Irradiation affects the structural, cellular and molecular components of jawbones

References

• Abraham AC, Agarwalla A, Yadavalli A, Liu JY, Tang SY. 2016. Microstructural and compositional contributions towards the mechanical behavior of aging human bone measured by cyclic and impact reference point indentation. Bone. 87:37–43.
   PubMed Web of Science ®Google Scholar
• Aitasalo K. 1986. Effect of irradiation on early enzymatic changes in healing mandibular periosteum and bone. A histochemical study on rats. Acta Radiol Oncol. 25(3):207–212.
   PubMed Web of Science ®Google Scholar
• Alikhani M, Khoo E, Alyami B, Raptis M, Salgueiro JM, Oliveira MS, Boskey A, Teixeira CC. 2012. Osteogenic effect of high-frequency acceleration on alveolar bone. J Dent Res. 91(4):413–419.
   PubMed Web of Science ®Google Scholar
• Alwood JS, Shahnazari M, Chicana B, Schreurs AS, Kumar A, Bartolini A, Shirazi-Fard Y, Globus RK. 2015. Ionizing radiation stimulates expression of pro-osteoclastogenic genes in marrow and skeletal tissue. J Interferon Cytokine Res. 35(6):480–487.
   PubMed Web of Science ®Google Scholar
• Aquino KAS. 2012. Sterilization by Gamma irradiation. Gamma radiat. 10:171–206.
   Google Scholar
• Asikainen P, Klemetti E, Kotilainen R, Vuillemin T, Sutter F, Voipio HM, Kullaa AM. 1998. Osseointegration of dental implants in bone irradiated with 40, 50 or 60 Gy doses. An experimental study with beagle dogs. Clin Oral Implants Res. 9(1):20–25.
   PubMed Web of Science ®Google Scholar
• Bailey AJ, Rhodes DN, Cater CW. 1964. Irradiation-induced crosslinking of collagen. Radiat Res. 22:606–621.
   PubMed Web of Science ®Google Scholar
• Bala Y, Depalle B, Farlay D, Douillard T, Meille S, Follet H, Chapurlat R, Chevalier J, Boivin G. 2012. Bone micromechanical properties are compromised during long-term alendronate therapy independently of mineralization. J Bone Miner Res. 27(4):825–834.
   PubMed Web of Science ®Google Scholar
• Balli E, Comelekoglu U, Yalin E, Yilmaz N, Aslantas S, Sögüt F, Berköz M, Yalin S. 2009. Exposure to gamma rays induces early alterations in skin in rodents: mechanical, biochemical, and structural responses. Ecotoxicol Environ Saf. 72(3):889–894.
   PubMed Web of Science ®Google Scholar
• Barcellos-Hoff MH. 1998. How do tissues respond to damage at the cellular level? The role of cytokines in irradiated tissues. Radiat Res. 150(5):S109–S20.
   PubMed Web of Science ®Google Scholar
• Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, Ritchie RO. 2011. Characterization of the effects of x-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials. 32(34):8892–8904.
   PubMed Web of Science ®Google Scholar
• Bernier J, Hall EJ, Giaccia A. 2004. Radiation oncology: a century of achievements. Nat Rev Cancer. 4(9):737–747.
   PubMed Web of Science ®Google Scholar
• Bolan PJ, Arentsen L, Sueblinvong T, Zhang Y, Moeller S, Carter JS, Downs LS, Ghebre R, Yee D, Froelich J, Hui S. 2013. Water-fat MRI for assessing changes in bone marrow composition due to radiation and chemotherapy in gynecologic cancer patients. J Magn Reson Imaging. 38(6):1578–1584.
   PubMed Web of Science ®Google Scholar
• Bonyadi M, Waldman SD, Liu D, Aubin JE, Grynpas MD, Stanford WL. 2003. Mesenchymal progenitor self-renewal deficiency leads to age-dependent osteoporosis in Sca-1/Ly-6a null mice. Proc Natl Acad Sci USA. 100(10):5840–5845.
   PubMed Web of Science ®Google Scholar
• Brasseur M, Brogniez V, Grégoire V, Reychler H, Lengelé B, D’Hoore W, Nyssen-Behets C. 2006. Effects of irradiation on bone remodelling around mandibular implants: an experimental study in dogs. Int J Oral Maxillofac Surg. 35(9):850–855.
   PubMed Web of Science ®Google Scholar
• Cao X, Wu X, Frassica D, Yu B, Pang L, Xian L, Wan M, Lei W, Armour M, Tryggestad E, et al. 2011. Irradiation induces bone injury by damaging bone marrow microenvironment for stem cells. Proc Natl Acad Sci USA. 108(4):1609–1614.
   PubMed Web of Science ®Google Scholar
• Centrella M, Casinghino S, Kim J, Pham T, Rosen V, Wozney J, McCarthy TL. 1995. Independent changes in type I and type II receptors for transforming growth factor beta induced by bone morphogenetic protein 2 parallel expression of the osteoblast phenotype. Mol Cell Biol. 15(6):3273–3281.
   PubMed Web of Science ®Google Scholar
• Centrella M, McCarthy TL, Canalis E. 1991. Current concepts review: transforming growth factor-β and remodeling of bone. J Bone Joint Surg. 73(9):1418–1428.
   PubMed Web of Science ®Google Scholar
• Chandra A, Lin T, Tribble MB, Zhu J, Altman AR, Tseng WJ, Zhang Y, Akintoye SO, Cengel K, Liu XS, et al. 2014. PTH1-34 alleviates radiotherapy-induced local bone loss by improving osteoblast and osteocyte survival. Bone. 67:33–40.
   PubMed Web of Science ®Google Scholar
• Chandra A, Lin T, Zhu J, Tong W, Huo Y, Jia H, Zhang Y, Liu XS, Cengel K, Xia B, et al. 2015. PTH1-34 blocks radiation-induced osteoblast apoptosis by enhancing DNA repair through canonical Wnt pathway. J Biol Chem. 290(1):157–167.
   PubMed Web of Science ®Google Scholar
• Chang DJ, Ji C, Kim KK, Casinghino S, McCarthy TL, Centrella M. 1998. Reduction in transforming growth factor β1 receptor 1 expression and transcription factor CBFa1 on bone cells by glucocorticoid. J Biol Chem. 273(9):4892–4896.
   PubMed Web of Science ®Google Scholar
• Chatterjee M, Faot F, Correa C, Duyck J, Naert I, Vandamme K. 2017. A robust methodology for the quantitative assessment of the rat jawbone microstructure. Int J Oral Sci. 9(2):87–94.
   PubMed Web of Science ®Google Scholar
• Connell PP, Hellman S. 2009. Advances in radiotherapy and implications for the next century: a historical perspective. Cancer Res. 69(2):383–392.
   PubMed Web of Science ®Google Scholar
• Costa S, Reagan MR. 2019. Therapeutic irradiation: consequences for bone and bone marrow adipose tissue. Front Endocrinol. 10:1–7.
   PubMed Web of Science ®Google Scholar
• Curi MM, Cardoso CL, de Lima HG, Kowalski LP, Martins MD. 2016. Histopathologic and histomorphometric analysis of irradiation injury in bone and the surrounding soft tissues of the jaws. J Oral Maxillofac Surg. 74(1):190–199.
   PubMed Web of Science ®Google Scholar
• Curi MM, Oliveira dos Santos M, Feher O, Faria JC, Rodrigues ML, Kowalski LP. 2007. Management of extensive osteoradionecrosis of the mandible with radical resection and immediate microvascular reconstruction. J Oral Maxillofac Surg. 65(3):434–438.
   PubMed Web of Science ®Google Scholar
• Dai QG, Zhang P, Wu YQ, Ma XZ, Pang J, Jiang LY, Fang B. 2014. Ovariectomy induces osteoporosis in the maxillary alveolar bone: an in vivo micro-CT and histomorphometric analysis in rats. Oral Dis. 20(5):514–520.
   PubMed Web of Science ®Google Scholar
• Damek-Poprawa M, Both S, Wright AC, Maity A, Akintoye SO. 2013. Onset of mandible and tibia osteoradionecrosis: a comparative pilot study in the rat. Oral Surg Oral Med Oral Pathol Oral Radiol. 115(2):201–211.
   PubMed Web of Science ®Google Scholar
• de Oliveira JAG, do Amaral Escada AL, Alves Rezende MCR, Mathor MB, Alves Claro APR. 2012. Analysis of the effects of irradiation in osseointegrated dental implants. Clin Oral Implants Res. 23(4):511–514.
   PubMed Web of Science ®Google Scholar
• De Souza Faloni APS, Schoenmaker T, Azari A, Katchburian E, Cerri PS, De Vries TJ, Everts V. 2011. Jaw and long bone marrows have a different osteoclastogenic potential. Calcif Tissue Int. 88(1):63–74.
   PubMed Web of Science ®Google Scholar
• Dekker H, Bravenboer N, van Dijk D, Bloemena E, Rietveld DHF, ten Bruggenkate CM, Schulten EAJM. 2018. The irradiated human mandible: a quantitative study on bone vascularity. Oral Oncology. 87:126–130.
   PubMed Web of Science ®Google Scholar
• Dekker H, Schulten EAJM, van Ruijven L, van Essen HW, Blom GJ, Bloemena E, ten Bruggenkate CM, Kullaa AM, Bravenboer N. 2020. Bone microarchitecture and turnover in the irradiated human mandible. J Cranio-Maxillo-Facial Surg. 48(8):733–740.
   PubMed Web of Science ®Google Scholar
• Deloch L, Derer A, Hueber AJ, Herrmann M, Schett GA, Wolfelschneider J, Hahn J, Ruhle PF, Stillkrieg W, Fuchs J, et al. 2018. U.S. Gaipl, low-dose radiotherapy ameliorates advanced arthritis in hTNF-alpha tg mice by particularly positively impacting on. Front Immunol. 9:1834.
   PubMed Web of Science ®Google Scholar
• Dholam KP, Gurav SV. 2012. Dental implants in irradiated jaws: a literature review. J Can Res Ther. 8(6):85–93.
   Google Scholar
• Domazetovic V, Marcucci G, Iantomasi T, Brandi ML, Vincenzini MT. 2017. Oxidative stress in bone remodeling: role of antioxidants. Clin Cases Miner Bone Metab. 14(2):209–216.
   PubMedGoogle Scholar
• Donaubauer AJ, Deloch L, Becker I, Fietkau R, Frey B, Gaipl US. 2020. The influence of radiation on bone and bone cells – differential effects on osteoclasts and osteoblasts. Int J Mol Sci. 21(17):6377.
   Web of Science ®Google Scholar
• Dudziak ME, Saadeh PB, Mehrara BJ, Steinbrech DS, Greenwald JA, Gittes GK, Longaker MT. 2000. The effects of ionizing radiation on osteoblast-like cells in vitro. Plast Reconstr Surg. 106(5):1049–1061.
   PubMed Web of Science ®Google Scholar
• Elliott SP, Jarosek SL, Alanee SR, Konety BR, Dusenbery KE, Virnig BA. 2011. Three-dimensional external beam radiotherapy for prostate cancer increases the risk of hip fracture. Cancer. 117(19):4557–4565.
   PubMed Web of Science ®Google Scholar
• Epstein JB, Lunn R, Le N, Stevenson-Moore P. 1998. Periodontal attachment loss in patients after head and neck radiation therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 86(6):673–677.
   PubMed Web of Science ®Google Scholar
• Ergun H, Howland WJ. 1980. Postradiation atrophy of mature bone. CRC Crit Rev Diagn Imaging. 12(3):225–243.
   PubMedGoogle Scholar
• Ewing J. 1926. Radiation osteitis. Acta Radiol. 6(1–6):399–412.
   Google Scholar
• Faot F, Chatterjee M, de Camargos GV, Duyck J, Vandamme K. 2015. Micro-CT analysis of the rodent jaw bone micro-architecture: a systematic review. Bone Rep. 2 (2):14–24.
   PubMedGoogle Scholar
• Fathima NN, Madhan B, Rao JR, Nair BU, Ramasami T. 2004. Interaction of aldehydes with collagen: effect on thermal, enzymatic and conformational stability. Int J Biol Macromol. 34(4):241–247.
   PubMed Web of Science ®Google Scholar
• Feng X, McDonald JM. 2011. Disorders of bone remodeling. Annu Rev Pathol. 6:121–145.
   PubMed Web of Science ®Google Scholar
• Fontani F, Marcucci G, Iantomasi T, Brandi ML, Vincenzini MT. 2015. Glutathione, N-acetylcysteine and lipoic acid down-regulate starvation-induced apoptosis, RANKL/OPG ratio and sclerostin in osteocytes: involvement of JNK and ERK1/2 signalling. Calcif Tissue Int. 96(4):335–346.
   PubMed Web of Science ®Google Scholar
• Fornetti J, Welm AL, Stewart SA. 2018. Understanding the bone in cancer metastasis. J Bone Miner Res. 33(12):2099–2113.
   PubMed Web of Science ®Google Scholar
• Fritz KS, Petersen DR. 2011. Exploring the biology of lipid peroxidation-derived protein carbonylation. Chem Res Toxicol. 24(9):1411–1419.
   PubMed Web of Science ®Google Scholar
• Gal TJ, Munoz-Antonia T, Muro-Cacho CA, Klotch DW. 2000. Radiation effects on osteoblasts in vitro: a potential role in osteoradionecrosis. Arch Otolaryngol Head Neck Surg. 126(9):1124–1128.
   PubMedGoogle Scholar
• Green DE, Adler BJ, Chan ME, Rubin CT. 2012. Devastation of adult stem cell pools by irradiation precedes collapse of trabecular bone quality and quantity. J Bone Miner Res. 27(4):749–759.
   PubMed Web of Science ®Google Scholar
• Green DE, Rubin CT. 2014. Consequences of irradiation on bone and marrow phenotypes, and its relation to disruption of hematopoietic precursors. Bone. 63:87–94.
   PubMed Web of Science ®Google Scholar
• Heinonen V, Ruotsalainen TJ, Paavola L, Mikkonen JJ, Asikainen P, Koistinen AP, Kullaa AM. 2018. Alveolar bone remodeling after tooth extraction in irradiated mandible: an experimental study with canine model. Ultrastruct Pathol. 42(2):124–132.
   PubMed Web of Science ®Google Scholar
• Henriksen K, Bollerslev J, Everts V, Karsdal MA. 2011. Osteoclast activity and subtypes as a function of physiology and pathology-implications for future treatments of osteoporosis. Endocr Rev. 32(1):31–63.
   PubMed Web of Science ®Google Scholar
• Henriksen K, Neutzsky-Wulff AV, Bonewald LF, Karsdal MA. 2009. Local communication on and within bone controls bone remodeling. Bone. 44(6):1026–1033.
   PubMed Web of Science ®Google Scholar
• Hommez GM, De Meerleer GO, De Neve WJ, De Moor RJ. 2012. Effect of radiation dose on the prevalence of apical periodontitis-a dosimetric analysis. Clin Oral Investig. 16(6):1543–1547.
   PubMed Web of Science ®Google Scholar
• Hopewell JW. 2003. Radiation-therapy effects on bone density. Med Pediatr Oncol. 41(3):208–211.
   PubMedGoogle Scholar
• Huang B, Yao Q, Huang Y, Zhang L, Yao Y, Gong P, Tang H. 2018. Combination use of BMP2 and VEGF165 promotes osseointegration and stability of titanium implants in irradiated bone. BioMed Res Int. 2018:1–11.
   Web of Science ®Google Scholar
• Huang B, Zhang Q, Yuan Y, Xin N, He K, Huang Y, Tang H, Gong P. 2018. Sema3a inhibits the differentiation of Raw264.7 cells to osteoclasts under 2Gy radiation by reducing inflammation. PLoS One. 13(7):e0200000.
   PubMed Web of Science ®Google Scholar
• Hui SK, Fairchild GR, Kidder LS, Sharma M, Bhattacharya M, Jackson S, Le C, Petryk A, Islam MS, Yee D. 2013. The influence of therapeutic radiation on the patterns of bone remodeling in ovary-intact and ovariectomized mice. Calcif Tissue Int. 92(4):372–384.
   PubMed Web of Science ®Google Scholar
• Jacobsson M, Jonsson A, Albrektsson T, Turesson I. 1985. Alterations in bone regenerative capacity after low level gamma irradiation. A quantitative study. Scand J Plast Reconstr Surg. 19(3):231–236.
   PubMed Web of Science ®Google Scholar
• Jegoux F, Malard O, Goyenvalle E, Aguado E, Daculsi G. 2010. Radiation effects on bone healing and reconstruction: interpretation of the literature. Oral Surgery Oral Med. 109(2):173–184.
   PubMed Web of Science ®Google Scholar
• Jereczek-Fossa BA, Orecchia R. 2002. Radiotherapy-induced mandibular bone complications. Cancer Treat Rev. 28(1):65–74.
   PubMed Web of Science ®Google Scholar
• Jonsson EL, Erngren I, Engskog M, Haglöf J, Arvidsson T, Hedeland M, Petterson C, Laurell G, Nestor M. 2019. Exploring radiation response in two head and neck squamous carcinoma cell lines through metabolic profiling. Front Oncol. 9:825.
   PubMed Web of Science ®Google Scholar
• Kajarabille N, Díaz-Castro J, Hijano S, López-Frías M, López-Aliaga I, Ochoa JJ. 2013. A new insight to bone turnover: role of ω-3 polyunsaturated fatty acids. Sci World J. 2013:1–16.
   Google Scholar
• Kim SG, Kim YU, Park JC, Oh YK. 2001. Effects of presurgical and post-surgical irradiation on the healing process of Medpor in dogs. Int J Oral Maxillofac Surg. 30(5):438–442.
   PubMed Web of Science ®Google Scholar
• Kimble RB, Srivastava S, Ross FP, Matayoshi A, Pacifici R. 1996. Estrogen deficiency increases the ability of stromal cells to support murine osteoclastogenesis via an interleukin-1 and tumor necrosis factor-mediated stimulation of macrophage colony-stimulating factor production. J Biol Chem. 271(46):28890–28897.
   PubMed Web of Science ®Google Scholar
• King MA, Casarett GW, Weber DA. 1979. A study of irradiated bone: I. histopathologic and physiologic changes. J Nucl Med. 20(11):1142–1149.
   PubMed Web of Science ®Google Scholar
• Kondo H, Searby ND, Mojarrab R, Phillips J, Alwood J, Yumoto K, Almeida EA, Limoli CL, Globus RK. 2009. Total-body irradiation of postpubertal mice with (137)Cs acutely compromises the microarchitecture of cancellous bone and increases osteoclasts. Radiat Res. 171(3):283–289.
   PubMed Web of Science ®Google Scholar
• Kubota H, Miyawaki D, Mukumoto N, Ishihara T, Matsumura M, Hasegawa T, Akashi M, Kiyota N, Shinomiya H, Teshima M, et al. 2021. Risk factors for osteoradionecrosis of the jaw in patients with head and neck squamous cell carcinoma. Radiat Oncol. 16(1):1–11.
   PubMed Web of Science ®Google Scholar
• Lanyon LE. 1993. Osteocytes, strain detection, bone modeling and remodeling. Calcif Tissue Int. 53(S1):S102–S107.
   PubMedGoogle Scholar
• Lau P, Baumstark-Khan C, Hellweg CE, Reitz G. 2010. X-irradiation-induced cell cycle delay and DNA double-strand breaks in the murine osteoblastic cell line OCT-1. Radiat Environ Biophys. 49(2):271–280.
   PubMed Web of Science ®Google Scholar
• Lee R, Britz-McKibbin P. 2010. Metabolomic studies of radiation-induced apoptosis of human leukocytes by capillary electrophoresis-mass spectrometry and flow cytometry: adaptive cellular responses to ionizing radiation. Electrophoresis. 31(14):2328–2337.
   PubMed Web of Science ®Google Scholar
• Leibbrandt A, Penninger JM. 2008. RANK/RANKL: regulators of Immune responses and bone physiology. Ann NY Acad Sci. 1143:123–150.
   PubMed Web of Science ®Google Scholar
• Li HH, Wang YW, Chen R, Zhou B, Ashwell JD, Jr., Fornace AJ. 2015. Ionizing radiation impairs T cell activation by affecting metabolic reprogramming. Int J Biol Sci. 11(7):726–736.
   PubMed Web of Science ®Google Scholar
• Limirio PHJO, Soares PBR, Emi ETP, Lopes CDA, Rocha FS, Batista JD, Rabelo GD, Dechichi P. 2019. Ionizing radiation and bone quality: timedependent effects. Radiat Oncol. 14(1):2–8.
   PubMedGoogle Scholar
• Liu H, Wang Z, Zhang X, Qiao Y, Wu S, Dong F, Chen Y. 2013. Selection of candidate radiation biomarkers in the serum of rats exposed to gamma-rays by GC/TOFMS-based metabolomics. Radiat Prot Dosimetry. 154(1):9–17.
   PubMed Web of Science ®Google Scholar
• Lorimore SA, Coates PJ, Scobie GE, Milne G, Wright EG. 2001. Inflammatory-type responses after exposure to ionizing radiation in vivo: a mechanism for radiation-induced bystander effects? Oncogene. 20(48):7085–7095.
   PubMed Web of Science ®Google Scholar
• Manna SK, Krausz KW, Bonzo JA, Idle JR, Gonzalez FJ. 2013. Metabolomics reveals aging-associated attenuation of noninvasive radiation biomarkers in mice: potential role of polyamine catabolism and incoherent DNA damage-repair. J Proteome Res. 12(5):2269–2281.
   PubMed Web of Science ®Google Scholar
• Marathe N, Rangaswami H, Zhuang S, Boss GR, Pilz RB. 2012. Pro-survival effects of 17β-estradiol on osteocytes are mediated by nitric oxide/cGMP via differential actions of cGMP-dependent protein kinases I and II. J Biol Chem. 287(2):978–988.
   PubMed Web of Science ®Google Scholar
• Marques MA, Dib LL. 2004. Periodontal changes in patients undergoing radiotherapy. J Periodontol. 75(9):1178–1187.
   PubMed Web of Science ®Google Scholar
• Maslennikova A, Kochueva M, Ignatieva N, Vitkin A, Zakharkina O, Kamensky V, Sergeeva E, Kiseleva E, Bagratashvili V. 2015. Effects of gamma irradiation on collagen damage and remodeling. Int J Radiat Biol. 91(3):240–247.
   PubMed Web of Science ®Google Scholar
• Mello ASS, Santos PLD, Marquesi A, Queiroz TP, Margonar R, Faloni APS. 2018. Some aspects of bone remodeling around dental implants. Rev Clin Periodoncia Implantol Rehabil Oral. 11(1):49–53.
   Google Scholar
• Menon SS, Uppal M, Randhawa S, Cheema MS, Aghdam N, Usala RL, Ghosh SP, Cheema AK, Dritschilo A. 2016. Radiation metabolomics: current status and future directions. Front Oncol. 6:20– 10.
   PubMed Web of Science ®Google Scholar
• Misch CE, Bidez MW, Sharawy M. 2001. A bioengineered implant for a predetermined bone cellular response to loading forces. a literature review and case reports. J Periodontol. 72(9):1276–1286.
   PubMed Web of Science ®Google Scholar
• Mitchell MJ, Logan PM. 1998. Radiation-induced changes in bone. Radiographics. 18(5):1125–1136.
   PubMed Web of Science ®Google Scholar
• Nguyen H, Morgan DA, Forwood MR. 2007. Sterilization of allograft bone: effects of gamma irradiation on allograft biology and biomechanics. Cell Tissue Bank. 8(2):93–105.
   PubMedGoogle Scholar
• Nishimura RD, Roumanas E, Beumer J, Moy PK, Shimizu KT. 1998. Restoration of irradiated patients using osseointegrated implants: current perspectives. J Prosthet Dent. 79(6):641–647.
   PubMed Web of Science ®Google Scholar
• Nishiyama K, Inaba F, Higashihara T, Kitatani K, Kozuka T. 1992. Radiation osteoporosis—an assessment using single energy quantitative computed tomography. Eur Radiol. 2(4):322–325.
   Google Scholar
• Oest ME, Policastro CG, Mann KA, Zimmerman ND, Damron TA. 2018. Longitudinal effects of single hindlimb radiation therapy on bone strength and morphology at local and Contralateral Sites. J Bone Miner Res. 33(1):99–112.
   PubMed Web of Science ®Google Scholar
• Omi M, Mishina T. 2020. Role of osteoclasts in oral homeostasis and jawbone diseases. Oral Sci Int. 18(1):14–27.
   PubMed Web of Science ®Google Scholar
• Parikka V, Lehenkari P, Sassi ML, Halleen J, Risteli J, Harkonen P, Vaananen HK. 2001. Estrogen reduces the depth of resorption pits by disturbing the organic bone matrix degradation activity of mature osteoclasts. Endocrinology. 142(12):5371–5378.
   PubMed Web of Science ®Google Scholar
• Patterson AD, Li H, Eichler GS, Krausz KW, Weinstein JN, Jr. Fornace AJ, Gonzalez FJ, Idle JR. 2008. UPLC-ESI-TOFMS-based metabolomics and gene expression dynamics inspector self-organizing metabolomic maps as tools for understanding the cellular response to ionizing radiation. Anal Chem. 80(3):665–674.
   PubMed Web of Science ®Google Scholar
• Pendleton MM, Emerzian SR, Liu J, Tang SY, O’Connell GD, Alwood JS, Keaveny TM. 2019. Effects of ex vivo ionizing radiation on collagen structure and whole-bone mechanical properties of mouse vertebrae. Bone. 128:115043.
   PubMed Web of Science ®Google Scholar
• Pepper MS. 1997. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 8(1):21–43.
   PubMedGoogle Scholar
• Poort LJ, Ludlage JHB, Lie N, Böckmann RA, Odekerken JCE, Hoebers FJ, Kessler PAWH. 2017. The histological and histomorphometric changes in the mandible after radiotherapy: an animal model. J Craniomaxillofac Surg. 45(5):716–721.
   PubMed Web of Science ®Google Scholar
• Poulsen RC, Moughan PJ, Kruger MC. 2007. Long-chain polyunsaturated fatty acids and the regulation of bone metabolism. Exp Biol Med. 232(10):1275–1288.
   Web of Science ®Google Scholar
• Pramojanee SN, Pratchayasakul W, Chattipakorn N, Chattipakorn SC. 2012. Low-dose dental irradiation decreases oxidative stress in osteoblastic MC3T3-E1 cells without any changes in cell viability, cellular proliferation and cellular apoptosis. Arch. Oral Biol. 57(3):252–256.
   PubMed Web of Science ®Google Scholar
• Quinn JMW, Gillespie MT. 2005. Modulation of osteoclast formation. Biochem Biophys Res Commun. 328(3):739–745.
   PubMed Web of Science ®Google Scholar
• Rabelo GD, Beletti ME, Dechichi P. 2010. Histological analysis of the alterations on cortical bone channels network after radiotherapy: a rabbit study. Microsc Res Tech. 73(11):1015–1018.
   PubMed Web of Science ®Google Scholar
• Ritchlin CT, Haas-Smith SA, Li P, Hicks DG, Schwarz EM. 2003. Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis. J Clin Invest. 111(6):821–831.
   PubMed Web of Science ®Google Scholar
• Rohrer MD, Kim Y, Fayos JV. 1979. The effect of cobalt-60 irradiation on monkey mandibles. Oral Surg Oral Med Oral Pathol. 48(5):424–440.
   PubMedGoogle Scholar
• Sakurai T, Sawada Y, Yoshimoto M, Kawai M, Miyakoshi J. 2007. Radiation-induced reduction of osteoblast differentiation in C2C12 cells. JRR. 48(6):515–521.
   PubMed Web of Science ®Google Scholar
• Shimizu Y, Ishida T, Hosomichi J, Kaneko S, Hatano K, Ono t. 2013. Soft diet causes greater alveolar osteopenia in the mandible than in the maxilla. Arch Oral Biol. 58(8):907–911.
   PubMed Web of Science ®Google Scholar
• Singh SP, Parviainen I, Dekker H, Schulten EAJM, ten Bruggenkate CM, Bravenboer N, Mikkonen JJ, Turunen MJ, Koistinen AP, Kullaa AM. 2015. Raman Microspectroscopy Demonstrates Alterations in Human Mandibular Bone after Radiotherapy. J Anal Bioanal Tech. 6(6):276.
   Google Scholar
• Smith MR, Lee WC, Brandman J, Wang Q, Botteman M, Pashos CL. 2005. Gonadotropin-releasing hormone agonists and fracture risk: a claims-based cohort study of men with nonmetastatic prostate cancer. J Clin Oncol. 23(31):7897–7903.
   PubMed Web of Science ®Google Scholar
• Soares PBR, Soares CJ, Justino PH, Limirio O, Lara VC, Moura CCG, Barbosa DZ. 2020. Biomechanical and morphological changes produced by ionizing radiation on bone tissue surrounding dental implant. J Appl Oral Sci. 28:1–8.
   Web of Science ®Google Scholar
• Szymczyk KH, Shapiro IM, Adams CS. 2004. Ionizing radiation sensitizes bone cells to apoptosis. Bone. 34(1):148–156.
   PubMed Web of Science ®Google Scholar
• Tanaka TI, Chan HL, Tindle DI, MacEachern M, Oh TJ. 2013. Updated clinical considerations for dental implant therapy in irradiated head and neck cancer patients. J Prosthodont. 22(6):432–438.
   PubMedGoogle Scholar
• Tate MLK, Adamson JR, Tami AE, Bauer TW. 2004. The Osteocyte. Int J Biochem Cell Biol. 36(1):1–8.
   PubMed Web of Science ®Google Scholar
• Tyburski JB, Patterson AD, Krausz KW, Slavík J, Jr. Fornace AJ, Gonzalez FJ, Idle JR. 2008. Radiation metabolomics. 1. identification of minimally invasive urine biomarkers for gamma-radiation exposure in mice. Radiat Res. 170(1):1–14.
   PubMed Web of Science ®Google Scholar
• Villars F, Guillotin B, Amedee T, Dutoya S, Bordenave L, Bareille R, Amedee J. 2002. Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication. Am J Physiol Cell Physiol. 282(4):C775–C785.
   PubMed Web of Science ®Google Scholar
• Vit JP, Rosselli F. 2003. Role of the ceramide-signaling pathways in ionizing radiation-induced apoptosis. Oncogene. 22(54):8645–8652.
   PubMed Web of Science ®Google Scholar
• Wada T, Nakashima T, Hiroshi N, Penninger JM. 2006. RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol Med. 12(1):17–25.
   PubMed Web of Science ®Google Scholar
• Walsh NC, Crotti TN, Goldring SR, Gravallese EM. 2005. Rheumatic diseases: the effects of inflammation on bone. Immunol Rev. 208:228–251.
   PubMed Web of Science ®Google Scholar
• Weinlaender M, Beumer J, Kenney EB, Lekovic V, Holmes R, Moy PK, Hanns P, Jr 2006. Histomorphometric and fluorescence microscopic evaluation of interfacial bone healing around 3 different dental implants before and after radiation therapy. Int J Oral Maxillofac Implants. 21(2):212–224.
   PubMed Web of Science ®Google Scholar
• Wernle JD, Damron TA, Allen MJ, Mann KA. 2010. Local irradiation alters bone morphology and increases bone fragility in a mouse model. J Biomech. 43(14):2738–2746.
   PubMed Web of Science ®Google Scholar
• Willey JS, Lloyd SAJ, Nelson GA, Bateman TA. 2011. Ionizing radiation and bone loss: space exploration and clinical therapy applications. Clin Rev Bone Miner Metab. 9(1):54–62.
   PubMedGoogle Scholar
• Willey JS, Lloyd SA, Robbins ME, Bourland JD, Smith-Sielicki H, Bowman LC, Norrdin RW, Bateman TA. 2008. Early increase in osteoclast number in mice after whole-body irradiation with 2 Gy X rays. Radiat. Res. 170(3):388–392.
   PubMed Web of Science ®Google Scholar
• Williams HJ, Davies AM. 2006. The effect of X-rays on bone: a pictorial review. Eur Radiol. 16(3):619–633.
   PubMed Web of Science ®Google Scholar
• Xu X, Li R, Zhou Y, Zou Q, Ding Q, Wang J, Jin W, Hua G, Gao J. 2017. Dysregulated systemic lymphocytes affect the balance of osteogenic/adipogenic differentiation of bone mesenchymal stem cells after local irradiation. Stem Cell Res Ther. 8(1):71.
   PubMedGoogle Scholar
• Xu W, Xu L, Chen M, Mao YT, Xie ZG, Wu SL, Dong QR. 2012. The effects of low dose X-irradiation on osteoblastic MC3T3-E1 cells in vitro. BMC Musculoskelet. Disord. 13:94.
   PubMed Web of Science ®Google Scholar
• Xu YQ, Zhao TM, Xu WJ, Ding Y. 2013. Periodontal microstructure change and tooth movement pattern under different force magnitudes in ovariectomized rats: an in-vivo microcomputed tomography study. Am J Orthod Dentofacial Orthop. 143(6):828–836.
   PubMed Web of Science ®Google Scholar
• Zhai J, He F, Wang J, Chen J, Tong L, Zhu G. 2019. Influence of radiation exposure pattern on the bone injury and osteoclastogenesis in a rat model. Int J Mol Med. 44(6):2265–2275.
   PubMed Web of Science ®Google Scholar
• Zhang J, Qiu X, Xi K, Hu W, Pei H, Nie J, Wang Z, Ding J, Shang P, Li B, et al. 2018. Therapeutic ionizing radiation induced bone loss: a review of in vivo and in vitro findings. Connect Tissue Res. 59(6):509–522.
   PubMed Web of Science ®Google Scholar
• Zhuang XM, Zhou B. 2020. Exosome secreted by human gingival fibroblasts in radiation therapy inhibits osteogenic differentiation of bone mesenchymal stem cells by transferring miR-23a. Biomed Pharmacother. 131:110672.
   PubMed Web of Science ®Google Scholar