Abstract
The aim of this work is to show that the bones with marrow, treated as a quasi-porous media, can be successfully used to study the effects of ovariectomy-induced osteoporosis. Proton one-dimensional (1D) nuclear magnetic resonance (NMR) T 2-distribution and two-dimensional (2D) T 2–T 2 exchange maps combined with histological images were used to measure the proximal part of the femoris, diaphysis and distal epiphysis of ovariectomized and non-ovariectomized Wistar albino rats. The 1D normalized T 2 distributions showed four peaks which were associated with protons in four major pools: (1) the protons from bounded water to collagenous matrix; (2) fluids in osteocyte lacunae and canaliculi channels; (3) fluids in secondary pores like Haversian and transverse Volkmann canals and (4) soft matter like bone marrow and fluids in primary pores like trabecular bone cavities. The peak’s association and hierarchical structure of pores in femoral bone were supported by a 2D T 2–T 2 exchange map and by a series of dehydration experiments monitored by NMR measurements. The bone marrow narrows the T 2-distributions, increasing resolution, but will not influence significantly the peaks positions; therefore, the NMR relaxometry is a valuable tool to characterize the pore distributions and effects of induced osteoporosis in diverse bones sections.
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W. Koopman, M. Moreland, Arthritis and Allied Conditions: A Textbook of Rheumatology, 15th edn. (Lipincott Williams & Wilkins, Philadelphia, 2004), pp. 78–96
L. Cardoso, S.P. Fritton, G. Gailani, M. Benalla, S.C. Cowin, J. Biomech. 46, 253–265 (2013)
E.A. Martin, E.L. Ritman, R.T. Turner, Bone 32, 261–267 (2003)
C.C. Netto, V.C. Vieira, L.P. Marinheiro, S. Agellon, H. Weiler, M.R. Marostica Jr., Arq. Bras. Endocrinol. Metab. 56, 259–264 (2012)
W.S.S. Jee, W. Yao, J. Musculoskel. Neuron. Interact. 1, 193–207 (2001)
D. Sharma, C. Ciani, P.A. Ramirez Marin, J.D. Levy, S.B. Doty, S.P. Fritton, Bone 51, 488–497 (2012)
J.E.M. Brouwers, B. van Rietbergen, R. Huiskes, K. Ito, Osteoporos. Int. 20, 1823–1835 (2009)
H.A. Tanriverdi, A. Barut, S. Sarikaya, Eur. J. Obstet. Gynecol. Reprod. Biol. 120, 63–68 (2005)
M. Jablonski, V.M. Gun’ko, A.P. Golovan, R. Leboda, J. Skubiszewska-Zieba, R. Pluta, V.V. Turov, J. Colloid Interface Sci. 392, 446–462 (2013)
R.I. Chelcea, R.S. Şipos, R. Fechete, D. Moldovan, I. Şuş, Z. Pávai, D.E. Demco, Sudia UBB Chemia LX (1), 57–70 (2015)
R.S. Şipos, R. Fechete, D. Moldovan, I. Şuş, S. Szasz, Z. Pávai, Open. Life Sci. 10, 379–387 (2015)
R.S. Şipoş, R. Fechete, R.I. Chelcea, D. Moldovan, Z. Pap, Z. Pávai, D.E. Demco, Rom. J. Morphol. Embryol. 56(2), 743–752 (2015)
P. Fantazzini, C. Garavaglia, M. Palombarini, R.J.S. Brown, G. Giavaresi, R. Giardino, Magn. Reson. Imaging 22, 689–695 (2004)
T.M. Link, S. Majumdar, P. Augat, J.C. Lin, D. Newitt, Y. Lu, N.E. Lane, H.K. Genant, J. Bone Miner. Res. 13, 1175–1182 (1998)
S. Majumdar, H.K. Genant, Osteoporosis Int. 5, 79–92 (1995)
S. Anumula, S.L. Wehrli, J. Magland, A.C. Wright, F.W. Wehrli, Bone 46, 1391–1399 (2010)
R.A. Horch, J.S. Nyman, D.F. Gochberg, R.D. Dortch, M.D. Does, Magn. Reson. Med. 64, 680–687 (2010)
R.A. Horch, D.F. Gochberg, J.S. Nyman, M.D. Does, Magn. Reson. Med. 68, 1774–1784 (2012)
Q. Ni, A. De Los Santos, H. Lam, Y.X. Qin, Adv. Sp. Res. 40, 1703–1710 (2007)
R.A. Horch, D.F. Gochberg, J.S. Nyman, M.D. Does, PLoS One 6(e16359), 1–5 (2011)
J.S. Nyman, Q. Ni, D.P. Nicolella, X. Wang, Bone 42, 193–199 (2008)
F.W. Wehrli, J. Magn. Reson. 229, 35–48 (2013)
J.S. Nyman, A. Roy, X. Shen, R.L. Acuna, J.H. Tyler, X. Wang, J. Biomech. 39, 931–938 (2006)
W.C. Bae, P.C. Chen, C.B. Chung, K. Masuda, D. D’Lima, J. Du, J. Bone Miner. Res. 27, 848–857 (2012)
R. Biswas, W. Bae, E. Diaz, K. Masuda, C.B. Chung, G.M. Bydder, J. Du, Bone 50, 749–755 (2012)
R.A. Horch, J.C. Gore, M.D. Does, Magn. Reson. Med. 66, 24–31 (2011)
J.S. Nyman, L.E. Gorochow, R.A. Horch, S. Uppuganti, A. Zein-Sabatto, M.K. Manhard, M.D. Does, J. Mech. Behav. Biomed. Mater. 22, 136–145 (2013)
P.A. Timmins, J.C. Wall, Bone Water Calcif. Tissue Res. 23, 1–5 (1977)
N.A. Andreollo, E.F. Santos, M.R. Araújo, L.R. Lopes, ABCD Arq. Bras. Cir. Dig. 25, 49–51 (2012)
P. Sengupta, Biomed. Int. 2, 81–89 (2011)
R.S. Sipos, Z. Pap, A.S. Szalai, I. Sus, A.V. Gabor, Z. Pavai, K. Branzaniuc, Acta Med. Marisiensis 56, 479–483 (2010)
L. Monteilhet, J.P. Korb, J. Mitchell, P.J. McDonald, Phys. Rev. E 74, 061404 (2006)
L. Venkataramanan, Y.Q. Song, M.D. Hurlimann, IEEE Trans. Sign. Proc. 50, 1017–1026 (2002)
Y.Q. Song, L. Venkataramanan, M.D. Hürlimann, M. Flaum, P. Frulla, C. Straley, Magn. Reson. 154, 261–268 (2002)
M.D. Hürlimann, M. Flaum, L. Venkataramanan, C. Flaum, R. Freedman, G.J. Hirasaki, Magn. Reson. Imag. 21, 305–310 (2003)
K.E. Washburn, P.T. Callaghan, Phys. Rev. Lett. 97, 175502 (2006)
D. Moldovan, R. Fechete, D.E. Demco, E. Culea, B. Blümich, Diffus. Fundam. 10, 20.1–20.3 (2009)
R. Fechete, D. Moldovan, D.E. Demco, B. Blümich, Diffus. Fundam. 10, 14.1–14.3 (2009)
K.E. Washburn, P.T. Callaghan, J. Magn. Reson. 186, 337–340 (2007)
E. Tonning, D. Polders, P.T. Callaghan, S.B. Engelsen, J. Magn. Reson. 188, 10–23 (2007)
G.C. Borgia, R.J.S. Brown, P. Fantazzini, J. Magn. Reson. 147, 273–285 (2000)
P. Fantazzini, R.J.S. Brown, G.C. Borgia, Magn. Reson. Imaging 21, 227–234 (2003)
D. Moldovan, R. Fechete, D.E. Demco, E. Culea, B. Blümich, V. Herrmann, M. Heinz, Macromol. Chem. Phys. 211, 1579–1594 (2010)
D. Moldovan, R. Fechete, D.E. Demco, E. Culea, B. Blümich, V. Herrmann, M. Heinz, J. Magn. Reson. 208, 156–162 (2011)
Z.F. Zhang, L.Z. Xiao, H.B. Liu, F. Deng, X. Li, T.L. An, V. Anferov, S. Anferova, Appl. Magn. Reson. 44, 849–857 (2013)
S.C. Cowin, G. Gailani, M. Benalla, Philos. Trans. R. Soc. A 367, 3401–3444 (2009)
W.F. Neuman, T.Y. Toribara, B.J. Mulryan, J. Am. Chem. Soc. 75, 4239–4242 (1953)
F.W. Wehrli, M.A. Fernandez-Seara, Ann. Biomed. Eng. 33, 79–86 (2005)
S.M. Tommasini, A. Trinward, A.S. Acerbo, F. Carlo, L.M. Miller, S. Judex, Bone 50, 596–604 (2012)
H. Fonseca, D. Moreira-Gonçalves, M. Vaz, M.H. Fernandes, R. Ferreira, F. Amado, M.P. Mota, J.A. Duarte, J. Bone Miner. Metab. 30, 281–292 (2012)
Y. Uyar, Y. Baytur, U. Inceboz, B.C. Demir, G. Gumuser, K. Ozbilgin, Maturitas 63, 261–267 (2009)
Acknowledgments
This work was supported by a grant of Romanian National Authority for Scientific Research, CNCS-UEFISCDI, Project Number PN-II-IDEI-307/2011. R. F. would like to acknowledge Prof. Bernhard Blümich for useful discussions.
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Şipos, R.S., Fechete, R., Moldovan, D. et al. Ovariectomy-Induced Osteoporosis Evaluated by 1H One- and Two-Dimensional NMR Transverse Relaxometry. Appl Magn Reson 47, 1419–1437 (2016). https://doi.org/10.1007/s00723-016-0839-8
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DOI: https://doi.org/10.1007/s00723-016-0839-8