Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Catheter-integrated soft multilayer electronic arrays for multiplexed sensing and actuation during cardiac surgery

Nature Biomedical Engineering volume 4, pages 997–1009 (2020)Cite this article

Subjects

This article has been updated

Abstract

The rigidity and relatively primitive modes of operation of catheters equipped with sensing or actuation elements impede their conformal contact with soft-tissue surfaces, limit the scope of their uses, lengthen surgical times and increase the need for advanced surgical skills. Here, we report materials, device designs and fabrication approaches for integrating advanced electronic functionality with catheters for minimally invasive forms of cardiac surgery. By using multiphysics modelling, plastic heart models and Langendorff animal and human hearts, we show that soft electronic arrays in multilayer configurations on endocardial balloon catheters can establish conformal contact with curved tissue surfaces, support high-density spatiotemporal mapping of temperature, pressure and electrophysiological parameters and allow for programmable electrical stimulation, radiofrequency ablation and irreversible electroporation. Integrating multimodal and multiplexing capabilities into minimally invasive surgical instruments may improve surgical performance and patient outcomes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Multimodal, multiplexed soft sensors and actuators for minimally invasive surgery.
Fig. 2: Design, assembly and characterization of the array of 3D pressure sensors.
Fig. 3: Therapeutic functions.
Fig. 4: Simultaneous, multimodal operation.
Fig. 5: Multifunctionality of instrumented balloon catheters demonstrated with Langendorff rabbit heart models.
Fig. 6: Endocardial electrophysiological studies on Langendorff human heart models.

Similar content being viewed by others

Data availability

The main data supporting the results in this study are available within the paper and its Supplementary Information. Source data for the figures are available from figshare with the identifier https://doi.org/10.6084/m9.figshare.12631835.

Code availability

The custom MATLAB software for data analysis can be downloaded from https://github.com/optocardiography.

Change history

  • 10 September 2020

    The Peer Review file originally published with this Article was an old version; the updated file is now available.

References

  1. Biere, S. S. et al. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 379, 1887–1892 (2012).

    PubMed  Google Scholar 

  2. Bacha, E. & Kalfa, D. Minimally invasive paediatric cardiac surgery. Nat. Rev. Cardiol. 11, 24–34 (2014).

    PubMed  Google Scholar 

  3. Martens, T. P. et al. Percutaneous cell delivery into the heart using hydrogels polymerizing in situ. Cell Transplant. 18, 297–304 (2009).

    PubMed  PubMed Central  Google Scholar 

  4. Oxley, T. J. et al. Minimally invasive endovascular stent-electrode array for high-fidelity, chronic recordings of cortical neural activity. Nat. Biotechnol. 34, 320–327 (2016).

    CAS  PubMed  Google Scholar 

  5. Kim, D.-H. et al. Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics. Nat. Mater. 9, 511–517 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Dukkipati, S. R. et al. Visual balloon-guided point-by-point ablation: reliable, reproducible, and persistent pulmonary vein isolation. Circ. Arrhythm. Electrophysiol. 3, 266–273 (2010).

    PubMed  Google Scholar 

  7. Wazni, O., Wilkoff, B. & Saliba, W. Catheter ablation for atrial fibrillation. N. Engl. J. Med. 365, 2296–2304 (2011).

    CAS  PubMed  Google Scholar 

  8. Kim, D.-H. et al. Materials for multifunctional balloon catheters with capabilities in cardiac electrophysiological mapping and ablation therapy. Nat. Mater. 10, 316–323 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Roche, E. T. et al. A light-reflecting balloon catheter for atraumatic tissue defect repair. Sci. Transl. Med. 7, 306ra149 (2015).

    PubMed  Google Scholar 

  10. Lee, S. P. et al. Catheter-based systems with integrated stretchable sensors and conductors in cardiac electrophysiology. Proc. IEEE 103, 682–689 (2015).

    CAS  Google Scholar 

  11. Kim, Y., Parada, G. A., Liu, S. & Zhao, X. Ferromagnetic soft continuum robots. Sci. Robot. 4, eaax7329 (2019).

    Google Scholar 

  12. Ashammakhi, N. et al. Minimally invasive and regenerative therapeutics. Adv. Mater. 31, 1804041 (2019).

    Google Scholar 

  13. Fang, H. et al. Capacitively coupled arrays of multiplexed flexible silicon transistors for long-term cardiac electrophysiology. Nat. Biomed. Eng. 1, 0038 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Hua, Q. et al. Skin-inspired highly stretchable and conformable matrix networks for multifunctional sensing. Nat. Commun. 9, 244 (2018).

    PubMed  PubMed Central  Google Scholar 

  15. Chung, H. U. et al. Binodal, wireless epidermal electronic systems with in-sensor analytics for neonatal intensive care. Science 363, eaau0780 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Sharma, T., Aroom, K., Naik, S., Gill, B. & Zhang, J. X. Flexible thin-film PVDF-TrFE based pressure sensor for smart catheter applications. Ann. Biomed. Eng. 41, 744–751 (2013).

    PubMed  Google Scholar 

  17. Klinker, L. et al. Balloon catheters with integrated stretchable electronics for electrical stimulation, ablation and blood flow monitoring. Extrem. Mech. Lett. 3, 45–54 (2015).

    Google Scholar 

  18. Lee, K. et al. Microneedle drug eluting balloon for enhanced drug delivery to vascular tissue. J. Control. Release 321, 174–183 (2020).

    CAS  PubMed  Google Scholar 

  19. Liu, Z. et al. Transcatheter self-powered ultrasensitive endocardial pressure sensor. Adv. Funct. Mater. 29, 1807560 (2019).

    Google Scholar 

  20. Bergmann, O. et al. Dynamics of cell generation and turnover in the human heart. Cell 161, 1566–1575 (2015).

    CAS  PubMed  Google Scholar 

  21. Xu, S. et al. Assembly of micro/nanomaterials into complex, three-dimensional architectures by compressive buckling. Science 347, 154–159 (2015).

    CAS  PubMed  Google Scholar 

  22. Wu, J.-F. Scanning approaches of 2-D resistive sensor arrays: a review. IEEE Sens. J. 17, 914–925 (2016).

    Google Scholar 

  23. Gustafsson, S. E. Transient plane source techniques for thermal conductivity and thermal diffusivity measurements of solid materials. Rev. Sci. Instrum. 62, 797–804 (1991).

    CAS  Google Scholar 

  24. Webb, R. C. et al. Ultrathin conformal devices for precise and continuous thermal characterization of human skin. Nat. Mater. 12, 938–944 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Krishnan, S. R. et al. Epidermal electronics for noninvasive, wireless, quantitative assessment of ventricular shunt function in patients with hydrocephalus. Sci. Transl. Med. 10, eaat8437 (2018).

    PubMed  Google Scholar 

  26. Yokoyama, K. et al. Novel contact force sensor incorporated in irrigated radiofrequency ablation catheter predicts lesion size and incidence of steam pop and thrombus. Circ. Arrhythm. Electrophysiol. 1, 354–362 (2008).

    PubMed  Google Scholar 

  27. Ariyarathna, N., Kumar, S., Thomas, S. P., Stevenson, W. G. & Michaud, G. F. Role of contact force sensing in catheter ablation of cardiac arrhythmias: evolution or history repeating itself? JACC Clin. Electrophysiol. 4, 707–723 (2018).

    PubMed  Google Scholar 

  28. Yousef, H., Boukallel, M. & Althoefer, K. Tactile sensing for dexterous in-hand manipulation in robotics—a review. Sens. Actuator A 167, 171–187 (2011).

    CAS  Google Scholar 

  29. Costa, P., Ribeiro, S. & Lanceros-Mendez, S. Mechanical vs. electrical hysteresis of carbon nanotube/styrene–butadiene–styrene composites and their influence in the electromechanical response. Compos. Sci. Technol. 109, 1–5 (2015).

    CAS  Google Scholar 

  30. Jang, K.-I. et al. Self-assembled three dimensional network designs for soft electronics. Nat. Commun. 8, 15894 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Dewire, J. & Calkins, H. State-of-the-art and emerging technologies for atrial fibrillation ablation. Nat. Rev. Cardiol. 7, 129–138 (2010).

    PubMed  Google Scholar 

  32. Maor, E. et al. Pulsed electric fields for cardiac ablation and beyond: A state-of-the-art review. Heart Rhythm 16, 1112–1120 (2019).

    PubMed  Google Scholar 

  33. Hjouj, M. & Rubinsky, B. Magnetic resonance imaging characteristics of nonthermal irreversible electroporation in vegetable tissue. J. Membr. Biol. 236, 137–146 (2010).

    CAS  PubMed  Google Scholar 

  34. Ramer, O. Integrated optic electrooptic modulator electrode analysis. IEEE J. Quantum Electron. 18, 386–392 (1982).

    Google Scholar 

  35. Nath, S., DiMarco, J. P. & Haines, D. E. Basic aspects of radiofrequency catheter ablation. J. Cardiovasc. Electrophysiol. 5, 863–876 (1994).

    CAS  PubMed  Google Scholar 

  36. McClintock, R. Strain gauge calibration device for extreme temperatures. Rev. Sci. Instrum. 30, 715–718 (1959).

    Google Scholar 

  37. Hur, S.-G., Kim, D.-J., Kang, B.-D. & Yoon, S.-G. Effect of the deposition temperature on temperature coefficient of resistance in CuNi thin film resistors. J. Vac. Sci. Technol. B 22, 2698–2701 (2004).

    CAS  Google Scholar 

  38. Pikul, J. et al. Stretchable surfaces with programmable 3D texture morphing for synthetic camouflaging skins. Science 358, 210–214 (2017).

    CAS  PubMed  Google Scholar 

  39. Gloschat, C. et al. RHYTHM: an open source imaging toolkit for cardiac panoramic optical mapping. Sci. Rep. 8, 2921 (2018).

    PubMed  PubMed Central  Google Scholar 

  40. Aras, K. K., Faye, N. R., Cathey, B. & Efimov, I. R. Critical volume of human myocardium necessary to maintain ventricular fibrillation. Circ. Arrhythm. Electrophysiol. 11, e006692 (2018).

    PubMed  Google Scholar 

  41. Rodenhauser, A. et al. PFEIFER: Preprocessing framework for electrograms intermittently fiducialized from experimental recordings. J. Open Source Softw. 3, 472 (2018).

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I.R.E. and J.A.R. acknowledge support from the Leducq Foundation project RHYTHM and R01-HL141470. This project was supported by the National Institute of General Medical Sciences of the National Institutes of Health under grant nos. P41 GM103545 and R24 GM136986, and the Nora Eccles Harrison Cardiovascular Research and Training Institute (CVRTI). K.A. acknowledges support from the National Institutes of Health K99-HL148523-01A1. X.C. acknowledges support from National Key R&D Program of China (grant 2018YFA0108100) and China Scholarship Council. This work made use of the NUFAB facility of Northwestern University’s NUANCE Center, which has received support from the Soft and Hybrid Nanotechnology Experimental (SHyNE) Resource (NSF ECCS-1542205); the MRSEC program (NSF DMR-1720139) at the Materials Research Center; the International Institute for Nanotechnology (IIN); the Keck Foundation; and the State of Illinois, through the IIN.

Author information

Author notes

  1. These authors contributed equally: Mengdi Han, Lin Chen, Kedar Aras.

Authors and Affiliations

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

    Mengdi Han, Hangbo Zhao, Bohan Sun, Wubin Bai, Yuhang Ma, Wei Lu, Enming Song, Clifford Liu, Jeffrey B. Model, Roozbeh Ghaffari, Yonggang Huang & John A. Rogers

  2. Departments of Civil and Environmental Engineering, Northwestern University, Evanston, IL, USA

    Lin Chen, Kan Li & Yonggang Huang

  3. State Key Laboratory for Mechanical Behavior of Materials, School of Materials Science and Engineering, Xi’an Jiaotong University, Xi’an, China

    Lin Chen & Guanjun Yang

  4. Department of Biomedical Engineering, The George Washington University, Washington, DC, USA

    Kedar Aras, Ndeye Rokhaya Faye & Igor R. Efimov

  5. Key Laboratory of Mechanism Theory and Equipment Design of Ministry of Education, School of Mechanical Engineering, Tianjin University, Tianjin, China

    Cunman Liang

  6. Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, China

    Xuexian Chen

  7. Department of Aerospace and Mechanical Engineering, University of Southern California, Los Angeles, CA, USA

    Hangbo Zhao

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

    Kan Li, Quansan Yang, Yonggang Huang & John A. Rogers

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

    Kan Li, Wubin Bai, Yonggang Huang & John A. Rogers

  10. Department of Engineering, University of Cambridge, Cambridge, UK

    Kan Li

  11. Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD, USA

    Bohan Sun

  12. Frederick Seitz Materials Research Laboratory, University of Illinois at Urbana–Champaign Urbana, Champaign, IL, USA

    Jae-Hwan Kim & John A. Rogers

  13. Department of Electrical and Computer Engineering, University of Illinois at Urbana–Champaign Urbana, Champaign, IL, USA

    Jae-Hwan Kim

  14. School of Chemical Engineering and Technology, Tianjin University, Tianjin, China

    Yuhang Ma

  15. Department of Chemistry, University of Illinois at Urbana–Champaign Urbana, Champaign, IL, USA

    Janice Mihyun Baek & Yujin Lee

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

    Roozbeh Ghaffari & John A. Rogers

  17. Department of Surgery, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    John A. Rogers

  18. Department of Chemistry, Northwestern University, Evanston, IL, USA

    John A. Rogers

  19. Department of Electrical Engineering and Computer Science, Northwestern University, Evanston, IL, USA

    John A. Rogers

Authors
  1. Mengdi Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kedar Aras
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cunman Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xuexian Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hangbo Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ndeye Rokhaya Faye
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bohan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jae-Hwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Wubin Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Quansan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Yuhang Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Wei Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Enming Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Janice Mihyun Baek
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Yujin Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Clifford Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Jeffrey B. Model
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Guanjun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Roozbeh Ghaffari
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Yonggang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Igor R. Efimov
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. John A. Rogers
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.H., L.C., K.A., R.G., Y.H., I.R.E. and J.A.R. conceived the ideas, designed the experiments and wrote the manuscript; L.C., K.L. and G.Y. performed mechanical, electrical and thermal modelling. M.H., C. Liang, B.S., J.-H.K., Q.Y., Y.M., E.S., J.M.B., Y.L., C. Liu and J.B.M. fabricated the devices; M.H., X.C., H.Z., B.S., W.B., Y.M. and W.L. performed in vitro data collection and analysis; M.H., K.A., H.Z. and N.R.F. performed ex vivo data collection and analysis.

Corresponding authors

Correspondence to Yonggang Huang, Igor R. Efimov or John A. Rogers.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Peer reviewer reports are available.

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

Supplementary information

Supplementary Information

Supplementary notes, figures, tables and video captions.

Reporting Summary

Supplementary Video 1

Temperature mapping using the multiplexing circuit with proper grounding.

Supplementary Video 2

Pressure mapping on a porcine heart.

Supplementary Video 3

Electrogram mapping on a rabbit heart.

Supplementary Video 4

Temperature mapping during radiofrequency ablation.

Supplementary Video 5

Electrogram mapping on a human heart.

Peer-review information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, M., Chen, L., Aras, K. et al. Catheter-integrated soft multilayer electronic arrays for multiplexed sensing and actuation during cardiac surgery. Nat Biomed Eng 4, 997–1009 (2020). https://doi.org/10.1038/s41551-020-00604-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41551-020-00604-w

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing