Braz J Med Biol Res. J Med Biol Res. 2014;47(10):842–849.
    1. Brandt KD. Response of joint structures to inactivity and to reloading after immobilization. Arthritis Rheum. 2003;49(2):267–271. Review.
    1. Del Carlo R, Galvão M, Viloria M, Natali A, Barbosa A, Monteiro B, et al. Imobilização prolongada e remobilização da articulação fêmoro-tíbio-patelar de ratos: estudo clínico e microscópico. Arq Bras Med Vet Zootec. 2007;59(2):363–370.
    1. Ju YI, Sone T, Okamoto T, Fukunaga M. Jump exercise during remobilization restores integrity of the trabecular architecture after tail suspension in young rats. J Appl Physiol. 2008;104(6):1594–1600.
    1. Ocarino N, Silva J, Santiago L, Rocha C, Marubayashi U, Serakides R. Treadmill training before and/or after ovariectomy is more effective in preventing osteopenia in adult female rats. Sci Sports. 2009;24(1):52–55.
    1. Booth FW, Kelso JR. Effect of hind-limb immobilization on contractile and histochemical properties of skeletal muscle. Pflugers Arch. 1973;342(3):231–238.
    1. Matheus JP, Gomide LB, Oliveira JG, Volpon JB, Shimano AC. Efeitos da estimulação elétrica neuromuscular durante a imobilização nas propriedades mecânicas do músculo esquelético. Rev Bras Med Esporte. 2007;13(1):55–59.
    1. Richette P, Corvol M, Bardin T. Estrogens, cartilage, and osteoarthritis. Joint Bone Spine. 2003;70(4):257–262.
    1. Roman-Blas JA, Castañeda S, Largo R, Herrero-Beaumont G. Osteoarthritis associated with estrogen deficiency. 241Arthritis Res Ther. 2009;11(5) Review.
    1. Ando A, Suda H, Hagiwara Y, Onoda Y, Chimoto E, Saijo Y, et al. Reversibility of immobilization-induced articular cartilage degeneration after remobilization in rat knee joints. Tohoku J Exp Med. 2011;224(2):77–85.
    1. Vanwanseele B, Lucchinetti E, Stüssi E. The effects of immobilization on the characteristics of articular cartilage: current concepts and future directions. Osteartrites Cartilage. 2002;10(5):408–419. Review.
    1. Cavolina JM, Evans GL, Harris SA, Zhang M, Westerlind KC, Turner RT. The effects of orbital spaceflight on bone histomorphometry and messenger ribonucleic acid levels for bone matrix proteins and skeletal signaling peptides in ovariectomized growing rats. Endocrinology. 1997;138(4):1567–1576.
    1. Christensen B, Dyrberg E, Aagaard P, Kjaer M, Langberg H. Short-term immobilization and recovery affect skeletal muscle but not collagen tissue turnover in humans. J Appl Physiol (1985) 2008;105(6):1845–1851.
    1. Christensen B, Dyrberg E, Aagaard P, Enehjelm S, Krogsgaard M, Kjaer M, et al. Effects of long-term immobilization and recovery on human triceps surae and collagen turnover in the Achilles tendon in patients with healing ankle fracture. J Appl Physiol (1985) 2008;105(2):420–426.
    1. Arakaki K, Kitamura N, Kurokawa T, Onodera S, Kanaya F, Gong JP, et al. Joint immobilization inhibits spontaneous hyaline cartilage regeneration induced by a novel double-network gel implantation. J Mater Sci Mater Med. 2011;22(2):417–425.
    1. Hagiwara Y, Ando A, Chimoto E, Saijo Y, Ohmori-Matsuda K, Itoi E. Changes of articular cartilage after immobilization in a rat knee contracture model. J Orthop Res. 2009;27(2):236–242.
    1. Iqbal K. Effects of immobilization on chondrocytes and pericellular matrix in articular cartilage of patella in rats. J Morphol Sci. 2012;29(1):8–11.
    1. Iqbal K, Khan Y, Minhas LA. Effects of immobilization on thickness of superficial zone of articular cartilage of patella in rats. Indian J Orthop. 2012;46(4):391–394.
    1. Wolff RB, Gomes RC, do Amaral VC, Silva PL, Simoncini T, Prosdocimi FC, et al. Effects of hyperprolactinemia on the tibial epiphyseal plate of mice treated with sex hormones. Gynecol Endocrinol. 2015:1–4. Epub ahead of pint.
    1. Magliano M. Menopausal arthralgia: fact or fiction. Maturitas. 2010;67(1):29–33. Review.
    1. Narmoneva DA, Cheung HS, Wang JY, Howell DS, Setton LA. Altered swelling behavior of femoral cartilage following joint immobilization in a canine model. J Orthop Res. 2002;20(1):83–91.
    1. Leroux MA, Cheung HS, Bau JY, Wang JY, Howell DS, Setton LA. Altered mechanics and histomorphometry of canine tibial cartilage following joint immobilization. Osteartrites Cartilage. 2001;9(7):633–640.
    1. Portinho D, Boin VG, Bertolini GR. Efeitos Sobre o Tecido Ósseo e Cartilagem Articular Provocados Pela Imobilização e Remobilização em Ratos Wistar. Rev Bras Med Esporte. 2008;14(5):408–411.
    1. Cassilhas RE, Reis IT, Venâncio D, Fernandes J, Tufik S, Mello MT. Animal model for progressive resistance exercise : a detailed description of model and its implications for basic research in exercise. Motriz. 2013;19(1):178–184.
    1. Nascimento V, Krause W, Neto, Gonçalves L, Maifrino LB, Souza RR, Gama EF. Morphoquantitative analysis revealed Triceps Brachialis muscle hypertrophy by specific Resistance training equipment in rats. J Morphol Sci. 2013;30(4):276–280.
    1. Oliveira M, Oliveira B, Peres M, Coêlho J, Florindo P, Louzada M. Análise densitométrica e biomecânica de tíbias de ratos submetidos à suspensão pela cauda e exercício físico resistido. 292Arch Health Invest. 2013;2
    1. Oliveira BR, Silva ME, Medeiros RA, Apolinário-Coêlho J. A influência do treinamento físico resistido no tecido ósseo de ratos osteopênicos induzidos por suspensão pela cauda. 3009Arch Heal Investig. 2013;2(2)
    1. Chang TK, Huang CH, Huang CH, Chen HC, Cheng CK. The influence of long-term treadmill exercise on bone mass and articular cartilage in ovariectomized rats. BMC Musculoskelet Disord. 2010;11(185)
    1. Nagase H, Kashiwagi M. Aggrecanases and cartilage matrix degradation. Arthritis Res Ther. 2003;5(2):94–103. Review.
    1. Gonçalves G, Melo EG, Gomes MG, Nunes VA, Rezende CM. Effects of chondroitin sulfate and sodium hyaluronate on chondrocytes and extracellular matrix of articular cartilage in dogs with degenerative joint disease. Arq Bras Med Vet Zootec. 2008;60(1):93–102.

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