Skip to main content
Top
Published in: Radiation Oncology 1/2019

Open Access 01-12-2019 | Ionizing Radiation | Research

Ionizing radiation and bone quality: time-dependent effects

Authors: Pedro Henrique Justino Oliveira Limirio, Priscilla Barbosa Ferreira Soares, Eduardo Tadashi Pinto Emi, Camila de Carvalho Almança Lopes, Flaviana Soares Rocha, Jonas Dantas Batista, Gustavo Davi Rabelo, Paula Dechichi

Published in: Radiation Oncology | Issue 1/2019

Login to get access

Abstract

Background

The aim of this study was to evaluate the ionizing radiation (IR) effects on rat bone 30 and 60 days after irradiation.

Methods

Wistar rats were submitted to IR (30 Gy) on the left leg and were euthanized after 30 and 60 days. The legs were divided into four groups according to the treatment and euthanization time: C30 and C60 (right leg–without IR), IR30 and IR60 (left leg-with IR).

Results

CT analysis showed more radiodensity in C60 compared with other groups, and IR60 showed more radiodensity than IR30. In histomorphometric analysis, C30 showed lower bone matrix values compared with IR30 and C60. Lacunarity analyses showed more homogeneous bone channel distribution in C30 than IR30. ATR-FTIR showed decrease in ratio of mature and immature crosslinks in IR30 compared with C30. Crystallinity Index was decrease in IR60 compared with C60. The Amide III + Collagen/HA ratio was increased in C60 compared with C30; however this ratio decreased in IR60 compared with IR30. Biomechanical analysis showed lower values in IR groups in both time.

Conclusions

IR damaged bone quality and decreased stiffness. Moreover, the results suggested that the deleterious effects of IR increased in the late time points.
Literature
1.
go back to reference Phulpin B, Dolivet G, Marie PY, Poussier S, Huger S, Bravetti P, et al. Feasibility of treating irradiated bone with intramedullary delivered autologous mesenchymal stem cells. J Biomed Biotechnol. 2011;2011:560257.CrossRef Phulpin B, Dolivet G, Marie PY, Poussier S, Huger S, Bravetti P, et al. Feasibility of treating irradiated bone with intramedullary delivered autologous mesenchymal stem cells. J Biomed Biotechnol. 2011;2011:560257.CrossRef
2.
go back to reference Engleman MA, Woloschak G, Small W Jr. Radiation-induced skeletal injury. Cancer Treat Res. 2006;128:155–69.CrossRef Engleman MA, Woloschak G, Small W Jr. Radiation-induced skeletal injury. Cancer Treat Res. 2006;128:155–69.CrossRef
3.
go back to reference Lerouxel E, Moreau A, Bouler JM, Giumelli B, Daculsi G, Weiss P, et al. Effects of high doses of ionising radiation on bone in rats: a new model for evaluation of bone engineering. Br J Oral Maxillofac Surg. 2009;47:602–7.CrossRef Lerouxel E, Moreau A, Bouler JM, Giumelli B, Daculsi G, Weiss P, et al. Effects of high doses of ionising radiation on bone in rats: a new model for evaluation of bone engineering. Br J Oral Maxillofac Surg. 2009;47:602–7.CrossRef
4.
go back to reference Jegoux F, Malard O, Goyenvalle E, Aguado E, Daculsi G. Radiation effects on bone healing and reconstruction: interpretation of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109:173–84.CrossRef Jegoux F, Malard O, Goyenvalle E, Aguado E, Daculsi G. Radiation effects on bone healing and reconstruction: interpretation of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109:173–84.CrossRef
5.
go back to reference Feldmeier JJ. Hyperbaric oxygen therapy and delayed radiation injuries (soft tissue and bony necrosis): 2012 update. Undersea Hyperb Med. 2012;39:1121–39.PubMed Feldmeier JJ. Hyperbaric oxygen therapy and delayed radiation injuries (soft tissue and bony necrosis): 2012 update. Undersea Hyperb Med. 2012;39:1121–39.PubMed
6.
go back to reference Sonstevold T, Johannessen AC, Stuhr L. A rat model of radiation injury in the mandibular area. Radiat Oncol. 2015;10:129.CrossRef Sonstevold T, Johannessen AC, Stuhr L. A rat model of radiation injury in the mandibular area. Radiat Oncol. 2015;10:129.CrossRef
7.
go back to reference Desmons S, Heger M, Delfosse C, Falgayrac G, Sarrazin T, Delattre C, et al. A preliminary investigation into the effects of X-ray radiation on superficial cranial vascularization. Calcif Tissue Int. 2009;84:379–87.CrossRef Desmons S, Heger M, Delfosse C, Falgayrac G, Sarrazin T, Delattre C, et al. A preliminary investigation into the effects of X-ray radiation on superficial cranial vascularization. Calcif Tissue Int. 2009;84:379–87.CrossRef
8.
go back to reference Cao X, Wu X, Frassica D, Yu B, Pang L, Xian L, et al. Irradiation induces bone injury by damaging bone marrow microenvironment for stem cells. Proc Natl Acad Sci U S A. 2011;108:1609–14.CrossRef Cao X, Wu X, Frassica D, Yu B, Pang L, Xian L, et al. Irradiation induces bone injury by damaging bone marrow microenvironment for stem cells. Proc Natl Acad Sci U S A. 2011;108:1609–14.CrossRef
9.
go back to reference Sakurai T, Sawada Y, Yoshimoto M, Kawai M, Miyakoshi J. Radiation-induced reduction of osteoblast differentiation in C2C12 cells. J Radiat Res. 2007;48:515–21.CrossRef Sakurai T, Sawada Y, Yoshimoto M, Kawai M, Miyakoshi J. Radiation-induced reduction of osteoblast differentiation in C2C12 cells. J Radiat Res. 2007;48:515–21.CrossRef
10.
go back to reference Jia D, Gaddy D, Suva LJ, Corry PM. Rapid loss of bone mass and strength in mice after abdominal irradiation. Radiat Res. 2011;176:624–35.CrossRef Jia D, Gaddy D, Suva LJ, Corry PM. Rapid loss of bone mass and strength in mice after abdominal irradiation. Radiat Res. 2011;176:624–35.CrossRef
11.
go back to reference Tins BJ, Garton M, Cassar-Pullicino VN, Tyrrell PN, Lalam R, Singh J. Stress fracture of the pelvis and lower limbs including atypical femoral fractures-a review. Insights into imaging. 2015;6:97–110.CrossRef Tins BJ, Garton M, Cassar-Pullicino VN, Tyrrell PN, Lalam R, Singh J. Stress fracture of the pelvis and lower limbs including atypical femoral fractures-a review. Insights into imaging. 2015;6:97–110.CrossRef
12.
go back to reference Allaveisi F, Hashemi B, Mortazavi SM. Effect of gamma sterilization on microhardness of the cortical bone tissue of bovine femur in presence of N-acetyl-L-cysteine free radical scavenger. Phys Med. 2014;30:314–9.CrossRef Allaveisi F, Hashemi B, Mortazavi SM. Effect of gamma sterilization on microhardness of the cortical bone tissue of bovine femur in presence of N-acetyl-L-cysteine free radical scavenger. Phys Med. 2014;30:314–9.CrossRef
13.
go back to reference Nyman JS, Reyes M, Wang X. Effect of ultrastructural changes on the toughness of bone. Micron. 2005;36:566–82.CrossRef Nyman JS, Reyes M, Wang X. Effect of ultrastructural changes on the toughness of bone. Micron. 2005;36:566–82.CrossRef
14.
go back to reference Imbert L, Gourion-Arsiquaud S, Villarreal-Ramirez E, Spevak L, Taleb H, van der Meulen MCH, et al. Dynamic structure and composition of bone investigated by nanoscale infrared spectroscopy. PLoS One. 2018;13:e0202833.CrossRef Imbert L, Gourion-Arsiquaud S, Villarreal-Ramirez E, Spevak L, Taleb H, van der Meulen MCH, et al. Dynamic structure and composition of bone investigated by nanoscale infrared spectroscopy. PLoS One. 2018;13:e0202833.CrossRef
15.
go back to reference Bala Y, Farlay D, Boivin G. Bone mineralization: from tissue to crystal in normal and pathological contexts. Osteoporos Int. 2013;24:2153–66.CrossRef Bala Y, Farlay D, Boivin G. Bone mineralization: from tissue to crystal in normal and pathological contexts. Osteoporos Int. 2013;24:2153–66.CrossRef
16.
go back to reference Paschalis EP, Mendelsohn R, Boskey AL. Infrared assessment of bone quality: a review. Clin Orthop Relat Res. 2011;469:2170–8.CrossRef Paschalis EP, Mendelsohn R, Boskey AL. Infrared assessment of bone quality: a review. Clin Orthop Relat Res. 2011;469:2170–8.CrossRef
17.
go back to reference Rocha FS, Dias PC, Limirio PH, Lara VC, Batista JD, Dechichi P. High doses of ionizing radiation on bone repair: is there effect outside the irradiated site? Injury. 2017;48:671–3.CrossRef Rocha FS, Dias PC, Limirio PH, Lara VC, Batista JD, Dechichi P. High doses of ionizing radiation on bone repair: is there effect outside the irradiated site? Injury. 2017;48:671–3.CrossRef
18.
go back to reference Rabelo GD, Beletti ME, Dechichi P. Histological analysis of the alterations on cortical bone channels network after radiotherapy: a rabbit study. Microsc Res Tech. 2010;73:1015–8.CrossRef Rabelo GD, Beletti ME, Dechichi P. Histological analysis of the alterations on cortical bone channels network after radiotherapy: a rabbit study. Microsc Res Tech. 2010;73:1015–8.CrossRef
19.
go back to reference Limirio P, da Rocha Junior HA, Morais RB, Hiraki KRN, Balbi APC, Soares PBF, et al. Influence of hyperbaric oxygen on biomechanics and structural bone matrix in type 1 diabetes mellitus rats. PLoS One. 2018;13:e0191694.CrossRef Limirio P, da Rocha Junior HA, Morais RB, Hiraki KRN, Balbi APC, Soares PBF, et al. Influence of hyperbaric oxygen on biomechanics and structural bone matrix in type 1 diabetes mellitus rats. PLoS One. 2018;13:e0191694.CrossRef
20.
go back to reference Soares PB, Nunes SA, Franco SD, Pires RR, Zanetta-Barbosa D, Soares CJ. Measurement of elastic modulus and Vickers hardness of surround bone implant using dynamic microindentation--parameters definition. Braz Dent J. 2014;25:385–90.CrossRef Soares PB, Nunes SA, Franco SD, Pires RR, Zanetta-Barbosa D, Soares CJ. Measurement of elastic modulus and Vickers hardness of surround bone implant using dynamic microindentation--parameters definition. Braz Dent J. 2014;25:385–90.CrossRef
21.
go back to reference Batista JD, Zanetta-Barbosa D, Cardoso SV, Dechichi P, Rocha FS, Pagnoncelli RM. Effect of low-level laser therapy on repair of the bone compromised by radiotherapy. Lasers Med Sci. 2014;29:1913–8.CrossRef Batista JD, Zanetta-Barbosa D, Cardoso SV, Dechichi P, Rocha FS, Pagnoncelli RM. Effect of low-level laser therapy on repair of the bone compromised by radiotherapy. Lasers Med Sci. 2014;29:1913–8.CrossRef
22.
go back to reference Schultze-Mosgau S, Lehner B, Rodel F, Wehrhan F, Amann K, Kopp J, et al. Expression of bone morphogenic protein 2/4, transforming growth factor-beta1, and bone matrix protein expression in healing area between vascular tibia grafts and irradiated bone-experimental model of osteonecrosis. Int J Radiat Oncol Biol Phys. 2005;61:1189–96.CrossRef Schultze-Mosgau S, Lehner B, Rodel F, Wehrhan F, Amann K, Kopp J, et al. Expression of bone morphogenic protein 2/4, transforming growth factor-beta1, and bone matrix protein expression in healing area between vascular tibia grafts and irradiated bone-experimental model of osteonecrosis. Int J Radiat Oncol Biol Phys. 2005;61:1189–96.CrossRef
23.
go back to reference Fenner M, Park J, Schulz N, Amann K, Grabenbauer GG, Fahrig A, et al. Validation of histologic changes induced by external irradiation in mandibular bone. An experimental animal model. J Craniomaxillofac Surg. 2010;38:47–53.CrossRef Fenner M, Park J, Schulz N, Amann K, Grabenbauer GG, Fahrig A, et al. Validation of histologic changes induced by external irradiation in mandibular bone. An experimental animal model. J Craniomaxillofac Surg. 2010;38:47–53.CrossRef
24.
go back to reference Lucatto SC, Guilherme A, Dib LL, Segreto HR, Alves MT, Gumieiro EH, et al. Effects of ionizing radiation on bone neoformation: histometric study in Wistar rats tibiae. Acta Cir Bras. 2011;26:475–80.CrossRef Lucatto SC, Guilherme A, Dib LL, Segreto HR, Alves MT, Gumieiro EH, et al. Effects of ionizing radiation on bone neoformation: histometric study in Wistar rats tibiae. Acta Cir Bras. 2011;26:475–80.CrossRef
25.
go back to reference Onem E, Baksi BG, Sogur E. Changes in the fractal dimension, feret diameter, and lacunarity of mandibular alveolar bone during initial healing of dental implants. Int J Oral Maxillofac Implants. 2012;27:1009–13.PubMed Onem E, Baksi BG, Sogur E. Changes in the fractal dimension, feret diameter, and lacunarity of mandibular alveolar bone during initial healing of dental implants. Int J Oral Maxillofac Implants. 2012;27:1009–13.PubMed
26.
go back to reference Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, Ritchie RO. Characterization of the effects of x-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials. 2011;32:8892–904.CrossRef Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, Ritchie RO. Characterization of the effects of x-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials. 2011;32:8892–904.CrossRef
27.
go back to reference Tchanque-Fossuo CN, Gong B, Poushanchi B, Donneys A, Sarhaddi D, Gallagher KK, et al. Raman spectroscopy demonstrates Amifostine induced preservation of bone mineralization patterns in the irradiated murine mandible. Bone. 2013;52:712–7.CrossRef Tchanque-Fossuo CN, Gong B, Poushanchi B, Donneys A, Sarhaddi D, Gallagher KK, et al. Raman spectroscopy demonstrates Amifostine induced preservation of bone mineralization patterns in the irradiated murine mandible. Bone. 2013;52:712–7.CrossRef
28.
go back to reference Bailey AJ, Rhodes DN, Cater CW. Irradiation-induced crosslinking of collagen. Radiat Res. 1964;22:606–21.CrossRef Bailey AJ, Rhodes DN, Cater CW. Irradiation-induced crosslinking of collagen. Radiat Res. 1964;22:606–21.CrossRef
29.
go back to reference Abraham AC, Agarwalla A, Yadavalli A, Liu JY, Tang SY. Microstructural and compositional contributions towards the mechanical behavior of aging human bone measured by cyclic and impact reference point indentation. Bone. 2016;87:37–43.CrossRef Abraham AC, Agarwalla A, Yadavalli A, Liu JY, Tang SY. Microstructural and compositional contributions towards the mechanical behavior of aging human bone measured by cyclic and impact reference point indentation. Bone. 2016;87:37–43.CrossRef
30.
go back to reference Bala Y, Depalle B, Farlay D, Douillard T, Meille S, Follet H, et al. Bone micromechanical properties are compromised during long-term alendronate therapy independently of mineralization. J Bone Miner Res Off J Am Soc Bone Miner Res. 2012;27:825–34.CrossRef Bala Y, Depalle B, Farlay D, Douillard T, Meille S, Follet H, et al. Bone micromechanical properties are compromised during long-term alendronate therapy independently of mineralization. J Bone Miner Res Off J Am Soc Bone Miner Res. 2012;27:825–34.CrossRef
31.
go back to reference Farlay D, Panczer G, Rey C, Delmas PD, Boivin G. Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Miner Metab. 2010;28:433–45.CrossRef Farlay D, Panczer G, Rey C, Delmas PD, Boivin G. Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Miner Metab. 2010;28:433–45.CrossRef
32.
go back to reference Rocha FS, Limirio PH, Zanetta-Barbosa D, Batista JD, Dechichi P. The effects of ionizing radiation on the growth plate in rat tibiae. Microsc Res Tech. 2016;79:1147–51.CrossRef Rocha FS, Limirio PH, Zanetta-Barbosa D, Batista JD, Dechichi P. The effects of ionizing radiation on the growth plate in rat tibiae. Microsc Res Tech. 2016;79:1147–51.CrossRef
33.
go back to reference Kubisz L, Polomska M. FT NIR Raman studies on gamma-irradiated bone. Spectrochim Acta A Mol Biomol Spectrosc. 2007;66:616–25.CrossRef Kubisz L, Polomska M. FT NIR Raman studies on gamma-irradiated bone. Spectrochim Acta A Mol Biomol Spectrosc. 2007;66:616–25.CrossRef
34.
go back to reference Bozkurt O, Bilgin MD, Evis Z, Pleshko N, Severcan F. Early alterations in bone characteristics of type I diabetic rat femur: a Fourier transform infrared (FT-IR) imaging study. Appl Spectrosc. 2016;70:2005–15.CrossRef Bozkurt O, Bilgin MD, Evis Z, Pleshko N, Severcan F. Early alterations in bone characteristics of type I diabetic rat femur: a Fourier transform infrared (FT-IR) imaging study. Appl Spectrosc. 2016;70:2005–15.CrossRef
35.
go back to reference Harrington MJ, Gupta HS, Fratzl P, Waite JH. Collagen insulated from tensile damage by domains that unfold reversibly: in situ X-ray investigation of mechanical yield and damage repair in the mussel byssus. J Struct Biol. 2009;167:47–54.CrossRef Harrington MJ, Gupta HS, Fratzl P, Waite JH. Collagen insulated from tensile damage by domains that unfold reversibly: in situ X-ray investigation of mechanical yield and damage repair in the mussel byssus. J Struct Biol. 2009;167:47–54.CrossRef
36.
go back to reference Nguyen H, Morgan DA, Forwood MR. Sterilization of allograft bone: effects of gamma irradiation on allograft biology and biomechanics. Cell Tissue Bank. 2007;8:93–105.CrossRef Nguyen H, Morgan DA, Forwood MR. Sterilization of allograft bone: effects of gamma irradiation on allograft biology and biomechanics. Cell Tissue Bank. 2007;8:93–105.CrossRef
37.
go back to reference Burr DB. The contribution of the organic matrix to bone’s material properties. Bone. 2002;31:8–11.CrossRef Burr DB. The contribution of the organic matrix to bone’s material properties. Bone. 2002;31:8–11.CrossRef
38.
go back to reference Turner CH. Determinants of skeletal fragility and bone quality. J Musculoskelet Neuronal Interact. 2002;2:527–8.PubMed Turner CH. Determinants of skeletal fragility and bone quality. J Musculoskelet Neuronal Interact. 2002;2:527–8.PubMed
Metadata
Title
Ionizing radiation and bone quality: time-dependent effects
Authors
Pedro Henrique Justino Oliveira Limirio
Priscilla Barbosa Ferreira Soares
Eduardo Tadashi Pinto Emi
Camila de Carvalho Almança Lopes
Flaviana Soares Rocha
Jonas Dantas Batista
Gustavo Davi Rabelo
Paula Dechichi
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Radiation Oncology / Issue 1/2019
Electronic ISSN: 1748-717X
DOI
https://doi.org/10.1186/s13014-019-1219-y

Other articles of this Issue 1/2019

Radiation Oncology 1/2019 Go to the issue