DOI QR코드

DOI QR Code

Effect of Dietary Calcium on Spinal Bone Fusion in an Ovariectomized Rat Model

  • Cho, Jae-Hoon (Department of Neurosurgery, School of Medicine, Kyungpook National University) ;
  • Cho, Dae-Chul (Department of Neurosurgery, School of Medicine, Kyungpook National University) ;
  • Yu, Song-Hee (Department of Neurosurgery, School of Medicine, Kyungpook National University) ;
  • Jeon, Young-Hoon (Department of Anesthesiology and Pain Medicine, School of Dentistry, Kyungpook National University) ;
  • Sung, Joo-Kyung (Department of Neurosurgery, School of Medicine, Kyungpook National University) ;
  • Kim, Kyoung-Tae (Department of Neurosurgery, School of Medicine, Kyungpook National University)
  • Received : 2012.04.10
  • Accepted : 2012.10.04
  • Published : 2012.10.28

Abstract

Objective : To evaluate the effect of calcium supplementation on spinal bone fusion in ovariectomized (OVX) rats. Methods : Sixteen female Sprague Dawley rats underwent bilateral ovariectomy at 12 weeks of age to induce osteoporosis and were randomly assigned to two groups : control group (n=8) and calcium-supplemented group (OVX-Ca, n=8). Autologous spinal bone fusion surgery was performed on both groups 8 weeks later. After fusion surgery, the OVX-Ca group was supplemented with calcium in drinking water for 8 weeks. Blood was obtained 4 and 8 weeks after fusion surgery. Eight weeks after fusion surgery, the rats were euthanized and the L4-5 spine removed. Bone fusion status and fusion volume were evaluated by manual palpation and three-dimensional computed tomography. Results : The mean fusion volume in the L4-5 spine was significantly greater in the OVX-Ca group ($71.80{\pm}8.06mm^3$) than in controls ($35.34{\pm}8.24mm^3$) (p<0.01). The level of osteocalcin, a bone formation marker, was higher in OVX-Ca rats than in controls 4 weeks ($610.08{\pm}10.41$ vs. $551.61{\pm}12.34$ ng/mL) and 8 weeks ($552.05{\pm}19.67$ vs. $502.98{\pm}22.76$ ng/mL) after fusion surgery (p<0.05). The level of C-terminal telopeptide fragment of type I collagen, a bone resorption marker, was significantly lower in OVX-Ca rats than in controls 4 weeks ($77.07{\pm}12.57$ vs. $101.75{\pm}7.20$ ng/mL) and 8 weeks ($69.58{\pm}2.45$ vs. $77.15{\pm}4.10$ ng/mL) after fusion surgery (p<0.05). A mechanical strength test showed that the L4-5 vertebrae in the OVX-Ca group withstood a 50% higher maximal load compared with the controls (p<0.01). Conclusion : Dietary calcium given to OVX rats after lumbar fusion surgery improved fusion volume and mechanical strength in an ovariectomized rat model.

Keywords

References

  1. Abe Y, Takahata M, Ito M, Irie K, Abumi K, Minami A : Enhancement of graft bone healing by intermittent administration of human parathyroid hormone (1-34) in a rat spinal arthrodesis model. Bone 41 : 775- 785, 2007 https://doi.org/10.1016/j.bone.2007.06.025
  2. Balena R, Toolan BC, Shea M, Markatos A, Myers ER, Lee SC, et al. : The effects of 2-year treatment with the aminobisphosphonate alendronate on bone metabolism, bone histomorphometry, and bone strength in ovariectomized nonhuman primates. J Clin Invest 92 : 2577-2586, 1993 https://doi.org/10.1172/JCI116872
  3. Boden SD : Overview of the biology of lumbar spine fusion and principles for selecting a bone graft substitute. Spine (Phila Pa 1976) 27 : S26- S31, 2002 https://doi.org/10.1097/00007632-200208151-00007
  4. Borgstrom F, Strom O, Marin F, Kutahov A, Ljunggren O : Cost effectiveness of teriparatide and PTH(1-84) in the treatment of postmenopausal osteoporosis. J Med Econ 13 : 381-392, 2010 https://doi.org/10.3111/13696998.2010.499072
  5. Bridwell KH, Sedgewick TA, O'Brien MF, Lenke LG, Baldus C : The role of fusion and instrumentation in the treatment of degenerative spondylolisthesis with spinal stenosis. J Spinal Disord 6 : 461-472, 1993 https://doi.org/10.1097/00002517-199306060-00001
  6. Chen H, Hayakawa D, Emura S, Ozawa Y, Okumura T, Shoumura S : Effect of low or high dietary calcium on the morphology of the rat femur. Histol Histopathol 17 : 1129-1135, 2002
  7. Dempster DW, Cosman F, Kurland ES, Zhou H, Nieves J, Woelfert L, et al. : Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis : a paired biopsy study. J Bone Miner Res 16 : 1846-1853, 2001 https://doi.org/10.1359/jbmr.2001.16.10.1846
  8. Dempster DW, Lindsay R : Pathogenesis of osteoporosis. Lancet 341 : 797-801, 1993 https://doi.org/10.1016/0140-6736(93)90570-7
  9. Diamond TH, Clark WA, Kumar SV : Histomorphometric analysis of fracture healing cascade in acute osteoporotic vertebral body fractures. Bone 40 : 775-780, 2007 https://doi.org/10.1016/j.bone.2006.10.009
  10. Erulkar JS, Grauer JN, Patel TC, Panjabi MM : Flexibility analysis of posterolateral fusions in a New Zealand white rabbit model. Spine (Phila Pa 1976) 26 : 1125-1130, 2001 https://doi.org/10.1097/00007632-200105150-00006
  11. Fischgrund JS, Mackay M, Herkowitz HN, Brower R, Montgomery DM, Kurz LT : 1997 Volvo Award winner in clinical studies. Degenerative lumbar spondylolisthesis with spinal stenosis : a prospective, randomized study comparing decompressive laminectomy and arthrodesis with and without spinal instrumentation. Spine (Phila Pa 1976) 22 : 2807-2812, 1997 https://doi.org/10.1097/00007632-199712150-00003
  12. France JC, Yaszemski MJ, Lauerman WC, Cain JE, Glover JM, Lawson KJ, et al. : A randomized prospective study of posterolateral lumbar fusion. Outcomes with and without pedicle screw instrumentation. Spine (Phila Pa 1976) 24 : 553-560, 1999 https://doi.org/10.1097/00007632-199903150-00010
  13. French DL, Muir JM, Webber CE : The ovariectomized, mature rat model of postmenopausal osteoporosis : an assessment of the bone sparing effects of curcumin. Phytomedicine 15 : 1069-1078, 2008 https://doi.org/10.1016/j.phymed.2008.06.007
  14. Fu L, Tang T, Miao Y, Hao Y, Dai K : Effect of 1,25-dihydroxy vitamin D3 on fracture healing and bone remodeling in ovariectomized rat femora. Bone 44 : 893-898, 2009 https://doi.org/10.1016/j.bone.2009.01.378
  15. Gala J, Díaz-Curiel M, de la Piedra C, Calero J : Short- and long-term effects of calcium and exercise on bone mineral density in ovariectomized rats. Br J Nutr 86 : 521-527, 2001 https://doi.org/10.1079/BJN2001428
  16. Garcia-Contreras F, Paniagua R, Avila-Diaz M, Cabrera-Munoz L, Martinez- Muniz I, Foyo-Niembro E, et al. : Cola beverage consumption induces bone mineralization reduction in ovariectomized rats. Arch Med Res 31 : 360-365, 2000 https://doi.org/10.1016/S0188-4409(00)00090-4
  17. Gasser JA, Ingold P, Venturiere A, Shen V, Green JR : Long-term protective effects of zoledronic acid on cancellous and cortical bone in the ovariectomized rat. J Bone Miner Res 23 : 544-551, 2008
  18. Gezici AR, Ergun R, Gurel K, Yilmaz F, Okay O, Bozdogan O : The effect of risedronate on posterior lateral spinal fusion in a rat model. J Korean Neurosurg Soc 46 : 45-51, 2009 https://doi.org/10.3340/jkns.2009.46.1.45
  19. Giannoudis P, Tzioupis C, Almalki T, Buckley R : Fracture healing in osteoporotic fractures : is it really different? A basic science perspective. Injury 38 Suppl 1 : S90-S99, 2007
  20. Grases F, Sanchis P, Prieto RM, Perello J, Lopez-Gonzalez AA : Effect of tetracalcium dimagnesium phytate on bone characteristics in ovariectomized rats. J Med Food 13 : 1301-1306, 2010 https://doi.org/10.1089/jmf.2009.0152
  21. Hao YJ, Zhang G, Wang YS, Qin L, Hung WY, Leung K, et al. : Changes of microstructure and mineralized tissue in the middle and late phase of osteoporotic fracture healing in rats. Bone 41 : 631-638, 2007 https://doi.org/10.1016/j.bone.2007.06.006
  22. Hidaka C, Goshi K, Rawlins B, Boachie-Adjei O, Crystal RG : Enhancement of spine fusion using combined gene therapy and tissue engineering BMP-7-expressing bone marrow cells and allograft bone. Spine (Phila Pa 1976) 28 : 2049-2057, 2003 https://doi.org/10.1097/01.BRS.0000091661.11228.C3
  23. Honig S : Osteoporosis -- new treatments and updates. Bull NYU Hosp Jt Dis 68 : 166-170, 2010
  24. Huang RC, Khan SN, Sandhu HS, Metzl JA, Cammisa FP Jr, Zheng F, et al. : Alendronate inhibits spine fusion in a rat model. Spine (Phila Pa 1976) 30 : 2516-2522, 2005 https://doi.org/10.1097/01.brs.0000186470.28070.7b
  25. Kasukawa Y, Miyakoshi N, Maekawa S, Nozaka K, Noguchi H, Shimada Y : Effects of alfacalcidol on muscle strength, muscle fatigue, and bone mineral density in normal and ovariectomized rats. Biomed Res 31 : 273-279, 2010 https://doi.org/10.2220/biomedres.31.273
  26. Kitazawa R, Imai Y, Fukase M, Fujita T : Effects of continuous infusion of parathyroid hormone and parathyroid hormone-related peptide on rat bone in vivo : comparative study by histomorphometry. Bone Miner 12 : 157-166, 1991 https://doi.org/10.1016/0169-6009(91)90029-Y
  27. Kornblum MB, Fischgrund JS, Herkowitz HN, Abraham DA, Berkower DL, Ditkoff JS : Degenerative lumbar spondylolisthesis with spinal stenosis : a prospective long-term study comparing fusion and pseudarthrosis. Spine (Phila Pa 1976) 29 : 726-733; discussion 733-734, 2004 https://doi.org/10.1097/01.BRS.0000119398.22620.92
  28. Lehman RA Jr, Kuklo TR, Freedman BA, Cowart JR, Mense MG, Riew KD : The effect of alendronate sodium on spinal fusion : a rabbit model. Spine J 4 : 36-43, 2004 https://doi.org/10.1016/S1529-9430(03)00427-3
  29. Li YF, Zhou CC, Li JH, Luo E, Zhu SS, Feng G, et al. : The effects of combined human parathyroid hormone (1-34) and zoledronic acid treatment on fracture healing in osteoporotic rats. Osteoporos Int 23 : 1463-1474, 2012 https://doi.org/10.1007/s00198-011-1751-6
  30. Matkovic V, Heaney RP : Calcium balance during human growth : evidence for threshold behavior. Am J Clin Nutr 55 : 992-996, 1992
  31. Nagahama K, Kanayama M, Togawa D, Hashimoto T, Minami A : Does alendronate disturb the healing process of posterior lumbar interbody fusion? A prospective randomized trial. J Neurosurg Spine 14 : 500- 507, 2011 https://doi.org/10.3171/2010.11.SPINE10245
  32. Nordin BE, Heaney RP : Calcium supplementation of the diet : justified by present evidence. BMJ 300 : 1056-1060, 1990 https://doi.org/10.1136/bmj.300.6731.1056
  33. O'Loughlin PF, Cunningham ME, Bukata SV, Tomin E, Poynton AR, Doty SB, et al. : Parathyroid hormone (1-34) augments spinal fusion, fusion mass volume, and fusion mass quality in a rabbit spinal fusion model. Spine (Phila Pa 1976) 34 : 121-130, 2009 https://doi.org/10.1097/BRS.0b013e318191e687
  34. Park SB, Lee YJ, Chung CK : Bone mineral density changes after ovariectomy in rats as an osteopenic model : stepwise description of double dorso-lateral approach. J Korean Neurosurg Soc 48 : 309-312, 2010 https://doi.org/10.3340/jkns.2010.48.4.309
  35. Proceedings of a symposium. Consensus Development Conference on Osteoporosis. October 19-20, 1990, Copenhagen, Denmark. Am J Med 91 : 1S-68, 1991
  36. Shiraishi A, Miyabe S, Nakano T, Umakoshi Y, Ito M, Mihara M : The combination therapy with alfacalcidol and risedronate improves the mechanical property in lumbar spine by affecting the material properties in an ovariectomized rat model of osteoporosis. BMC Musculoskelet Disord 10 : 66, 2009 https://doi.org/10.1186/1471-2474-10-66
  37. Shuid AN, Mohamad S, Mohamed N, Fadzilah FM, Mokhtar SA, Abdullah S, et al. : Effects of calcium supplements on fracture healing in a rat osteoporotic model. J Orthop Res 28 : 1651-1656, 2010 https://doi.org/10.1002/jor.21180
  38. Takahata M, Ito M, Abe Y, Abumi K, Minami A : The effect of anti-resorptive therapies on bone graft healing in an ovariectomized rat spinalarthrodesis model. Bone 43 : 1057-1066, 2008 https://doi.org/10.1016/j.bone.2008.08.124
  39. West JL 3rd, Bradford DS, Ogilvie JW : Results of spinal arthrodesis with pedicle screw-plate fixation. J Bone Joint Surg Am 73 : 1179-1184, 1991
  40. Xu SW, Wang JW, Li W, Wang Y, Zhao GF : [Osteoporosis impairs fracture healing of tibia in a rat osteoporotic model]. Zhonghua Yi Xue Za Zhi 84 : 1205-1209, 2004
  41. Yee AJ, Bae HW, Friess D, Robbin M, Johnstone B, Yoo JU : Accuracy and interobserver agreement for determinations of rabbit posterolateral spinal fusion. Spine (Phila Pa 1976) 29 : 1308-1313, 2004 https://doi.org/10.1097/01.BRS.0000127184.43765.61
  42. Zdeblick TA : A prospective, randomized study of lumbar fusion. Preliminary results. Spine (Phila Pa 1976) 18 : 983-991, 1993 https://doi.org/10.1097/00007632-199306150-00006

Cited by

  1. The effects of C osmos caudatus (ulam raja) on dynamic and cellular bone histomorphometry in ovariectomized rats vol.6, pp.None, 2012, https://doi.org/10.1186/1756-0500-6-239
  2. The role of carnitine on ovariectomy and inflammation-induced osteoporosis in rats vol.238, pp.12, 2012, https://doi.org/10.1177/1535370213502614
  3. Preventive Effects of Collagen Peptide from Deer Sinew on Bone Loss in Ovariectomized Rats vol.2014, pp.None, 2012, https://doi.org/10.1155/2014/627285
  4. Management of Osteoporosis in Spine Surgery vol.23, pp.4, 2012, https://doi.org/10.5435/jaaos-d-14-00042
  5. Perioperative Medical Management of Spine Surgery Patients With Osteoporosis : vol.77, pp.suppl4, 2012, https://doi.org/10.1227/neu.0000000000000939
  6. Variables Affecting Fusion Rates in the Rat Posterolateral Spinal Fusion Model with Autogenic/Allogenic Bone Grafts: A Meta-analysis vol.44, pp.11, 2012, https://doi.org/10.1007/s10439-016-1701-8
  7. Platycodin D Inhibits Osteoclastogenesis by Repressing the NFATc1 and MAPK Signaling Pathway vol.118, pp.4, 2017, https://doi.org/10.1002/jcb.25763
  8. The Therapeutic Effects of Combination Therapy with Curcumin and Alendronate on Spine Fusion Surgery in the Ovariectomized Rats vol.14, pp.2, 2012, https://doi.org/10.14245/kjs.2017.14.2.35
  9. Medical optimization of lumbar fusion in the osteoporotic patient vol.13, pp.1, 2018, https://doi.org/10.1007/s11657-018-0427-7
  10. Perioperative Medical Treatment to Improve Surgical Outcomes: Management of Osteoporosis vol.54, pp.1, 2019, https://doi.org/10.4055/jkoa.2019.54.1.18
  11. Osteoporosis and Spine Surgery : A Critical Analysis Review vol.8, pp.6, 2012, https://doi.org/10.2106/jbjs.rvw.19.00160
  12. Pre-Clinical Models in Implant Dentistry: Past, Present, Future vol.9, pp.11, 2012, https://doi.org/10.3390/biomedicines9111538