Intra-volume processing of gelatine hydrogel by femtosecond laser-induced cavitation

Abstract

Cell oxygenation and nutrition are crucial for the viability of tissue-engineered constructs, and different alternatives are currently being developed to achieve an adequate vascularisation of the engineered tissue. One of the alternatives is the generation of channel-like patterns in a bioconstruct. Here, the formation of full-formed channels inside hydrogels by laser-induced cavitation was investigated. A near-infrared, femtosecond laser beam focused with a high numerical aperture was employed to obtain intra-volume modifications of a block of gelatine hydrogel. Characterisation of the laser-processed gelatine was carried out by optical microscopy and epifluorescence microscopy right after and 24 h after the laser process. Rheology analyses on the unprocessed gelatine blocks were conducted to better understand the cavitation mechanism taking place during the intense laser interaction. Different cavitation patterns were observed at varying dose values by changing the repetition rate and the overlap between successive pulses while keeping the laser fluence and the number of passes fixed. This way, cavitation bubble features and behaviour can be controlled to optimise the formation of intra-volume channels in the gelatine volume. Results showed that the generation of fully formed channels was linked to the formation of large non-spherical cavitation bubbles during the laser interaction at high dose and low repetition rates. In conclusion, the formation of fully formed channels was made possible with a near-infrared, femtosecond laser beam strongly focused inside gelatine hydrogel blocks through laser-induced cavitation at high dose and low repetition rates.

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Data availability

The authors confirm that the data supporting the findings of this study are available within the article.

References

  1. 1.

    Novosel EC, Kleinhans C, Kluger PJ (2011) Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev

  2. 2.

    Yuksel E, Choo J, Wettergreen M, Liebschner M (2005) Challenges in soft tissue engineering. Semin Plast Surg 19:261–270. https://doi.org/10.1055/s-2005-919721

    Article  PubMed Central  Google Scholar 

  3. 3.

    Ruprecht V, Monzo P, Ravasio A et al (2017) How cells respond to environmental cues - insights from bio-functionalized substrates. J Cell Sci 130:51–61. https://doi.org/10.1242/jcs.196162

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Lapointe VLS, Fernandes AT, Bell NC et al (2013) Nanoscale topography and chemistry affect embryonic stem cell self-renewal and early differentiation. Adv Healthc Mater 2:1644–1650. https://doi.org/10.1002/adhm.201200382

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Mandal BB, Kundu SC (2009) Cell proliferation and migration in silk fibroin 3D scaffolds. Biomaterials 30:2956–2965. https://doi.org/10.1016/j.biomaterials.2009.02.006

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Rose JB, Pacelli S, El Haj AJ et al (2014) Gelatin-based materials in ocular tissue engineering. Materials (Basel) 7:3106–3135. https://doi.org/10.3390/ma7043106

    CAS  Article  Google Scholar 

  7. 7.

    Hoque M, Nuge T, Yeow T et al (2015) Gelatin based scaffolds for tissue engineering-a review. Polym Res J 9:15

    Google Scholar 

  8. 8.

    Parenteau-Bareil R, Gauvin R, Berthod F (2010) Collagen-based biomaterials for tissue engineering applications. Materials (Basel) 3:1863–1887. https://doi.org/10.3390/ma3031863

    CAS  Article  Google Scholar 

  9. 9.

    Ozbolat IT (2015) Bioprinting scale-up tissue and organ constructs for transplantation. Trends Biotechnol 33:395–400. https://doi.org/10.1016/j.tibtech.2015.04.005

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Murphy SV, Atala A (2014) 3D bioprinting of tissues and organs. Nat Biotechnol 32:773–785. https://doi.org/10.1038/nbt.2958

    CAS  Article  Google Scholar 

  11. 11.

    Bajaj P, Schweller RM, Khademhosseini A et al (2014) 3D biofabrication strategies for tissue engineering and regenerative medicine. Annu Rev Biomed Eng 16:247–276. https://doi.org/10.1146/annurev-bioeng-071813-105155

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Lubatschowski H, Maatz G, Heisterkamp A et al (2000) Application of ultrashort laser pulses for intrastromal refractive surgery. Graefes Arch Clin Exp Ophthalmol 238:33–39. https://doi.org/10.1007/s004170050006

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Vogel A, Noack J, Hüttman G, Paltauf G (2005) Mechanisms of femtosecond laser nanosurgery of cells and tissues. Appl. Phys. B Lasers Opt

  14. 14.

    Applegate MB, Coburn J, Partlow BP et al (2015) Laser-based three-dimensional multiscale micropatterning of biocompatible hydrogels for customized tissue engineering scaffolds. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1509405112

  15. 15.

    Hribar KC, Meggs K, Liu J et al (2015) Three-dimensional direct cell patterning in collagen hydrogels with near-infrared femtosecond laser. Sci Rep. https://doi.org/10.1038/srep17203

  16. 16.

    Smith NI, Fujita K, Nakamura O, Kawata S (2001) Three-dimensional subsurface microprocessing of collagen by ultrashort laser pulses. Appl Phys Lett. https://doi.org/10.1063/1.1347392

  17. 17.

    Gattass RR, Mazur E (2008) Femtosecond laser micromachining in transparent materials. Nat Photonics 2:219–225. https://doi.org/10.1038/nphoton.2008.48

    CAS  Article  Google Scholar 

  18. 18.

    Itoh K, Watanabe W, Nolte S, Schaffer CB (2006) Ultrafast processes for bulk modification of transparent materials. MRS Bull 31:620–625. https://doi.org/10.1557/mrs2006.159

    CAS  Article  Google Scholar 

  19. 19.

    Hemmer E, Benayas A, Légaré F, Vetrone F (2016) Exploiting the biological windows: current perspectives on fluorescent bioprobes emitting above 1000 nm. Nanoscale Horizons 1:168–184. https://doi.org/10.1039/c5nh00073d

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Oujja M, Pérez S, Fadeeva E et al (2009) Three dimensional microstructuring of biopolymers by femtosecond laser irradiation. Appl Phys Lett 95. https://doi.org/10.1063/1.3274127

  21. 21.

    Gaspard S, Forster M, Huber C et al (2008) Femtosecond laser processing of biopolymers at high repetition rate. Phys Chem Chem Phys 10:6174–6181. https://doi.org/10.1039/b807870j

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Gaspard S, Oujja M, Abrusci C et al (2008) Laser induced foaming and chemical modifications of gelatine films. J Photochem Photobiol A Chem 193:187–192. https://doi.org/10.1016/j.jphotochem.2007.06.024

    CAS  Article  Google Scholar 

  23. 23.

    Pradhan DS, Keller KA, Sperduto SJH (2017) Fundamentals of laser-based hydrogel degradation and applications in cell and tissue engineering. Adv Healthc Mater. https://doi.org/10.1002/adhm.201700681

  24. 24.

    Taroni P, Bassi A, Comelli D et al (2009) Diffuse optical spectroscopy of breast tissue extended to 1100 nm. J Biomed Opt 14:054030. https://doi.org/10.1117/1.3251051

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Verit I, RIGOTHIER C, GEMINI L, et al (2019) Biofabrication of a vascular capillary by ultra-short laser pulses

  26. 26.

    Vogel A, Noack J, Nahen K et al (1999) Energy balance of optical breakdown in water at nanosecond to femtosecond time scales. Appl Phys B Lasers Opt 68:271–280. https://doi.org/10.1007/s003400050617

    CAS  Article  Google Scholar 

  27. 27.

    Vogel A, Venugopalan V (2003) Mechanisms of pulsed laser ablation of biological tissues. Chem Rev. https://doi.org/10.1021/cr010379n

  28. 28.

    Linz N, Freidank S, Liang XX, Vogel A (2016) Wavelength dependence of femtosecond laser-induced breakdown in water and implications for laser surgery. Phys Rev B. https://doi.org/10.1103/PhysRevB.94.024113

  29. 29.

    Juhasz T, Kastis GA, Suárez C et al (1996) Time-resolved observations of shock waves and cavitation bubbles generated by femtosecond laser pulses in corneal tissue and water. Lasers Surg Med 19:23–31. https://doi.org/10.1002/(SICI)1096-9101(1996)19:1<23::AID-LSM4>3.3.CO;2-2

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Loesel FH, Niemz MH, Bille JF, Juhasz T (1996) Laser-induced optical breakdown on hard and soft tissues and its dependence on the pulse duration: experiment and model. IEEE J Quantum Electron. https://doi.org/10.1109/3.538774

  31. 31.

    Centrale É, Université DL, Bernard C (2015) Caractérisation optique et acoustique d ’ une bulle générée par focalisation laser Résumé : Abstract

  32. 32.

    Kang W, Raphael M (2018) Acceleration-induced pressure gradients and cavitation in soft biomaterials. Sci Rep 8:2–13. https://doi.org/10.1038/s41598-018-34085-4

    CAS  Article  Google Scholar 

  33. 33.

    Kang W, Adnan A, O’Shaughnessy T, Bagchi A (2018) Cavitation nucleation in gelatin: experiment and mechanism. Acta Biomater 67:295–306. https://doi.org/10.1016/j.actbio.2017.11.030

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank Dr. Béatrice L’Azou and Dr. Gilles Lemagnen (LTPIB laboratory, associated Professor at Bordeaux University) for support with the rheology analyses and the interesting discussions.

Funding

The French National Association of Research and Technology (Grant no2017/0579) provided support and funding.

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Correspondence to Isabel Vérit.

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Vérit, I., Gemini, L., Fricain, JC. et al. Intra-volume processing of gelatine hydrogel by femtosecond laser-induced cavitation. Lasers Med Sci 36, 197–206 (2021). https://doi.org/10.1007/s10103-020-03081-4

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Keywords

  • Femtosecond laser-gelatine interaction
  • Laser-induced cavitation
  • Microvascularisation
  • Laser-induced intravolumique channels