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Conformal piezoelectric systems for clinical and experimental characterization of soft tissue biomechanics

Abstract

Mechanical assessment of soft biological tissues and organs has broad relevance in clinical diagnosis and treatment of disease. Existing characterization methods are invasive, lack microscale spatial resolution, and are tailored only for specific regions of the body under quasi-static conditions. Here, we develop conformal and piezoelectric devices that enable in vivo measurements of soft tissue viscoelasticity in the near-surface regions of the epidermis. These systems achieve conformal contact with the underlying complex topography and texture of the targeted skin, as well as other organ surfaces, under both quasi-static and dynamic conditions. Experimental and theoretical characterization of the responses of piezoelectric actuator–sensor pairs laminated on a variety of soft biological tissues and organ systems in animal models provide information on the operation of the devices. Studies on human subjects establish the clinical significance of these devices for rapid and non-invasive characterization of skin mechanical properties.

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Figure 1: Thin, compliant modulus sensor (CMS) based on nanoribbons of PZT in arrays of mechanical actuators and sensors.
Figure 2: Experimental and theoretical analysis of the device operation.
Figure 3: Modulus measurements on ex vivo female and male skin samples as a function of time before and after application of a moisturizing lotion.
Figure 4: CMS mapping of pathologies located on various body regions.
Figure 5: Spatial mapping with a rotatable CMS system and in vivo evaluations on a cancer patient (basal cell carcinoma).
Figure 6: Ex vivo CMS measurements on bovine organs.

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References

  1. Elias, P. M. Stratum corneum defensive functions: An integrated view. J. Gen. Intern. Med. 20, 183–200 (2005).

    Google Scholar 

  2. Charkoudian, N. Skin blood flow in adult human thermoregulation: How it works, when it does not, and why. Mayo Clin. Proc. 78, 603–612 (2003).

    Article  Google Scholar 

  3. Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241–254 (2005).

    Article  CAS  Google Scholar 

  4. Friberg, S. E. Micelles, microemulsions, liquid crystals, and the structure of stratum corneum lipids. J. Soc. Cosmet. Chem. 41, 155–171 (1990).

    CAS  Google Scholar 

  5. Reiger, M. M. & Deem, D. Skin moisturizers. II. The efects of cosmetic ingredients on human SC. J. Soc. Cosmet. Chem. 25, 253–262 (1974).

    Google Scholar 

  6. Magnenat-Thalmann, N. et al. A computational skin model: Fold and wrinkle formation. IEEE Trans. Inf. Technol. Biomed. 6, 317–323 (2002).

    Article  Google Scholar 

  7. Batisse, D., Bazin, R. & Baldeweck, T. Influence of age on the wrinkling capacities of skin. Skin Res. Technol. 8, 148–154 (2002).

    Article  Google Scholar 

  8. Alexander, H. & Cook, T. Variations with age in the mechanical properties of human skin in vivo. J. Tissue Viabil. 16, 6–11 (2006).

    Article  CAS  Google Scholar 

  9. Leveque, J. L., Rigal, J. de, Agache, P. G. & Monneur, C. Influence of ageing on the in vivo extensibility of human skin at a low stress. Arch. Dermatol. Res. 269, 127–135 (1980).

    Article  CAS  Google Scholar 

  10. Li, C., Guan, G., Reif, R., Huang, Z. & Wang, R. K. Determining elastic properties of skin by measuring surface waves from an impulse mechanical stimulus using phase-sensitive optical coherence tomography. J. R. Soc. Interface 9, 831–841 (2012).

    Article  Google Scholar 

  11. Hendriks, F. M. Mechanical Behaviour of Human Epidermal and Dermal Layers In Vivo (Technische Universiteit Eindhoven, 2005).

    Google Scholar 

  12. Diridollou, S. et al. Sex and site dependent variations in thickness and mechanical properties of human skin in vivo. Int. J. Cosmet. Sci. 22, 421–435 (2000).

    Article  CAS  Google Scholar 

  13. Kashibuchi, N., Hirai, Y., O’Goshi, K. & Tagami, H. Three-dimensional analyses of individual corneocytes with atomic force microscope: Morphological changes related to age, location and to the pathologic skin conditions. Skin Res. Technol. 8, 203–211 (2002).

    Article  Google Scholar 

  14. Lulevich, V., Zink, T., Chen, H-Y., Liu, F-T. & Liu, G. Cell mechanics using atomic force microscopy-based single-cell compression. Langmuir 22, 8151–8155 (2006).

    Article  CAS  Google Scholar 

  15. Elias, P. M. Structure and function of the stratum corneum permeability barrier. Drug Dev. Res. 13, 97–105 (1988).

    Article  CAS  Google Scholar 

  16. Lumpkin, E. A. & Caterina, M. J. Mechanisms of sensory transduction in the skin. Nature 445, 858–865 (2007).

    Article  CAS  Google Scholar 

  17. Bommannan, D., Potts, R. O. & Guy, R. H. Examination of stratum corneum barrier function in vivo by infrared spectroscopy. J. Invest. Dermatol. 95, 403–408 (1990).

    Article  CAS  Google Scholar 

  18. Diridollou, S. et al. In vivo model of the mechanical properties of the human skin under suction. Skin Res. Technol. 6, 214–221 (2000).

    Article  Google Scholar 

  19. Hendriks, F. M. et al. A numerical-experimental method to characterize the non-linear mechanical behaviour of human skin. Skin Res. Technol. 9, 274–283 (2003).

    Article  CAS  Google Scholar 

  20. Sanders, R. Torsional elasticity of human skin in vivo. Pflüg. Arch. 342, 255–260 (1973).

    Article  CAS  Google Scholar 

  21. Berardesca, E., de Rigal, J., Leveque, J. L. & Maibach, H. I. In vivo biophysical characterization of skin physiological differences in races. Dermatology 182, 89–93 (1991).

    Article  CAS  Google Scholar 

  22. Sugihara, T., Ohura, T., Homma, K. & Igawa, H. H. The extensibility in human skin: Variation according to age and site. Br. J. Plast. Surg. 44, 418–422 (1991).

    Article  CAS  Google Scholar 

  23. Fischer-Cripps, A. C. Critical review of analysis and interpretation of nanoindentation test data. Surf. Coat. Technol. 200, 4153–4165 (2006).

    Article  CAS  Google Scholar 

  24. Gennisson, J. L. et al. Assessment of elastic parameters of human skin using dynamic elastography. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51, 980–989 (2004).

    Article  Google Scholar 

  25. Dagdeviren, C. et al. Conformable amplified lead zirconate titanate sensors with enhanced piezoelectric response for cutaneous pressure monitoring. Nature Commun. 5, 4496 (2014).

    Article  CAS  Google Scholar 

  26. Christensen, R. Theory of Viscoelasticity: An Introduction (Elsevier, 1982).

    Google Scholar 

  27. Then, C., Vogl, T. J. & Silber, G. Method for characterizing viscoelasticity of human gluteal tissue. J. Biomech. 45, 1252–1258 (2012).

    Article  CAS  Google Scholar 

  28. Cui, T., Lin, C-W., Chien, C. H., Chao, Y. J. & Van Zee, J. W. Service life estimation of liquid silicone rubber seals in polymer electrolyte membrane fuel cell environment. J. Power Sources 196, 1216–1221 (2011).

    Article  CAS  Google Scholar 

  29. Cheng, H. et al. A viscoelastic model for the rate effect in transfer printing. J. Appl. Mech. 80, 041019–041019 (2013).

    Article  Google Scholar 

  30. Lin, I-K. et al. Viscoelastic mechanical behavior of soft microcantilever-based force sensors. Appl. Phys. Lett. 93, 251907 (2008).

    Article  Google Scholar 

  31. Barel, A. O., Lambrecht, R. & Clarys, P. Mechanical function of the skin: State of the art. Curr. Probl. Dermatol. 26, 69–83 (1998).

    Article  CAS  Google Scholar 

  32. Silver, F. H., Seehra, G. P., Freeman, J. W. & DeVore, D. Viscoelastic properties of young and old human dermis: A proposed molecular mechanism for elastic energy storage in collagen and elastin. J. Appl. Polym. Sci. 86, 1978–1985 (2002).

    Article  CAS  Google Scholar 

  33. Stark, H. L. Directional variations in the extensibility of human skin. Br. J. Plast. Surg. 30, 105–114 (1977).

    Article  CAS  Google Scholar 

  34. Ryu, H. S., Joo, Y. H., Kim, S. O., Park, K. C. & Youn, S. W. Influence of age and regional differences on skin elasticity as measured by the Cutometer. Skin Res. Technol. 14, 354–358 (2008).

    Article  Google Scholar 

  35. Escoffier, C. et al. Age-related mechanical properties of human skin: An in vivo study. J. Invest. Dermatol. 93, 353–357 (1989).

    Article  CAS  Google Scholar 

  36. Grahame, R. & Holt, P. J. L. The influence of ageing on the in vivo elasticity of human skin. Gerontology 15, 121–139 (1969).

    Article  CAS  Google Scholar 

  37. Pawlaczyk, M., Lelonkiewicz, M. & Wieczorowski, M. Age-dependent biomechanical properties of the skin. Postepy Dermatol. Alergol. 30, 302–306 (2013).

    Article  Google Scholar 

  38. Luengo, & Galliano, A. Scanning Probe Microscopy for Industrial Applications: Nanomechanical Characterization Vol. 12 (John Wiley, 2013).

    Google Scholar 

  39. Richter, T., Müller, J. H., Schwarz, U. D., Wepf, R. & Wiesendanger, R. Investigation of the swelling of human skin cells in liquid media by tapping mode scanning force microscopy. Appl. Phys. A 72, S125–S128 (2001).

    Article  Google Scholar 

  40. Xu, W. et al. Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLoS ONE 7, e46609 (2012).

    Article  CAS  Google Scholar 

  41. Nguyen, T. D. et al. Piezoelectric nanoribbons for monitoring cellular deformations. Nature Nanotech. 7, 587–593 (2012).

    Article  CAS  Google Scholar 

  42. Fernandez-Teran, M. A. & Hurle, J. M. Myocardial fiber architecture of the human heart ventricles. Anat. Rec. 204, 137–147 (1982).

    Article  CAS  Google Scholar 

  43. Dagdeviren, C. et al. Conformal piezoelectric energy harvesting and storage from motions of the heart, lung, and diaphragm. Proc. Natl Acad. Sci. USA 111, 1927–1932 (2014).

    Article  CAS  Google Scholar 

  44. Calle, M., Lozano, A. E., de Abajo, J., de la Campa, J. G. & Álvarez, C. Design of gas separation membranes derived of rigid aromatic polyimides. 1. Polymers from diamines containing di-tert-butyl side groups. J. Membr. Sci. 365, 145–153 (2010).

    Article  CAS  Google Scholar 

  45. Dagdeviren, C. et al. Transient, biocompatible electronics and energy harvesters based on ZnO. Small 9, 3398–3404 (2013).

    Article  CAS  Google Scholar 

  46. Balooch, G. et al. TGF-β regulates the mechanical properties and composition of bone matrix. Proc. Natl Acad. Sci. USA 102, 18813–18818 (2005).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Research supported by the US Department of Energy, Office of Basic Energy Sciences, Division of Materials Sciences and Engineering under Award # DE-FG02-07ER46471, through the Frederick Seitz Materials Research Laboratory at the University of Illinois at Urbana-Champaign. C.D. thanks Cavit Dagdeviren and YongAn Huang for their useful suggestions in device design, and V. Merkle for her assistance during DMA tests of ex vivo organ tissues. M.M. acknowledge support from the European Union (ERDF) and the Free State of Saxony via the ESF project 100098212 InnoMedTec. M.M. thanks G. Cuniberti from TU Dresden for fruitful discussions and for supporting an internship by J.A.R.

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Contributions

C.D. and J.A.R. designed the research; C.D., P.J., G.B., K.U., O.G., P.L.T., J.R.C., M.M., M.J.S. and J.A.R. performed the research; C.D., Y.Shi., R.C.W., Y.H. and J.A.R. contributed new reagents/analytic tools; Y.Su assisted in designing the device structure; C.D., Y.Shi, P.J., G.B., P.L.T., J.R.C., A.S.T., M.J.S., Y.H. and J.A.R. analysed data; and C.D., Y.Shi, R.G., G.B., M.J.S., Y.H. and J.A.R. wrote the paper.

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Correspondence to John A. Rogers.

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Dagdeviren, C., Shi, Y., Joe, P. et al. Conformal piezoelectric systems for clinical and experimental characterization of soft tissue biomechanics. Nature Mater 14, 728–736 (2015). https://doi.org/10.1038/nmat4289

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