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Journal of Bone and Mineral Metabolism

, Volume 37, Issue 1, pp 18–27 | Cite as

Short-term and long-term effects of osteoporosis on incisor teeth and femoral bones evaluated by Raman spectroscopy and energy dispersive X-ray analysis in ovariectomized rats

  • Fernanda Rossi PaolilloEmail author
  • Renan Arnon Romano
  • Luciana de Matos
  • Airton Abrahão Martin
  • Francisco Eduardo Gontijo Guimarães
  • Jarbas Caiado de Castro Neto
  • Vanderlei Salvador Bagnato
Original Article

Abstract

There are few published data on the relationship between loss of bone mass due to osteoporosis and poor tooth quality. This study analyzed the effects of osteoporosis on incisor teeth and femoral bones using optical techniques in rats. Twenty female Wistar rats aged 6 months (n = 20) were randomized into two groups: control group, non-ovariectomized rats (n = 10); ovariectomy group, ovariectomized rats to induce osteoporosis (n = 10). Each group was subdivided randomly into two groups containing five rats each as follows. Control group 1: non-ovariectomized rats euthanized at the age of 9 or 3 months post-ovariectomy (n = 5); Control group 2: non-ovariectomized rats euthanized at the age of 1 year or 6 months post-ovariectomy (n = 5); ovariectomy group 1: ovariectomized rats euthanized at the age of 9 months or 3 months post-ovariectomy (n = 5); ovariectomy group 2: ovariectomized rats euthanized at the age of 1 year or 6 months post-ovariectomy (n = 5). The incisor teeth and femoral bones of Wistar rats were removed to perform Raman spectroscopy using an excitation laser at 785 nm. In addition, an energy-dispersive X-ray spectrometer system was used to evaluate calcium (Ca) and phosphorus (P). The main findings included significant changes (p < 0.05) for phosphate and carbonate band areas for both incisor teeth and femur bones. In addition, there was significant negative correlation between the P concentration and phosphate/carbonate ratio (lower P content–larger ratio, p < 0.05) for incisor teeth and femoral bones. The proline and CH2 wag band areas were significantly reduced only for the incisor teeth (p < 0.05). Therefore, Raman spectroscopy assessed the compositional, physicochemical and structural changes in hard tissue. The current study also pointed out the possible action mechanisms of these changes, bone fracture risk and dental fragility. It is important to emphasize that poor dental quality may also occur due to osteoporosis.

Keywords

Raman spectroscopy EDX Tooth Bone Osteoporosis 

Notes

Acknowledgements

We would like to thank the São Paulo Research Foundation (FAPESP)—Grant no. 2013/14001-9 and 2013/07276-1 (CEPOF—CEPID Program).

Funding

This study was funded by the São Paulo Research Foundation (FAPESP)—Grant no. 2013/14001-9 and 2013/07276-1 (CEPOF—CEPID Program).

Compliance with ethical standards

Ethical standards

This study was approved by the Ethics Committee of the São Carlos Institute of Physics (IFSC), University of São Paulo (USP) in São Carlos, Brazil (number 08/2014). All animal procedures were performed according to the principles in the Guide for the Care and Use of Laboratory Animals.

Conflict of interest

No competing financial interests exist.

References

  1. 1.
    Tu Q, Chang C (2012) Diagnostic applications of Raman spectroscopy. Nanomedicine Nanotechnol Biol Med 8:545–558CrossRefGoogle Scholar
  2. 2.
    Moreira LM, Silveira L Jr, Santos FV, Lyon JP, Rocha R, Zângaro RA, Villaverde AB, Pacheco MT (2008) Raman spectroscopy: a powerful technique for biochemical analysis and diagnosis. J Spectrosc 22:1–19CrossRefGoogle Scholar
  3. 3.
    Carden A, Morris MD (2000) Application of vibrational spectroscopy to the study of mineralized tissues (review). J Biomed Opt 5:259–268CrossRefGoogle Scholar
  4. 4.
    Boskey AL (2007) Mineralization of bones and teeth. Elements 3:385–391CrossRefGoogle Scholar
  5. 5.
    Pascart T, Cortet B, Olejnik C, Paccou J, Migaud H, Cotten A, Delannoy Y, During A, Hardouin P, Penel G, Falgayrac G (2016) Bone samples extracted from embalmed subjects are not appropriate for the assessment of bone quality at the molecular level using Raman spectroscopy. Anal Chem 88:2777–2783CrossRefGoogle Scholar
  6. 6.
    Pascart T, Falgayrac G, Migaud H, Quinchon JF, Norberciak L, Budzik JF, Paccou J, Cotten A, Penel G, Cortet B (2017) Region specific Raman spectroscopy analysis of the femoral head reveals that trabecular bone is unlikely to contribute to non-traumatic osteonecrosis. Sci Rep 7:97CrossRefGoogle Scholar
  7. 7.
    Buckley K, Matousek P, Parker AW, Goodship AE (2012) Raman spectroscopy reveals differences in collagen secondary structure which relate to the levels of mineralization in bones that have evolved for different functions. J Raman Spectrosc 43:1237–1243CrossRefGoogle Scholar
  8. 8.
    Paschalis EP, Fratzl P, Gamsjaeger S, Hassler N, Brozek W, Eriksen EF, Eriksen EF, Rauch F, Glorieux FH, Shane E, Dempster D, Cohen A, Recker R, Klaushofer K (2016) Aging versus postmenopausal osteoporosis: bone composition and maturation kinetics at actively-forming trabecular surfaces of female subjects aged 1 to 84 years. J Bone Miner Res 31:347–357CrossRefGoogle Scholar
  9. 9.
    Carneiro J, Leblond CP (1959) Role of osteoblasts and odontoblasts in secreting the collagen of bone and dentin, as shown by radioautography in mice given tritium-labelled glycine. Exp Cell Res 18:291–300CrossRefGoogle Scholar
  10. 10.
    Wang Z, McCauley LK (2011) Osteoclasts and odontoclasts: signaling pathways to development and disease. Oral Dis 17:129–142CrossRefGoogle Scholar
  11. 11.
    Yokose S, Zhungfeng C, Tajima Y, Fujieda K, Katayama I, Katayama T (1998) The effects of estrogen deficiency on glycosylation of odontoblasts in rats. J Endod 24:645–647CrossRefGoogle Scholar
  12. 12.
    Kim M, Yang WK, Baek J, Kim JJ, Kim WK, Lee YK (2005) The effect of estrogen deficiency on rat pulpodentinal complex. J Korean Acad Conserv Dent 30:402–408CrossRefGoogle Scholar
  13. 13.
    Xu T, Yan M, Wang Y, Wang Z, Xie L, Tang C, Zhang G, Yu J (2014) Estrogen deficiency reduces the dentinogenic capacity of rat lower incisors. Mol Histol 45:11–19CrossRefGoogle Scholar
  14. 14.
    Lu Y, Jin L, Lei G, Fu Y, Wang Y, Yu J (2016) Estrogen-mediated dental tissue regeneration. Histol Histopathol 31:1281–1289Google Scholar
  15. 15.
    Wang Y, Yan M, Yu Y, Wu J, Yu J, Fan Z (2013) Estrogen deficiency inhibits the odonto/osteogenic differentiation of dental pulp stem cells via activation of the NF-κB pathway. Cell Tissue Res 352:551–559CrossRefGoogle Scholar
  16. 16.
    Schour I, Steadman SR (1935) The growth pattern and daily rhythm of the incisor of the rat. Anat Rec 63:325–333CrossRefGoogle Scholar
  17. 17.
    Bhaskar SN (1953) Growth pattern of the rat mandible from 13 days insemination age to 30 days after birth. Am J Anat 92:1–53CrossRefGoogle Scholar
  18. 18.
    Jeffcoat M (2005) The association between osteoporosis and oral bone loss. J Periodontol 76:2125–2132CrossRefGoogle Scholar
  19. 19.
    Paolillo FR, Romano RA, de Matos L, Rodrigues PGS, Panhóca VH, Martin AA, Soares LE, de Castro Neto JC, Bagnato VS (2016) Fluorescence spectroscopy of teeth and bones of rats to assess demineralization: in vitro, in vivo and ex vivo studies. J Photochem Photobiol B 165:291–297CrossRefGoogle Scholar
  20. 20.
    Raisz LG (1999) Physiology and pathophysiology of bone remodeling. Clin Chem 45:1353–1358Google Scholar
  21. 21.
    Riggs BL, Khosla S, Melton LJ (1998) A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J Bone Miner Res 13:763–773CrossRefGoogle Scholar
  22. 22.
    McCreadie BR, Morris MD, Chen TC, Rao DS, Finney WF, Widjaja E, Goldstein SA (2006) Bone tissue compositional differences in women with and without osteoporotic fracture. Bone 39:1190–1195CrossRefGoogle Scholar
  23. 23.
    Inzana JA, Maher JR, Takahata M, Schwarz EM, Berger AJ, Awad HA (2013) Bone fragility beyond strength and mineral density: Raman spectroscopy predicts femoral fracture toughness in a murine model of rheumatoid arthritis. J Biomech 46:723–730CrossRefGoogle Scholar
  24. 24.
    Richards-Kortum R, Sevick-Muraca E (1996) Quantitative optical spectroscopy for tissue diagnosis. Annu Rev Phys Chem 47:555–606CrossRefGoogle Scholar
  25. 25.
    Adabbo M, Paolillo FR, Bossini PS, Rodrigues NC, Bagnato VS, Parizotto NA (2016) Effects of low-level laser therapy applied before treadmill training on recovery of injured skeletal muscle in Wistar rats. Photomed Laser Surg 34:187–193CrossRefGoogle Scholar
  26. 26.
    Goodyear SR, Gibson IR, Skakle JMS, Wells RPK, Aspden RM (2009) A comparison of cortical and trabecular bone from C57 Black 6 mice using Raman spectroscopy. Bone 44:899–907CrossRefGoogle Scholar
  27. 27.
    Morris MD, Mandair GS (2011) Raman assessment of bone quality. Clin Orthop Relat Res 469:2160–2169CrossRefGoogle Scholar
  28. 28.
    Lerner UH (2006) Bone remodeling in post-menopausal osteoporosis. J Dent Res 85:584–595CrossRefGoogle Scholar
  29. 29.
    Hadjidakis DJ, Androulakis II (2006) Bone remodeling. Ann N Y Acad Sci 1092:385–396CrossRefGoogle Scholar
  30. 30.
    Matsumoto Y, Mikuni-Takagaki Y, Kozai Y, Miyagawa K, Naruse K, Wakao H, Kawamata R, Kashima I, Sakurai T (2009) Prior treatment with vitamin K2 significantly improves the efficacy of risedronate. Osteoporos Int 20:1863–1872CrossRefGoogle Scholar
  31. 31.
    Paschalis EP, Betts F, DiCarlo E, Mendelsohn R, Boskey AL (1997) FTIR microspectroscopic analysis of human iliac crest biopsies from untreated osteoporotic bone. Calcif Tissue Int 61:487–492CrossRefGoogle Scholar
  32. 32.
    Kazanci M, Roschger P, Paschalis EP, Klaushofer K, Fratzl P (2006) Bone osteonal tissues by Raman spectral mapping: orientation–composition. J Struct Biol 156:489–496CrossRefGoogle Scholar
  33. 33.
    Davison KS, Siminoski K, Adachi JD, Hanley DA, Goltzman D, Hodsman AB, Robert J, Kaiser S, Olszynski WP, Papaioannou A, Ste-Marie LG, Kendler DL, Tenenhouse A, Brown JP (2006) Bone strength: the whole is greater than the sum of its parts. In Semin Arthritis Rheum 36:22–31CrossRefGoogle Scholar
  34. 34.
    Yerramshetty JS, Lind C, Akkus O (2006) The compositional and physicochemical homogeneity of male femoral cortex increases after the sixth decade. Bone 39:1236–1243CrossRefGoogle Scholar
  35. 35.
    Boskey AL, Spevak L, Paschalis E, Doty SB, McKee MD (2002) Osteopontin deficiency increases mineral content and mineral crystallinity in mouse bone. Calcif Tissue Int 71:145–154CrossRefGoogle Scholar
  36. 36.
    Faibish D, Ott SM, Boskey AL (2006) Mineral changes in osteoporosis: a review. Clin Orthop Relat Res 443:28–38CrossRefGoogle Scholar
  37. 37.
    Yerramshetty JS, Akkus O (2008) The associations between mineral crystallinity and the mechanical properties of human cortical bone. Bone 42:476–482CrossRefGoogle Scholar
  38. 38.
    Buckley K, Kerns JG, Vinton J, Gikas PD, Smith C, Parker AW, Matousek P, Goodship AE (2015) Towards the in vivo prediction of fragility fractures with Raman spectroscopy. J Raman Spectrosc 46:610–618CrossRefGoogle Scholar
  39. 39.
    Paschalis EP, Gamsjaeger S, Dempster D, Jorgetti V, Borba V, Boguszewski CL, Klaushofer K, Moreira CA (2017) Fragility fracture incidence in chronic obstructive pulmonary disease (COPD) patients associates with nanoporosity, mineral/matrix ratio, and pyridinoline content at actively bone-forming trabecular surfaces. J Bone Miner Res 32:165–171CrossRefGoogle Scholar
  40. 40.
    Rey C, Collins B, Goehl T, Dickson IR, Glimcher MJ (1989) The carbonate environment in bone mineral: a resolution-enhanced Fourier transform infrared spectroscopy study. Calcif Tissue Int 45:157–164CrossRefGoogle Scholar
  41. 41.
    Meghji S, Morrison MS, Henderson B, Arnett TR (2001) pH dependence of bone resorption: mouse calvarial osteoclasts are activated by acidosis. Am J Physiol Endocrinol Metab 280:E112–E119CrossRefGoogle Scholar
  42. 42.
    Ager JW, Nalla RK, Balooch G, Kim G, Pugach M, Habelitz S, Marshall GW, Kinney JH, Ritchie RO (2006) On the increasing fragility of human teeth with age: a deep-UV resonance Raman study. J Bone Miner Res 21:1879–1887CrossRefGoogle Scholar
  43. 43.
    Weinstock M, Leblond CP (1974) Synthesis, migration, and release of precursor collagen by odontoblasts as visualized by radioautography after [3H] proline administration. J Cell Biol 60:92–127CrossRefGoogle Scholar
  44. 44.
    Rosenbloom J, Harsch M, Jimenez S (1973) Hydroxyproline content determines the denaturation temperature of chick tendon collagen. Arch Biochem Biophys 158:478–484CrossRefGoogle Scholar
  45. 45.
    Paolillo AR, Paolillo FR, Silva AMH, Reiff RBM, Bagnato VS, Alves JM (2015) Effects of infrared laser on the bone repair assessed by X-ray microtomography (μct) and histomorphometry. In: Proceedings of SPIE biophotonics, South America, Rio de Janeiro, 9531 (95313N-1–95313N-7)Google Scholar

Copyright information

© The Japanese Society for Bone and Mineral Research and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Fernanda Rossi Paolillo
    • 1
    Email author
  • Renan Arnon Romano
    • 1
  • Luciana de Matos
    • 1
  • Airton Abrahão Martin
    • 2
    • 3
  • Francisco Eduardo Gontijo Guimarães
    • 1
  • Jarbas Caiado de Castro Neto
    • 1
  • Vanderlei Salvador Bagnato
    • 1
  1. 1.Optics Group from São Carlos Institute of Physics (IFSC)University of São Paulo (USP)São CarlosBrazil
  2. 2.Department of Physics from Federal University of Piauí (UFPI)Campus Universitário Ministro Petrônio Portella, Bairro Ininga, TeresinaBairro IningaBrazil
  3. 3.Department of Biomedical Engineering from Brazil University (UnBr)ItaqueraBrazil

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