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Adhesive bioelectronics for sutureless epicardial interfacing

Nature Electronics volume 6, pages 779–789 (2023)Cite this article

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Abstract

Bioadhesive devices can be used to create conformable tissue–device interfaces without suturing. However, the development of such technology faces challenges related to the need for external stimuli or long periods of time for tissue adhesion, fatigue-related breakdown of the stretchable electrodes and the use of solid substrates with non-uniform surface coverage of the tissue. Here, we report a bioelectronic patch that is capable of instantaneous and conformable tissue adhesion on a heart for precise cardiac monitoring. The patch is composed of three layers: an ionically conductive tissue adhesive, a viscoelastic networked film and a fatigue-resistant conducting composite. The system provides conformable tissue adhesion in less than 0.5 s without external stimuli, spontaneous modulus matching based on efficient strain adaptivity and small resistance changes of less than 0.2% at 50.0% tensile strain after 1,000 stretching cycles. We show that the patch can be used for the long-term measurement of electrocardiogram signals (up to four weeks of implantation) in awake rats without causing tissue damage, as well as spatiotemporal mapping in a myocardial ischaemia reperfusion model.

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Fig. 1: Overall concept and mechanism of SAFIE.
Fig. 2: Mechanical characterizations of E-SHN with Alg-CA layer for cardiac tissue conformality and adhesiveness.
Fig. 3: Electrical and mechanical properties of EGaIn/SHP composite as electrodes and their biointerfacing capability.
Fig. 4: Acute site-specific cardiac signal recording and stimulation via in vivo test on a rat’s heart.
Fig. 5: ECG signal recording and stimulation in awake rats compared with conventional suturing.

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Data availability

Source data are provided with this paper. The other data that support the findings of this study are available from the corresponding authors upon reasonable request.

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Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) grant by the Korea government (MSIT) (nos. 2020R1C1C1005567, RS-2023-00208262 and 2022M3E5E9018583). This research was also supported by the Institute for Basic Science (IBS-R015-D1).

Author information

Author notes

  1. These authors contributed equally: Heewon Choi, Yewon Kim, Sumin Kim.

Authors and Affiliations

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

    Heewon Choi, Yewon Kim, Hyunjin Jung, Sungjun Lee & Donghee Son

  2. Center for Neuroscience Imaging Research, Institute for Basic Science (IBS), Suwon, Republic of Korea

    Heewon Choi, Yewon Kim, Sumin Kim, Hyunjin Jung, Sungjun Lee, Kyoungryong Kim, Mikyung Shin & Donghee Son

  3. Department of Intelligent Precision Healthcare Convergence, Sungkyunkwan University, Suwon, Republic of Korea

    Sumin Kim, Kyoungryong Kim & Mikyung Shin

  4. Center for Biomaterials, Biomedical Research Institute, Korea Institute of Science and Technology, Seoul, Republic of Korea

    Hyung-Seop Han

  5. Division of Cardiology, Department of Internal Medicine, Heart Vascular Stroke Institute, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea

    Ju Youn Kim

  6. Department of Biomedical Engineering, Sungkyunkwan University, Suwon, Republic of Korea

    Mikyung Shin

  7. Department of Superintelligence Engineering, Sungkyunkwan University, Suwon, Republic of Korea

    Donghee Son

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Contributions

This project was originally proposed by D.S. M.S. and D.S. supervised the project. H.C., Y.K. and S.K. conducted all the experiments with assistance from H.J., S.L., K.K., M.S. and D.S. H.J. analysed the strain distribution on the SAFIE patch using a mechanical simulation software. H.-S.H. and J.Y.K. provided the interpretation of the biological and histological data. H.C., Y.K., S.K., M.S. and D.S. analysed the data and prepared the manuscript with input from all the co-authors.

Corresponding authors

Correspondence to Mikyung Shin or Donghee Son.

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Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Electronics thanks Xiaozhong Qiu, Tae-Woo Lee and Kyoseung Sim for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Comparison of stable ECG recording of SAFIE patch to that of conventional ECG sensors without tissue adhesion and conformability.

Optimized SAFIE patch via adhesion coating on network substrate to record stable cardiac signals for long periods.

Source data

Extended Data Fig. 2 ECG signals and their spatiotemporal map data of the simplified MI model using the SAFIE.

(i), (ii), and (iii) ECG signals correspond to normal heart rhythms, ST segment evaluation, and ventricular fibrillation, respectively. Their ECG signals are shown as the spatiotemporal map data.

Source data

Extended Data Fig. 3 The ECG monitoring by the SAFIE patch in a rat MIR model.

a, Observation of raw 4-channel ECG signals from the SAFIE patch in the disease model. b, Surface ECG signals (left inset graphs) and activation map before (left) and after (right) myocardial infarction. c, Histological image of the heart tissue with infarcted region (purple) stained by Masson’s-trichrome (MT) reagents.

Source data

Extended Data Fig. 4 Spatiotemporal mapping of the ECG signals recorded by the SAFIE patch with the 8 screen-printed EGaIn/SHP composite electrodes.

a, Various screen-printed EGaIn/SHP composites on the SHP substrate with different line-shaped patterns (200 – 1000 μm). b, Electrical resistance value of printed interconnects versus line width. c, Photograph of the SAFIE patch with 8 channels attached onto rat’s heart. Data points are means ± s.e.m. (n = 3). d, Normalized ECG signals recorded from the multichannel SAFIE patch. The blue-dashed box indicates the magnified view (10 times) of the 3rd peak where the 1st peak with a specific pattern of an inverted triangle shape is detected from each channel. e, Activation map during the sinus rhythm. f, Epicardial spatiotemporal mapping achieved during the sinus rhythm every 0.5 ms. All the map data were interpolated with K-nearest neighbors interpolation algorithm.

Source data

Extended Data Fig. 5 Histological analysis.

a–c, H&E stained histological appearance of the heart tissues dissected after 3 days of (a) only surgical procedures (for example, no treatment), (b) suturing of the patch without Alg-CA layer, and (c) implantation of the SAFIE. The image was magnified ×1 (left), ×5 (middle), and ×20 (right) to show each region where epicardial devices were implanted (red boxes) or not (blue boxes).

Source data

Extended Data Fig. 6 Histological analysis at 1-week and 4-week implantation of the SAFIE patch.

a–d, Representative histological images at 1 week (a, b) and 4 weeks (c, d) for the control group without any implantation (a, c) and the SAFIE group (b, d) stained with hematoxylin and eosin (H&E) (left panels) and Masson’s trichrome (MT) agents (right panels)). The boxes indicate the region where epicardial device was either implanted (red) or not applied (blue).

Source data

Supplementary information

Supplementary Information

Supplementary Notes 1–14, Table 1, Figs. 1–39 and captions for Supplementary Videos 1–9.

Reporting Summary

Supplementary Video 1

Three-dimensional reconstructed Alg-CA-coated E-SHN patch by confocal z-stack images.

Supplementary Video 2

In vivo test for the instantaneous conformal adhesion of the E-SHN coated with Alg-CA on rat’s heart.

Supplementary Video 3

Instantaneous underwater tissue adhesion of E-SHN with Alg-CA ex vivo in small and large animals. E-SHN quickly and evenly attached without any additional pressure on both rat and porcine heart organs and maintained adhesion during rinsing with PBS (1×, pH 7.4) and blood.

Supplementary Video 4

Comparison of conformability and adhesiveness of E-SHN with Alg-CA (SAFIE), E-SHN without Alg-CA, solid film with Alg-CA and solid film without Alg-CA on rat’s heart. An uncovered area existed in the solid film with/without Alg-CA, and a slip occurred in the E-SHN and solid film without Alg-CA within 60 s. The SAFIE patch showed stable adhesion and full coverage of the rat heart.

Supplementary Video 5

In vivo stimulation with the SAFIE patch on rat’s heart. Heart rhythms were not synchronized in the subthreshold voltage stimulation (for example, 1.0 Vpp) but were synchronized over the threshold voltage stimulation (for example, 1.5 Vpp).

Supplementary Video 6

A rat-based simplified MI model prepared after implantation of the SAFIE patch on the heart.

Supplementary Video 7

Spatiotemporal mapping of ECG signals during sinus rhythm from the eight-channel SAFIE patch.

Supplementary Video 8

In vivo implantation of the SAFIE patch. Total implantation time was less than 1 min and proceeded without any damage to the heart tissue of the rat.

Supplementary Video 9

Real-time ECG signal recording of a freely moving rat from four sensing channels of the SAFIE patch three days after implantation. Real-time bpm analysis was also conducted using LabChart software.

Supplementary Data

Source data for the supplementary figures.

Source data

Source Data Fig. 2

Source data for Fig. 2.

Source Data Fig. 3

Source data for Fig. 3.

Source Data Fig. 4

Source data for Fig. 4.

Source Data Fig. 5

Source data for Fig. 5.

Source Data Extended Data Figs. 1–6

Source data for Extended Data Figs. 1–6.

Source Data Fig. 3

Original CDX file for Fig. 3e(iii),(iv).

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Choi, H., Kim, Y., Kim, S. et al. Adhesive bioelectronics for sutureless epicardial interfacing. Nat Electron 6, 779–789 (2023). https://doi.org/10.1038/s41928-023-01023-w

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