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Lasers in Medical Science

, Volume 33, Issue 2, pp 375–384 | Cite as

Laser surface modification of decellularized extracellular cartilage matrix for cartilage tissue engineering

  • Eva Goldberg-BockhornEmail author
  • Silke Schwarz
  • Rachana Subedi
  • Alexander Elsässer
  • Ricarda Riepl
  • Paul Walther
  • Ludwig Körber
  • Roman Breiter
  • Karl Stock
  • Nicole Rotter
Original Article

Abstract

The implantation of autologous cartilage as the gold standard operative procedure for the reconstruction of cartilage defects in the head and neck region unfortunately implicates a variety of negative effects at the donor site. Tissue-engineered cartilage appears to be a promising alternative. However, due to the complex requirements, the optimal material is yet to be determined. As demonstrated previously, decellularized porcine cartilage (DECM) might be a good option to engineer vital cartilage. As the dense structure of DECM limits cellular infiltration, we investigated surface modifications of the scaffolds by carbon dioxide (CO2) and Er:YAG laser application to facilitate the migration of chondrocytes inside the scaffold. After laser treatment, the scaffolds were seeded with human nasal septal chondrocytes and analyzed with respect to cell migration and formation of new extracellular matrix proteins. Histology, immunohistochemistry, SEM, and TEM examination revealed an increase of the scaffolds’ surface area with proliferation of cell numbers on the scaffolds for both laser types. The lack of cytotoxic effects was demonstrated by standard cytotoxicity testing. However, a thermal denaturation area seemed to hinder the migration of the chondrocytes inside the scaffolds, even more so after CO2 laser treatment. Therefore, the Er:YAG laser seemed to be better suitable. Further modifications of the laser adjustments or the use of alternative laser systems might be advantageous for surface enlargement and to facilitate migration of chondrocytes into the scaffold in one step.

Keywords

Cartilage Chondrocytes Surface modification Tissue engineering Er:YAG laser Carbon dioxide laser 

Notes

Acknowledgments

The authors thank G. Cudek, K. Hasch, and M. Jerg for the excellent technical support.

Compliance with ethical standards

The study has been approved by the University of Ulm Ethical Committee (Ethic application number 152/08) and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Sobol E, Shekhter A, Guller A, Baum O, Baskov A (2011) Laser-induced regeneration of cartilage. J Biomed Opt 16:80902.  https://doi.org/10.1117/1.3614565 CrossRefGoogle Scholar
  2. 2.
    Chang JS, Becker SS, Park SS (2004) Nasal reconstruction: the state of the art. Curr Opin Otolaryngol Head Neck Surg 12:336–343CrossRefPubMedGoogle Scholar
  3. 3.
    Menick FJ (2010) Nasal reconstruction. Plast Reconstr Surg 125:138e–150e.  https://doi.org/10.1097/PRS.0b013e3181d0ae2b CrossRefPubMedGoogle Scholar
  4. 4.
    Scheithauer MO, Rotter N, Lindemann J, Schulz M, Rettinger G, Veit JA (2013) The auricle’s cavum conchae composite graft in nasal reconstruction. Am J Rhinol Allergy 27:53–57.  https://doi.org/10.2500/ajra.2013.27.3883 CrossRefGoogle Scholar
  5. 5.
    Mischkowski RA, Domingos-Hadamitzky C, Siessegger M, Zinser MJ, Zoller JE (2008) Donor-site morbidity of ear cartilage autografts. Plast Reconstr Surg 121:79–87CrossRefPubMedGoogle Scholar
  6. 6.
    Varadharajan K, Sethukumar P, Anwar M, Patel K (2015) Complications associated with the use of autologous costal cartilage in rhinoplasty: a systematic review. Aesthetic Surg J 35:644–652.  https://doi.org/10.1093/asj/sju117 CrossRefGoogle Scholar
  7. 7.
    Bermueller C, Schwarz S, Elsaesser AF, Sewing J, Baur N, von Bomhard A, Scheithauer M, Notbohm H, Rotter N (2013) Marine collagen scaffolds for nasal cartilage repair: prevention of nasal septal perforations in a new orthotopic rat model using tissue engineering techniques. Tissue Eng A 19:2201–2214CrossRefGoogle Scholar
  8. 8.
    Feldmann EM, Sundberg J, Bobbili B, Schwarz S, Gatenholm P, Rotter N (2013) Description of a novel approach to engineer cartilage with porous bacterial nanocellulose for reconstruction of a human auricle. J Biomater ApplGoogle Scholar
  9. 9.
    Rotter N, Bucheler M, Haisch A, Wollenberg B, Lang S (2007) Cartilage tissue engineering using resorbable scaffolds. J Tissue Eng Regen Med 1:411–416CrossRefPubMedGoogle Scholar
  10. 10.
    Watson D, Reuther MS (2014) Tissue-engineered cartilage for facial plastic surgery. Curr Opin Otolaryngol Head Neck Surg 22:300–306.  https://doi.org/10.1097/MOO.0000000000000068 CrossRefPubMedGoogle Scholar
  11. 11.
    Benders KEM, van Weeren PR, Badylak SF, Saris DBF, Dhert WJA, Malda J, van Weeren PR, Badylak SF, Saris DBF, Dhert WJA, Malda J (2013) Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol 31:169–176.  https://doi.org/10.1016/j.tibtech.2012.12.004 CrossRefPubMedGoogle Scholar
  12. 12.
    Brown BN, Badylak SF (2014) Extracellular matrix as an inductive scaffold for functional tissue reconstruction. Transl Res 163:268–285.  https://doi.org/10.1016/j.trsl.2013.11.003 CrossRefPubMedGoogle Scholar
  13. 13.
    Schwarz S, Elsaesser AFF, Koerber L, Goldberg-Bockhorn E, Seitz AMM, Bermueller C, Dürselen L, Ignatius A, Breiter R, Rotter N, Dürselen L, Ignatius A, Breiter R, Rotter N (2012) Processed xenogenic cartilage as innovative biomatrix for cartilage tissue engineering: effects on chondrocyte differentiation and function. J Tissue Eng Regen Med.  https://doi.org/10.1002/term.1650
  14. 14.
    Schwarz S, Koerber L, Elsaesser AFF, Goldberg-Bockhorn E, Seitz AMM, Dürselen L, Ignatius A, Walther P, Breiter R, Rotter N, Durselen L, Ignatius A, Walther P, Breiter R, Rotter N (2012) Decellularized cartilage matrix as a novel biomatrix for cartilage tissue-engineering applications. Tissue Eng A 18:2195–2209.  https://doi.org/10.1089/ten.tea.2011.0705 CrossRefGoogle Scholar
  15. 15.
    Kurella A, Dahotre NB (2005) Review paper: surface modification for bioimplants: the role of laser surface engineering. J Biomater Appl 20:5–50.  https://doi.org/10.1177/0885328205052974 CrossRefPubMedGoogle Scholar
  16. 16.
    Sobol E, Sviridov A, Omel’chenko A, Bagratashvili V, Kitai M, Harding SE, Jones N, Jumel K, Mertig M, Pompe W, Ovchinnikov Y, Shekhter A, Svistushkin V (2000) Laser reshaping of cartilage. Biotechnol Genet Eng Rev 17:553–578CrossRefPubMedGoogle Scholar
  17. 17.
    Wong BJ, Milner TE, Kim HK, Chao K, Sun CH, Sobol EN, Nelson JS (2000) Proteoglycan synthesis in porcine nasal cartilage grafts following Nd:YAG (lambda = 1.32 microns) laser-mediated reshaping. Photochem Photobiol 71:218–224CrossRefPubMedGoogle Scholar
  18. 18.
    Meister J, Franzen R, Gavenis K, Zaum M, Stanzel S, Gutknecht N, Schmidt-Rohlfing B (2009) Ablation of articular cartilage with an erbium:YAG laser: an ex vivo study using porcine models under real conditions-ablation measurement and histological examination. Lasers Surg Med 41:674–685.  https://doi.org/10.1002/lsm.20848 CrossRefPubMedGoogle Scholar
  19. 19.
    Juran CM, Dolwick MF, McFetridge PS (2015) Engineered microporosity: enhancing the early regenerative potential of decellularized temporomandibular joint discs. Tissue Eng Part A 21:829–839.  https://doi.org/10.1089/ten.tea.2014.0250 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Keane TJ, Badylak SF (2014) Biomaterials for tissue engineering applications. Semin Pediatr Surg 23:112–118.  https://doi.org/10.1053/j.sempedsurg.2014.06.010 CrossRefPubMedGoogle Scholar
  21. 21.
    Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA (2015) Repair and tissue engineering techniques for articular cartilage Eleftherios. Nat Rev Rheumatol 11:21–34.  https://doi.org/10.1530/ERC-14-0411.Persistent CrossRefPubMedGoogle Scholar
  22. 22.
    Sivayoham E, Woolford TJ (2012) Current opinion on auricular reconstruction. Curr Opin Otolaryngol Head Neck Surg 20:287–290.  https://doi.org/10.1097/MOO.0b013e328355b1d9 CrossRefPubMedGoogle Scholar
  23. 23.
    Uppal RS, Sabbagh W, Chana J, Gault DT (2008) Donor-site morbidity after autologous costal cartilage harvest in ear reconstruction and approaches to reducing donor-site contour deformity. Plast Reconstr Surg 121:1949–1955CrossRefPubMedGoogle Scholar
  24. 24.
    Kim H-S, Park S-S, Kim M-H, Kim M-S, Kim S-K, Lee K-C (2014) Problems associated with alloplastic materials in rhinoplasty. Yonsei Med J 55:1617–1623.  https://doi.org/10.3349/ymj.2014.55.6.1617 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Romo T, Kwak ES (2006) Nasal grafts and implants in revision rhinoplasty. Facial Plast Surg Clin North Am 14(373–87):vii.  https://doi.org/10.1016/j.fsc.2006.06.006 Google Scholar
  26. 26.
    Goldberg-Bockhorn E, Schwarz S, Elsässer A, Seitz A, Körber L, Dürselen L, Ignatius A, Feldmann E-M, Scheithauer M, Breiter R, Rotter N (2014) Physical characterization of decellularized cartilage matrix for reconstructive rhinosurgery. Laryngorhinootologie 93:756–763.  https://doi.org/10.1055/s-0034-1384531 CrossRefPubMedGoogle Scholar
  27. 27.
    Elsaesser AF, Bermueller C, Schwarz S, Koerber L, Breiter R, Rotter N (2014) In vitro cytotoxicity and in vivo effects of a decellularized xenogeneic collagen scaffold in nasal cartilage repair. Tissue Eng Part A 20:1668–1678.  https://doi.org/10.1089/ten.TEA.2013.0365 CrossRefPubMedGoogle Scholar
  28. 28.
    Tateya I, Shiotani A, Satou Y, Tomifuji M, Morita S, Muto M, Ito J (2015) Transoral surgery for laryngo-pharyngeal cancer—the paradigm shift of the head and cancer treatment. Auris Nasus Larynx.  https://doi.org/10.1016/j.anl.2015.06.013
  29. 29.
    Kamalski DM a, Wegner I, Tange R a, Vincent R, Stegeman I, van der Heijden GJM, Grolman W (2014) Outcomes of different laser types in laser-assisted stapedotomy: a systematic review. Otol Neurotol 35:1046–1051.  https://doi.org/10.1097/MAO.0000000000000270 CrossRefPubMedGoogle Scholar
  30. 30.
    Janda P, Sroka R, Baumgartner R, Grevers G, Leunig A (2001) Laser treatment of hyperplastic inferior nasal turbinates: a review. Lasers Surg Med 28:404–413.  https://doi.org/10.1002/lsm.1068 CrossRefPubMedGoogle Scholar
  31. 31.
    Sautter NB, Smith TL (2016) Treatment of hereditary hemorrhagic telangiectasia-related epistaxis. Otolaryngol Clin N Am 49:639–654.  https://doi.org/10.1016/j.otc.2016.02.010 CrossRefGoogle Scholar
  32. 32.
    Leclère FM, Vogt PM, Casoli V, Vlachos S, Mordon S (2015) Laser-assisted cartilage reshaping for protruding ears: a review of the clinical applications. Laryngoscope 125:2067–2071.  https://doi.org/10.1002/lary.25260 CrossRefPubMedGoogle Scholar
  33. 33.
    Leclère FM, Petropoulos I, Buys B, Mordon S (2010) Laser assisted septal cartilage reshaping (LASCR): a prospective study in 12 patients. Lasers Surg Med 42:693–698.  https://doi.org/10.1002/lsm.20958 CrossRefPubMedGoogle Scholar
  34. 34.
    Holden PK, Li C, Da Costa V, Sun CH, Bryant SV, Gardiner DM, Wong BJ (2009) The effects of laser irradiation of cartilage on chondrocyte gene expression and the collagen matrix. Lasers Surg Med 41:487–491CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Riggs K, Keller M, Humphreys TR (2007) Ablative laser resurfacing: high-energy pulsed carbon dioxide and erbium:yttrium-aluminum-garnet. Clin Dermatol 25:462–473.  https://doi.org/10.1016/j.clindermatol.2007.07.003 CrossRefPubMedGoogle Scholar
  36. 36.
    Walsh JT, Flotte TJ, Deutsch TF (1989) Er:YAG laser ablation of tissue: effect of pulse duration and tissue type on thermal damage. Lasers Surg Med 9:314–326CrossRefPubMedGoogle Scholar
  37. 37.
    Hale GM, Querry MR (1973) Optical constants of water in the 200-nm to 200-microm wavelength region. Appl Opt 12:555–563CrossRefPubMedGoogle Scholar
  38. 38.
    Zachary CB (2000) Modulating the Er:YAG laser. Lasers Surg Med 26:223–226CrossRefPubMedGoogle Scholar
  39. 39.
    Khatri KA, Ross V, Grevelink JM, Magro CM, Anderson RR (1999) Comparison of erbium:YAG and carbon dioxide lasers in resurfacing of facial rhytides. Arch Dermatol 135:391–397CrossRefPubMedGoogle Scholar
  40. 40.
    Whipple TL, Marotta JJ, May TC, Caspari RB, Meyers JF (1987) Electron microscopy of CO2-laser-induced effects in human fibrocartilage. Lasers Surg Med 7:184–188CrossRefPubMedGoogle Scholar
  41. 41.
    Janik I, Starek I, Hlozek Z, Hubacek J, Novotny R, Dvorackova J (2009) Histomorphological transformation of the auricular cartilage after carbon dioxide laser-assisted Mustarde otoplasty. An experimental study. Lasers Med Sci 24:433–437CrossRefPubMedGoogle Scholar
  42. 42.
    Walsh JT, Flotte TJ, Anderson RR, Deutsch TF (1988) Pulsed CO2 laser tissue ablation: effect of tissue type and pulse duration on thermal damage. Lasers Surg Med 8:108–118CrossRefPubMedGoogle Scholar
  43. 43.
    Chen LY, Manche EE (2016) Comparison of femtosecond and excimer laser platforms available for corneal refractive surgery. Curr Opin Ophthalmol 27:316–322.  https://doi.org/10.1097/ICU.0000000000000268 CrossRefPubMedGoogle Scholar
  44. 44.
    Su E, Sun H, Juhasz T, Wong BJF (2014) Preclinical investigations of articular cartilage ablation with femtosecond and pulsed infrared lasers as an alternative to microfracture surgery. J Biomed Opt 19:98001.  https://doi.org/10.1117/1.JBO.19.9.098001 CrossRefPubMedGoogle Scholar
  45. 45.
    Haffner C, Folwaczny M, Hickel R, Horch HH (2004) Ablation of temporomandibular joint structures of a pig with a fibre-guided 308nm excimer laser light—an in vitro investigation. J Cranio-Maxillofacial Surg 32:360–364.  https://doi.org/10.1016/j.jcms.2004.05.006 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2017

Authors and Affiliations

  • Eva Goldberg-Bockhorn
    • 1
    Email author
  • Silke Schwarz
    • 2
  • Rachana Subedi
    • 1
  • Alexander Elsässer
    • 1
  • Ricarda Riepl
    • 1
  • Paul Walther
    • 3
  • Ludwig Körber
    • 4
  • Roman Breiter
    • 5
  • Karl Stock
    • 6
  • Nicole Rotter
    • 7
  1. 1.Department of Otorhinolaryngology, Head and Neck SurgeryUlm University Medical CenterUlmGermany
  2. 2.Department of AnatomyParacelsus Medical University, Salzburg and NuernbergNuernbergGermany
  3. 3.Central Facility for Electron MicroscopyUlm UniversityUlmGermany
  4. 4.Institute of Bioprocess EngineeringErlangen UniversityErlangenGermany
  5. 5.Chair of Medical Bio-TechnologyUniversity of ErlangenErlangenGermany
  6. 6.Institut für Lasertechnologien in der Medizin und Meßtechnikan der Universität UlmUlmGermany
  7. 7.Department of OtorhinolaryngologyMannheim University Medical CenterMannheimGermany

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