Temporary Tattoo Electrodes for brain recordings in clinical settings

RESEARCH

September 2020

Laura M. Ferrari1*, E. Ismailova3*, F.Greco2*

1 Université Côte d’Azur, INRIA, Sophia Antipolis, France.
2 Institute of Solid State Physics, Graz University of Technology, Austria.
3 Ecole Nationale Supérieure des Mines de Saint Etienne, Department of Bioelectronics, Gardanne, France.
*Email: laura.ferrari@inria.fr , ismailova@emse.fr , francesco.greco@tugraz.at

Temporary Tattoo Electrodes (TTEs) are dry and conformable electrodes that are able to capture weak surface electrophysiological signals while being imperceptible for the user. We demonstrated the use and characterised TTEs in a clinical electroencephalography (EEG) monitoring set-up, proving for the first time the compatibility of a dry electrode with magnetoencephalography (MEG) sensors (Figure 1) (1).

Figure 1. Temporary Tattoo Electrodes (TTEs) in Electroencephalography/magnetoencephalography (EEG/MEG) recordings. a) Exemplification of EEG and MEG coupling with the human head. b) A TTE released on the scalp, in Oz position (according to the 10–20 international system). c) Colorized SEM micrograph (45° tilted view, scale bar = 400 μm) of the micrometric tattoo film released on a skin replica. d) Simultaneous MEG (sensor in right posterior location) and EEG (Oz location) recordings with TTEs. In both modalities, the presence of alpha waves appears after 8 s. e) MEG recording, with TTEs on the subject’s head, depicted onto a head map. The signal is shown fractioned in the Alpha (8–12 Hz) band. (a, b, d, e) Images adapted from (1) ; c) image adapted from (12).

Tattoo technology is an emerging solution for broad skin-contact applications, especially with sensing purposes (2, 3, 4, 5). Today the challenge in human health biomonitoring is the possibility to have access to high-quality and long term health data through a seamless interface (6, 7). In that way we will improve the user experience while enabling continuous remote biomonitoring.

In relation to brain assessments the gold standard are Ag/AgCl wet electrodes, owing to their high signal quality (8). These sensors are in use in clinical practice since many decades, although they have shown their limitations in terms of long term stability and comfort. Especially in EEG assessment, patient preparation is a long and tedious procedure that does not permit to fully exploit the information accessible from the biosignal. High-density EEG (hdEEG) recordings are limited due to the gel leakage across adjacent electrodes, creating short-circuits, and the drying of the gel (within some hours) requires frequent maintenance of the mountage practically impairing long term assessments (9). These drawbacks are especially highlighted in the evaluation of epileptic patients. hdEEG (> 100 electrodes) (10) would give access to precise localization of the epileptic foci, necessary for surgery, while biomonitoring over days would allow the capturing of epileptic seizures, key in patients evaluation.

In clinical practice, EEG recordings are frequently coupled with MEG. While EEG records electric field changes in the brain, MEG senses variations in the magnetic field induced by modifications of the electric field generated by the same population of neurons (Figure 1a). Simultaneous EEG/MEG recordings are essential in understanding of dynamic cognitive processes, owing to their high temporal resolution, and are often adopted in focal epilepsy diagnostics. The compatibility of the EEG setup with the MEG instrumentation is a key concern in the clinical brain evaluation. Beside the adoption of low noise amplifiers, ferromagnetic materials, particularly in electrodes, are forbidden in order to avoid the generation of magnetic artefacts. Furthermore, the bulky geometry of EEG electrodes is also a limiting factor. Their vertical profiles have to be minimized to allow an efficient coupling with the MEG sensor. (11)

In order to provide an advanced technological advanced solution to overcome these limitations we have developed all-polymeric TTEs capable of conformably adhere to the skin creating an imperceptible interface between the human body and the electronics (Figure 1b). TTEs have been fabricated by inkjet printing of conducting polymer, poly(3,4-ethylenedioxythiophene) : polystyrene sulfonate (PEDOT:PSS), onto commercially available temporary tattoo paper. Tattoo paper has a layered structure which enables the release of a micrometric polymer decal film onto skin, when paper is pressed against it and wet with water. Owing to their low thickness (~ 1 μm) TTEs provide an ultraconformal adhesion to the target surface (Figure 1c) (12), acting as a second skin on it (see a demonstration video at LAMPSE TUGraz website). TTEs have been recently adopted in the recording of many electrophysiological signals, as electromyography (EMG) and electrocardiography (ECG), demonstrating their outstanding capabilities in interfacing with human body also in long-term study (48 h of skin-contact impedance measurements). TTEs have been also demonstrated as a novel concept of pierceable electrodes with hairs growing through and not impairing the signal (e.g. EMG) recording (12). It is well known that hair growth is an important issue in cutaneous technologies. For instance, hair growth causes sensor displacement and signal loss in clinical long-term electrophysiology.

In our last study (1) we investigated the TTEs’ capability in recording  the most challenging surface electrophysiological signal, the EEG (the weakest with the lowest frequency content). In order to understand the biosignal transduction we modelled the skin/electrode impedance highlighting how dry conformable interfaces differ from wet (or thicker dry) sensors. The TTEs’ working principle relies on a capacitive coupling with the underlying biological tissues, across a complete dry interface (the first layer of the skin, the stratum corneum). We have then deepened our investigation developing a complete model for the biosignal transduction in conformable electrodes (work under submission).

Regardless of their impedance characteristics, such ultrathin electrodes allowed for a high-quality signal transduction of biopotentials accessible from the skin. TTEs efficiently recorded multiple brain signals in different experimental set-up, with a signal quality comparable at all with those of gold standard Ag/AgCl electrodes (Figure 2). TTEs were able to record well-defined alpha waves, the most studied rhythm of the brain, during multiple sessions (from 30s to 2 min) both in a shielded room and in a hospital evaluation room, where no special units such as a faraday cage or impedance matching components were used (Figure 2a,b). TTEs . Notably, both TTEs and Ag/AgCl electrodes were also able to catch slow waves (0.5–4.5Hz), whose acquisition is usually challenging.

TTEs have also been characterized through the recording of auditory evoked potential (AEP), enabling the detection of the characteristic neurological response, the N100 (Figure 2c). Evoked potentials are time-locked task-oriented events, induced by an external stimulus (in our case bursts of brief sinusoidal auditory stimuli), with an amplitude lower than 10 μV.  From the clear shape of the recorded AEPs we calculated the SNR, finding a higher value, 4.07 (absolute value) with TTEs, in comparison with 3.36 of the Ag/AgCl electrodes. Owing to the high signal quality recording, together with an easy electrode placement and long-term recording capability, TTEs show a good potential for their further implementation in clinical cognitive brain assessments, long-term neuromonitoring at home and application in BCI for disabled persons.

We then performed simultaneous MEG/EEG recordings,. proving the parallel acquisition of well visible alpha waves (Figure 1d). NA neural activity was also clearly visible from MEG recordings, at different frequencies, without any high-density magnetic flux appearance in the EEG electrode proximity (Figure 1e). The EEG and MEG recordings were also performed simultaneously providing well visible alpha waves (Figure 1e). In MEG, the high number of sensors allows restitution of the brain activity mapping with a great spatial resolution. Using a skin-mimicking phantom, we explored the feasibility of hdEEG through tattoo electrodes, suggesting that TTEs can allow for double electrodes’ density (e.g. 20 mm center-to-center distance) with respect to the Ag/AgCl case. The compatibility of TTEs with MEG and their hdEEG capability are aimed to offer advanced tools for neurodegenerative disease diagnostics, as the localization of neuropathological activities. These evaluations were aimed to provide a valuable input for the successful application of ultrathin electronic tattoos in multimodal brain monitoring and diagnosis, showing their real application and benefits in clinical settings.

Figure 2. Multiple EEG recordings with TTEs on human scalp. a) Close-up of a TTE released on the scalp after 12 h from application (top, scale bar = 1cm). Close-up of an Ag/AgCl electrode (bottom, scale bar = 1 cm). b) Superimposed PSD (dB) during alpha wave recordings from TTEs (red) and Ag/AgCl electrodes (blue). The insert at the bottom left shows the electrodes placement with used derivation (Tz–Cz). c) Auditory Evoked Potential recorded with both TTEs (red) and Ag/AgCl electrodes (blue), with N100- an auditory evoked potential component.(a, b, c) Images adapted from (1).

 

References

  1. Ferrari, L. M., et al., Conducting polymer tattoo electrodes in clinical electro-and magneto-encephalography. npj Flexible Electronics 2020, 4 (1), 1-9.
  2. Alberto, J., et al., fully Untethered Battery-free Biomonitoring electronic tattoo with Wireless energy Harvesting. Scientific reports 2020, 10 (1), 1-11.
  3. Kabiri Ameri, S., et al., Graphene Electronic Tattoo Sensors. ACS nano 2017, 11 (8), 7634-7641.
  4. Kim, J., et al., Wearable biosensors for healthcare monitoring. Nature biotechnology 2019, 37 (4), 389-406.
  5. Zucca, A., et al., Tattoo conductive polymer nanosheets for skin-contact applications. Advanced healthcare materials 2015, 4 (7), 983-90.
  6. Liu, Y., et al., Lab-on-skin: a review of flexible and stretchable electronics for wearable health monitoring. ACS nano 2017, 11 (10), 9614-9635.
  7. Nawrocki, R. A., Super‐and Ultrathin Organic Field‐Effect Transistors: from Flexibility to Super‐and Ultraflexibility. Advanced Functional Materials 2019, 29 (51), 1906908.
  8. Tallgren, P., et al., Evaluation of commercially available electrodes and gels for recording of slow EEG potentials. Clinical Neurophysiology 2005, 116 (4), 799-806.
  9. da Silva, F. L., EEG and MEG: relevance to neuroscience. Neuron 2013, 80 (5), 1112-1128.
  10. Srinivasan, R., et al., Estimating the spatial Nyquist of the human EEG. Behavior Research Methods, Instruments, & Computers 1998, 30 (1), 8-19.
  11. Puce, A.; Hämäläinen, M., A review of issues related to data acquisition and analysis in EEG/MEG studies. Brain sciences 2017, 7 (6), 58.
  12. Ferrari, L. M., et al., Ultraconformable temporary tattoo electrodes for electrophysiology. Advanced Science 2018, 5 (3).

Author Biographies:

Laura M. Ferrari is Post-Doc researcher at Université Côte d’Azur (UCA), INRIA, Sophia Antipolis (France). She was awarded the “AAP Jeunes chercheurs UCA/Ville de Nice” with a 2-years funded project. She got her PhD at the Biorobotics institute, Center for MicroBiorobotics of Istituto Italiano di Tecnologia at Scuola Superiore Sant’Anna (Italy), where she then worked as research fellow. She has experiences with start-ups and hospitals, where she worked as scientific consultant and sr researcher. Her research activity is on the development of novel technologies for human health biomonitoring, through a multidisciplinary approach, with main applications in neuroscience. Her fields of expertise are: tattoo electronics and conformable interfaces, inkjet printing, biosensing, electrophysiology, bioelectronics. She is author of 8 peer-reviewed full paper as first author and 1 international patent.

Francesco Greco is Assistant Professor at Institute of Solid State Physics, Graz University of Technology (Austria) where he leads the Laboratory of Applied Materials for Printed and Soft Electronics (LAMPSe). He was Associate Professor at School of Advanced Science and Engineering, Waseda University, Tokyo (Japan) and Researcher at Center for MicroBiorobotics of Istituto Italiano di Tecnologia, (Italy). His research focuses on functional polymer materials for actuators and sensors, fabrication/patterning through printing or Direct Laser Writing methods, ultraconformable tattoo electronics and  their applications in soft and bio-robotics, organic bioelectronics, smart biointerfaces, medicine. He is the author of around 50 peer-reviewed full papers, 7 international patents and serves as Research Topic Editor of Frontiers in Materials.

Esma Ismailova is an Associate Professor in the Bioelectronics Department at Ecole National Superieur des Mines de Saint-Etienne (EMSE). She received her BSc. in Physics at the National University of Uzbekistan and obtained a Master’s degree in Polymer Science at Strasbourg University in France where she also completed her PhD in Chemistry and Chemical Physics. She then joined the Laboratory for Organic Electronics at Cornell University, NY, USA as a postdoctoral researcher. In 2010 she joined BEL as a postdoctoral fellow where she worked on developing microfabrication platform for soft biocompatible neural implants and advanced to becoming a permanent staff member in 2012. Her current research group works on the development of organic electronic sensors for applications in healthcare using wearable smart textile and biocompatible systems. She is the leading organizer of the Electronic Textiles Symposia for the Materials Research Society in the USA and Europe. She is also the principal scientist in multiple projects sponsored by the EU and French research funding agencies as well as industry oriented organizations such as BpiFrance (French Public Investment Bank).

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