Hyperbaric Oxygen Therapy Influence on Irradiated Bone Repair and Collagen Orientation

Authors

DOI:

https://doi.org/10.33448/rsd-v9i11.9948

Keywords:

Ionizing radiation; Hyperbaric oxygenation; Osteogenesis; Collagen.

Abstract

The present study aimed to evaluate the effects of HBO on bone repair after ionizing radiation, by using histomorphometry, computed tomography and polarization microscopy. Twenty male Wistar rats were used. One radiation dose (30 Gy) was administered on the left leg in all animals, and after 30 days, bone defects were created in both femurs. Then, 10 animals received daily HBO sessions (2.5 ATA for 90 minutes), and all animals were euthanized 5 or 7 days after surgery. The femurs were separated into 4 groups (n=5) for each euthanasia time interval: Control (Right femur: Non-irradiated and Non-HBO), RXT (Left femur: Irradiated and Non-HBO), HBO (Right femur: Non-irradiated with HBO), RXT+HBO (Left femur: Irradiated with HBO). The bone cortical and defects were evaluated. Data were analyzed using the Kolmogorov-Smirnov tests, unpaired t-test, and ANOVA with Bonferroni correction. Higher HU values and new bone formation were observed in Control and HBO groups, with improved repair. Group HBO showed predominant Yellow/Orange/Red birefringence of collagen in the defect area. HBO improved bone repair in physiological conditions, with increased blood vessels and bone formation. However, it was not efficient in improving repair and collagen orientation in bone after high doses of ionizing radiation.

References

Al Hadi, H., Smerdon, G. R., Fox, S. W. (2015) Hyperbaric oxygen therapy accelerates osteoblast differentiation and promotes bone formation. J Dent. 3(3), 382-8. doi: 10.1016/j.jdent.2014.10.006.

An, H., Lee, J. T., Oh, S. E., Park, K. M., Hu, K. S., Kim, S., Chung, M. K. (2019) Adjunctive hyperbaric oxygen therapy for irradiated rat calvarial defects. J Periodontal Implant Sci. 49(1), 2–13. doi: 10.5051/jpis.2019.49.1.2

Bach-Gansmo, F. L., Irvine, S. C., Brüel, A., Thomsen, J. S., Birkedal, H. (2013) Calcified cartilage islands in rat cortical bone. Calcif Tissue Int. 92(4), 330-8. doi: 10.1007/s00223-012-9682-6.

Bai, J., Wang, Y., Wang, J., Zhai, J., He, F., Zhu, G. (2020) Irradiation-induced senescence of bone marrow mesenchymal stem cells aggravates osteogenic differentiation dysfunction via paracrine signaling. Am J Physiol Cell Physiol. 318(5), C1005-C1017. doi: 10.1152/ajpcell.00520.2019.

Batista, J. D., Zanetta-Barbosa, D., Cardoso, S. V., Dechichi, P., Rocha, F. S., Pagnoncelli, R. M. (2014) Effect of low-level laser therapy on repair of the bone compromised by radiotherapy. Lasers Med Sci. 29(6), 1913-8. doi: 10.1007/s10103-014-1602-8.

Bromage, T. G., Goldman, H. M., McFarlin, S. C., Warshaw, J., Boyde, A., Riggs, C. M. (2003) Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat Rec B New Anat. 274(1), 157-68. doi: 10.1002/ar.b.10031.

Choudhury, R. (2018) Hypoxia and hyperbaric oxygen therapy: A review. International Int J Gen Med. 11, 431–442. doi: 10.2147/IJGM.S172460.

Chouinard, A. F., Giasson, L., Fortin, M. (2016) Hyperbaric Oxygen Therapy for Head and Neck Irradiated Patients with Special Attention to Oral and Maxillofacial Treatments. J Can Dent Assoc. 82, g24. Retrieved from https://jcda.ca/g24.

Dieleman, F. J., Phan, T. T. T., van den Hoogen, F. J. A., Kaanders, J. H. A. M., Merkx, M. A. W. (2017) The efficacy of hyperbaric oxygen therapy related to the clinical stage of osteoradionecrosis of the mandible. Int J Oral Maxillofac Surg. 46(4), 428-433. doi: 10.1016/j.ijom.2016.12.004.

Gajendrareddy, P. K., Junges, R., Cygan, G., Zhao, Y., Marucha, P. T., Engeland, C. G. (2017) Increased oxygen exposure alters collagen expression and tissue architecture during ligature-induced periodontitis. J Periodontal Res. 52(3), 644–649. doi: 10.1111/jre.12408.

Gardin, C., Bosco, G., Ferroni, L., Quartesan, S., Rizzato, A., Tatullo, M., Zavan, B. (2020) Hyperbaric Oxygen Therapy Improves the Osteogenic and Vasculogenic Properties of Mesenchymal Stem Cells in the Presence of Inflammation In Vitro. Int J Mol Sci. 20;21(4), 1452. doi: 10.3390/ijms21041452.

Georgiadis, M., Müller, R., Schneider, P. (2016) Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils. J R Soc Interface. 13(119), 20160088. doi: 10.1098/rsif.2016.0088.

Grassmann, J. P., Schneppendahl, J., Hakimi, A. R., Herten, M., Betsch, M., Lögters, T. T., Thelen, S., Sager, M., Wild, M., Windolf, J., Jungbluth, P., Hakimi, M. (2015) Hyperbaric oxygen therapy improves angiogenesis and bone formation in critical sized diaphyseal defects. J Orthop Res. 33(4), 513-20. doi: 10.1002/jor.22805.

Hopewell, J. W. (2003) Radiation-therapy effects on bone density. Med Pediatr Oncol. 41(3), 208-11. doi: 10.1002/mpo.10338.

Jereczek-Fossa, B. A., Orecchia, R. (2002) Radiotherapy-induced mandibular bone complications. Cancer Treat Rev. 28(1), 65-74. doi: 10.1053/ctrv.2002.0254.

Kawada, S., Wada, E., Matsuda, R., Ishii, N. (2013) Hyperbaric Hyperoxia Accelerates Fracture Healing in Mice. Plos ONE 8(8), e72603.

Lerouxel, E., Moreau, A., Bouler, J. M., Giumelli, B., Daculsi, G., Weiss, P., Malard, O. (2009) Effects of high doses of ionising radiation on bone in rats: a new model for evaluation of bone engineering. Br J Oral Maxillofac Surg. 47(8), 602-607. doi: 10.1371/journal.pone.0072603

Limirio, P. H. J. O., da Rocha Junior, H. A., Morais, R. B., Hiraki, K. R. N., Balbi, A. P. C., Soares, P. B. F., Dechichi, P. (2018) Influence of hyperbaric oxygen on biomechanics and structural bone matrix in type 1 diabetes mellitus rats. PLoS One. 13(2), e0191694. doi: 10.1371/journal.pone.0191694

Limirio, P. H. J. O., Soares, P. B. F., Emi, E. T. P., Lopes, C. C. A., Rocha, F. S., Batista, J. D., Rabelo, G. D., Dechichi, P. (2019) Ionizing radiation and bone quality: time-dependent effects. Radiat Oncol. 14(1), 15. doi: 10.1186/s13014-019-1219-y.

Lin, S. S., Ueng, S. W., Niu, C. C., Yuan, L. J., Yang, C. Y., Chen, W. J., Lee, M. S., Chen, J. K. (2014) Effects of hyperbaric oxygen on the osteogenic differentiation of mesenchymal stem cells. BMC Musculoskelet Disord. 25;15, 56. doi: 10.1186/1471-2474-15-56.

Mendes, E. M., Irie, M. S., Rabelo, G. D., Borges, J. S., Dechichi, P., Diniz, R. S., Soares, P. B. F. (2019) Effects of ionizing radiation on woven bone: influence on the osteocyte lacunar network, collagen maturation, and microarchitecture. Clin Oral Investig. 24, 2763–2771. doi: 10.1007/s00784-019-03138-x.

Molteni, R. (2013) Prospects and challenges of rendering tissue density in Hounsfield units for cone beam computed tomography. Oral Surg Oral Med Oral Pathol Oral Radiol. 116(1), 105-19. doi: 10.1016/j.oooo.2013.04.013.

Ohrnell, L. O., Branemark, R., Nyman, J., Nilsson, P., Thomsen, P. (1997) Effects of irradiation on the biomechanics of osseointegration. An experimental in vivo study in rats. Scandinavian journal of plastic and reconstructive surgery and hand surgery. 31(4), 281-93. doi: 10.3109/02844319709008974.

Park, K. M., Kim, C., Park, W., Park, Y. B., Chung, M. K., Kim, S. (2019) Bone Regeneration Effect of Hyperbaric Oxygen Therapy Duration on Calvarial Defects in Irradiated Rats. Biomed Res Int. 2019; 9051713. doi: 10.1155/2019/9051713.

Pauwels, R, Jacobs, R., Singer, S. R. Mupparapu M. (2015) CBCT-based bone quality assessment: are Hounsfield units applicable? Dentomaxillofac Radiol. 44(1):20140238. doi: 10.1259/dmfr.20140238.

Rabelo, G. D., Beletti, M. E., Dechichi, P. (2010) Histological analysis of the alterations on cortical bone channels network after radiotherapy: A rabbit study. Microsc Res Tech. 73(11), 1015-8. doi: 10.1002/jemt.20826.

Raggio, B. S., Winters, R. (2018) Modern management of osteoradionecrosis. Curr Opin Otolaryngol Head Neck Surg. 26(4), 254-259. doi: 10.1097/MOO.0000000000000459.

Rocha, F. S., Dias, P. C., Limirio, P. H., Lara, V. C., Batista, J. D., Dechichi, P. (2017) High doses of ionizing radiation on bone repair: is there effect outside the irradiated site? Injury. 48(3), 671-673. doi: 10.1016/j.injury.2016.11.033.

Rocha, F. S., Gomes Moura, C. C., Rocha Rodrigues, D. B., Zanetta-Barbosa, D., Nakamura Hiraki, K. R., Dechichi, P. (2015) Influence of hyperbaric oxygen on the initial stages of bone healing. Oral Surg Oral Med Oral Pathol Oral Radiol. 120(5), 581-587. doi: 10.1016/j.oooo.2015.06.039.

Rocha, F. S., Limirio, P. H., Zanetta-Barbosa, D., Batista, J. D., Dechichi, P. (2016) The effects of ionizing radiation on the growth plate in rat tibiae. Microsc Res Tech. 79(12), 1147-1151. doi: 10.1002/jemt.22769.

Sen, C. K. (2009) Wound healing essentials: let there be oxygen. Wound Repair Regen. 17(1), 1–18. doi: 10.1111/j.1524-475X.2008.00436.x.

Shipov, A., Zaslansky, P., Riesemeier, H., Segev, G., Atkins, A., Shahar, R. (2013) Unremodeled endochondral bone is a major architectural component of the cortical bone of the rat (Rattus norvegicus). J Struct Biol. 183(2), 132-40. doi: 10.1016/j.jsb.2013.04.010

Sirin, Y., Olgac, V., Dogru-Abbasoglu, S., Tapul, L., Aktas, S., Soley, S. (2011) The influence of hyperbaric oxygen treatment on the healing of experimental defects filled with different bone graft substitutes. Int J Med Sci. 8(2), 114–125. doi: 10.7150/ijms.8.114.

Soares, P. B. F., Soares, C. J., Limirio, P. H. J. O., de Jesus, R. N. R., Dechichi, P., Spin-Neto, R., Zanetta-Barbosa, D. (2019) Effect of ionizing radiation after-therapy interval on bone: histomorphometric and biomechanical characteristics. Clin Oral Investig. 23(6), 2785-2793. doi: 10.1007/s00784-018-2724-3.

Sroussi, H. Y., Epstein, J. B., Bensadoun, R. J., Saunders, D. P., Lalla, R. V., Migliorati, C. A., Heaivilin, N., Zumsteg, Z. A. (2017) Common oral complications of head and neck cancer radiation therapy: mucositis, infections, saliva change, fibrosis, sensory dysfunctions, dental caries, periodontal disease, and osteoradionecrosis. Cancer Med. 6(12), 2918-2931. doi: 10.1002/cam4.1221.

Stone, H. B., Coleman, C. N., Anscher, M. S., McBride, W. H. (2003) Effects of radiation on normal tissue: consequences and mechanisms. Lancet Oncol. 4(9), 529-36. doi: 10.1016/s1470-2045(03)01191-4.

Thom, S. R. (2011) Hyperbaric oxygen: its mechanisms and efficacy. Plast Reconstr Surg 127(Suppl 1), 131S–141S. doi: 10.1097/PRS.0b013e3181fbe2bf.

Thom, S. R. (2009) Oxidative stress is fundamental to hyperbaric oxygen therapy. J Appl Physiol. 106(3), 988-95. doi: 10.1152/japplphysiol.91004.2008.

Vieira, A. E., Repeke, C. E., Ferreira Junior, S. B., Colavite, P. M., Biguetti, C. C., Oliveira, R. C., Assis, G. F., Taga, R., Trombone, A. P., Garlet, G. P. (2015) Intramembranous bone healing process subsequent to tooth extraction in mice: micro-computed tomography, histomorphometric and molecular characterization. PLoS One. 10(5), e0128021. doi: 10.1371/journal.pone.0128021.

Wang, I. C., Wen-Neng Ueng, S., Yuan, L. J., Tu, Y. K., Lin, S. S., Wang, C. R., Tai, C. L., Wang, K. C. (2005) Early administration of hyperbaric oxygen therapy in distraction osteogenesis: a quantitative study in New Zealand rabbits. The Journal of Trauma. 58(6), 1230-5. doi: 10.1097/01.ta.0000169872.38849.b0.

Downloads

Published

20/11/2020

How to Cite

Rocha, F. S., Rezende , L. G. P. de ., Reis , D. C. S. dos ., Rabelo, G. D., Filice, L. de S. C. . ., Zanetta-Barbosa, D., & Dechichi, P. (2020). Hyperbaric Oxygen Therapy Influence on Irradiated Bone Repair and Collagen Orientation. Research, Society and Development, 9(11), e4339119948. https://doi.org/10.33448/rsd-v9i11.9948

Issue

Section

Health Sciences