Top

Osteoporosis International

Published in:

01-04-2017 | Original Article

Jumping exercise preserves bone mineral density and mechanical properties in osteopenic ovariectomized rats even following established osteopenia

Authors: R . Okubo, L. S. Sanada, V. A. Castania, M. J. Q. Louzada, F. J. A. de Paula, N. Maffulli, A. C. Shimano

Published in: Osteoporosis International | Issue 4/2017

Abstract

Summary

The effects of jump training on bone structure before and after ovariectomy-induced osteopenia in rats were investigated. Jumping exercise induced favorable changes in bone mineral density, bone mechanical properties, and bone formation/resorption markers. This exercise is effective to prevent bone loss after ovariectomy even when osteopenia is already established.

Introduction

The present study investigated the effects of jump training on bone structure before and after ovariectomy-induced osteopenia in 80 10-week-old Wistar rats.

Methods

Forty rats (prevention program) were randomly allocated to one of four equal groups (n = 10): sham-operated sedentary (SHAM-SEDp), ovariectomized (OVX) sedentary (OVX-SEDp), sham-operated exercised (SHAM-EXp), and OVX exercised (OVX-EXp). SHAM-EXp and OVX-EXp animals began training 3 days after surgery. Another 40 rats (treatment program) were randomly allocated into another four groups (n = 10): sham-operated sedentary (SHAM-SEDt), OVX sedentary (OVX-SEDt), sham-operated exercised (SHAM-EXt), and OVX exercised (OVX-EXt). SHAM-EXt and OVX-EXt animals began training 60 days after surgery. The rats in the exercised groups jumped 20 times/day, 5 days/week, to a height of 40 cm for 12 weeks. At the end of the experimental period, serum osteocalcin, follicle-stimulating hormone (FSH) dosage, dual X-ray absorptiometry (DXA), histomorphometry, and biomechanical tests were analyzed.

Results

The OVX groups showed higher values of FSH and body weight (p < 0.05). DXA showed that jump training significantly increased bone mineral density of the femur and fifth lumbar vertebra (p < 0.05). The stiffness of the left femur and fifth lumbar vertebra in the exercised groups was greater than that of the sedentary groups (p < 0.05). Ovariectomy induced significant difference in bone volume (BV/TV, percent), trabecular separation (Tb.Sp, micrometer), and trabecular number (Tb.N, per millimeter) (p < 0.05) compared to sham operation. Jump training in the OVX group induced significant differences in BV/TV, Tb.Sp, and Tb.N and decreased osteoblast number per bone perimeter (p < 0.05) compared with OVX nontraining, in the prevention groups. Osteocalcin dosage showed higher values in the exercised groups (p < 0.05).

Conclusions

Jumping exercise induced favorable changes in bone mineral density, bone mechanical properties, and bone formation/resorption markers. Jump training is effective to prevent bone loss after ovariectomy even when osteopenia is already established.

Kanis JA (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int 4(6):368–381CrossRefPubMed

Sirola J, Diaz Curiel M, Honkanen R, Iwamoto J (2011) New issues in the management of osteoporosis. J Osteoporos 2011:582789. doi:10.4061/2011/582789 PubMedPubMedCentral

Compston J (2011) Pathophysiology of atypical femoral fractures and osteonecrosis of the jaw. Osteoporos Int 22(12):2951–2961. doi:10.1007/s00198-011-1804-x CrossRefPubMed

Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA (2009) Exercise and bone mass in adults. Sports Med 39(6):439–468CrossRefPubMed

Abrahin O, Rodrigues RP, Marcal AC, Alves EA, Figueiredo RC, de Sousa EC (2016) Swimming and cycling do not cause positive effects on bone mineral density: a systematic review. Rev Bras Reumatol Engl Ed 56(4):345–351. doi:10.1016/j.rbre.2016.02.013 CrossRefPubMed

Nikander R, Sievanen H, Heinonen A, Kannus P (2005) Femoral neck structure in adult female athletes subjected to different loading modalities. J Bone Miner Res 20(3):520–528. doi:10.1359/JBMR.041119 CrossRefPubMed

Nikander R, Sievänen H, Heinonen A, Daly RM, Uusi-Rasi K, Kannus P (2010) Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med 8:47. doi:10.1186/1741-7015-8-47 CrossRefPubMedPubMedCentral

Ju YI, Sone T, Ohnaru K, Choi HJ, Choi KA, Fukunaga M (2013) Jump exercise during hindlimb unloading protect against the deterioration of trabecular bone microarchitecture in growing young rats. Springerplus 2(1):35. doi:10.1186/2193-1801-2-35 CrossRefPubMedPubMedCentral

Ju YI, Sone T, Ohnaru K, Choi HJ, Fukunaga M (2012) Differential effects of jump versus running exercise on trabecular architecture during remobilization after suspension-induced osteopenia in growing rats. J Appl Physiol (1985) 112(5):766–772. doi:10.1152/japplphysiol.01219.2011 CrossRef

10.

Kato T, Terashima T, Yamashita T, Hatanaka Y, Honda A, Umemura Y (2006) Effect of low-repetition jump training on bone mineral density in young women. J Appl Physiol (1985) 100(3):839–843. doi:10.1152/japplphysiol.00666.2005 CrossRef

11.

Lespessailles E, Gadois C, Lemineur G, Do-Huu JP, Benhamou L (2007) Bone texture analysis on direct digital radiographic images: precision study and relationship with bone mineral density at the os calcis. Calcif Tissue Int 80(2):97–102. doi:10.1007/s00223-006-0216-y CrossRefPubMed

12.

McKay HA, MacLean L, Petit M, MacKelvie-O’Brien K, Janssen P, Beck T, Khan KM (2005) “Bounce at the Bell”: a novel program of short bouts of exercise improves proximal femur bone mass in early pubertal children. Br J Sports Med 39(8):521–526. doi:10.1136/bjsm.2004.014266 CrossRefPubMedPubMedCentral

13.

Kalu DN (1991) The ovariectomized rat model of postmenopausal bone loss. Bone Miner 15(3):175–191CrossRefPubMed

14.

Wronski TJ, Dann LM, Scott KS, Cintron M (1989) Long-term effects of ovariectomy and aging on the rat skeleton. Calcif Tissue Int 45(6):360–366CrossRefPubMed

15.

Wronski TJ, Dann LM, Horner SL (1989) Time course of vertebral osteopenia in ovariectomized rats. Bone 10(4):295–301CrossRefPubMed

16.

Lelovas PP, Xanthos TT, Thoma SE, Lyritis GP, Dontas IA (2008) The laboratory rat as an animal model for osteoporosis research. Comparative medicine 58(5):424–430PubMedPubMedCentral

17.

Li M, Shen Y, Wronski TJ (1997) Time course of femoral neck osteopenia in ovariectomized rats. Bone 20(1):55–61CrossRefPubMed

18.

Umemura Y, Ishiko T, Tsujimoto H, Miura H, Mokushi N, Suzuki H (1995) Effects of jump training on bone hypertrophy in young and old rats. Int J Sports Med 16(6):364–367. doi:10.1055/s-2007-973021 CrossRefPubMed

19.

Umemura Y, Ishiko T, Yamauchi T, Kurono M, Mashiko S (1997) Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res 12(9):1480–1485. doi:10.1359/jbmr.1997.12.9.1480 CrossRefPubMed

20.

Ju YI, Sone T, Ohnaru K, Tanaka K, Yamaguchi H, Fukunaga M (2014) Effects of different types of jump impact on trabecular bone mass and microarchitecture in growing rats. PLoS One 9(9):e107953. doi:10.1371/journal.pone.0107953 CrossRefPubMedPubMedCentral

21.

Falcai MJ, Zamarioli A, Okubo R, de Paula FJ, Volpon JB (2015) The osteogenic effects of swimming, jumping, and vibration on the protection of bone quality from disuse bone loss. Scand J Med Sci Sports 25(3):390–397. doi:10.1111/sms.12240 CrossRefPubMed

22.

Hogan HA, Ruhmann SP, Sampson HW (2000) The mechanical properties of cancellous bone in the proximal tibia of ovariectomized rats. J Bone Miner Res 15(2):284–292. doi:10.1359/jbmr.2000.15.2.284 CrossRefPubMed

23.

Monteiro LO, Macedo AP, Shimano RC, Shimano AC, Yanagihara GR, Ramos J, Paulini MR, Tocchini de Figueiredo FA, Gonzaga MG, Issa JP (2016) Effect of treatment with simvastatin on bone microarchitecture of the femoral head in an osteoporosis animal model. Microsc Res Tech 79(8):684–690. doi:10.1002/jemt.22682 CrossRefPubMed

24.

Revell PA (1983) Histomorphometry of bone. J Clin Pathol 36(12):1323–1331CrossRefPubMedPubMedCentral

25.

Flieger J, Karachalios T, Khaldi L, Raptou P, Lyritis G (1998) Mechanical stimulation in the form of vibration prevents postmenopausal bone loss in ovariectomized rats. Calcif Tissue Int 63(6):510–514CrossRefPubMed

26.

Joo YI, Sone T, Fukunaga M, Lim SG, Onodera S (2003) Effects of endurance exercise on three-dimensional trabecular bone microarchitecture in young growing rats. Bone 33(4):485–493CrossRefPubMed

27.

Snow-Harter C, Marcus R (1991) Exercise, bone mineral density, and osteoporosis. Exerc Sport Sci Rev 19:351–388CrossRefPubMed

28.

Swissa-Sivan A, Azoury R, Statter M, Leichter I, Nyska A, Nyska M, Menczel J, Samueloff S (1990) The effect of swimming on bone modeling and composition in young adult rats. Calcif Tissue Int 47(3):173–177CrossRefPubMed

29.

Honda A, Sogo N, Nagasawa S, Kato T, Umemura Y (2008) Bones benefits gained by jump training are preserved after detraining in young and adult rats. J Appl Physiol (1985) 105(3):849–853. doi:10.1152/japplphysiol.00902.2007 CrossRef

30.

Umemura Y, Nagasawa S, Sogo N, Honda A (2008) Effects of jump training on bone are preserved after detraining, regardless of estrogen secretion state in rats. J Appl Physiol (1985) 104(4):1116–1120. doi:10.1152/japplphysiol.00937.2007 CrossRef

31.

Huang TH, Lin SC, Chang FL, Hsieh SS, Liu SH, Yang RS (2003) Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone. J Appl Physiol (1985) 95(1):300–307. doi:10.1152/japplphysiol.01076.2002 CrossRef

32.

Iwamoto J, Shimamura C, Takeda T, Abe H, Ichimura S, Sato Y, Toyama Y (2004) Effects of treadmill exercise on bone mass, bone metabolism, and calciotropic hormones in young growing rats. J Bone Miner Metab 22(1):26–31. doi:10.1007/s00774-003-0443-5 CrossRefPubMed

33.

Xie L, Jacobson JM, Choi ES, Busa B, Donahue LR, Miller LM, Rubin CT, Judex S (2006) Low-level mechanical vibrations can influence bone resorption and bone formation in the growing skeleton. Bone 39(5):1059–1066. doi:10.1016/j.bone.2006.05.012 CrossRefPubMed

34.

Yang P, Jia B, Ding C, Wang Z, Qian A, Shang P (2009) Whole-body vibration effects on bone before and after hind-limb unloading in rats. Aviat Space Environ Med 80(2):88–93CrossRefPubMed

35.

Kuller LH, Gutai JP, Meilahn E, Matthews KA, Plantinga P (1990) Relationship of endogenous sex steroid hormones to lipids and apoproteins in postmenopausal women. Arteriosclerosis 10(6):1058–1066CrossRefPubMed

36.

Barengolts EI, Curry DJ, Bapna MS, Kukreja SC (1993) Effects of endurance exercise on bone mass and mechanical properties in intact and ovariectomized rats. J Bone Miner Res 8(8):937–942. doi:10.1002/jbmr.5650080806 CrossRefPubMed

37.

Yarrow JF, Conover CF, Purandare AV, Bhakta AM, Zheng N, Conrad B, Altman MK, Franz SE, Wronski TJ, Borst SE (2008) Supraphysiological testosterone enanthate administration prevents bone loss and augments bone strength in gonadectomized male and female rats. Am J Phys Endocrinol Metab 295(5):E1213–E1222. doi:10.1152/ajpendo.90640.2008 CrossRef

38.

Fu SW, Zeng GF, Zong SH, Zhang ZY, Zou B, Fang Y, Lu L, Xiao DQ (2014) Systematic review and meta-analysis of the bone protective effect of phytoestrogens on osteoporosis in ovariectomized rats. Nutr Res 34(6):467–477. doi:10.1016/j.nutres.2014.05.003 CrossRefPubMed

39.

Wu ZX, Lei W, Hu YY, Wang HQ, Wan SY, Ma ZS, Sang HX, Fu SC, Han YS (2008) Effect of ovariectomy on BMD, micro-architecture and biomechanics of cortical and cancellous bones in a sheep model. Med Eng Phys 30(9):1112–1118. doi:10.1016/j.medengphy.2008.01.007 CrossRefPubMed

40.

Chen L, Yang L, Yao M, Cui XJ, Xue CC, Wang YJ, Shu B (2016) Biomechanical characteristics of osteoporotic fracture healing in ovariectomized rats: a systematic review. PLoS One 11(4):e0153120. doi:10.1371/journal.pone.0153120 CrossRefPubMedPubMedCentral

41.

Johnston BD, Ward WE (2015) The ovariectomized rat as a model for studying alveolar bone loss in postmenopausal women. Biomed Res Int 2015:635023. doi:10.1155/2015/635023 CrossRefPubMedPubMedCentral

42.

Komori T (2015) Animal models for osteoporosis. Eur J Pharmacol 759:287–294. doi:10.1016/j.ejphar.2015.03.028 CrossRefPubMed

43.

Aswar UM, Mohan V, Bodhankar SL (2012) Antiosteoporotic activity of phytoestrogen-rich fraction separated from ethanol extract of aerial parts of Cissus quadrangularis in ovariectomized rats. Indian J Pharmacol 44(3):345–350. doi:10.4103/0253-7613.96310 CrossRefPubMedPubMedCentral

44.

Honda A, Umemura Y, Nagasawa S (2001) Effect of high-impact and low-repetition training on bones in ovariectomized rats. J Bone Miner Res 16(9):1688–1693. doi:10.1359/jbmr.2001.16.9.1688 CrossRefPubMed

45.

Turner RT, Vandersteenhoven JJ, Bell NH (1987) The effects of ovariectomy and 17 beta-estradiol on cortical bone histomorphometry in growing rats. J Bone Miner Res 2(2):115–122. doi:10.1002/jbmr.5650020206 CrossRefPubMed

46.

Turner CH (2006) Bone strength: current concepts. Ann N Y Acad Sci 1068:429–446. doi:10.1196/annals.1346.039 CrossRefPubMed

47.

Stengel SV, Kemmler W, Pintag R, Beeskow C, Weineck J, Lauber D, Kalender WA, Engelke K (2005) Power training is more effective than strength training for maintaining bone mineral density in postmenopausal women. J Appl Physiol (1985) 99(1):181–188. doi:10.1152/japplphysiol.01260.2004 CrossRef

48.

Fuchs RK, Bauer JJ, Snow CM (2001) Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res 16(1):148–156. doi:10.1359/jbmr.2001.16.1.148 CrossRefPubMed

49.

Heinonen A, Kannus P, Sievänen H, Oja P, Pasanen M, Rinne M, Uusi-Rasi K, Vuori I (1996) Randomised controlled trial of effect of high-impact exercise on selected risk factors for osteoporotic fractures. Lancet 348(9038):1343–1347. doi:10.1016/s0140-6736(96)04214-6 CrossRefPubMed

50.

Schett G, Kiechl S, Redlich K, Oberhollenzer F, Weger S, Egger G, Mayr A, Jocher J, Xu Q, Pietschmann P, Teitelbaum S, Smolen J, Willeit J (2004) Soluble RANKL and risk of nontraumatic fracture. JAMA 291(9):1108–1113. doi:10.1001/jama.291.9.1108 CrossRefPubMed

51.

Findlay DM, Atkins GJ (2011) Relationship between serum RANKL and RANKL in bone. Osteoporos Int 22(10):2597–2602. doi:10.1007/s00198-011-1740-9 CrossRefPubMed

52.

Uemura H, Yasui T, Miyatani Y, Yamada M, Hiyoshi M, Arisawa K, Irahara M (2008) Circulating profiles of osteoprotegerin and soluble receptor activator of nuclear factor kappaB ligand in post-menopausal women. J Endocrinol Investig 31(2):163–168CrossRef

53.

Anderson PH, Atkins GJ, Turner AG, Kogawa M, Findlay DM, Morris HA (2011) Vitamin D metabolism within bone cells: effects on bone structure and strength. Mol Cell Endocrinol 347(1–2):42–47. doi:10.1016/j.mce.2011.05.024 CrossRefPubMed

54.

Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Spelsberg TC, Riggs BL (1999) Estrogen stimulates gene expression and protein production of osteoprotegerin in human osteoblastic cells. Endocrinology 140(9):4367–4370. doi:10.1210/endo.140.9.7131 PubMed

Title: Jumping exercise preserves bone mineral density and mechanical properties in osteopenic ovariectomized rats even following established osteopenia
Authors: R . Okubo
L. S. Sanada
V. A. Castania
M. J. Q. Louzada
F. J. A. de Paula
N. Maffulli
A. C. Shimano
Publication date: 01-04-2017
Publisher: Springer London
Published in: Osteoporosis International / Issue 4/2017
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI: https://doi.org/10.1007/s00198-017-3905-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Jumping exercise preserves bone mineral density and mechanical properties in osteopenic ovariectomized rats even following established osteopenia

Abstract

Summary

Introduction

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Summary

Introduction

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 4/2017

Comparison of peripheral quantitative computed tomography forearm bone density versus DXA in rheumatoid arthritis patients and controls

The prevalence of osteoporosis and the rate of bone loss in Korean adults: the Chungju metabolic disease cohort (CMC) study

Socioeconomic inequality in clinical outcome among hip fracture patients: a nationwide cohort study

Frequency of discontinuation of injectable osteoporosis therapies in US patients over 2 years

Use of antipsychotics increases the risk of fracture: a systematic review and meta-analysis

Long-term effect of aromatase inhibitors on bone microarchitecture and macroarchitecture in non-osteoporotic postmenopausal women with breast cancer