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Research Article

Microstructured barbs on the North American porcupine quill enable easy tissue penetration and difficult removal

Woo Kyung Cho, James A. Ankrum, Dagang Guo, Shawn A. Chester, Seung Yun Yang, Anurag Kashyap, Georgina A. Campbell, Robert J. Wood, Ram K. Rijal, Rohit Karnik, Robert Langer, and Jeffrey M. Karp
  1. aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
  2. bHarvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA 02139;
  3. cDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139;
  4. dCenter for Biomaterials and Nano-Coating Research, State Key Laboratory for Mechanical Behavior of Materials, School of Material Science and Engineering, Xi´an Jiaotong University, Xi´an City, Shannxi Providence, 710049, China;
  5. eDepartment of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139;
  6. fHarvard Stem Cell Institute, Cambridge, MA 02138;
  7. gDepartment of Material Engineering, Trinity College, Oxford OX1 3BH, United Kingdom;
  8. hSchool of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138; and
  9. iDepartment of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139

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PNAS December 26, 2012 109 (52) 21289-21294; https://doi.org/10.1073/pnas.1216441109
Woo Kyung Cho
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
bHarvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA 02139;
cDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139;
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James A. Ankrum
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
bHarvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA 02139;
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Dagang Guo
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
dCenter for Biomaterials and Nano-Coating Research, State Key Laboratory for Mechanical Behavior of Materials, School of Material Science and Engineering, Xi´an Jiaotong University, Xi´an City, Shannxi Providence, 710049, China;
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Shawn A. Chester
eDepartment of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139;
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Seung Yun Yang
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
bHarvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA 02139;
fHarvard Stem Cell Institute, Cambridge, MA 02138;
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Anurag Kashyap
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
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Georgina A. Campbell
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
gDepartment of Material Engineering, Trinity College, Oxford OX1 3BH, United Kingdom;
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Robert J. Wood
hSchool of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138; and
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Ram K. Rijal
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
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Rohit Karnik
eDepartment of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139;
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Robert Langer
bHarvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA 02139;
cDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139;
iDepartment of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139
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  • For correspondence: jkarp@rics.bwh.harvard.edu rlanger@mit.edu
Jeffrey M. Karp
aDivision of Biomedical Engineering, Department of Medicine, Center for Regenerative Therapeutics, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115;
bHarvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA 02139;
fHarvard Stem Cell Institute, Cambridge, MA 02138;
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  • For correspondence: jkarp@rics.bwh.harvard.edu rlanger@mit.edu
  1. Edited by David A. Weitz, Harvard University, Cambridge, MA, and approved November 2, 2012 (received for review September 20, 2012)

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Abstract

North American porcupines are well known for their specialized hairs, or quills that feature microscopic backward-facing deployable barbs that are used in self-defense. Herein we show that the natural quill’s geometry enables easy penetration and high tissue adhesion where the barbs specifically contribute to adhesion and unexpectedly, dramatically reduce the force required to penetrate tissue. Reduced penetration force is achieved by topography that appears to create stress concentrations along regions of the quill where the cross sectional diameter grows rapidly, facilitating cutting of the tissue. Barbs located near the first geometrical transition zone exhibit the most substantial impact on minimizing the force required for penetration. Barbs at the tip of the quill independently exhibit the greatest impact on tissue adhesion force and the cooperation between barbs in the 0–2 mm and 2–4 mm regions appears critical to enhance tissue adhesion force. The dual functions of barbs were reproduced with replica molded synthetic polyurethane quills. These findings should serve as the basis for the development of bio-inspired devices such as tissue adhesives or needles, trocars, and vascular tunnelers where minimizing the penetration force is important to prevent collateral damage.

  • biomimicry
  • medical tape
  • microneedle
  • sutures
  • staples

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: jkarp{at}rics.bwh.harvard.edu or rlanger{at}mit.edu.
  • Author contributions: W.K.C., J.A.A., R.L., and J.M.K. designed research; W.K.C., J.A.A., D.G., S.A.C., S.Y.Y., A.K., G.A.C., and R.K.R. performed research; W.K.C., J.A.A., D.G., S.A.C., S.Y.Y., R.J.W., R.K., and J.M.K. analyzed data; and W.K.C., J.A.A., S.A.C., R.K., R.L., and J.M.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1216441109/-/DCSupplemental.

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Barbs enhance tissue penetration and adhesion
Woo Kyung Cho, James A. Ankrum, Dagang Guo, Shawn A. Chester, Seung Yun Yang, Anurag Kashyap, Georgina A. Campbell, Robert J. Wood, Ram K. Rijal, Rohit Karnik, Robert Langer, Jeffrey M. Karp
Proceedings of the National Academy of Sciences Dec 2012, 109 (52) 21289-21294; DOI: 10.1073/pnas.1216441109

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Barbs enhance tissue penetration and adhesion
Woo Kyung Cho, James A. Ankrum, Dagang Guo, Shawn A. Chester, Seung Yun Yang, Anurag Kashyap, Georgina A. Campbell, Robert J. Wood, Ram K. Rijal, Rohit Karnik, Robert Langer, Jeffrey M. Karp
Proceedings of the National Academy of Sciences Dec 2012, 109 (52) 21289-21294; DOI: 10.1073/pnas.1216441109
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