Bone neoformation induced by low level laser and methylene blue suggest early ossification in rats Laser and methylene blue induces bone neoformation
Journal of Lasers in Medical Sciences,
Vol. 13 (2022),
10 January 2022
,
Page e48
Abstract
Introduction: Bone healing depends on inflammation control and tissue repair time. Low-level laser therapy (LLLT) has been investigated to accelerate this process. Methylene blue (MB), together with LLLT, has been investigated for its antioxidant and anti-inflammatory potential; however, the effects of photosensitizers (photodynamic therapy, PDT) are controversial. This study aimed to verify whether the combination of MB and LLLT changes the course of the consolidation of experimental bone defects. Methods: Sixteen Wistar rats underwent femoral bone defects. In the control group (n= 4), LLLT simulations were performed without MB. The MB group (n= 4) received MB and simulation of LLLT. The LLLT group (n= 4) was exposed to LLLT. The PDT + LLLT group (n= 4) received MB and LLLT. At the end of 7 or 14 days, the animals were euthanized, and samples were collected. Results: PDT and LLLT induced osteogenic formation with cellularity (after seven days) and union of bony edges (14 days). On the seventh day, LLLT combined with PDT induced an increase (P< 0.05) of 484% in the area of bone neoformation compared to the control. On the fourteenth day, LLLT combined with PDT or alone increased (P < 0.05) the area of bone neoformation by 214% and 240% respectively, compared to the control group. The PDT/LLLT combination was associated with increased radiopacity (P< 0.038). Conclusion: The combined use of MB with LLLT initiated during the transoperative phase may stimulate the bone repair process in rats
Keywords:
- Bone, Laser, Methylene blue, Ossification
How to Cite
Dulce de Oliveira, F. L., Cardozo Nagato, A. ., Monteiro Aarestrup, F., & Vieira Aarestrup, B. J. . (2022). Bone neoformation induced by low level laser and methylene blue suggest early ossification in rats: Laser and methylene blue induces bone neoformation. Journal of Lasers in Medical Sciences, 13, e48. Retrieved from https://journals.sbmu.ac.ir/jlms/article/view/36689
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17. Theodoro, L. H., Longo, M., Novaes, V. C. N., Miessi, D. M. J., Ferro-Alves, M. L., Ervolino, E., . . . Garcia, V. G. (2017). Low-level laser and antimicrobial photodynamic therapy on experimental periodontitis in rats submitted to chemotherapy by 5-fluorouracil. Support Care Cancer, 25(10), 3261-3271. doi:10.1007/s00520-017-3738-0
18. Dos Santos, A. F., Terra, L. F., Wailemann, R. A., Oliveira, T. C., Gomes, V. M., Mineiro, M. F., . . . Labriola, L. (2017). Methylene blue photodynamic therapy induces selective and massive cell death in human breast cancer cells. BMC Cancer, 17(1), 194. doi:10.1186/s12885-017-3179-7
19. Barathan, M., Mariappan, V., Shankar, E. M., Abdullah, B. J., Goh, K. L., & Vadivelu, J. (2013). Hypericin-photodynamic therapy leads to interleukin-6 secretion by HepG2 cells and their apoptosis via recruitment of BH3 interacting-domain death agonist and caspases. Cell Death Dis, 4, e697. doi:10.1038/cddis.2013.219
20. Lo, V. C., Akens, M. K., Wise-Milestone, L., Yee, A. J., Wilson, B. C., & Whyne, C. M. (2013). The benefits of photodynamic therapy on vertebral bone are maintained and enhanced by combination treatment with bisphosphonates and radiation therapy. J Orthop Res, 31(9), 1398-1405. doi:10.1002/jor.22373
21. Schirmer, R. H., Adler, H., Pickhardt, M., & Mandelkow, E. (2011). "Lest we forget you--methylene blue...". Neurobiol Aging, 32(12), 2325 e2327-2316. doi:10.1016/j.neurobiolaging.2010.12.012
22. Xiong, Z. M., O'Donovan, M., Sun, L., Choi, J. Y., Ren, M., & Cao, K. (2017). Anti-Aging Potentials of Methylene Blue for Human Skin Longevity. Sci Rep, 7(1), 2475. doi:10.1038/s41598-017-02419-3
23. Bozkurt, B., Dumlu, E. G., Tokac, M., Ozkardes, A. B., Ergin, M., Orhun, S., & Kilic, M. (2015). Methylene blue as an antioxidant agent in experimentally-induced injury in rat liver. Bratisl Lek Listy, 116(3), 157-161. doi:10.4149/bll_2015_032
24. Ahn, H., Kang, S. G., Yoon, S. I., Ko, H. J., Kim, P. H., Hong, E. J., . . . Lee, G. S. (2017). Methylene blue inhibits NLRP3, NLRC4, AIM2, and non-canonical inflammasome activation. Sci Rep, 7(1), 12409. doi:10.1038/s41598-017-12635-6
25. Atamna, H., & Kumar, R. (2010). Protective role of methylene blue in Alzheimer's disease via mitochondria and cytochrome c oxidase. J Alzheimers Dis, 20 Suppl 2, S439-452. doi:10.3233/JAD-2010-100414
26. Veeranarayanan, S., Mohamed, M. S., Poulose, A. C., Rinya, M., Sakamoto, Y., Maekawa, T., & Kumar, D. S. (2018). Photodynamic therapy at ultra-low NIR laser power and X-Ray imaging using Cu3BiS3 nanocrystals. Theranostics, 8(19), 5231-5245. doi:10.7150/thno.25286
27. Nascimento, S. B., Cardoso, C. A., Ribeiro, T. P., Almeida, J. D., Albertini, R., Munin, E., & Arisawa, E. A. (2010). Effect of low-level laser therapy and calcitonin on bone repair in castrated rats: a densitometric study. Photomed Laser Surg, 28(1), 45-49. doi:10.1089/pho.2008.2396
28. Ribeiro, D. A., Paiotti, A. P., & Medalha, C. C. (2012). Dual role of cyclooxygenase-2 during tissue repair induced by low level laser therapy: an intriguing issue. J Cosmet Laser Ther, 14(4), 184-188. doi:10.3109/14764172.2012.685479
29. Moskvin, S. V. (2017). Low-Level Laser Therapy in Russia: History, Science and Practice. J Lasers Med Sci, 8(2), 56-65. doi:10.15171/jlms.2017.11
30. Farivar, S., Malekshahabi, T., & Shiari, R. (2014). Biological effects of low level laser therapy. J Lasers Med Sci, 5(2), 58-62.
31. Lee, J. H., Chiang, M. H., Chen, P. H., Ho, M. L., Lee, H. E., & Wang, Y. H. (2018). Anti-inflammatory effects of low-level laser therapy on human periodontal ligament cells: in vitro study. Lasers Med Sci, 33(3), 469-477. doi:10.1007/s10103-017-2376-6
32. Song, J. W., Li, K., Liang, Z. W., Dai, C., Shen, X. F., Gong, Y. Z., . . . Wang, Z. (2017). Low-level laser facilitates alternatively activated macrophage/microglia polarization and promotes functional recovery after crush spinal cord injury in rats. Sci Rep, 7(1), 620. doi:10.1038/s41598-017-00553-6
33. Tatmatsu-Rocha, J. C., Ferraresi, C., Hamblin, M. R., Damasceno Maia, F., do Nascimento, N. R., Driusso, P., & Parizotto, N. A. (2016). Low-level laser therapy (904nm) can increase collagen and reduce oxidative and nitrosative stress in diabetic wounded mouse skin. J Photochem Photobiol B, 164, 96-102. doi:10.1016/j.jphotobiol.2016.09.017
34. Yamada, K. (1991). Biological effects of low power laser irradiation on clonal osteoblastic cells (MC3T3-E1). Nihon Seikeigeka Gakkai Zasshi, 65(9), 787-799.
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36. Tim, C. R., Bossini, P. S., Kido, H. W., Malavazi, I., von Zeska Kress, M. R., Carazzolle, M. F., . . . Parizotto, N. A. (2016). Low-level laser therapy induces an upregulation of collagen gene expression during the initial process of bone healing: a microarray analysis. J Biomed Opt, 21(8), 88001. doi:10.1117/1.JBO.21.8.088001
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38. Jiang, C., Yang, W., Wang, C., Qin, W., Ming, J., Zhang, M., . . . Jiao, T. (2019). Methylene Blue-Mediated Photodynamic Therapy Induces Macrophage Apoptosis via ROS and Reduces Bone Resorption in Periodontitis. Oxid Med Cell Longev, 2019, 1529520. doi:10.1155/2019/1529520
39. Jawad, M. M., Husein, A., Azlina, A., Alam, M. K., Hassan, R., & Shaari, R. (2013). Effect of 940 nm low-level laser therapy on osteogenesis in vitro. J Biomed Opt, 18(12), 128001. doi:10.1117/1.JBO.18.12.128001
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2. Buza, J. A., 3rd, & Einhorn, T. (2016). Bone healing in 2016. Clin Cases Miner Bone Metab, 13(2), 101-105. doi:10.11138/ccmbm/2016.13.2.101
3. Whitehair, J. G., & Vasseur, P. B. (1992). Fractures of the femur. Vet Clin North Am Small Anim Pract, 22(1), 149-159. doi:10.1016/s0195-5616(92)50010-9
4. Souza, E. Q. M., Costa Klaus, A. E., Esposito Santos, B. F., Carvalho da Costa, M., Ervolino, E., Coelho de Lima, D., & Fernandes, L. A. (2020). Evaluations of hydroxyapatite and bioactive glass in the repair of critical size bone defects in rat calvaria. J Oral Biol Craniofac Res, 10(4), 422-429. doi:10.1016/j.jobcr.2020.07.014
5. Lewis, G. (1994). Effect of methylene blue on the fracture toughness of acrylic bone cement. Biomaterials, 15(12), 1024-1028. doi:10.1016/0142-9612(94)90085-x
6. Farkash, U., Bain, O., Gam, A., Nyska, M., & Sagiv, P. (2015). Low-intensity pulsed ultrasound for treating delayed union scaphoid fractures: case series. J Orthop Surg Res, 10, 72. doi:10.1186/s13018-015-0221-9
7. Leighton, R., Watson, J. T., Giannoudis, P., Papakostidis, C., Harrison, A., & Steen, R. G. (2017). Healing of fracture nonunions treated with low-intensity pulsed ultrasound (LIPUS): A systematic review and meta-analysis. Injury, 48(7), 1339-1347. doi:10.1016/j.injury.2017.05.016
8. Kieves, N. R., MacKay, C. S., Adducci, K., Rao, S., Goh, C., Palmer, R. H., & Duerr, F. M. (2015). High energy focused shock wave therapy accelerates bone healing. A blinded, prospective, randomized canine clinical trial. Vet Comp Orthop Traumatol, 28(6), 425-432. doi:10.3415/VCOT-15-05-0084
9. Auregan, J. C., Coyle, R. M., Danoff, J. R., Burky, R. E., Akelina, Y., & Rosenwasser, M. P. (2013). The rat model of femur fracture for bone and mineral research: An improved description of expected comminution, quantity of soft callus and incidence of complications. Bone Joint Res, 2(8), 149-154. doi:10.1302/2046-3758.28.2000171
10. Mostafavinia, A., Masteri Farahani, R., Abbasian, M., Vasheghani Farahani, M., Fridoni, M., Zandpazandi, S., . . . Bayat, M. (2015). Effect of Pulsed Wave Low-Level Laser Therapy on Tibial Complete Osteotomy Model of Fracture Healing With an Intramedullary Fixation. Iran Red Crescent Med J, 17(12), e32076. doi:10.5812/ircmj.32076
11. Bossini, P. S., Renno, A. C., Ribeiro, D. A., Fangel, R., Ribeiro, A. C., Lahoz Mde, A., & Parizotto, N. A. (2012). Low level laser therapy (830nm) improves bone repair in osteoporotic rats: similar outcomes at two different dosages. Exp Gerontol, 47(2), 136-142. doi:10.1016/j.exger.2011.11.005
12. Hoerth, R. M., Kerschnitzki, M., Aido, M., Schmidt, I., Burghammer, M., Duda, G. N., . . . Wagermaier, W. (2018). Correlations between nanostructure and micromechanical properties of healing bone. J Mech Behav Biomed Mater, 77, 258-266. doi:10.1016/j.jmbbm.2017.08.022
13. Tim, C. R., Bossini, P. S., Kido, H. W., Malavazi, I., von Zeska Kress, M. R., Carazzolle, M. F., . . . Renno, A. C. (2015). Effects of low-level laser therapy on the expression of osteogenic genes during the initial stages of bone healing in rats: a microarray analysis. Lasers Med Sci, 30(9), 2325-2333. doi:10.1007/s10103-015-1807-5
14. de Oliveira, L. S. S., de Araujo, A. A., de Araujo Junior, R. F., Barboza, C. A. G., Borges, B. C. D., & da Silva, J. S. P. (2017). Low-level laser therapy (780 nm) combined with collagen sponge scaffold promotes repair of rat cranial critical-size defects and increases TGF-beta, FGF-2, OPG/RANK and osteocalcin expression. Int J Exp Pathol, 98(2), 75-85. doi:10.1111/iep.12226
15. Rosa, L. P., da Silva, F. C., Nader, S. A., Meira, G. A., & Viana, M. S. (2015). Antimicrobial photodynamic inactivation of Staphylococcus aureus biofilms in bone specimens using methylene blue, toluidine blue ortho and malachite green: An in vitro study. Arch Oral Biol, 60(5), 675-680. doi:10.1016/j.archoralbio.2015.02.010
16. Rosa, L. P., da Silva, F. C., Vieira, R. L., Tanajura, B. R., da Silva Gusmao, A. G., de Oliveira, J. M., . . . Bagnato, V. S. (2017). Application of photodynamic therapy, laser therapy, and a cellulose membrane for calcaneal pressure ulcer treatment in a diabetic patient: A case report. Photodiagnosis Photodyn Ther, 19, 235-238. doi:10.1016/j.pdpdt.2017.06.011
17. Theodoro, L. H., Longo, M., Novaes, V. C. N., Miessi, D. M. J., Ferro-Alves, M. L., Ervolino, E., . . . Garcia, V. G. (2017). Low-level laser and antimicrobial photodynamic therapy on experimental periodontitis in rats submitted to chemotherapy by 5-fluorouracil. Support Care Cancer, 25(10), 3261-3271. doi:10.1007/s00520-017-3738-0
18. Dos Santos, A. F., Terra, L. F., Wailemann, R. A., Oliveira, T. C., Gomes, V. M., Mineiro, M. F., . . . Labriola, L. (2017). Methylene blue photodynamic therapy induces selective and massive cell death in human breast cancer cells. BMC Cancer, 17(1), 194. doi:10.1186/s12885-017-3179-7
19. Barathan, M., Mariappan, V., Shankar, E. M., Abdullah, B. J., Goh, K. L., & Vadivelu, J. (2013). Hypericin-photodynamic therapy leads to interleukin-6 secretion by HepG2 cells and their apoptosis via recruitment of BH3 interacting-domain death agonist and caspases. Cell Death Dis, 4, e697. doi:10.1038/cddis.2013.219
20. Lo, V. C., Akens, M. K., Wise-Milestone, L., Yee, A. J., Wilson, B. C., & Whyne, C. M. (2013). The benefits of photodynamic therapy on vertebral bone are maintained and enhanced by combination treatment with bisphosphonates and radiation therapy. J Orthop Res, 31(9), 1398-1405. doi:10.1002/jor.22373
21. Schirmer, R. H., Adler, H., Pickhardt, M., & Mandelkow, E. (2011). "Lest we forget you--methylene blue...". Neurobiol Aging, 32(12), 2325 e2327-2316. doi:10.1016/j.neurobiolaging.2010.12.012
22. Xiong, Z. M., O'Donovan, M., Sun, L., Choi, J. Y., Ren, M., & Cao, K. (2017). Anti-Aging Potentials of Methylene Blue for Human Skin Longevity. Sci Rep, 7(1), 2475. doi:10.1038/s41598-017-02419-3
23. Bozkurt, B., Dumlu, E. G., Tokac, M., Ozkardes, A. B., Ergin, M., Orhun, S., & Kilic, M. (2015). Methylene blue as an antioxidant agent in experimentally-induced injury in rat liver. Bratisl Lek Listy, 116(3), 157-161. doi:10.4149/bll_2015_032
24. Ahn, H., Kang, S. G., Yoon, S. I., Ko, H. J., Kim, P. H., Hong, E. J., . . . Lee, G. S. (2017). Methylene blue inhibits NLRP3, NLRC4, AIM2, and non-canonical inflammasome activation. Sci Rep, 7(1), 12409. doi:10.1038/s41598-017-12635-6
25. Atamna, H., & Kumar, R. (2010). Protective role of methylene blue in Alzheimer's disease via mitochondria and cytochrome c oxidase. J Alzheimers Dis, 20 Suppl 2, S439-452. doi:10.3233/JAD-2010-100414
26. Veeranarayanan, S., Mohamed, M. S., Poulose, A. C., Rinya, M., Sakamoto, Y., Maekawa, T., & Kumar, D. S. (2018). Photodynamic therapy at ultra-low NIR laser power and X-Ray imaging using Cu3BiS3 nanocrystals. Theranostics, 8(19), 5231-5245. doi:10.7150/thno.25286
27. Nascimento, S. B., Cardoso, C. A., Ribeiro, T. P., Almeida, J. D., Albertini, R., Munin, E., & Arisawa, E. A. (2010). Effect of low-level laser therapy and calcitonin on bone repair in castrated rats: a densitometric study. Photomed Laser Surg, 28(1), 45-49. doi:10.1089/pho.2008.2396
28. Ribeiro, D. A., Paiotti, A. P., & Medalha, C. C. (2012). Dual role of cyclooxygenase-2 during tissue repair induced by low level laser therapy: an intriguing issue. J Cosmet Laser Ther, 14(4), 184-188. doi:10.3109/14764172.2012.685479
29. Moskvin, S. V. (2017). Low-Level Laser Therapy in Russia: History, Science and Practice. J Lasers Med Sci, 8(2), 56-65. doi:10.15171/jlms.2017.11
30. Farivar, S., Malekshahabi, T., & Shiari, R. (2014). Biological effects of low level laser therapy. J Lasers Med Sci, 5(2), 58-62.
31. Lee, J. H., Chiang, M. H., Chen, P. H., Ho, M. L., Lee, H. E., & Wang, Y. H. (2018). Anti-inflammatory effects of low-level laser therapy on human periodontal ligament cells: in vitro study. Lasers Med Sci, 33(3), 469-477. doi:10.1007/s10103-017-2376-6
32. Song, J. W., Li, K., Liang, Z. W., Dai, C., Shen, X. F., Gong, Y. Z., . . . Wang, Z. (2017). Low-level laser facilitates alternatively activated macrophage/microglia polarization and promotes functional recovery after crush spinal cord injury in rats. Sci Rep, 7(1), 620. doi:10.1038/s41598-017-00553-6
33. Tatmatsu-Rocha, J. C., Ferraresi, C., Hamblin, M. R., Damasceno Maia, F., do Nascimento, N. R., Driusso, P., & Parizotto, N. A. (2016). Low-level laser therapy (904nm) can increase collagen and reduce oxidative and nitrosative stress in diabetic wounded mouse skin. J Photochem Photobiol B, 164, 96-102. doi:10.1016/j.jphotobiol.2016.09.017
34. Yamada, K. (1991). Biological effects of low power laser irradiation on clonal osteoblastic cells (MC3T3-E1). Nihon Seikeigeka Gakkai Zasshi, 65(9), 787-799.
35. Briteno-Vazquez, M., Santillan-Diaz, G., Gonzalez-Perez, M., Gallego-Izquierdo, T., Pecos-Martin, D., Plaza-Manzano, G., & Romero-Franco, N. (2015). Low power laser stimulation of the bone consolidation in tibial fractures of rats: a radiologic and histopathological analysis. Lasers Med Sci, 30(1), 333-338. doi:10.1007/s10103-014-1673-6
36. Tim, C. R., Bossini, P. S., Kido, H. W., Malavazi, I., von Zeska Kress, M. R., Carazzolle, M. F., . . . Parizotto, N. A. (2016). Low-level laser therapy induces an upregulation of collagen gene expression during the initial process of bone healing: a microarray analysis. J Biomed Opt, 21(8), 88001. doi:10.1117/1.JBO.21.8.088001
37. Alves, A. M. M., de Miranda Fortaleza, L. M., Filho, A., Ferreira, D. C. L., da Costa, C. L. S., Viana, V. G. F., . . . Soares, L. E. S. (2018). Evaluation of bone repair after application of a norbixin membrane scaffold with and without laser photobiomodulation (lambda 780 nm). Lasers Med Sci, 33(7), 1493-1504. doi:10.1007/s10103-018-2506-9
38. Jiang, C., Yang, W., Wang, C., Qin, W., Ming, J., Zhang, M., . . . Jiao, T. (2019). Methylene Blue-Mediated Photodynamic Therapy Induces Macrophage Apoptosis via ROS and Reduces Bone Resorption in Periodontitis. Oxid Med Cell Longev, 2019, 1529520. doi:10.1155/2019/1529520
39. Jawad, M. M., Husein, A., Azlina, A., Alam, M. K., Hassan, R., & Shaari, R. (2013). Effect of 940 nm low-level laser therapy on osteogenesis in vitro. J Biomed Opt, 18(12), 128001. doi:10.1117/1.JBO.18.12.128001
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