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Miniaturized electromechanical devices for the characterization of the biomechanics of deep tissue

Nature Biomedical Engineering volume 5, pages 759–771 (2021)Cite this article

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Abstract

Evaluating the biomechanics of soft tissues at depths well below their surface, and at high precision and in real time, would open up diagnostic opportunities. Here, we report the development and application of miniaturized electromagnetic devices, each integrating a vibratory actuator and a soft strain-sensing sheet, for dynamically measuring the Young’s modulus of skin and of other soft tissues at depths of approximately 1–8 mm, depending on the particular design of the sensor. We experimentally and computationally established the operational principles of the devices and evaluated their performance with a range of synthetic and biological materials and with human skin in healthy volunteers. Arrays of devices can be used to spatially map elastic moduli and to profile the modulus depth-wise. As an example of practical medical utility, we show that the devices can be used to accurately locate lesions associated with psoriasis. Compact electronic devices for the rapid and precise mechanical characterization of living tissues could be used to monitor and diagnose a range of health disorders.

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Fig. 1: Millimetre-scale electromechanical systems for sensing of soft-tissue elastic moduli.
Fig. 2: Experimental and simulation results of the device operation.
Fig. 3: Modulus measurements on hydrogels and on porcine and human skin.
Fig. 4: Designs for modulus sensing and depth profiling of multilayer samples.
Fig. 5: Measurements of skin lesions via miniaturized designs of the EMM sensors.
Fig. 6: Multiplexed arrays of EMM sensors for spatial mapping of tissue modulus.

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Data availability

The data supporting the results in this study are available within the paper and its Supplementary Information. The raw patient data are available from the authors, subject to approval from Northwestern University’s Institutional Review Board.

References

  1. Joodaki, H. & Panzer, M. B. Skin mechanical properties and modeling: a review. Proc. Inst. Mech. Eng. H 232, 323–343 (2018).

    Article  PubMed  Google Scholar 

  2. Pawlaczyk, M., Lelonkiewicz, M. & Wieczorowski, M. Age-dependent biomechanical properties of the skin. Postepy Dermatol. Alergol. 5, 302–306 (2013).

    Article  Google Scholar 

  3. Pandya, H. J., Chen, W., Goodell, L. A., Foran, D. J. & Desai, J. P. Mechanical phenotyping of breast cancer using MEMS: a method to demarcate benign and cancerous breast tissues. Lab Chip 14, 4523–4532 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Leblanc, N. et al. Durometer measurements of skin induration in venous disease. Dermatol. Surg. 23, 285–287 (1997).

    CAS  PubMed  Google Scholar 

  5. Khanna, D. et al. Standardization of the modified Rodnan skin score for use in clinical trials of systemic sclerosis. J. Scleroderma Relat. Disord. 2, 11–18 (2017).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  7. 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  PubMed  Google Scholar 

  8. 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  PubMed  Google Scholar 

  9. 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  PubMed  Google Scholar 

  10. Zheng, Y. & Mak, A. F. T. Effective elastic properties for lower limb soft tissues from manual indentation experiment. IEEE Trans. Rehabil. Eng. 7, 257–267 (1999).

    Article  CAS  PubMed  Google Scholar 

  11. 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  PubMed  Google Scholar 

  12. 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  PubMed  Google Scholar 

  13. Agache, P. G., Monneur, C., Leveque, J. L. & Rigal, J. D. Mechanical properties and Young’s modulus of human skin in vivo. Arch. Dermatol. Res. 269, 221–232 (1980).

    Article  CAS  PubMed  Google Scholar 

  14. 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 

  15. 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  PubMed  Google Scholar 

  16. Castera, L., Vilgrain, V. & Angulo, P. Noninvasive evaluation of NAFLD. Nat. Rev. Gastroenterol. Hepatol. 10, 666–675 (2013).

    Article  CAS  PubMed  Google Scholar 

  17. Manduca, A. et al. Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med. Image Anal. 5, 237–254 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Rogers, J. A., Someya, T. & Huang, Y. Materials and mechanics for stretchable electronics. Science 327, 1603–1607 (2010).

    Article  CAS  PubMed  Google Scholar 

  19. Huang, C.-T., Shen, C.-L., Tang, C.-F. & Chang, S.-H. A wearable yarn-based piezo-resistive sensor. Sens. Actuators A 141, 396–403 (2008).

    Article  CAS  Google Scholar 

  20. Dagdeviren, C. et al. Conformal piezoelectric systems for clinical and experimental characterization of soft tissue biomechanics. Nat. Mater. 14, 728–736 (2015).

    Article  CAS  PubMed  Google Scholar 

  21. Yu, X. et al. Needle-shaped ultrathin piezoelectric microsystem for guided tissue targeting via mechanical sensing. Nat. Biomed. Eng. 2, 165–172 (2018).

    Article  CAS  PubMed  Google Scholar 

  22. Lipomi, D. J. et al. Skin-like pressure and strain sensors based on transparent elastic films of carbon nanotubes. Nat. Nanotechnol. 6, 788–792 (2011).

    Article  CAS  PubMed  Google Scholar 

  23. Son, D. et al. Multifunctional wearable devices for diagnosis and therapy of movement disorders. Nat. Nanotechnol. 9, 397–404 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Yeh, W.-C. et al. Elastic modulus measurements of human liver and correlation with pathology. Ultrasound Med. Biol. 28, 467–474 (2002).

    Article  PubMed  Google Scholar 

  25. Yu, X. et al. Skin-integrated wireless haptic interfaces for virtual and augmented reality. Nature 575, 473–479 (2019).

    Article  CAS  PubMed  Google Scholar 

  26. He, W. et al. Study on Young’s modulus of thin films on Kapton by microtensile testing combined with dual DIC system. Surf. Coat. Technol. 308, 273–279 (2016).

    Article  CAS  Google Scholar 

  27. Kroner, E., Maboudian, R. & Arzt, E. Adhesion characteristics of PDMS surfaces during repeated pull-off force measurements. Adv. Eng. Mater. 12, 398–404 (2010).

    Article  CAS  Google Scholar 

  28. Zhang, Y. et al. Experimental and theoretical studies of serpentine microstructures bonded to prestrained elastomers for stretchable electronics. Adv. Funct. Mater. 24, 2028–2037 (2014).

    Article  CAS  Google Scholar 

  29. Swanson, E. C., Weathersby, E. J., Cagle, J. C. & Sanders, J. E. Evaluation of force sensing resistors for the measurement of interface pressures in lower limb prosthetics. J. Biomech. Eng. 141, 101009 (2019).

    Article  Google Scholar 

  30. 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  PubMed  Google Scholar 

  31. Kalra, A., Lowe, A. & Al-Jumaily, A. M. Mechanical behaviour of skin: a review. J. Mater. Sci. Eng. 5, 1000254 (2016).

    Google Scholar 

  32. Geerlings, M. et al. In vitro indentation to determine the mechanical properties of epidermis. J. Biomech. 44, 1176–1181 (2011).

    Article  Google Scholar 

  33. Wang, L. et al. Ultrasoft and highly stretchable hydrogel optical fibers for in vivo optogenetic modulations. Adv. Optical Mater. 6, 1800427 (2018).

    Article  CAS  Google Scholar 

  34. Sun, J. Y. et al. Highly stretchable and tough hydrogels. Nature 489, 133–136 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Garcia, M. & Angelini, T. E. A method for eliminating the need to know when contact is made with soft surfaces: data processing and error analysis. Biotribology 20, 100109 (2019).

    Article  Google Scholar 

  36. Leong, S. S. et al. Stiffness and anisotropy effect on shear wave elastography: a phantom and in vivo renal study. Ultrasound Med. Biol. 46, 34–45 (2019).

    Article  PubMed  Google Scholar 

  37. Pejovi-Mili, A., Brito, J. A., Gyorffy, J. & Chettle, D. R. Ultrasound measurements of overlying soft tissue thickness at four skeletal sites suitable for in vivo X-ray fluorescence. Med. Phys. 29, 2687–2691 (2002).

    Article  CAS  Google Scholar 

  38. Akkus, O., Oguz, A., Uzunlulu, M. & Kizilgul, M. Evaluation of skin and subcutaneous adipose tissue thickness for optimal insulin injection. J. Diabetes Metab. 3, 1000216 (2012).

    Article  CAS  Google Scholar 

  39. Kiliaridis, S. & Kälebo, P. Masseter muscle thickness measured by ultrasonography and its relation to facial morphology. J. Dent. Res. 70, 1262–1265 (1991).

    Article  CAS  PubMed  Google Scholar 

  40. Jain, S. M., Pandey, K., Lahoti, A. & Rao, P. K. Evaluation of skin and subcutaneous tissue thickness at insulin injection sites in Indian, insulin naive, type-2 diabetic adult population. Indian J. Endocrinol. Metab. 17, 864–870 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Pedersen, L. & Jemec, G. B. E. Mechanical properties and barrier function of the skin. Acta Derm. Venereol. 86, 308–311 (2006).

    Article  PubMed  Google Scholar 

  42. Laiacona, D. et al. Non-invasive in vivo quantification of human skin tension lines. Acta Biomaterialia 88, 141–148 (2019).

    Article  CAS  PubMed  Google Scholar 

  43. Jacquet, E., Josse, G., Khatyr, F. & Garcin, C. A new experimental method for measuring skin’s natural tension. Skin Res. Technol. 14, 1–7 (2008).

    PubMed  Google Scholar 

  44. Storchle, P. et al. Standardized ultrasound measurement of subcutaneous fat patterning: high reliability and accuracy in groups ranging from lean to obese. Ultrasound Med. Biol. 43, 427–438 (2017).

    Article  PubMed  Google Scholar 

  45. Yoshitake, Y., Takai, Y., Kanehisa, H. & Shinohara, M. Muscle shear modulus measured with ultrasound shear-wave elastography across a wide range of contraction intensity. Muscle Nerve 50, 103–113 (2014).

    Article  PubMed  Google Scholar 

  46. Shinohara, M., Sabra, K., Gennisson, J., Fink, M. & Tanter, M. Real-time visualization of muscle stiffness distribution with ultrasound shear wave imaging during muscle contraction. Muscle Nerve 42, 438–441 (2010).

    Article  PubMed  Google Scholar 

  47. Lewis-Beck, C., Abouzaid, S., Xie, L., Baser, O. & Kim, E. Analysis of the relationship between psoriasis symptom severity and quality of life, work productivity, and activity impairment among patients with moderate-to-severe psoriasis using structural equation modeling. Patient Prefer. Adherence 7, 199–205 (2013).

    PubMed  PubMed Central  Google Scholar 

  48. Kim, S. D., Huh, C. H., Seo, K. I., Suh, D. H. & Youn, J. I. Evaluation of skin surface hydration in Korean psoriasis patients: a possible factor influencing psoriasis. Clin. Exp. Dermatol. 27, 147–152 (2002).

    Article  CAS  PubMed  Google Scholar 

  49. Dobrev, H. In vivo study of skin mechanical properties in psoriasis vulgaris. Acta Derm. Venereol. 80, 263–266 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Chen, C. et al. Ultrasound assessment of skin thickness and stiffness: the correlation with histology and clinical score in systemic sclerosis. Arthritis Res. Ther. 43, 427–438 (2017).

    Google Scholar 

  51. Wang, L., Yan, F., Yang, Y., Xiang, X. & Qiu, L. Quantitative assessment of skin stiffness in localized scleroderma using ultrasound shear-wave elastography. Ultrasound Med. Biol. 43, 1339–1347 (2017).

    Article  PubMed  Google Scholar 

  52. Samani, A., Zubovits, J. & Plewes, D. Elastic moduli of normal and pathological human breast tissues: an inversion-technique-based investigation of 169 samples. Phys. Med. Biol. 52, 1565–1576 (2007).

    Article  PubMed  Google Scholar 

  53. Kim, T.-S. et al. Regional thickness of facial skin and superficial fat: application to the minimally invasive procedures. Clin. Anat. 32, 1008–1018 (2019).

    Article  PubMed  Google Scholar 

  54. Annaidh, A. N., Bruyère, K., Destrade, M., Gilchrist, M. D. & Otténio, M. Characterization of the anisotropic mechanical properties of excised human skin. J. Mech. Behav. Biomed. 5, 139–148 (2012).

    Article  Google Scholar 

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Acknowledgements

This work was supported by the Querrey/Simpson Institute for Bioelectronics at Northwestern University. We acknowledge the use of facilities in the Micro and Nanotechnology Laboratory for device fabrication and the Frederick Seitz Materials Research Laboratory for Advanced Science and Technology for device measurement at the University of Illinois at Urbana-Champaign. E.S., K.Y., D.L., J.Z. and X.Y. acknowledge the support from City University of Hong Kong (grant nos. 9610423, 9667199, 9667221), Research Grants Council of the Hong Kong Special Administrative Region (grant no. 21210820), and Shenzhen Science and Technology Innovation Commission (grant no. JCYJ20200109110201713). Z.X. acknowledges support from the National Natural Science Foundation of China (grant no. 12072057) and Fundamental Research Funds for the Central Universities (grant no. DUT20RC(3)032). S.M.W. acknowledges support of the MSIT (Ministry of Science and ICT), Korea, under the ICT Creative Consilience programme (IITP-2020-0-01821), supervised by the IITP (Institute for Information & Communications Technology Planning & Evaluation), and support by the Nano Material Technology Development Program (2020M3H4A1A03084600) through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT of Korea. Y.M. acknowledges the support from the Natural Science Foundation of China (nos. 51961145108 and 61975035) and the Science and Technology Commission of Shanghai Municipality (nos. 19XD1400600 and 20501130700). Y.H. acknowledges support from the NSF (CMMI1635443).

Author information

Author notes

  1. These authors contributed equally: Enming Song, Zhaoqian Xie, Wubin Bai, Haiwen Luan.

Authors and Affiliations

  1. Institute of Optoelectronics, Fudan University, Shanghai, China

    Enming Song

  2. Department of Biomedical Engineering, City University of Hong Kong, Hong Kong, China

    Enming Song, Kuanming Yao, Dengfeng Li, Jingkun Zhou & Xinge Yu

  3. State Key Laboratory of Structural Analysis for Industrial Equipment, Department of Engineering Mechanics, Dalian University of Technology, Dalian, China

    Zhaoqian Xie & Xu Guo

  4. Ningbo Institute of Dalian University of Technology, Ningbo, China

    Zhaoqian Xie & Xu Guo

  5. Querrey Simpson Institute for Bioelectronics, Northwestern University, Evanston, IL, USA

    Wubin Bai, Haiwen Luan, Huang-Yu Chen, Surabhi Madhvapathy, Mengdi Han, Daniel J. Myers, Shuai Xu, Jan-Kai Chang, Yonggang Huang & John A. Rogers

  6. Department of Applied Physical Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Wubin Bai

  7. Unmanned System Research Institute, Northwestern Polytechnical University, Xi’an, China

    Bowen Ji

  8. Department of Aerospace Engineering, The Pennsylvania State University, University Park, PA, USA

    Xin Ning

  9. Frederick Seitz Materials Research Laboratory, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Yu Xia, Janice Mihyun Baek, Yujin Lee & Jae-Hwan Kim

  10. Department of Mechanical Engineering, Northwestern University, Evanston, IL, USA

    Raudel Avila, Yonggang Huang & John A. Rogers

  11. Department of Electrical and Computer Engineering, Sungkyunkwan University, Suwon, Republic of Korea

    Sang Min Won

  12. Department of Materials Science, State Key Laboratory of ASIC and Systems, Fudan University, Shanghai, China

    Xinyuan Zhang & Yongfeng Mei

  13. Department of Dermatology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    Daniel J. Myers & Shuai Xu

  14. Department of Civil and Environmental Engineering, Northwestern University, Evanston, IL, USA

    Yonggang Huang

  15. Department of Materials Science and Engineering, Northwestern University, Evanston, IL, USA

    Yonggang Huang & John A. Rogers

  16. Department of Biomedical Engineering, Northwestern University, Evanston, IL, USA

    John A. Rogers

  17. Department of Neurological Surgery, Northwestern University, Evanston, IL, USA

    John A. Rogers

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Contributions

E.S., Z.X., W.B., X.Y., Y.H. and J.A.R. designed the research. E.S., Z.X., W.B., H.L., X.N., Y.X., J.M.B., Y.L., H.-Y.C., J.-H.K., S.M., S.M.W., X.Z., D.J.M., M.H., S.X., J.-K.C., X.Y., Y.H. and J.A.R. performed the research. E.S., Z.X., W.B., B.J., R.A., K.Y., D.L., J.Z. Y.M., X.G., J.-K.C., X.Y., Y.H. and J.A.R. analysed the data. Z.X., E.S., B.J., R.A., X.G., Y.H. and J.A.R. performed structural designs and mechanical modelling. E.S., Z.X., W.B., X.Y., Y.H. and J.A.R. wrote the paper.

Corresponding authors

Correspondence to Jan-Kai Chang, Xinge Yu, Yonggang Huang or John A. Rogers.

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The authors declare no competing interests.

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Peer review information Nature Biomedical Engineering thanks Jianyong Ouyang, Levent Beker and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary methods, figures, tables and video captions.

Reporting Summary

Supplementary Video 1

Vibration of a magnet in slow motion at 50 Hz and sine-wave voltage amplitude of 5 V, captured using a high-speed camera.

Supplementary Video 2

Visualization of the vibration of a magnet in slow motion at 50 Hz on artificial skin, with a travelling amplitude of ~300 μm.

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Song, E., Xie, Z., Bai, W. et al. Miniaturized electromechanical devices for the characterization of the biomechanics of deep tissue. Nat Biomed Eng 5, 759–771 (2021). https://doi.org/10.1038/s41551-021-00723-y

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