Skip to main content
SpringerLink
Log in

An Asymmetric Natural Nanofiber with Rapid Temperature Responsive Detachability Inspired by Andrias davidianus for Full-Thickness Skin Wound Healing

  • Research Article
  • Published:
Advanced Fiber Materials Aims and scope Submit manuscript

Abstract

Wound dressing management is critical in healthcare, and frequent dressing changes for full-thickness skin wounds can hinder healing. Nanofiber dressings that resemble the extracellular matrix, have gained popularity in wound repair, however, it is challenging to explore how to frequently change it without affecting healing processing and avoiding secondary damage. Here, we developed a self-adhesive and detachable nanofiber dressing inspired by Andrias davidianus. Our asymmetric nanofiber dressing exhibits strong adhesion (26 kPa), to the wound at high temperature (approximately 25 °C) to the wound surface and can be easily detached (4 kPa) at low temperature (below 8 °C), enabling painless dressing changes that minimize secondary injuries. The dressing comprises an outer layer of polylactic acid which provides mechanical property, support, and pollution resistance, with an inner layer of nanofibrous membrane, composed of gelatin and Andrias davidianus skin secretions, which promotes cellular migration, enhances wound healing and possesses inherent antimicrobial properties. Furthermore, the all-natural nanofiber dressings can be prepared on a large scale and offer favorable biocompatibility to meet the basic requirements of wound dressings. These findings demonstrate the potential applicability of our multilayer nanofiber dressing for advancing wound healing practices.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

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

References

  1. Zhang X, Lv R, Chen L, Sun R, Zhang Y, Sheng R, Du T, Li Y, Qi Y. A multifunctional janus electrospun nanofiber dressing with biofluid draining, monitoring, and antibacterial properties for wound healing. ACS Appl Mater Interfaces. 2022;14:12984.

    Article  CAS  PubMed  Google Scholar 

  2. Dong Y, Cui M, Qu J, Wang X, Kwon SH, Barrera J, Elvassore N, Gurtner GC. Conformable hyaluronic acid hydrogel delivers adipose-derived stem cells and promotes regeneration of burn injury. Acta Biomater. 2020;108:56.

    Article  CAS  PubMed  Google Scholar 

  3. Jayarama Reddy V, Radhakrishnan S, Ravichandran R, Mukherjee S, Balamurugan R, Sundarrajan S, Ramakrishna S. Nanofibrous structured biomimetic strategies for skin tissue regeneration. Wound Repair Regen. 2013;21:1.

    Article  PubMed  Google Scholar 

  4. Feng JJ, See JL, Choke A, Ooi A, Chong SJ. Biobrane for burns of the pubic region: minimizing dressing changes. Mil Med Res. 2018;5:29.

    PubMed  PubMed Central  Google Scholar 

  5. Yang M, Fei X, Tian J, Xu L, Wang Y, Li Y. A starch-regulated adhesive hydrogel dressing with controllable separation properties for painless dressing change. J Mater Chem B. 2022;10:6026.

    Article  CAS  PubMed  Google Scholar 

  6. Li ZY, Zhang XJ, Gao YM, Song Y, Sands MX, Zhou SB, Li QF, Zhang J. Photo-responsive hydrogel for contactless dressing change to attenuate secondary damage and promote diabetic wound healing. Adv Healthc Mater. 2023;1:e2202770.

    Article  Google Scholar 

  7. Blakeney BA, Tambralli A, Anderson JM, Andukuri A, Lim DJ, Dean DR, Jun HW. Cell infiltration and growth in a low density, uncompressed three-dimensional electrospun nanofibrous scaffold. Biomaterials. 2011;32:1583.

    Article  CAS  PubMed  Google Scholar 

  8. Rahmati M, Mills DK, Urbanska AM, Saeb MR, Venugopal JR, Ramakrishna S, Mozafari M. Electrospinning for tissue engineering applications. Prog Mater Sci. 2021;117: 100721.

    Article  CAS  Google Scholar 

  9. Huang C, Thomas NL. Fabrication of porous fibers via electrospinning: strategies and applications. Polym Rev. 2019;60:595.

    Article  Google Scholar 

  10. Jiang S, Deng J, Jin Y, Qian B, Lv W, Zhou Q, Mei E, Neisiany RE, Liu Y, You Z, Pan J. Breathable, antifreezing, mechanically skin-like hydrogel textile wound dressings with dual antibacterial mechanisms. Bioact Mater. 2023;21:313–23.

    CAS  PubMed  Google Scholar 

  11. Yue Y, Gong X, Jiao W, Li Y, Yin X, Si Y, Yu J, Ding B. In-situ electrospinning of thymol-loaded polyurethane fibrous membranes for waterproof, breathable, and antibacterial wound dressing application. J Colloid Interface Sci. 2021;592:310–8.

    Article  CAS  PubMed  Google Scholar 

  12. Yang Y, Du Y, Zhang J, Zhang H, Guo B. Structural and functional design of electrospun nanofibers for hemostasis and wound healing. Adv Fiber Mater. 2022;4:1027–57.

    Article  CAS  Google Scholar 

  13. Liu J, Ye L, Sun Y, Hu M, Chen F, Wegner S, Mailander V, Steffen W, Kappl M, Butt HJ. Elastic superhydrophobic and photocatalytic active films used as blood repellent dressing. Adv Mater. 2020;32: e1908008.

    Article  PubMed  Google Scholar 

  14. Sun J, Chen T, Zhao B, Fan W, Shen Y, Wei H, Zhang M, Zheng W, Peng J, Wang J, Wang Y, Fan L, Chu Y, Chen L, Yang C. Acceleration of oral wound healing under diabetes mellitus conditions using bioadhesive hydrogel. ACS Appl Mater Interfaces. 2023;15:416.

    Article  CAS  PubMed  Google Scholar 

  15. Chen T, Chen Y, Rehman HU, Chen Z, Yang Z, Wang M, Li H, Liu H. Ultratough, self-healing, and tissue-adhesive hydrogel for wound dressing. ACS Appl Mater Interfaces. 2018;10:33523.

    Article  CAS  PubMed  Google Scholar 

  16. Azuma K, Nishihara M, Shimizu H, Itoh Y, Takashima O, Osaki T, Itoh N, Imagawa T, Murahata Y, Tsuka T, Izawa H, Ifuku S, Minami S, Saimoto H, Okamoto Y, Morimoto M. Biological adhesive based on carboxymethyl chitin derivatives and chitin nanofibers. Biomaterials. 2015;42:20.

    Article  CAS  PubMed  Google Scholar 

  17. Song YH, Ji E, Joo KI, Seo JH. Development of mechanically reinforced bioadhesive electrospun nanofibers using cellulose acetate–levan complexes. Cellulose. 2022;30:1685.

    Article  Google Scholar 

  18. Kim S, Ko J, Choi JH, Kang JY, Lim C, Shin M, Lee DW, Kim JW. Antigen-antibody interaction-derived bioadhesion of bacterial cellulose nanofibers to promote topical wound healing. Adv Funct Mater. 2022;32:2110557.

    Article  CAS  Google Scholar 

  19. Ku SH, Park CB. Combined effect of mussel-inspired surface modification and topographical cues on the behavior of skeletal myoblasts. Adv Healthc Mater. 2013;2:1445.

    Article  CAS  PubMed  Google Scholar 

  20. Ku SH, Park CB. Human endothelial cell growth on mussel-inspired nanofiber scaffold for vascular tissue engineering. Biomaterials. 2010;31:9431.

    Article  CAS  PubMed  Google Scholar 

  21. Kim BJ, Choi YS, Cha HJ. Reinforced multifunctionalized nanofibrous scaffolds using mussel adhesive proteins. Angew Chem Int Ed. 2012;51:675.

    Article  CAS  Google Scholar 

  22. Li Q, Shen X, Liu C, Xing D. Facile wound dressing replacement: carbon dots for dissolving alginate hydrogels via competitive complexation. Int J Biol Macromol. 2023;240: 124455.

    Article  CAS  PubMed  Google Scholar 

  23. Zhang K, Bai X, Yuan Z, Cao X, Jiao X, Li Y, Qin Y, Wen Y, Zhang X. Layered nanofiber sponge with an improved capacity for promoting blood coagulation and wound healing. Biomaterials. 2019;204:70.

    Article  CAS  PubMed  Google Scholar 

  24. An H, Zhang M, Zhou L, Huang Z, Duan Y, Wang C, Gu Z, Zhang P, Wen Y. Anti-dehydration and rapid trigger-detachable multifunctional hydrogels promote scarless therapeutics of deep burn. Adv Funct Mater. 2023;33:2211182.

    Article  CAS  Google Scholar 

  25. Deng J, Tang Y, Zhang Q, Wang C, Liao M, Ji P, Song J, Luo G, Chen L, Ran X, Wei Z, Zheng L, Dang R, Liu X, Zhang H, Zhang YS, Zhang X, Tan H. A Bioinspired medical adhesive derived from skin secretion of andrias davidianus for wound healing. Adv Funct Mater. 2019;29:1809110.

    Article  Google Scholar 

  26. Dang R, Chen L, Sefat F, Li X, Liu S, Yuan X, Ning X, Zhang YS, Ji P, Zhang X. A natural hydrogel with prohealing properties enhances tendon regeneration. Small. 2022;1:e2105255.

    Article  Google Scholar 

  27. Zhang X, Jiang L, Li X, Zheng L, Dang R, Liu X, Wang X, Chen L, Zhang YS, Zhang J, Yang D. A bioinspired hemostatic powder derived from the skin secretion of andrias davidianus for rapid hemostasis and intraoral wound healing. Small. 2022;18: e2101699.

    Article  PubMed  Google Scholar 

  28. Zheng L, Wang Q, Zhang YS, Zhang H, Tang Y, Zhang Y, Zhang W, Zhang X. A hemostatic sponge derived from skin secretion of Andrias davidianus and nanocellulose. Chem Eng J. 2021;1:416.

    Google Scholar 

  29. Liu X, Mao X, Ye G, Wang M, Xue K, Zhang Y, Zhang H, Ning X, Zhao M, Song J, Zhang YS, Zhang X. Bioinspired Andrias davidianus-Derived wound dressings for localized drug-elution. Bioact Mater. 2022;15:482.

    PubMed  PubMed Central  Google Scholar 

  30. Li T, Sun M, Wu S. State-of-the-art review of electrospun gelatin-based nanofiber dressings for wound healing applications. Nanomaterials. 2022;12:784.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Dong Y, Rodrigues M, Li X, Kwon SH, Kosaric N, Khong S, Gao Y, Wang W, Gurtner GC. Injectable and tunable gelatin hydrogels enhance stem cell retention and improve cutaneous wound healing. Adv Funct Mater. 2017;27:1606619.

    Article  Google Scholar 

  32. Tao B, Lin C, Qin X, Yu Y, Guo A, Li K, Tian H, Yi W, Lei D, Chen Y, Chen L. Fabrication of gelatin-based and Zn(2+)-incorporated composite hydrogel for accelerated infected wound healing. Mater Today Bio. 2022;13: 100216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wang L, Mao L, Qi F, Li X, Wajid Ullah M, Zhao M, Shi Z, Yang G. Synergistic effect of highly aligned bacterial cellulose/gelatin membranes and electrical stimulation on directional cell migration for accelerated wound healing. Chem Eng J. 2021;424: 130563.

    Article  CAS  Google Scholar 

  34. Yang X, Li L, Yang D, Nie J, Ma G. Electrospun core-shell fibrous 2D scaffold with biocompatible poly(glycerol sebacate) and poly-l-lactic acid for wound healing. Adv Fiber Mater. 2020;2:105–17.

    Article  CAS  Google Scholar 

  35. Ren Y, Huang L, Wang Y, Mei L, Fan R, He M, Wang C, Tong A, Chen H, Guo G. Stereocomplexed electrospun nanofibers containing poly (lactic acid) modified quaternized chitosan for wound healing. Carbohydr Polym. 2020;247: 116754.

    Article  CAS  PubMed  Google Scholar 

  36. Jiang Y, Zhang X, Zhang W, Wang M, Yan L, Wang K, et al. Infant skin friendly adhesive hydrogel patch activated at body temperature for bioelectronics securing and diabetic wound healing. ACS Nano. 2022;16:8662–76.

    Article  CAS  PubMed  Google Scholar 

  37. Zhang L, Wang S, Wang Z, Liu Z, Xu X, Liu H, Wang D, Tian Z. Temperature-mediated phase separation enables strong yet reversible mechanical and adhesive hydrogels. ACS Nano. 2023;14:13948–60.

    Article  Google Scholar 

  38. Lv Y, Xu Y, Sang X, Li C, Liu Y, Guo Q, et al. PLLA-gelatin composite fiber membranes incorporated with functionalized CeNPs as a sustainable wound dressing substitute promoting skin regeneration and scar remodeling. J Mater Chem B. 2022;10:1116–27.

    Article  CAS  PubMed  Google Scholar 

  39. Dias JR, Baptista-Silva S, Oliveira CM, Sousa A, Oliveira AL, Bártolo PJ, et al. In situ crosslinked electrospun gelatin nanofibers for skin regeneration. Eur Polym J. 2017;95:161–73.

    Article  CAS  Google Scholar 

  40. Rodrigo-Navarro A, Sankaran S, Dalby MJ, del Campo A, Salmeron-Sanchez M. Engineered living biomaterials Nat Rev Mater. 2021;6:1175.

    Article  Google Scholar 

  41. Xue J, Wu T, Dai Y, Xia Y. Electrospinning and electrospun nanofibers: methods, materials, and applications. Chem Rev. 2019;119:5298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhang YZ, Venugopal J, Huang ZM, Lim CT, Ramakrishna S. Crosslinking of the electrospun gelatin nanofibers. Polymer. 2006;47:2911.

    Article  CAS  Google Scholar 

  43. Bahrami S, Solouk A, Mirzadeh H, Seifalian AM. Electroconductive polyurethane/graphene nanocomposite for biomedical applications. Compos B Eng. 2019;168:421.

    Article  CAS  Google Scholar 

  44. Li M, Dong Y, Wang M, Lu X, Li X, Yu J, Ding B. Hydrogel/nanofibrous membrane composites with enhanced water retention, stretchability and self-healing capability for wound healing. Compos B Eng. 2023;257: 110672.

    Article  CAS  Google Scholar 

  45. Dias JR, Granja PL, Bártolo PJ. Advances in electrospun skin substitutes. Prog Mater Sci. 2016;84:314.

    Article  Google Scholar 

  46. Liu W, Xie R, Zhu J, Wu J, Hui J, Zheng X, Huo F. A temperature responsive adhesive hydrogel for fabrication of flexible electronic sensors. Npj Flex Electron. 2022;6:68.

    Article  CAS  Google Scholar 

  47. Zhou L, Zeng Z, Liu S, Min T, Zhang W, Bian X, Du H, Zhang P, Wen Y. Multifunctional DNA hydrogel enhances stemness of adipose-derived stem cells to activate immune pathways for guidance burn wound regeneration. Adv Funct Mater. 2022;32:2207466.

    Article  CAS  Google Scholar 

  48. Shi S, Si Y, Han Y, Wu T, Iqbal MI, Fei B, Li R, Hu J, Qu J. Recent progress in protective membranes fabricated via electrospinning: advanced materials, biomimetic structures, and functional applications. Adv Mater. 2022;34: e2107938.

    Article  PubMed  Google Scholar 

  49. Wu Y, Liu H, Li B, Jokisalo J, Kosonen R, Cheng Y, Zhao W, Yuan X. Evaluation and modification of the weighting formulas for mean skin temperature of human body in winter conditions. Energy Build. 2020;229: 110390.

    Article  Google Scholar 

  50. Daelemans L, van Paepegem W, Hooge DR, Clerck KD. Excellent nanofiber adhesion for hybrid polymer materials with high toughness based on matrix interdiffusion during chemical conversion. Adv Funct Mater. 2019;29:1807434.

    Article  Google Scholar 

  51. Kimna C, Bauer MG, Lutz TM, Mansi S, Akyuz E, Doganyigit Z, et al. Multifunctional “Janus-Type” bilayer films combine broad-range tissue adhesion with guided drug release. Adv Funct Mater. 2022;32:2105721.

    Article  CAS  Google Scholar 

  52. Gregory DA, Tripathi L, Fricker ATR, Asare E, Orlando I, Raghavendran V, Roy I. Bacterial cellulose: a smart biomaterial with diverse applications. Mater Sci Eng R Rep. 2021;145: 100623.

    Article  Google Scholar 

  53. Chen S, John JV, Carthy AM, Carlson MA, Li X, Xie J. Fast transformation of 2D nanofiber membranes into pre-molded 3D scaffolds with biomimetic and oriented porous structure for biomedical applications. Appl Phys Rev. 2020;7:021406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Carvalho T, Ezazi NZ, Correia A, Vilela C, Santos HA, Freire CSR. Gelatin-lysozyme nanofibrils electrospun patches with improved mechanical, antioxidant, and bioresorbability properties for myocardial regeneration applications. Adv Funct Mater. 2022;32:2113390.

    Article  CAS  Google Scholar 

  55. Liu X, Wu M, Wang M, Hu Q, Liu J, Duan Y, Liu B. Direct synthesis of photosensitizable bacterial cellulose as engineered living material for skin wound repair. Adv Mater. 2022;34:e2109010.

    Article  PubMed  Google Scholar 

  56. Du XY, Li Q, Wu G, Chen S. Multifunctional micro/nanoscale fibers based on microfluidic spinning technology. Adv Mater. 2019;31:e1903733.

    Article  PubMed  Google Scholar 

  57. Xia Y, Yang H, Li S, Zhou S, Wang L, Tang Y, Cheng C, Haag R. Multivalent polyanionic 2D nanosheets functionalized nanofibrous stem cell-based neural scaffolds. Adv Funct Mater. 2021;31:2010145.

    Article  CAS  Google Scholar 

  58. Luo Z, Cui H, Guo J, Yao J, Fang X, Yan F, Wang B, Mao H. Poly(ionic liquid)/Ce-based antimicrobial nanofibrous membrane for blocking drug-resistance dissemination from MRSA-infected wounds. Adv Funct Mater. 2021;31:2100336.

    Article  CAS  Google Scholar 

  59. Wang Q, Feng Y, He M, Zhao W, Qiu L, Zhao C. A hierarchical janus nanofibrous membrane combining direct osteogenesis and osteoimmunomodulatory functions for advanced bone regeneration. Adv Funct Mater. 2020;31:2008906.

    Article  Google Scholar 

  60. Du J, Yao Y, Wang M, Su R, Li X, Yu J, Ding B. Programmable building of radially gradient nanofibrous patches enables deployment, bursting bearing capability, and stem cell recruitment. Adv Funct Mater. 2022;32:2109833.

    Article  CAS  Google Scholar 

  61. Roshanbinfar K, Vogt L, Ruther F, Roether JA, Boccaccini AR, Engel FB. Nanofibrous composite with tailorable electrical and mechanical properties for cardiac tissue engineering. Adv Funct Mater. 2020;30:1908612.

    Article  CAS  Google Scholar 

  62. Ceylan H, Urel M, Erkal TS, Tekinay AB, Dana A, Guler MO. Mussel inspired dynamic cross-linking of self-healing peptide nanofiber network. Adv Funct Mater. 2013;23:2081.

    Article  CAS  Google Scholar 

  63. Liu C, Wang S, Wang N, Yu J, Liu YT, Ding B. From 1D nanofibers to 3D nanofibrous aerogels: a marvellous evolution of electrospun SiO(2) nanofibers for emerging applications. Nano Lett. 2022;14:194.

    Article  CAS  Google Scholar 

  64. Xu B, Li A, Wang R, Zhang J, Ding Y, Pan D, Shen Z. Elastic janus film for wound dressings: unidirectional biofluid transport and effectively promoting wound healing. Adv Funct Mater. 2021;31:2105265.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (52273120, 21975019, T2222029, and U21A20396), CAS Project for Young Scientists in Basic Research (YSBR-012), Incubation Foundation of Beijing Institute for Stem Cell and Regenerative Medicine (2022FH125, 2023FH122) and, the China Scholarship Council (No. 202206465017), the Fundamental Research Funds for the Central Universities (FRFTP-20-019A2, FRF-BR-20-03B), and the Project was supported by the Science Fund of Shandong Laboratory of Advanced Materials and Green Manufacturing (Yantai) (AMGM2023F04), and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA16020802).

Author information

Author notes

  1. Zhe Huang, Heng An and Haitao Guo contributed equally to this work.

Authors and Affiliations

  1. School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Haidian District, Beijing, 100083, China

    Zhe Huang, Heng An, Zhen Gu & Yongqiang Wen

  2. State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing, 100101, China

    Haitao Guo, Shen Ji & Qi Gu

  3. Beijing Institute for Stem Cell and Regenerative Medicine, Chaoyang District, Beijing, 100101, China

    Qi Gu

  4. University of Chinese Academy of Sciences, Huairou District, Beijing, 100049, China

    Haitao Guo & Qi Gu

Authors
  1. Zhe Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heng An
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haitao Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shen Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qi Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhen Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yongqiang Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhen Gu or Yongqiang Wen.

Ethics declarations

Conflict of Interest

The authors declare no competing financial interest.

Ethical Approval

Animal experiments were approved by the Biological and Medical Ethics Committee of the Institute of Zoology, Chinese Academy of Sciences (ethics approval letter No. IOZ-IACUC-2020–087).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, Z., An, H., Guo, H. et al. An Asymmetric Natural Nanofiber with Rapid Temperature Responsive Detachability Inspired by Andrias davidianus for Full-Thickness Skin Wound Healing. Adv. Fiber Mater. 6, 473–488 (2024). https://doi.org/10.1007/s42765-023-00364-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42765-023-00364-7

Keywords

Search

Navigation