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Marine collagen scaffolds and photobiomodulation on bone healing process in a model of calvaria defects

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Abstract

Introduction

Collagen from marine esponges has been used as a promising material for tissue engineering proposals. Similarly, photobiomodulation (PBM) is able of modulating inflammatory processes after an injury, accelerating soft and hard tissue healing and stimulating neoangiogenesis. However, the effects of the associated treatments on bone tissue healing have not been studied yet. In this context, the present study aimed to evaluate the biological temporal modifications (using two experimental periods) of marine sponge collagen or sponging (SPG) based scaffold and PBM on newly formed bone using a calvaria bone defect model.

Material and Methods

Wistar rats were distributed into two groups: SPG or SPG/PBM and euthanized into two different experimental periods (15 and 45 days post-surgery). A cranial critical bone defect was used to evaluate the effects of the treatments. Histology, histomorfometry and immunohistological analysis were performed.

Results

Histological findings demonstrated that SPG/PBM-treated animals, 45 days post-surgery, demonstrated a higher amount of connective and newly formed bone tissue at the region of the defect compared to CG. Notwithstanding, no difference among groups were observed in the histomorphometry. Interestingly, for both anti-transforming growth factor-beta (TGF-β) and anti-vascular endothelial growth factor (VEGF) immunostaining, higher values for SPG/PBM, at 45 days post-surgery could be observed.

Conclusion

It can be concluded that the associated treatment can be considered as a promising therapeutical intervention.

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References

  1. Blais M, Parenteau-Bareil R, Cadau S, Berthod F (2013) Concise review: tissue-engineered skin and nerve regeneration in burn treatment. Stem Cells Transl Med 2:545–551

    Article  CAS  Google Scholar 

  2. Pozzolini M, Scarfì S, Gallus L, Castellano M, Vicini S, Cortese K et al (1847) Production, characterization and biocompatibility evaluation of collagen membranes derived from marine sponge chondrosia reniformis Nardo. Mar Drugs 2018:111–131

    Google Scholar 

  3. Silva TH, Moreira-Silva J, Marques ALP, Domingues A, Bayon Y, Reis RL (2014) Marine origin collagens and its potential applications. Marine Drugs 16:5881–5901

    Article  CAS  Google Scholar 

  4. Lin Z, Solomon KL, Zhang X, Pavlos NJ, Abel T, Willers C et al (2011) In vitro evaluation of natural marine sponge collagen as a scaffold for bone tissue engineering. Int J Biol Sci 7:968–977

    Article  CAS  Google Scholar 

  5. Zdarta J, Norman M, Smułek W, Moszyński D, Kaczorek E, Stelling AL et al (2017) Spongin-based scaffolds from Hippospongia communis demosponge as an effective support for lipase immobilization. Catalysts 7:147–167

    Article  CAS  Google Scholar 

  6. Widdowson JP, Picton AJ, Vince V, Wright CJ, Mearns-Spragg A (2018) In vivo comparison of jellyfish and bovine collagen sponges as prototype medical devices. J Biomed Mater Res Part B Appl Biomater 106:1524–1533

    Article  CAS  Google Scholar 

  7. Parisi JR, Avanzi IR, Santana AF, Renno ACM, Andrade AL, Fortulan CA et al (2018) Incorporation of collagen from marine sponges (spongin) into hydroxyapatite samples: characterization and in vitro biological evaluation. Mar Biotechnol 21:30–37

    Article  CAS  Google Scholar 

  8. Exposito JY, Cluzel C, Garrone R, Lethias C (2002) Evolution of collagens. Anat Rec 268:302–316

    Article  CAS  Google Scholar 

  9. Green D, Howard D, Yang X, Kelly M, Oreffo ROCOC (2003) Natural marine sponge fiber skeleton: a biomimetic scaffold. Tissue Eng 9:1156–1166

    Article  CAS  Google Scholar 

  10. Iwatsubo T, Kishi R, Miura T, Ohzono T, Yamaguchi T (2015) Formation of hydroxyapatite skeletal materials from hydrogel matrices via artificial biomineralization. J Phys Chem B 119:8793–8799

    Article  CAS  Google Scholar 

  11. Tim CR, Pinto KNZ, Rossi BRO, Fernandes K, Matsumoto MA, Parizotto NA et al (2014) Low-level laser therapy enhances the expression of osteogenic factors during bone repair in rats. Lasers Med Sci 29:147–156

    Article  Google Scholar 

  12. Magri AMP, Fernandes KR, Assis L, Mendes NA, da Silva Santos ALY, de Oliveira DE et al (2015) Photobiomodulation and bone healing in diabetic rats: evaluation of bone response using a tibial defect experimental model. Lasers Med Sci 30:1949–1957

    Article  Google Scholar 

  13. Hamblin MR (2018) Mechanisms and mitochondrial redox signaling in photobiomodulation. Photochem Photobiol 94:199–212

    Article  CAS  Google Scholar 

  14. Diniz IMA, Carreira ACO, Sipert CR, Uehara CM, Moreira MSN, Freire L et al (2018) Photobiomodulation of mesenchymal stem cells encapsulated in an injectable rhBMP4-loaded hydrogel directs hard tissue bioengineering. J Cell Physiol 233:4907–4918

    Article  CAS  Google Scholar 

  15. Hak DJ, Fitzpatrick D, Bishop JA, Marsh JL, Tilp S, Schnettler R et al (2014) Delayed union and nonunions: Epidemiology, clinical issues, and financial aspects. Injury [Internet] 45:S3–7. https://doi.org/10.1016/j.injury.2014.04.002

    Article  Google Scholar 

  16. Ruh AC, Frigo L, Cavalcanti MFXB, Svidnicki P, Vicari VN, Lopes-Martins RAB et al (2018) Laser photobiomodulation in pressure ulcer healing of human diabetic patients: gene expression analysis of inflammatory biochemical markers. Lasers Med Sci. 33:165–171

    Article  Google Scholar 

  17. Karu T (2013) Is it time to consider photobiomodulation as a drug equivalent? Photomed Laser Surg 31:189–191

    Article  CAS  Google Scholar 

  18. Huang YY, Chen ACH, Carroll JD, Hamblin MR (2009) Biphasic dose response in low level lightherapy. Dose Response 7:358–383

    Article  Google Scholar 

  19. Hamblin MR, Huang YY, Sharma SK, Carroll J (2011) Biphasic dose response in low level light therapy—an update. Dose Response 9:602–618

    PubMed  PubMed Central  Google Scholar 

  20. Naeser MA, Hamblin MR (2011) Potential for transcranial laser or LED therapy to treat stroke, traumatic brain injury, and neurodegenerative disease. Photomed Laser Surg 29:443–446

    Article  Google Scholar 

  21. de Almeida TG, Alves MBR, Batissaco L, Torres MA, de Andrade AFC, Mingoti RD et al (2019) Does low-level laser therapy on degenerated ovine testes improve post-thawed sperm characteristics? Lasers Med Sci 34:1001–1009

    Article  Google Scholar 

  22. Ravera S, Ferrando S, Agas D, De Angelis N, Raffetto M, Sabbieti MG et al (2019) 1064 nm Nd:YAG laser light affects transmembrane mitochondria respiratory chain complexes. J Biophotonics 12:1–7

    Article  CAS  Google Scholar 

  23. Bossini PS, Muniz Renno AC, Ribeiro DA, Fangel R, Peitl O, Zanotto ED et al (2011) Biosilicate® and low-level laser therapy improve bone repair in osteoporotic rats. J Tissue Eng Regen Med 5:229–237

    Article  CAS  Google Scholar 

  24. de Andrade ALM, Parisi JR, Parizotto NA, Luna GF, de Oliveira Leal ÂM, Brassolatti P et al (2018) Photobiomodulation effect on the proliferation of adipose tissue mesenchymal stem cells. Lasers Med Sci 34:677–683

    Article  Google Scholar 

  25. Fávaro-Pípi E, Ribeiro DA, Ribeiro JU, Bossini P, Oliveira P, Parizotto NA et al (2011) Low-level laser therapy induces differential expression of osteogenic genes during bone repair in rats. Photomed Laser Surg 29:311–317

    Article  CAS  Google Scholar 

  26. Tim CR, Bossini PS, Kido HW, Malavazi I, von Zeska Kress MR, Carazzolle MF et al (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 21:088001–88009

    Article  Google Scholar 

  27. Swatschek D, Schatton W, Kellermann J, Müller WEG, Kreuter J (2002) Marine sponge collagen: isolation, characterization and effects on the skin parameters surface-pH, moisture and sebum. Eur J Pharm Biopharm 53:107–113

    Article  CAS  Google Scholar 

  28. Özel T, Bártolo PJ, Ceretti E, De Ciurana Gay JD, Rodríguez CA, Da Silva JVL (2016) Biomedical devices: design, prototyping, and manufacturing. Wiley, Hoboken, pp 1–190

    Book  Google Scholar 

  29. Lopez-Heredia MA, Sa Y, Salmon P, De Wijn JR, Wolke JGC, Jansen JA (2012) Bulk properties and bioactivity assessment of porous polymethylmethacrylate cement loaded with calcium phosphates under simulated physiological conditions. Acta Biomater 8:3120–3127

    Article  CAS  Google Scholar 

  30. Wang L, Yoon DM, Spicer PP, Henslee AM, Scott DW, Wong ME et al (2013) Characterization of porous polymethylmethacrylate space maintainers for craniofacial reconstruction. J Biomed Mater Res Part B Appl Biomater 101:813–825

    Article  CAS  Google Scholar 

  31. Magri AMP, Fernandes KR, Kido HW, Fernandes GS, de Fermino S, Gabbai-Armelin PR, et al (2019) Bioglass/PLGA associated to photobiomodulation: effects on the healing process in an experimental model of calvarial bone defect. J Mater Sci Mater Med [Internet] 30:105–114. https://doi.org/10.1007/s10856-019-6307-x

    Article  CAS  Google Scholar 

  32. Tim CR, Bossini PS, Kido HW, Malavazi I, von Zeska Kress MR, Carazzolle MF et al (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 30:2325–2333

    Article  Google Scholar 

  33. Sarvestani FK, Dehno NS, Nazhvani SD, Bagheri MH, Abbasi S, Khademolhosseini Y et al (2017) Effect of low-level laser therapy on fracture healing in rabbits effect of low-level laser therapy on fracture healing in rabbits. Laser Ther 26:189–193

    Article  Google Scholar 

  34. de Freitas NR, Guerrini LB, Esper LA, Sbrana MC, da Dalben G, Soares S et al (2018) Evaluation of photobiomodulation therapy associated with guided bone regeneration in critical size defects. In vivo study. J Appl Oral Sci 26:0244–255

    Google Scholar 

  35. de Oliveira LSS, de Araújo AA, de Araújo Júnior RF, Barboza CAG, Borges BCD, da Silva JSP (2017) Low-level laser therapy (780 nm) combined with collagen sponge scaffold promotes repair of rat cranial critical-size defects and increases TGF-β, FGF-2, OPG/RANK and osteocalcin expression. Int J Exp Pathol 98:75–85

    Article  CAS  Google Scholar 

  36. Majidinia M, Sadeghpour A, Yousefi B (2018) The roles of signaling pathways in bone repair and regeneration. J Cell Physiol 233:2937–2948

    Article  CAS  Google Scholar 

  37. Yang YQ, Tan YY, Wong R, Wenden A, Zhang LK, Rabie ABM (2012) The role of vascular endothelial growth factor in ossification. Int J Oral Sci 4:64–68

    Article  CAS  Google Scholar 

  38. Zhou Y, Huang R, Fan W, Prasadam I, Crawford R, Xiao Y (2018) Mesenchymal stromal cells regulate the cell mobility and the immune response during osteogenesis through secretion of vascular endothelial growth factor A. J Tissue Eng Regen Med 12:e566–e578

    Article  CAS  Google Scholar 

  39. Hosseinpour S, Fekrazad R, Arany PR, Ye Q (2019) Molecular impacts of photobiomodulation on bone regeneration: a systematic review. Prog Biophys Mol Biol 4:005–18

    Google Scholar 

Download references

Acknowledgements

Authors would like to thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the scholarship (grant no. 2016/13636-9). This research was supported by fellowships from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Finance Code 001.

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Correspondence to M. A. Cruz.

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The Animal Care Committee guidelines of the Federal University of São Paulo (CEUA no. 4331220318) approved the present study and national guidelines for the care and use of laboratory animals were observed.

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Cruz, M.A., Fernandes, K.R., Parisi, J.R. et al. Marine collagen scaffolds and photobiomodulation on bone healing process in a model of calvaria defects. J Bone Miner Metab 38, 639–647 (2020). https://doi.org/10.1007/s00774-020-01102-4

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  • DOI: https://doi.org/10.1007/s00774-020-01102-4

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