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Fully implantable and bioresorbable cardiac pacemakers without leads or batteries

Nature Biotechnology volume 39, pages 1228–1238 (2021)Cite this article

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Abstract

Temporary cardiac pacemakers used in periods of need during surgical recovery involve percutaneous leads and externalized hardware that carry risks of infection, constrain patient mobility and may damage the heart during lead removal. Here we report a leadless, battery-free, fully implantable cardiac pacemaker for postoperative control of cardiac rate and rhythm that undergoes complete dissolution and clearance by natural biological processes after a defined operating timeframe. We show that these devices provide effective pacing of hearts of various sizes in mouse, rat, rabbit, canine and human cardiac models, with tailored geometries and operation timescales, powered by wireless energy transfer. This approach overcomes key disadvantages of traditional temporary pacing devices and may serve as the basis for the next generation of postoperative temporary pacing technology.

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Fig. 1: Materials, design features and proposed utilization of a bioresorbable, implantable, leadless, battery-free cardiac pacemaker.
Fig. 2: Ex vivo demonstrations of bioresorbable cardiac pacemakers on mouse and rabbit hearts and human cardiac tissue.
Fig. 3: Treatment of AV block using a bioresorbable, leadless cardiac pacemaker in an ex vivo Langendorff-perfused mouse model.
Fig. 4: Demonstration of a bioresorbable, leadless cardiac pacemaker in an in vivo canine model.
Fig. 5: Implantation and operation of a bioresorbable, leadless cardiac pacemaker in a chronic in vivo rat model.
Fig. 6: Bioresorbability studies of the leadless cardiac pacemaker.
Fig. 7: Biocompatibility and toxicity studies of a bioresorbable, leadless cardiac pacemaker.

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Data availability

All data that support the findings of this study are included in the manuscript. Source data are provided with this paper.

Code availability

The software for the analysis of optical mapping data, custom MATLAB software (RHYHTM) and custom scripts used in the study are freely available for download at https://github.com/optocardiography.

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Acknowledgements

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 Resource (NSF no. ECCS-1542205); the MRSEC program (NSF no. DMR-1720139) at the Materials Research Center; the International Institute for Nanotechnology (IIN); the Keck Foundation; and the State of Illinois, through the IIN. This work was also performed in part at The George Washington University Nanofabrication and Imaging Center. We acknowledge support from the Leducq Foundation projects RHYTHM and R01-HL141470 (to I.R.E. and J.A.R.). R.T.Y. acknowledges support from the American Heart Association Predoctoral Fellowship (no. 19PRE34380781). R.A. acknowledges support from the National Science Foundation Graduate Research Fellowship (NSF no. 1842165) and the Ford Foundation Predoctoral Fellowship. Z.X. acknowledges the 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). B.P.K. and D.J. acknowledge support from a research donation by Mr and Mrs Ronald and JoAnne Willens. We thank NU Comprehensive Transplant Center Microsurgery Core for help with cardiac implantation surgical procedures. We also thank the Washington Regional Transplant Community, heart organ donors and families of the donors; our research would not have been possible without their generous donations and support.

Author information

Author notes

  1. These authors contributed equally: Yeon Sik Choi, Rose T. Yin, Anna Pfenniger and Jahyun Koo.

Authors and Affiliations

  1. Center for Bio-Integrated Electronics, Northwestern University, Evanston, IL, USA

    Yeon Sik Choi, Jahyun Koo, Geumbee Lee, Seung Min Lee, Hyoyoung Jeong, Joohee Kim, Hong-Joon Yoon, Anthony Banks, Yonggang Huang & John A. Rogers

  2. Querrey Simpson Institute for Biotechnology, Northwestern University, Evanston, IL, USA

    Yeon Sik Choi, Jahyun Koo, Geumbee Lee, Hyoyoung Jeong, Joohee Kim, Hong-Joon Yoon, Anthony Banks & John A. Rogers

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

    Yeon Sik Choi, Geumbee Lee, Hong-Joon Yoon, Yonggang Huang & John A. Rogers

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

    Rose T. Yin, Yun Qiao & Igor R. Efimov

  5. Feinberg School of Medicine, Cardiology, Northwestern University, Chicago, IL, USA

    Anna Pfenniger, Amy Burrell, Beth Geist, David Johnson, Bradley P. Knight & Rishi K. Arora

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

    Raudel Avila, Chenhang Li, Yonggang Huang & John A. Rogers

  7. Department of Surgery, The George Washington University, Washington, DC, USA

    K. Benjamin Lee & Sheena W. Chen

  8. Center for Cardiovascular Research, Washington University School of Medicine, St. Louis, MO, USA

    Gang Li

  9. Department of Cardiothoracic Surgery, Veteran Affairs Medical Center, Washington, DC, USA

    Alejandro Murillo-Berlioz & Gregory D. Trachiotis

  10. Department of Anatomy and Cell Biology, The George Washington University School of Medicine and Health Sciences, Washington, DC, USA

    Alexi Kiss & Tatiana Efimova

  11. The George Washington Cancer Center, The George Washington University School of Medicine and Health Sciences, Washington, DC, USA

    Alexi Kiss & Tatiana Efimova

  12. Comprehensive Transplant Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    Shuling Han & Zheng Jenny Zhang

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

    Shuling Han & Zheng Jenny Zhang

  14. State Key Laboratory of Structural Analysis for Industrial Equipment, Department of Engineering Mechanics, International Research Center for Computational Mechanics, Dalian University of Technology, Dalian, China

    Zhaoqian Xie

  15. Materials Research Laboratory, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Yu-Yu Chen

  16. School of Advanced Materials Science and Engineering, Sungkyunkwan University, Suwon, Republic of Korea

    Hong-Joon Yoon

  17. Department of Materials Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Seung-Kyun Kang

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

    Seung-Kyun Kang

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

    Chad R. Haney, Alan Varteres Sahakian & John A. Rogers

  20. Center for Advanced Molecular Imaging, Northwestern University, Evanston, IL, USA

    Chad R. Haney

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

    Alan Varteres Sahakian

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

    Yonggang Huang

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

    John A. Rogers

Authors
  1. Yeon Sik Choi
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  2. Rose T. Yin
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Contributions

Y.S.C., R.T.Y., A.P., J. Koo, R.K.A., I.R.E. and J.A.R. led the development of the concepts, designed the experiments and interpreted results. Y.S.C. and R.T.Y. led the experimental work with support from coauthors. R.T.Y., A.P., K.B.L., S.W.C., A.M.-B., S.H., A. Burrell, B.G. and R.K.A. performed in vivo surgery and associated pre-operative and post-operative procedures. R.T.Y., Y.Q. and G. Li performed ex vivo optical mapping. R.A., C.L., Z.X. and Y.H. performed computational modeling and simulations. R.K.A., I.R.E. and J.A.R. supervised the entire project. Y.S.C., R.T.Y., A.P., R.K.A., I.R.E. and J.A.R. wrote the paper. All authors read and approve the final manuscript.

Corresponding authors

Correspondence to Rishi K. Arora, Igor R. Efimov or John A. Rogers.

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The authors declare no competing interests.

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Peer review information Nature Biotechnology thanks the anonymous reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Illustrations that compare use scenarios of conventional temporary pacemakers and the bioresorbable, implantable, leadless, battery-free devices reported here.

a, Schematic illustration that demonstrates the existing clinical approach for using conventional temporary pacemakers. (i) An external generator connects through wired, percutaneous interfaces to pacing electrodes attached to the myocardium. Temporary transvenous leads are affixed to the myocardium either passively with tines or actively with extendable/retractable screws. (ii) The pacing leads can become enveloped in fibrotic tissue at the electrode-myocardium interface, which increases the risk of myocardial damage and perforation during lead removal. As a result, temporary epicardial leads placed at the time of open heart surgery are often cut and allowed to retract to avoid the risk of removal by traction. b, The proposed approach is uniquely enabled by the bioresorbable, leadless device introduced here. (i) Electrical stimulation paces the heart via inductive wireless power transfer, as needed throughout the post-operative period. (ii) Following resolution of pacing needs or insertion of a permanent device, the implanted device dissolves into the body, thereby eliminating the need for extraction.

Extended Data Fig. 2 Design of bioresorbable, implantable, leadless, battery-free cardiac pacemaker.

a, Dimensions of the device: (top) x,y-view; (bottom) x,z-view. The minimum length of the device is 15.8 mm. The total length can be altered to meet requirements for the target application, simply by changing the length of the extension electrode. b, Dimensions of the contact pad. PLGA encapsulation covers the top surface of the contact electrode to leave only the bottom of contact electrode exposed.

Extended Data Fig. 3 Modeling and experimental studies of mechanical reliability of the bioresorbable, leadless cardiac pacemaker.

a, Photograph (left) and FEA (right) results for devices during compressive buckling (20%). Scale bar, 10 mm. b, c, d, Photograph of twisted (180°) and bent (bend radius = 4 mm) devices. Scale bar, 10 mm. e, Output voltage of a device as a function of bending radius (left), compression (middle), and twist angle (right) at different distances between the Rx and Tx coils (black, 1 mm; red 6 mm). n = 3 independent samples.

Source data

Extended Data Fig. 4 Electrical performance characteristics of the wireless power transfer system.

a, Schematic illustration of the circuit diagram for the transmission of RF power. Monophasic electrical pulses (programmed duration; alternative current) are generated by a waveform generator at ~13.5 MHz (Agilent 33250 A, Agilent Technologies, USA). The voltage can be further increased with an amplifier (210 L, Electronics & innovation, Ltd., USA). The generated waveforms (that is input power) are delivered to the Tx coil (3 turns, 20 mm diameter). This RF power is transferred to the Mg Rx coil (17 turns, 12 mm diameter) of an implanted bioresorbable cardiac pacemaker. The received waveform is transformed into a direct current output via the RF diode to stimulate the targeted tissue. b, Measured RF behavior of the stimulator (black, S11; red, phase). The resonance frequency is ~13.5 MHz. c, Simulation results for inductance (L) and Q factor as a function of frequency. d, An alternating current (sine wave) applied to the Tx coil. The resonance frequency and input voltage (that is transmitting voltage) are ~13.5 MHz and 7 Vpp, respectively. e, Example direct current output of ~13.2 V wirelessly generated via the Rx coil of the bioresorbable device. f, Output voltage as a function of transmitting frequency. At the resonance frequency (~13.5 MHz) of the receiver coil (transmitting voltage = 7 V), the device produces a maximum output voltage of ~13.2 V. g, Output voltage as a function of the distance between the Tx and Rx coils (transmitting voltage = 10 Vpp; transmitting frequency = ~13.5 MHz).

Source data

Supplementary Information

Supplementary Information

Supplementary Notes 1–5 and Figs. 1–17

Reporting Summary

Source data

Source Data Fig. 2

ECG, optical mapping data.

Source Data Fig. 3

ECG, optical mapping data.

Source Data Fig. 4

ECG, output performance data.

Source Data Fig. 5

ECG data.

Source Data Fig. 7

Biocompatibility data.

Source Data Extended Data Fig. 3

Output performance data.

Source Data Extended Data Fig. 4

Output performance data.

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Choi, Y.S., Yin, R.T., Pfenniger, A. et al. Fully implantable and bioresorbable cardiac pacemakers without leads or batteries. Nat Biotechnol 39, 1228–1238 (2021). https://doi.org/10.1038/s41587-021-00948-x

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