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Cited by 27Bone Tissue Engineering MaterialsTissue Engineering and Regenerative MedicineSilk-based biomaterials and applications

Bioactive snail mucus-slime extract loaded chitosan scaffolds for hard tissue regeneration: the effect of mucoadhesive and antibacterial extracts on physical characteristics and bioactivity of chitosan matrix

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Perpelek, Merve, Tamburaci, Sedef, Aydemir, Selma, Tihminlioglu, Funda, Baykara, Basak, Karakasli, Ahmet, Havitcioglu, Hasan·2021·Biomedical Materials
DOI 10.1088/1748-605x/ac2352
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Abstract

Biobased extracts comprise various bioactive components and they are widely used in tissue engineering applications to increase bioactivity as well as physical characteristics of biomaterials. Among animal sources, garden snail Helix aspersa has come into prominence with its antibacterial and regenerative extracts and show potential in tissue regeneration. Thus, in this study, bioactive H. aspersa extracts (slime, mucus) were loaded in chitosan (CHI) matrix to fabricate porous scaffolds for hard tissue regeneration. Physical, chemical properties, antimicrobial activity was determined as well as in vitro bioactivity for bone and cartilage regeneration. Mucus and slime incorporation enhanced mechanical properties and biodegradation rate of CHI matrix. Scanning electron microscopy images showed that the average pore size of the scaffolds decreased with higher extract content. Mucus and slime extracts showed antimicrobial effect on two bacterial strains. In vitro cytotoxicity, osteogenic and chondrogenic activity of the scaffolds were evaluated with Saos-2 and SW1353 cell lines in terms of Alkaline phosphatase activity, biomineralization, GAG, COMP and hydroxyproline content. Cell viability results showed that extracts had a proliferative effect on Saos-2 and SW1353 cells when compared to the control group. Mucus and slime extract loading increased osteogenic and chondrogenic activity. Thus, the bioactive extract loaded CHI scaffolds showed potential for bone and cartilage regeneration with enhanced physical properties and in vitro bioactivity.

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  • C. aspersum mucus showed effective antibacterial activity against two different strains of Pseudomonas aeruginosa and Streptococcus pyogenes.

    “It is noted that C. aspersum mucus showed effective antibacterial activity against two different strains of Pseudomonas aeruginosa and Streptococcus pyogenes.”

    From Chemical Variability and Biological Potential of Cornu aspersum Mucus as a Source for the Development of New Cosmetic and Pharmaceutical Products (2025) · cites this paper as [78]

    Section 4.1.6 reports that H. aspersa mucus was effective against a P. aeruginosa strain in an earlier study. It does not report activity against two P. aeruginosa strains or Streptococcus pyogenes; this paper's own tests instead found activity against P. fluorescens and S. epidermidis (section 4.1.6; Table 2). (LLM, conf=0.88)

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Research works printed but not linked: 60

  1. Temenoff J S and Mikos A G 2000 Review: tissue engineering for regeneration of articular cartilage Biomaterials 21 431-4 · DOI
  2. O'driscoll S 1998 The healing and regeneration of articular cartilage J. Bone Joint Surg. Am. 80 1795-812 · DOI
  3. Awad H A, O'Keefe R J, Lee C H and Mao J J 2014 Bone tissue engineering: clinical challenges and emergent advances in orthopedic and craniofacial surgery Principle of Tissue Engineering 4th edn, ed R Lanza, R Langer and J Vacanti (Boston: Academic Press Inc) pp 1733-43 · DOI
  4. Li W J, Laurencin C T, Caterson E J, Tuan R S and Ko F K 2002 Electrospun nanofibrous structure: a novel scaffold for tissue engineering J. Biomed. Mater. Res. 60 613-21 · DOI
  5. Dolcimascolo A, Calabrese G, Conoci S and Parenti R 2019 Innovative biomaterials for tissue engineering Biomaterial-supported Tissue Reconstruction or Regeneration ed M Barbeck, O Jung, R Smeets and T Koržinskas (London: IntechOpen) pp 1-18 · DOI
  6. Ha T L B, Quan T M, Vu D N and Si D M 2013 Naturally derived biomaterials: preparation and application Regenerative Medicine and Tissue Engineering ed J A Andrades (London: IntechOpen) pp 247-69 · DOI
  7. Tamburaci S, Kimna C and Tihminlioglu F 2018 Novel phytochemical Cissus quadrangularis extract-loaded chitosan/Na-carboxymethyl cellulose-based scaffolds for bone regeneration J. Bioact. Compat. Polym. 33 1-18 · DOI
  8. Singh P, Gupta A, Qayoom I, Singh S and Kumar A 2020 Orthobiologics with phytobioactive cues: a paradigm in bone regeneration Biomed. Pharmacother. 130 110754 · DOI
  9. Irgin C, Çörekçi B and Ozan F 2016 Does stinging nettle (Urtica dioica) have an effect on bone formation in the expanded inter-premaxillary suture? Arch. Oral Biol. 69 13-18 · DOI
  10. Hadavi M et al 2017 Novel calcified gum Arabic porous nano-composite scaffold for bone tissue regeneration Biochem. Biophys. Res. Commun. 488 671-8 · DOI
  11. Brieva A et al 2008 Molecular basis for the regenerative properties of a secretion of the mollusk Cryptomphalus aspersa Skin Pharmacol. Physiol. 21 15-22 · DOI
  12. Trapella C et al 2018 HelixComplex snail mucus exhibits pro-survival, proliferative and pro-migration effects on mammalian fibroblasts Sci. Rep. 8 17665 1-10 · DOI · Paper page
  13. Tsoutsos D, Kakagia D and Tamparopoulos K 2009 The efficacy of Helix aspersa Müller extract in the healing of partial thickness burns: a novel treatment for open burn management protocols J. Dermatolog. Treat. 20 219-22 · DOI
  14. Otsuka-Fuchino H et al 1992 Bactericidal action of a glycoprotein from the body surface mucus of giant African snail Camp. Eiochem. Physiol. 101 607-13 · DOI
  15. Etim L B, Aleruchi C and Attah O G 2016 Antibacterial properties of snail mucus on bacteria isolated from patients with wound infection Br. Microbiol. Res. J. 11 1-9 · DOI
  16. Pitt S J, Graham M A, Dedi C G, Taylor-Harris P M and Gunn A 2015 Antimicrobial properties of mucus from the brown garden snail Helix aspersa Br. J. Biomed. Sci. 72 174-81 · DOI
  17. Ng T P T et al 2013 Snails and their trails: the multiple functions of trail-following in gastropods Biol. Rev. Camb. Phil. Soc. 88 683-700 · DOI
  18. Greistorfer S et al 2017 Snail mucus-glandular origin and composition in Helix pomatia Zoology 122 126-38 · DOI
  19. Angulo D E L and Sobral P J A 2016 Characterization of gelatin/chitosan scaffold blended with aloe vera and snail mucus for biomedical purpose Int. J. Biol. Macromol. 92 645-53 · DOI
  20. di Filippo M F et al 2020 Functional properties of chitosan films modified by snail mucus extract Int. J. Biol. Macromol. 143 126-35 · DOI
  21. Freier T, Koh H S, Kazazian K and Shoichet M S 2005 Controlling cell adhesion and degradation of chitosan films by N-acetylation Biomaterials 26 5872-8 · DOI
  22. Hoemann C D, El-Gabalawy H and McKee M D 2009 In vitro osteogenesis assays: influence of the primary cell source on alkaline phosphatase activity and mineralization Patho. Biol. 57 318-23 · DOI
  23. Li Z et al 2020 Biomechanically, structurally and functionally meticulously tailored polycaprolactone/silk fibroin scaffold for meniscus regeneration Theranostics 10 5090-106 · DOI
  24. Kim Y T et al 2012 The dynamic healing profile of human periodontal ligament stem cells: histological and immunohistochemical analysis using an ectopic transplantation model J. Periodontal. Res. 47 514-24 · DOI
  25. Brauker J H et al 1995 Neovascularization of synthetic membranes directed by membrane micro architecture J. Biomed. Mater. Res. 29 1517-24 · DOI · Paper page
  26. Klawitter J J and Hulbert S F 1971 application of porous ceramics for the attachment of load-bearing internal orthopedic applications J. Biomed. Mater. Res. A 2 161-8 · DOI
  27. Yang S, Leong K F, Du Z and Chua C K 2001 The design of scaffolds for use in tissue engineering part 1: traditional factors Tissue Eng. 7 679-89 · DOI · Paper page
  28. Whang K et al 1999 Engineering bone regeneration with bioabsorbable scaffolds with novel microarchitecture Tissue Eng. 5 35-51 · DOI
  29. Yannas I V, Lee E, Orgill D P and Skrabut E M 1989 Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin Proc. Natl Acad. Sci. 86 933-7 · DOI · Paper page
  30. Zhang Q, Lu H, Kawazoe N and Chen G 2014 Pore size effect of collagen scaffolds on cartilage regeneration Acta Biomater. 10 2005-13 · DOI
  31. Kramschuster A and Turng L S 2013 Fabrication of tissue engineering scaffolds Handbook of Biopolymers and Biodegradable Plastics ed S Ebnesajjad (UK: Elsevier Inc.) pp 427-46 · DOI
  32. Xie J et al 2006 Mechano-active scaffold design based on microporous poly(L-lactide-co-epsilon-caprolactone) for articular cartilage tissue engineering: dependence of porosity on compression force-applied mechanical behaviors Tissue Eng. 12 449-58 · DOI
  33. Cheng A et al 2019 Advances in porous scaffold design for bone and cartilage tissue engineering and regeneration Tissue Eng. B 25 14-29 · DOI
  34. Vishwanath V, Pramanik K and Biswas A 2016 Optimization and evaluation of silk fibroin-chitosan freeze-dried porous scaffolds for cartilage tissue engineering application J. Biomater. Sci., Polym. Ed. 27 657-74 · DOI
  35. Pawlicki J M et al 2004 The effect of molluscan glue proteins on gel mechanics J. Exp. Biol. 207 1127-35 · DOI
  36. Leceta I, Guerrero P and de la Caba K 2013 Functional properties of chitosan-based films Carbohydr. Polym. 93 339-46 · DOI
  37. Ibrahim M, Mahmoud A A, Osman O, Refaat A and El-Sayed E S M 2010 Molecular spectroscopic analysis of nano-chitosan blend as biosensor Spectrochim. Acta. A 77 802-6 · DOI
  38. Dona T M, Kingb C F, Chiub W Y and Peng C A 2006 Preparation and characterization of chitosan-g-poly(vinyl alcohol)/poly(vinyl alcohol) blends used for the evaluation of blood-contacting compatibility Carbohydr. Polym. 63 331-9 · DOI
  39. Skingsley D R, White A J and Weston A 2000 Analysis of pulmonate mucus by infrared spectroscopy J. Moll. Stud. 66 363-71 · DOI
  40. Pancake S J and Karnovsky M L 1971 The isolation and characterization of a mucopolysaccharide secreted by the snail, Otella lactea J. Biol. Chem. 264 253-62 · DOI
  41. Fathi M, Nasrabadi M N and Varshosaz J 2017 Characteristics of vitamin E-loaded nanofibres from dextran Int. J. Food Prop. 20 2665-74 · DOI
  42. Tallian C et al 2019 Lysozyme-responsive spray-dried chitosan particles for early detection of wound infection ACS Appl. Bio. Mater. 2 1331-9 · DOI
  43. Hutmacher D W, Goh J C H and Teoh S H 2001 An introduction to biodegradable materials for tissue engineering applications Ann. Acad. Med. Singap. 30 183-91 PMID: 11379417
  44. Cheung H Y, Lau K T, Lu T P and Hui D 2007 A critical review on polymer-based bio-engineered materials for scaffold development Composites B 38 291-300 · DOI
  45. Gill S R et al 2005 Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain J. Appl. Bacteriol. 187 2426-38 · DOI
  46. Scales B S, Dickson R P, LiPuma J J and Huffnagle G B 2014 Microbiology, genomics, and clinical significance of the Pseudomonas fluorescens species complex, an unappreciated colonizer of humans Clin. Microbiol. Rev. 27 927-48 · DOI
  47. Kantawong F et al 2016 Mucus of Achatina fulica stimulates mineralization and inflammatory response in dental pulp cells Turk. J. Biol. 40 353-9 · DOI
  48. Angulo D E et al 2019 Fabrication, characterization and in vitro cell study of gelatin-chitosan scaffolds: new perspectives of use of aloe vera and snail mucus for soft tissue engineering Mater. Chem. Phys. 234 268-80 · DOI
  49. Anselme K 2000 Osteoblast adhesion on biomaterials Biomaterials 21 667-81 · DOI
  50. Golub E E and Battaglia K B 2007 The role of alkaline phosphatase in mineralization Curr. Opin. Orthop. 18 444-8 · DOI
  51. Hauschka P V, Lian J B and Gallop P M 1975 Direct identification of the calcium-binding amino acid, gamma-carboxyglutamate, in mineralized tissue Proc. Natl Acad. Sci. USA 72 3925-9 · DOI
  52. Ignat'eva N Y, Danilov N A, Averkiev S V, Obrezkova M V and Lunin V V 2007 Determination of hydroxyproline in tissues and the evaluation of the collagen content of the tissues J. Anal. Chem. 62 51-57 · DOI
  53. Fournie J and Chetail M 1984 Calcium dynamics in land gastropods Am. Zool. 24 857-70 · DOI
  54. McKee M D and Cole W G 2012 Bone matrix and mineralization Pediatric Bone 2nd edn, ed F H Glorieux, J M Pettifor and H Jüppner (San Diego: Academic Press Inc.) pp 9-37 · DOI
  55. Caldeira J, Sousa A, Sousa D M and Barros D 2018 Extracellular matrix constitution and function for tissue regeneration and repair Peptides and Proteins as Biomaterials for Tissue Regeneration and Repair ed M A Barbosa and M C L Martins (UK:Woodhead Publishing Inc.) pp 29-72 · DOI
  56. Weinmann H and Ottow E 2007 Recent development in novel anticancer therapies Comprehensive Medicinal Chemistry II ed J B Taylor and D J Triggle (Amsterdam, Netherlands: Elsevier Science Inc.) pp 221-51 · DOI
  57. Nakatani S, Mano H, Sampei C, Shimizu J and Wada M 2009 Chondroprotective effect of the bioactive peptide prolyl-hydroxyproline in mouse articular cartilage in vitro and in vivo Osteoarthr. Cartil. 17 1620-7 · DOI
  58. Sharma A, Wood L D, Richardson J B, Roberts S and Kuiper N J 2007 Glycosaminoglycan profiles of repair tissue formed following autologous chondrocyte implantation differ from control cartilage Arthritis Res. Ther. 9 R79 · DOI
  59. Sodhi H and Panitch A 2020 Glycosaminoglycans in tissue engineering: a review Biomolecules 11 29 · DOI
  60. Hu J C Y and Athanasiou K A 2003 Structure and function of articular cartilage Handbook of Histology Methods for Bone and Cartilage ed Y H An and K L Martin (Totowa NJ: Humana Press Inc.) pp 73-95 · DOI

Cited by

Sorted by citations

Authors
Perpelek, M., Tamburaci, S., Aydemir, S., Tihminlioglu, F., Baykara, B., Karakasli, A., & Havitcioglu, H.
Affiliations
Dokuz Eylül University (TR)
ORCID
Venue
Biomedical Materials
Publisher
IOP Publishing
Published
2021-09-22
Volume
16
Issue
6
Pages
065008
ISSN
  • 1748-6041 (ISSN-L)
  • 1748-605X
DOI
10.1088/1748-605x/ac2352
OpenAlex
W3196750685
Cited by
27
References
0
Citations by year
2026: 3 · 2025: 7 · 2024: 4 · 2023: 11 · 2022: 2
FWCI
1.27
Type
journal article
Language
en
Update notices
correction (2023-05-11)
Open access
Licence
Locations
  • Biomedical Materials (publishedVersion)
  • PubMed (publishedVersion)
  • İYTE (İZMİR YÜKSEK TEKNOLOJİ ENSTİTÜSÜ) (submittedVersion)
Funders
  • İzmir Yüksek Teknoloji Enstitüsü
  • Aksaray Üniversitesi
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Physical Sciences › Materials Science › Biomaterials › Silk-based biomaterials and applications
Keywords
chitosan scaffolds, snail mucus, snail slime, Helix aspersa, hard tissue regeneration, bone regeneration, cartilage regeneration, mucoadhesion, antibacterial activity, osteogenic differentiation, chondrogenic differentiation, biodegradation, pore size, biomineralization, Saos-2 cells, SW1353 cells
MeSH terms
Animals, Anti-Bacterial Agents, Biological Products, Cell Line, Cell Survival, Helix, Snails, Mucus, Osteogenesis, Regeneration, Chondrogenesis, Tissue Engineering, Chitosan, Cell Proliferation, Tissue Scaffolds

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