Effects of ultrasound on estradiol level, bone mineral density, bone biomechanics and matrix metalloproteinase‑13 expression in ovariectomized rabbits

Xia,Lu; He,Hongchen; Guo,Hua; Qing,Yuxi; He,Cheng‑Qi

doi:10.3892/etm.2015.2673

Effects of ultrasound on estradiol level, bone mineral density, bone biomechanics and matrix metalloproteinase‑13 expression in ovariectomized rabbits

Authors:
- Lu Xia
- Hongchen He
- Hua Guo
- Yuxi Qing
- Cheng‑Qi He
View Affiliations

Affiliations: Department of Rehabilitation, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P.R. China
Published online on: August 6, 2015 https://doi.org/10.3892/etm.2015.2673
Pages: 1429-1436

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The aim of the present study was to observe the effect of ultrasound (US) on estradiol level, bone mineral density (BMD), bone biomechanics and matrix metalloproteinase‑13 (MMP‑13) expression in ovariectomized (OVX) rabbits. A total of 28 virgin New Zealand white rabbits were randomly assigned into the following groups: Control (control group), ovariectomy (OVX group), ovariectomy with ultrasound therapy (US group) and ovariectomy with estrogen replacement therapy group (ERT group). At 8 weeks after ovariectomy, the US group received ultrasound treatment while the ERT group were orally treated with conjugated estrogens, and the control and OVX groups remained untreated. The estradiol level, BMD and bone biomechanics, cartilage histology and the MMP‑13 expression were analyzed after the intervention. The results indicate that the US treatment increased estradiol level, BMD and bone biomechanical function. Furthermore, the US treatment appeared to improve the recovery of cartilage morphology and decreased the expression of MMP‑13 in OVX models. Furthermore, the results suggest that 10 days of US therapy was sufficient to prevent the reduction of estradiol, BMD and bone biomechanical function, to protect osteoarthritis cartilage structure, and to reduce MMP‑13 transcription and expression in OVX rabbits. Therefore, US treatment may be a potential treatment for postmenopausal osteoarthritis and osteoporosis.

View Figures

View References

1	Abramson SB and Attur M: Developments in the scientific understanding of osteoarthritis. Arthritis Res Ther. 11:2272009. View Article : Google Scholar : PubMed/NCBI
2	Tetlow LC, Adlam DJ and Woolley DE: Matrix metalloproteinase and proinflammatory cytokine production by chondrocytes of human osteoarthritic cartilage: Associations with degenerative changes. Arthritis Rheum. 44:585–594. 2001. View Article : Google Scholar : PubMed/NCBI
3	Knäuper V, López-Otin C, Smith B, Knight G and Murphy G: Biochemical characterization of human collagenase-3. J Biol Chem. 271:1544–1550. 1996. View Article : Google Scholar : PubMed/NCBI
4	Poole AR, Kobayashi M, Yasuda T, Laverty S, Mwale F, Kojima T, Sakai T, Wahl C, El-Maadawy S, Webb G, et al: Type II collagen degradation and its regulation in articular cartilage in osteoarthritis. Ann Rheum Dis. 61 (Suppl 2):ii78–ii81. 2002. View Article : Google Scholar : PubMed/NCBI
5	Sun SS, Ma HL, Liu CL, Huang CH, Cheng CK and Wei HW: Difference in femoral head and neck material properties between osteoarthritis and osteoporosis. Clin Biomech (Bristol, Avon). 23 (Suppl 1):S39–S47. 2008. View Article : Google Scholar : PubMed/NCBI
6	Cooley HM, Stankovich J and Jones G: The association between hormonal and reproductive factors and hand osteoarthritis. Maturitas. 45:257–265. 2003. View Article : Google Scholar : PubMed/NCBI
7	Wluka AE, Cicuttini FM and Spector TD: Menopause, oestrogens and arthritis. Maturitas. 35:183–199. 2000. View Article : Google Scholar : PubMed/NCBI
8	Ivey JL and Baylink DJ: Postmenopausal osteoporosis : Proposed roles of defective coupling and estrogen deficiency. Metab Bone Dis Relat Res. 3:3–7. 1981. View Article : Google Scholar : PubMed/NCBI
9	Høegh-Andersen P, Tankó LB, Andersen TL, Lundberg CV, Mo JA, Heegaard AM, Delaissé JM and Christgau S: Ovariectomized rats as a model of postmenopausal osteoarthritis: Validation and application. Arthritis Res Ther. 6:R169–R180. 2004. View Article : Google Scholar : PubMed/NCBI
10	Dai G, Wang S, Li J, Liu C and Liu Q: The validity of osteoarthritis model induced by bilateral ovariectomy in guinea pig. J Huazhong Univ Sci Technolog Med Sci. 26:716–719. 2006. View Article : Google Scholar : PubMed/NCBI
11	Turner R, Maran A, Lotinun S, Hefferan T, Evans GL, Zhang M and Sibonga JD: Animal models for osteoporosis. Rev Endocr Metab Disord. 2:117–127. 2001. View Article : Google Scholar : PubMed/NCBI
12	Kalu DN: The ovariectomized rat model of postmenopausal bone loss. Bone Miner. 15:175–191. 1991. View Article : Google Scholar : PubMed/NCBI
13	RomanBlas JA, Castañeda S, Largo R and Herrero-Beaumont G: Osteoarthritis associated with estrogen deficiency. Arthritis Res Ther. 11:2412009. View Article : Google Scholar : PubMed/NCBI
14	Grady D, Rubin SM, Petitti DB, Fox CS, Black D, Ettinger B, Ernster VL and Cummings SR: Hormone therapy to prevent disease and prolong life in postmenopausal women. Ann Intern Med. 117:1016–1037. 1992. View Article : Google Scholar : PubMed/NCBI
15	Gallagher JC and Sai AJ: Molecular biology of bone remodeling: Implications for new therapeutic targets for osteoporosis. Maturitas. 65:301–307. 2010. View Article : Google Scholar : PubMed/NCBI
16	Baker KG, Robertson VJ and Duck FA: A review of therapeutic ultrasound: Biophysical effects. Phys Ther. 81:1351–1358. 2001.PubMed/NCBI
17	Tsumaki N, Kakiuchi M, Sasaki J, Ochi T and Yoshikawa H: Low-intensity pulsed ultrasound accelerates maturation of callus in patients treated with opening-wedge high tibial osteotomy by hemicallotasis. J Bone Joint Surg Am. 86-A:2399–2405. 2004.PubMed/NCBI
18	Shimazaki A, Inui K, Azuma Y, Nishimura N and Yamano Y: Low-intensity pulsed ultrasound accelerates bone maturation in distraction osteogenesis in rabbits. J Bone Joint Surg Br. 82:1077–1082. 2000. View Article : Google Scholar : PubMed/NCBI
19	Cook SD, Salkeld SL, Patron LP, Doughty ES and Jones DG: The effect of low-intensity pulsed ultrasound on autologous osteochondral plugs in a canine model. Am J Sports Med. 36:1733–1741. 2008. View Article : Google Scholar : PubMed/NCBI
20	Perry MJ, Parry LK, Burton VJ, Gheduzzi S, Beresford JN, Humphrey VF and Skerry TM: Ultrasound mimics the effect of mechanical loading on bone formation in vivo on rat ulnae. Med Eng Phys. 31:42–47. 2009. View Article : Google Scholar : PubMed/NCBI
21	Unsworth J, Kaneez S, Harris S, Ridgway J, Fenwick S, Chenery D and Harrison A: Pulsed low intensity ultrasound enhances mineralisation in preosteoblast cells. Ultrasound Med Biol. 33:1468–1474. 2007. View Article : Google Scholar : PubMed/NCBI
22	Nishikori T, Ochi M, Uchio Y, Maniwa S, Kataoka H, Kawasaki K, Katsube K and Kuriwaka M: Effects of low-intensity pulsed ultrasound on proliferation and chondroitin sulfate synthesis of cultured chondrocytes embedded in Atelocollagen gel. J Biomed Mater Res. 59:201–206. 2002. View Article : Google Scholar : PubMed/NCBI
23	Parvizi J, Wu CC, Lewallen DG, Greenleaf JF and Bolander ME: Low-intensity ultrasound stimulates proteoglycan synthesis in rat chondrocytes by increasing aggrecan gene expression. J Orthop Res. 17:488–494. 1999. View Article : Google Scholar : PubMed/NCBI
24	Loyola-Sánchez A, Richardson J and MacIntyre NJ: Efficacy of ultrasound therapy for the management of knee osteoarthritis: A systematic review with meta-analysis. Osteoarthritis Cartilage. 18:1117–1126. 2010. View Article : Google Scholar : PubMed/NCBI
25	Warden SJ, Bennell KL, Forwood MR, McMeeken JM and Wark JD: Skeletal effects of low-intensity pulsed ultrasound on the ovariectomized rodent. Ultrasound Med Biol. 27:989–998. 2001. View Article : Google Scholar : PubMed/NCBI
26	Castañeda S, Largo R, Calvo E, Rodríguez-Salvanés F, Marcos ME, Díaz-Curiel M and Herrero-Beaumont G: Bone mineral measurements of subchondral and trabecular bone in healthy and osteoporotic rabbits. Skeletal Radiol. 35:34–41. 2006. View Article : Google Scholar : PubMed/NCBI
27	Zeng D, Luo Q, Lin H, Zhang J and He C: The effect of therapeutic ultrasound to apoptosis of chondrocyte and caspase-3 and caspase-8 expression in rabbit surgery-induced model of knee osteoarthritis. Rheumatol Int. 32:3771–3777. 2012. View Article : Google Scholar : PubMed/NCBI
28	Chen J, Huang LQ, Xia QJ and He C-Q: Effects of pulsed electromagnetic fields on the mRNA expression of CAII and RANK in ovariectomized rats. Rheumatol Int. 32:1527–1532. 2012. View Article : Google Scholar : PubMed/NCBI
29	Li S, Luo Q, Huang L, Hu Y, Xia Q and He C: Effects of pulsed electromagnetic fields on cartilage apoptosis signalling pathways in ovariectomised rats. Int Orthop. 35:1875–1882. 2011. View Article : Google Scholar : PubMed/NCBI
30	Mazess R, Collick B, Trempe J, Barden H and Hanson J: Performance evaluation of a dual energy x-ray bone densitometer. Calcif Tissue Int. 44:2281989. View Article : Google Scholar : PubMed/NCBI
31	Cohen B and Rushton N: Accuracy of DEXA measurement of bone mineral density after total hip arthroplasty. J Bone Joint Surg Br. 77:4791995.PubMed/NCBI
32	Mankin H, Dorfman H, Lippiello L and Zarins A: Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am. 53:523–537. 1971.PubMed/NCBI
33	Kanis JA: Estrogens, the menopause and osteoporosis. Bone. 19 (Suppl 5):185S–190S. 1996. View Article : Google Scholar : PubMed/NCBI
34	Lu T, Achari Y, Rattner JB and Hart DA: Evidence that estrogen receptor enhances MMP-13 promoter activity in HIG-82 cells and that this enhancement can be influenced by ligands and involves specific promoter sites. Biochem Cell Biol. 85:326–336. 2007. View Article : Google Scholar : PubMed/NCBI
35	Dören M: Estrogen therapy for prevention and treatment of osteoporosis. Maturitas. 43 (Suppl):S53–S56. 2002. View Article : Google Scholar : PubMed/NCBI
36	Torgerson DJ and Bell-Syer SE: Hormone replacement therapy and prevention of nonvertebral fractures: A meta-analysis of randomized trials. JAMA. 285:2891–2897. 2001. View Article : Google Scholar : PubMed/NCBI
37	Bourrin S, Ammann P, Bonjour JP and Rizzoli R: Recovery of proximal tibia bone mineral density and strength, but not cancellous bone architecture, after long-term bisphosphonate or selective estrogen receptor modulator therapy in aged rats. Bone. 30:195–200. 2002. View Article : Google Scholar : PubMed/NCBI
38	Buchtala V: Present state of ultrasound therapy. Dia Med. 22:2944–2950. 1950.PubMed/NCBI
39	Claes L and Willie B: The enhancement of bone regeneration by ultrasound. Prog Biophys Mol Biol. 93:384–398. 2007. View Article : Google Scholar : PubMed/NCBI
40	Chang WH, Sun JS, Chang SP and Lin JC: Study of thermal effects of ultrasound stimulation on fracture healing. Bioelectromagnetics. 23:256–263. 2002. View Article : Google Scholar : PubMed/NCBI
41	Dyson M: Non-thermal cellular effects of ultrasound. Br J Cancer. Suppl:165–171. 1982.
42	Sakurakichi K, Tsuchiya H, Uehara K, Yamashiro T, Tomita K and Azuma Y: Effects of timing of low-intensity pulsed ultrasound on distraction osteogenesis. J Orthop Res. 22:395–403. 2004. View Article : Google Scholar : PubMed/NCBI
43	Uglow MG, Peat RA, Hile MS, Bilston LE, Smith EJ and Little DG: Low-intensity ultrasound stimulation in distraction osteogenesis in rabbits. Clin Orthop Relat Res. 303–312. 2003.PubMed/NCBI
44	Tis JE, Meffert RH, Inoue N, McCarthy EF, Machen MS, McHale KA and Chao EY: The effect of low intensity pulsed ultrasound applied to rabbit tibiae during the consolidation phase of distraction osteogenesis. J Orthop Res. 20:793–800. 2002. View Article : Google Scholar : PubMed/NCBI
45	Lim D, Ko CY, Seo DH, Woo DG, Kim JM, Chun KJ and Kim HS: Low-intensity ultrasound stimulation prevents osteoporotic bone loss in young adult ovariectomized mice. J Orthop Res. 29:116–125. 2011. View Article : Google Scholar : PubMed/NCBI
46	Yang KGA, Saris DBF, Dhert WJA and Verbout AJ: Osteoarthritis of the knee: Current treatment options and future directions. Curr Orthop. 18:311–320. 2004. View Article : Google Scholar
47	Claassen H, Schluter M, Schunke M and Kurz B: Influence of 17beta-estradiol and insulin on type II collagen and protein synthesis of articular chondrocytes. Bone. 39:310–317. 2006. View Article : Google Scholar : PubMed/NCBI
48	Lee YJ, Lee EB, Kwon YJ, Lee JJ, Cho WS, Kim HA and Song YW: Effect of estrogen on the expression of matrix metalloproteinase (MMP)-1, MMP-3 and MMP-13 and tissue inhibitor of metalloproternase-1 in osteoarthritis chondrocytes. Rheumatol Int. 23:282–288. 2003. View Article : Google Scholar : PubMed/NCBI
49	Lu T, Achari Y, Sciore P and Hart DA: Estrogen receptor alpha regulates matrix metalloproteinase-13 promoter activity primarily through the AP-1 transcriptional regulatory site. Biochim Biophys Acta. 1762:719–731. 2006. View Article : Google Scholar : PubMed/NCBI
50	Gurkan I, Ranganathan A, Yang X, Horton WE Jr, Todman M, Huckle J, Pleshko N and Spencer RG: Modification of osteoarthritis in the guinea pig with pulsed low-intensity ultrasound treatment. Osteoarthritis Cartilage. 18:724–733. 2010. View Article : Google Scholar : PubMed/NCBI
51	Naito K, Watari T, Muta T, Furuhata A, Iwase H, Igarashi M, Kurosawa H, Nagaoka I and Kaneko K: Low-intensity pulsed ultrasound (LIPUS) increases the articular cartilage type II collagen in a rat osteoarthritis model. J Orthop Res. 28:361–369. 2009.
52	Park K, Hoffmeister B, Han DK and Hasty K: Therapeutic ultrasound effects on interleukin-1beta stimulated cartilage construct in vitro. Ultrasound Med Biol. 33:286–295. 2007. View Article : Google Scholar : PubMed/NCBI
53	Collaborative Group on Hormonal Factors in Breast Cancer, . Breast cancer and hormone replacement therapy: Collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Lancet. 350:1047–1059. 1997. View Article : Google Scholar : PubMed/NCBI
54	Grady D, Gebretsadik T, Kerlikowske K, Ernster V and Petitti D: Hormone replacement therapy and endometrial cancer risk: A meta-analysis. Obstet Gynecol. 85:304–313. 1995. View Article : Google Scholar : PubMed/NCBI
55	Rodriguez C, Patel AV, Calle EE, Jacob EJ and Thun MJ: Estrogen replacement therapy and ovarian cancer mortality in a large prospective study of US women. JAMA. 285:1460–1465. 2001. View Article : Google Scholar : PubMed/NCBI