Skip to main content
Top
Published in: Calcified Tissue International 5/2009

01-05-2009

A Preliminary Investigation into the Effects of X-Ray Radiation on Superficial Cranial Vascularization

Authors: Sophie Desmons, Michal Heger, Caroline Delfosse, Guillaume Falgayrac, Thierry Sarrazin, Claire Delattre, Sylvain Catros, Serge Mordon, Guillaume Penel

Published in: Calcified Tissue International | Issue 5/2009

Login to get access

Abstract

Radiation therapy (RT) is an established treatment modality for malignant neoplasms. RT induces tissue damage that may lead to osteoradionecrosis in more severe cases. Suitable animal models to study RT-induced changes in membranous craniofacial bone are currently not available. The aim of this study was therefore to quantify RT-induced changes in cranial microcirculation using a newly developed calvaria chamber model and to relate these changes to RT-induced histological damage. New Zealand white rabbits received a total radiation dose of 18.75 Gy through the calvaria chamber, and the number of vessels, the vessel length density (VLD), and angiogenic sprouting were quantified on a weekly basis during a 12-week period. At the end of 12 weeks, the RT-treated (n = 5) or control (n = 5) calvarias were biopsied for histopathological analysis. RT resulted in a steep reduction in the number of vessels and the VLD during the first 3 weeks, particularly in larger-diameter vessels, followed by a flat stabilization/remodeling phase in the subsequent 9 weeks that never restored to baseline values. Histomorphometric analysis revealed a high degree of osteocytic depletion, prominent hypocellularity in the lacunae and intraosseous vasculature, enlarged and nonconcentric Haversian systems, and a severely disorganized bone matrix in the RT-treated calvarias. Despite the prevalence of some angiogenic potential, the RT-induced effects in the early phase persisted in the intermediate to late phase, which may have contributed to the poor recovery of the RT-treated bone.
Literature
1.
go back to reference Mendes RL, Nutting CM, Harrington KJ (2002) Managing side effects of radiotherapy in head and neck cancer. Hosp Med 63:712–717PubMed Mendes RL, Nutting CM, Harrington KJ (2002) Managing side effects of radiotherapy in head and neck cancer. Hosp Med 63:712–717PubMed
2.
go back to reference Bond WR Jr, Matthews JL, Finney JW (1967) The influence of regional oxygenation on osteoradionecrosis. Oral Surg Oral Med Oral Pathol 23:99–113PubMedCrossRef Bond WR Jr, Matthews JL, Finney JW (1967) The influence of regional oxygenation on osteoradionecrosis. Oral Surg Oral Med Oral Pathol 23:99–113PubMedCrossRef
3.
go back to reference Marx RE (1983) Osteoradionecrosis: a new concept of its pathophysiology. J Oral Maxillofac Surg 41:283–288PubMedCrossRef Marx RE (1983) Osteoradionecrosis: a new concept of its pathophysiology. J Oral Maxillofac Surg 41:283–288PubMedCrossRef
4.
go back to reference Pappas GC (1969) Bone changes in osteoradionecrosis. A review. Oral Surg Oral Med Oral Pathol 27:622–630CrossRef Pappas GC (1969) Bone changes in osteoradionecrosis. A review. Oral Surg Oral Med Oral Pathol 27:622–630CrossRef
5.
6.
go back to reference Hom DB, Adams GL, Monyak D (1995) Irradiated soft tissue and its management. Otolaryngol Clin North Am 28:1003–1019PubMed Hom DB, Adams GL, Monyak D (1995) Irradiated soft tissue and its management. Otolaryngol Clin North Am 28:1003–1019PubMed
7.
go back to reference Urken ML, Buchbinder D, Costantino PD, Sinha U, Okay D, Lawson W, Biller HF (1998) Oromandibular reconstruction using microvascular composite flaps: report of 210 cases. Arch Otolaryngol Head Neck Surg 124:46–55PubMed Urken ML, Buchbinder D, Costantino PD, Sinha U, Okay D, Lawson W, Biller HF (1998) Oromandibular reconstruction using microvascular composite flaps: report of 210 cases. Arch Otolaryngol Head Neck Surg 124:46–55PubMed
8.
go back to reference Kroll SS, Schusterman MA, Reece GP, Miller MJ, Evans GR, Robb GL, Baldwin BJ (1996) Choice of flap and incidence of free flap success. Plast Reconstr Surg 98:459–463PubMedCrossRef Kroll SS, Schusterman MA, Reece GP, Miller MJ, Evans GR, Robb GL, Baldwin BJ (1996) Choice of flap and incidence of free flap success. Plast Reconstr Surg 98:459–463PubMedCrossRef
9.
go back to reference Winet H (1996) The role of microvasculature in normal and perturbed bone healing as revealed by intravital microscopy. Bone 19:39S–57SPubMedCrossRef Winet H (1996) The role of microvasculature in normal and perturbed bone healing as revealed by intravital microscopy. Bone 19:39S–57SPubMedCrossRef
10.
go back to reference Penel G, Delfosse C, Descamps M, Leroy G (2005) Composition of bone and apatitic biomaterials as revealed by intravital Raman microspectroscopy. Bone 36:893–901PubMedCrossRef Penel G, Delfosse C, Descamps M, Leroy G (2005) Composition of bone and apatitic biomaterials as revealed by intravital Raman microspectroscopy. Bone 36:893–901PubMedCrossRef
11.
go back to reference Takahashi S, Sugimoto M, Kotoura Y, Sasai K, Oka M, Yamamuro T (1994) Long-term changes in the haversian systems following high-dose irradiation. An ultrastructural and quantitative histomorphological study. J Bone Joint Surg Am 76:722–738PubMed Takahashi S, Sugimoto M, Kotoura Y, Sasai K, Oka M, Yamamuro T (1994) Long-term changes in the haversian systems following high-dose irradiation. An ultrastructural and quantitative histomorphological study. J Bone Joint Surg Am 76:722–738PubMed
12.
go back to reference Lopes CB, Pinheiro AL, Sathaiah S, Duarte J, Cristinamartins M (2005) Infrared laser light reduces loading time of dental implants: a Raman spectroscopic study. Photomed Laser Surg 23:27–31PubMedCrossRef Lopes CB, Pinheiro AL, Sathaiah S, Duarte J, Cristinamartins M (2005) Infrared laser light reduces loading time of dental implants: a Raman spectroscopic study. Photomed Laser Surg 23:27–31PubMedCrossRef
13.
go back to reference International Atomic Energy Agency (2005) Radiation oncology physics: a handbook for teachers and students. E.B. Podgorsak, sponsored by IAEA, Vienna International Atomic Energy Agency (2005) Radiation oncology physics: a handbook for teachers and students. E.B. Podgorsak, sponsored by IAEA, Vienna
14.
go back to reference Arnold M, Stas P, Kummermehr J, Schultz-Hector S, Trott KR (1998) Radiation-induced impairment of bone healing in the rat femur: effects of radiation dose, sequence and interval between surgery and irradiation. Radiother Oncol 48:259–265PubMedCrossRef Arnold M, Stas P, Kummermehr J, Schultz-Hector S, Trott KR (1998) Radiation-induced impairment of bone healing in the rat femur: effects of radiation dose, sequence and interval between surgery and irradiation. Radiother Oncol 48:259–265PubMedCrossRef
15.
go back to reference Wolf E, Roser K, Hahn M, Welkerling H, Delling G (1992) Enzyme and immunohistochemistry on undecalcified bone and bone marrow biopsies after embedding in plastic: a new embedding method for routine application. Virchows Arch A Pathol Anat Histopathol 420:17–24PubMedCrossRef Wolf E, Roser K, Hahn M, Welkerling H, Delling G (1992) Enzyme and immunohistochemistry on undecalcified bone and bone marrow biopsies after embedding in plastic: a new embedding method for routine application. Virchows Arch A Pathol Anat Histopathol 420:17–24PubMedCrossRef
16.
go back to reference Wood B, McNaughton D (2002) Raman excitation wavelength investigation of single red blood cells in vitro. J Raman Spectrosc 33:517–523CrossRef Wood B, McNaughton D (2002) Raman excitation wavelength investigation of single red blood cells in vitro. J Raman Spectrosc 33:517–523CrossRef
17.
go back to reference Wood B, Caspers P, Puppels GJ, Pandiancherri S, McNaughton D (2007) Resonance Raman spectroscopy of red blood cells using near-infrared laser excitation. Anal Bioanal Chem 387:1691–1703PubMedCrossRef Wood B, Caspers P, Puppels GJ, Pandiancherri S, McNaughton D (2007) Resonance Raman spectroscopy of red blood cells using near-infrared laser excitation. Anal Bioanal Chem 387:1691–1703PubMedCrossRef
18.
go back to reference Lakshmi RJ, Alexander M, Kurien J, Mahato KK, Kartha VB (2003) Osteoradionecrosis (ORN) of the mandible: a laser Raman spectroscopic study. Appl Spectrosc 57:1100–1116PubMedCrossRef Lakshmi RJ, Alexander M, Kurien J, Mahato KK, Kartha VB (2003) Osteoradionecrosis (ORN) of the mandible: a laser Raman spectroscopic study. Appl Spectrosc 57:1100–1116PubMedCrossRef
19.
go back to reference Penel G, Leroy G, Rey C, Bres E (1998) MicroRaman spectral study of the PO4 and CO3 vibrational modes in synthetic and biological apatites. Calcif Tissue Int 63:475–481PubMedCrossRef Penel G, Leroy G, Rey C, Bres E (1998) MicroRaman spectral study of the PO4 and CO3 vibrational modes in synthetic and biological apatites. Calcif Tissue Int 63:475–481PubMedCrossRef
20.
go back to reference Penel G, Leroy G, Rey C, Sombret B, Huvenne JP, Bres E (1997) Infrared and Raman microspectrometry study of fluor-fluor-hydroxy and hydroxy-apatite powders. J Mater Sci Mater Med 8:271–276PubMedCrossRef Penel G, Leroy G, Rey C, Sombret B, Huvenne JP, Bres E (1997) Infrared and Raman microspectrometry study of fluor-fluor-hydroxy and hydroxy-apatite powders. J Mater Sci Mater Med 8:271–276PubMedCrossRef
21.
go back to reference Legeros RZ (1994) Biological and synthetic apatites. In: Brown P, Constantz BE (eds) Hydroxyapatites and related compounds. CRC Press, Boca Raton, FL, pp 3–28 Legeros RZ (1994) Biological and synthetic apatites. In: Brown P, Constantz BE (eds) Hydroxyapatites and related compounds. CRC Press, Boca Raton, FL, pp 3–28
22.
go back to reference 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 45:157–164PubMedCrossRef 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 45:157–164PubMedCrossRef
23.
go back to reference Malizos KN, Papatheodorou LK (2005) The healing potential of the periosteum molecular aspects. Injury 36(Suppl 3):S13–S19PubMedCrossRef Malizos KN, Papatheodorou LK (2005) The healing potential of the periosteum molecular aspects. Injury 36(Suppl 3):S13–S19PubMedCrossRef
24.
go back to reference Aitasalo K (1986) Bone tissue response to irradiation and treatment model of mandibular irradiation injury. An experimental and clinical study. Acta Otolaryngol Suppl 428:1–54PubMed Aitasalo K (1986) Bone tissue response to irradiation and treatment model of mandibular irradiation injury. An experimental and clinical study. Acta Otolaryngol Suppl 428:1–54PubMed
25.
go back to reference Okunieff P, Wang X, Rubin P, Finkelstein JN, Constine LS, Ding I (1998) Radiation-induced changes in bone perfusion and angiogenesis. Int J Radiat Oncol Biol Phys 42:885–889PubMed Okunieff P, Wang X, Rubin P, Finkelstein JN, Constine LS, Ding I (1998) Radiation-induced changes in bone perfusion and angiogenesis. Int J Radiat Oncol Biol Phys 42:885–889PubMed
26.
go back to reference Neuman WF (1969) The milieu interieur of bone: Claude Bernard revisited. Fed Proc 28:1846–1850PubMed Neuman WF (1969) The milieu interieur of bone: Claude Bernard revisited. Fed Proc 28:1846–1850PubMed
27.
go back to reference McCarthy I (2006) The physiology of bone blood flow: a review. J Bone Joint Surg Am 88(Suppl 3):4–9PubMedCrossRef McCarthy I (2006) The physiology of bone blood flow: a review. J Bone Joint Surg Am 88(Suppl 3):4–9PubMedCrossRef
28.
go back to reference Briggs PJ, Moran CG, Wood MB (1998) Actions of endothelin-1, 2, and 3 in the microvasculature of bone. J Orthop Res 16:340–347PubMedCrossRef Briggs PJ, Moran CG, Wood MB (1998) Actions of endothelin-1, 2, and 3 in the microvasculature of bone. J Orthop Res 16:340–347PubMedCrossRef
29.
go back to reference Brinker MR, Lippton HL, Cook SD, Hyman AL (1990) Pharmacological regulation of the circulation of bone. J Bone Joint Surg Am 72:964–975PubMed Brinker MR, Lippton HL, Cook SD, Hyman AL (1990) Pharmacological regulation of the circulation of bone. J Bone Joint Surg Am 72:964–975PubMed
30.
go back to reference Dimitrievich GS, Fischer-Dzoga K, Griem ML (1984) Radiosensitivity of vascular tissue. I. Differential radiosensitivity of capillaries: a quantitative in vivo study. Radiat Res 99:511–535PubMedCrossRef Dimitrievich GS, Fischer-Dzoga K, Griem ML (1984) Radiosensitivity of vascular tissue. I. Differential radiosensitivity of capillaries: a quantitative in vivo study. Radiat Res 99:511–535PubMedCrossRef
31.
go back to reference O’Connor MM, Mayberg MR (2000) Effects of radiation on cerebral vasculature: a review. Neurosurgery 46:138–149; discussion 150–151PubMedCrossRef O’Connor MM, Mayberg MR (2000) Effects of radiation on cerebral vasculature: a review. Neurosurgery 46:138–149; discussion 150–151PubMedCrossRef
32.
go back to reference Fischer-Dzoga K, Dimitrievich GS, Griem ML (1984) Radiosensitivity of vascular tissue. II. Differential radiosensitivity of aortic cells in vitro. Radiat Res 99:536–546PubMedCrossRef Fischer-Dzoga K, Dimitrievich GS, Griem ML (1984) Radiosensitivity of vascular tissue. II. Differential radiosensitivity of aortic cells in vitro. Radiat Res 99:536–546PubMedCrossRef
33.
go back to reference Jacobsson M, Albrektsson T, Turesson I (1985) Dynamics of irradiation injury to bone tissue. A vital microscopic investigation. Acta Radiol Oncol 24:343–350PubMedCrossRef Jacobsson M, Albrektsson T, Turesson I (1985) Dynamics of irradiation injury to bone tissue. A vital microscopic investigation. Acta Radiol Oncol 24:343–350PubMedCrossRef
34.
go back to reference Jee W, Arnold JS (1960) Effect of internally deposited radioisotopes upon blood vessels of cortical bones. Proc Soc Exp Biol Med 105:351–356PubMed Jee W, Arnold JS (1960) Effect of internally deposited radioisotopes upon blood vessels of cortical bones. Proc Soc Exp Biol Med 105:351–356PubMed
35.
go back to reference Kenzora JE, Steele RE, Yosipovitch ZH, Glimcher MJ (1978) Experimental osteonecrosis of the femoral head in adult rabbits. Clin Orthop Relat Res:8–46 Kenzora JE, Steele RE, Yosipovitch ZH, Glimcher MJ (1978) Experimental osteonecrosis of the femoral head in adult rabbits. Clin Orthop Relat Res:8–46
36.
go back to reference King MA, Casarett GW, Weber DA (1979) A study of irradiated bone: I. histopathologic and physiologic changes. J Nucl Med 20:1142–1149PubMed King MA, Casarett GW, Weber DA (1979) A study of irradiated bone: I. histopathologic and physiologic changes. J Nucl Med 20:1142–1149PubMed
37.
go back to reference LaRue S, Wrigley RH, Powers BE (1987) A review of the effects of radiation-therapy on bone. Vet Radiol 28:17–22CrossRef LaRue S, Wrigley RH, Powers BE (1987) A review of the effects of radiation-therapy on bone. Vet Radiol 28:17–22CrossRef
38.
go back to reference Fajardo LF (1982) Pathology of radiation injury. Masson, New York Fajardo LF (1982) Pathology of radiation injury. Masson, New York
39.
go back to reference Narayan K, Cliff WJ (1982) Morphology of irradiated microvasculature: a combined in vivo and electron-microscopic study. Am J Pathol 106:47–62PubMed Narayan K, Cliff WJ (1982) Morphology of irradiated microvasculature: a combined in vivo and electron-microscopic study. Am J Pathol 106:47–62PubMed
40.
go back to reference Chen T, Burke KA, Zhan Y, Wang X, Shibata D, Zhao Y (2007) IL-12 facilitates both the recovery of endogenous hematopoiesis and the engraftment of stem cells after ionizing radiation. Exp Hematol 35:203–213PubMedCrossRef Chen T, Burke KA, Zhan Y, Wang X, Shibata D, Zhao Y (2007) IL-12 facilitates both the recovery of endogenous hematopoiesis and the engraftment of stem cells after ionizing radiation. Exp Hematol 35:203–213PubMedCrossRef
41.
go back to reference Desmons SO, Delfosse CJ, Rochon P, Buys B, Penel G, Mordon S (2008) Laser preconditioning of calvarial bone prior to an X-ray radiation injury: a preliminary in vivo study of the vascular response. Lasers Surg Med 40:28–37PubMedCrossRef Desmons SO, Delfosse CJ, Rochon P, Buys B, Penel G, Mordon S (2008) Laser preconditioning of calvarial bone prior to an X-ray radiation injury: a preliminary in vivo study of the vascular response. Lasers Surg Med 40:28–37PubMedCrossRef
Metadata
Title
A Preliminary Investigation into the Effects of X-Ray Radiation on Superficial Cranial Vascularization
Authors
Sophie Desmons
Michal Heger
Caroline Delfosse
Guillaume Falgayrac
Thierry Sarrazin
Claire Delattre
Sylvain Catros
Serge Mordon
Guillaume Penel
Publication date
01-05-2009
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 5/2009
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-009-9217-y

Other articles of this Issue 5/2009

Calcified Tissue International 5/2009 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.