Limited field radiation therapy results in decreased bone fracture toughness in a murine model

Fragility fractures are a well-known complication following oncologic radiotherapy, and it is suspected that radiation-induced embrittlement of bone within the treatment field may contribute to fracture risk. To explore this phenomenon, a mouse model (BALB/cJ) of fractionated, limited field, bilater...

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Published inPloS one Vol. 13; no. 10; p. e0204928
Main Authors Bartlow, Christopher M, Mann, Kenneth A, Damron, Timothy A, Oest, Megan E
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 03.10.2018
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Abstract Fragility fractures are a well-known complication following oncologic radiotherapy, and it is suspected that radiation-induced embrittlement of bone within the treatment field may contribute to fracture risk. To explore this phenomenon, a mouse model (BALB/cJ) of fractionated, limited field, bilateral hindlimb irradiation (4x5 Gy) was used. The effects of radiation on femoral (cortical) bone fracture toughness, morphology, and biochemistry-including advanced glycation end products (AGEs)-were quantified and compared to Sham group samples prior to irradiation and at 0, 4, 8, and 12 weeks post-irradiation. Additionally, alterations to bone fracture toughness mediated directly by radiation (independent of cellular mechanisms) were determined using devitalized mouse cadaver femurs. Finally, the contribution of AGEs to reduced fracture toughness was examined by artificially ribosylating mouse femurs ex vivo. These data demonstrate that in vivo irradiation results in an immediate (-42% at 0 weeks, p < 0.001) and sustained (-28% at 12 weeks, p < 0.001) decrease in fracture toughness with small changes in morphology (-5% in cortical area at 12 weeks), and minimal changes in bone composition (tissue mineral density, mineral:matrix ratio, and AGE content). Irradiation of devitalized femurs also reduced fracture toughness (-29%, p < 0.001), but to a lesser extent than was seen in vivo. While artificial ribosylation decreased fracture toughness with time, the extent of glycation needed to induce this effect exceeded the AGE accumulation that occurred in vivo. Overall, hindlimb irradiation induced a substantial and sustained decrease in bone fracture toughness. Approximately half of this decrease in fracture toughness is due to direct radiation damage, independent of cellular remodeling. Collagen glycation in vivo was not substantially altered, suggesting other matrix changes may contribute to post-radiotherapy bone embrittlement.
AbstractList Fragility fractures are a well-known complication following oncologic radiotherapy, and it is suspected that radiation-induced embrittlement of bone within the treatment field may contribute to fracture risk. To explore this phenomenon, a mouse model (BALB/cJ) of fractionated, limited field, bilateral hindlimb irradiation (4x5 Gy) was used. The effects of radiation on femoral (cortical) bone fracture toughness, morphology, and biochemistry—including advanced glycation end products (AGEs)—were quantified and compared to Sham group samples prior to irradiation and at 0, 4, 8, and 12 weeks post-irradiation. Additionally, alterations to bone fracture toughness mediated directly by radiation (independent of cellular mechanisms) were determined using devitalized mouse cadaver femurs. Finally, the contribution of AGEs to reduced fracture toughness was examined by artificially ribosylating mouse femurs ex vivo . These data demonstrate that in vivo irradiation results in an immediate (-42% at 0 weeks, p < 0.001) and sustained (-28% at 12 weeks, p < 0.001) decrease in fracture toughness with small changes in morphology (-5% in cortical area at 12 weeks), and minimal changes in bone composition (tissue mineral density, mineral:matrix ratio, and AGE content). Irradiation of devitalized femurs also reduced fracture toughness (-29%, p < 0.001), but to a lesser extent than was seen in vivo . While artificial ribosylation decreased fracture toughness with time, the extent of glycation needed to induce this effect exceeded the AGE accumulation that occurred in vivo . Overall, hindlimb irradiation induced a substantial and sustained decrease in bone fracture toughness. Approximately half of this decrease in fracture toughness is due to direct radiation damage, independent of cellular remodeling. Collagen glycation in vivo was not substantially altered, suggesting other matrix changes may contribute to post-radiotherapy bone embrittlement.
Fragility fractures are a well-known complication following oncologic radiotherapy, and it is suspected that radiation-induced embrittlement of bone within the treatment field may contribute to fracture risk. To explore this phenomenon, a mouse model (BALB/cJ) of fractionated, limited field, bilateral hindlimb irradiation (4x5 Gy) was used. The effects of radiation on femoral (cortical) bone fracture toughness, morphology, and biochemistry—including advanced glycation end products (AGEs)—were quantified and compared to Sham group samples prior to irradiation and at 0, 4, 8, and 12 weeks post-irradiation. Additionally, alterations to bone fracture toughness mediated directly by radiation (independent of cellular mechanisms) were determined using devitalized mouse cadaver femurs. Finally, the contribution of AGEs to reduced fracture toughness was examined by artificially ribosylating mouse femurs ex vivo. These data demonstrate that in vivo irradiation results in an immediate (-42% at 0 weeks, p < 0.001) and sustained (-28% at 12 weeks, p < 0.001) decrease in fracture toughness with small changes in morphology (-5% in cortical area at 12 weeks), and minimal changes in bone composition (tissue mineral density, mineral:matrix ratio, and AGE content). Irradiation of devitalized femurs also reduced fracture toughness (-29%, p < 0.001), but to a lesser extent than was seen in vivo. While artificial ribosylation decreased fracture toughness with time, the extent of glycation needed to induce this effect exceeded the AGE accumulation that occurred in vivo. Overall, hindlimb irradiation induced a substantial and sustained decrease in bone fracture toughness. Approximately half of this decrease in fracture toughness is due to direct radiation damage, independent of cellular remodeling. Collagen glycation in vivo was not substantially altered, suggesting other matrix changes may contribute to post-radiotherapy bone embrittlement.
Audience Academic
Author Damron, Timothy A
Mann, Kenneth A
Oest, Megan E
Bartlow, Christopher M
AuthorAffiliation Department of Orthopedic Surgery, State University of New York Upstate Medical University, Syracuse, New York, United States of America
University of Notre Dame, UNITED STATES
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Snippet Fragility fractures are a well-known complication following oncologic radiotherapy, and it is suspected that radiation-induced embrittlement of bone within the...
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SubjectTerms Advanced glycosylation end products
Age
Animal models
Animals
Biochemistry
Biology and Life Sciences
Biomechanical Phenomena
Biomechanics
Bone composition
Bone density
Bone mineral density
Bone surgery
Bones
Collagen
Cortical bone
Crack propagation
Disease Models, Animal
Embrittlement
Experiments
Female
Femoral Fractures - etiology
Femoral Fractures - metabolism
Femoral Fractures - physiopathology
Femur
Fracture toughness
Fractures
Fragility
Glycation End Products, Advanced - metabolism
Glycosylation
Health aspects
Irradiation
Joint surgery
Knee
Laboratory animals
Mechanical properties
Medicine and Health Sciences
Mice
Morphology
Murinae
Orthopedics
Post-irradiation
Radiation
Radiation damage
Radiation effects
Radiation therapy
Radiotherapy
Radiotherapy - adverse effects
Research and Analysis Methods
Ribosylation
Studies
X-Ray Microtomography
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Title Limited field radiation therapy results in decreased bone fracture toughness in a murine model
URI https://www.ncbi.nlm.nih.gov/pubmed/30281657
https://www.proquest.com/docview/2117789406
https://pubmed.ncbi.nlm.nih.gov/PMC6169919
https://doaj.org/article/a77f07656f434ae2a6c7c9d808706191
http://dx.doi.org/10.1371/journal.pone.0204928
Volume 13
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