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Bioinspired Materials for Wearable Diagnostics and Biosensors
ACS Biomaterials Science & Engineering ( IF 5.4 ) Pub Date : 2023-05-08 , DOI: 10.1021/acsbiomaterials.3c00348 Neelkanth M. Bardhan , Milica Radisic , Md Nurunnabi
ACS Biomaterials Science & Engineering ( IF 5.4 ) Pub Date : 2023-05-08 , DOI: 10.1021/acsbiomaterials.3c00348 Neelkanth M. Bardhan , Milica Radisic , Md Nurunnabi
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This article is part of the Bioinspired Materials for Wearable Diagnostics and Biosensors special issue. Over the past decades, smart nanomaterials and stimuli-responsive materials in the form of “wearable” biosensors (1) have found exciting medical applications in a vast array of health conditions, ranging from infectious diseases such as the COVID-19 pandemic to chronic conditions such as cancer. (2) Since the miniaturization of electronic components, and particularly since the explosion of “personal” computing in the developing world facilitated by the proliferation of the smartphone and other hand-held devices, wearable biosensors (3) (such as glucose-monitoring smart contact lenses, hybrid chemo-physical patch sensor for lactate and ECG measurements, or textile-based lactate sensors, as representative examples) have been fast-tracked to commercialization. This trend has been further accelerated by the simultaneous development in the processing and manufacturing techniques for highly conformable materials, (4) which can adapt to the nonuniform and heterogeneous biophysical environment of the human body. The question arises─why use bioinspired materials for wearable diagnostics and biosensors? The term “biomimicry” or “bioinspiration” refers to the process of understanding nature’s design principles in building highly complex models with a broad range of functions (such as mechanical or structural support, sensing, trafficking, molecular recognition, charge transport, self-assembly, self-replication, and so on) at various length scales, and using this knowledge to solve mankind’s challenges. (5) For example, natural living beings have figured out ways to synthesize lightweight, structural architectures at different hierarchical scales (6) from the atomic level to macroscopic organisms, at large volume and low cost, with highly optimized combinations of strength, stiffness, and toughness. (7) Inspired from natural materials, biomimetic material approaches have found numerous applications in the medical field, such as in drug delivery systems, (8) molecular beacons for noninvasive detection and imaging of infections (9) and real-time surgical guidance (10) for cancer treatment, organ-on-a-chip devices (11) for biomimetic cell culture, and tissue engineering to study drug metabolism, toxicity, and pathology, (12) among other examples. Therefore, it follows logically that researchers worldwide are taking inspiration from nature’s handbook to come up with creative solutions to designing wearable biosensors, which can interface nicely with human beings. To conform to the World Health Organization’s ASSURED diagnostic criteria (affordable, sensitive, specific, user-friendly, rapid, equipment-free, delivered) for ideal point-of-care diagnostic test systems, (13) which can be deployed both in the developed world and in resource-constrained settings, the need of the hour is to design, prototype, and validate flexible, wearable biosensors that can offer accurate and reliable real-time sensing of physiological biomarkers (3) for personalized health monitoring, along with a realization of the challenges and opportunities in this domain. (14) In this Special Issue, we bring you a number of original research and review articles that discuss the development of materials inspired from natural systems, with wide-ranging applications in wearable diagnostics, continuous health monitoring of biological signals, and biosensors for pathogen detection, as visualized in the word cloud in Figure 1. Figure 1. Key ideas and concepts discussed in this Special Issue on Bioinspired Materials for Wearable Diagnostics and Biosensors. We open the Special Issue with the report of fabrication of a core–sheath conductive fiber structure, mimicking mammalian skeletal muscle, by Chen and co-workers. (15) Using cation-induced assembly, MXene@alginate high-conductivity fibers were synthesized in a facile, scalable manner, at a high speed of 2 m/min. In one application, these fibers were integrated into textiles for wearable thermal management, allowing for Joule heating up to a temperature of 100 °C within 4 min, at low applied voltage. With heat application, these fibers showed the capability for cyclic contraction, with stress >40 times higher than mammalian skeletal muscle. By winding these fibers into springs, it was demonstrated that the material could be used as a reconfigurable dipole antenna for wireless monitoring of heat sources. The material was also shown to have excellent biocompatibility, by acting as a substrate for the differentiation of neural progenitor stem cells. Next, this Special Issue contains a comprehensive review on the emerging, exciting new field of wearable sweat biosensors by Dorval Courchesne and co-workers. (16) Among the various biofluids, sweat is a readily available body fluid, composed of many clinically relevant biomarkers like small ions, hormones, and proteins that can be used for health sensing. (17) However, compared to blood- or urine-based biosensors, sweat-based sensors must overcome the challenges posed by small sample volumes (∼10–30 μL), low concentration of analytes due to dilution, and the need to function in dry and solid skin matrices. In this review, Dorval Courchesne et al. have taken a deep dive into the components of sweat-based wearable sensors: the biorecognition element, a transducer, a scaffold, and an adhesive. More specifically, the ability to design and engineer biomimetic proteins has opened up diverse applications such as nutritional tracking, environment monitoring, and diagnostic detection by incorporating them into a whole new class of epidermal devices leveraging the chemistry of sweat. (18) Polymer-functionalized nanomaterials have long been explored as a way to enhance the properties of biomaterials, for imparting self-healing, mechanical, electrical, and chemical functionality, especially in the context of theranostics (19) for cancer and infectious diseases. By harnessing the unique composition of a protein–polymer composite, Dorval Courchesne and colleagues report here (20) the fabrication of Curli-PEDOT:PSS biocomposites with multifunctional properties. By tuning the ratio of the amyloid curli fibers, the highest conductivity could be attained at a 60:40 Curli:PEDOT/PSS mix. Furthermore, these composites are capable of water-induced self-healing, even in the presence of significant shear stresses in the environment. By genetically modifying the curli fibers, it is also made possible to add functionality such as a fluorescent protein tag, which could be used for optical sensing applications. Another bustling area of activity in the innovation domain for wearable devices and sensors is the field of hydrogel materials, with versatile applications owing to their softness, stretchability, biocompatibility, and rapid response to stimuli. Khademhosseini and co-workers have provided a comprehensive review (21) of the state-of-the-art in bioinspired hydrogel materials, with special focus on wearable devices such as electronic skin for tactile or temperature sensing, smart contact lenses for glucose monitoring in diabetes, and microneedles for drug delivery, sensing, and wound healing, to name a few. By tuning the hydrogel-forming precursor material, it has been made possible to mimic the structure–function properties of human skin, skeletal muscle, and other structural elements to suit the intended applications. Furthermore, this review summarizes the power and data transmission requirements for wearable devices, by investigating wearable batteries, supercapacitors, and low-power wireless communication protocols to enable real-time data monitoring and remote control of these biosensors. As a practical example of the power of hydrogel networks, Sparks and colleagues have demonstrated a Q-peptide hydrogel that promotes attachment, migration, and survival of keratinocytes, leading to a higher fraction of wound closure in an equine model of wound healing, (22) as well as helping modulate the biomechanical function of healing tissues. As alluded to in the previous review article by Khademhosseini et al., one of the major limitations of wearable devices and biosensors is their continuous power requirements, which is complicated by the constraints of bulky, expensive batteries requiring regular charging or replacement. To overcome this limitation, Dagdeviren and co-workers propose (23) strategies of harnessing the human body’s continuous energy generation to power wearable devices, thereby allowing for seamless integration of such biosensors. In this exhaustive review, the authors have looked at “self-powered” devices, (24) with a focus on piezoelectric energy harvesting. Numerous configurations and structures are studied, combining nonconventional patterning techniques such as kirigami and auxetics, to better conform to the curvilinear geometry of the human body. Combining these innovative wearable sensors with machine learning techniques has allowed for new applications in clinical monitoring for personalized healthcare, such as enabling nonverbal communication in patients with neurodegenerative conditions such as ALS, or gait monitoring for sports medicine and therapy. Similar to the concept of the piezoelectric-mediated power harvesting techniques discussed above, Haick and colleagues have discussed designing self-powered devices using triboelectric nanosensors in a thorough review. (25) Based on the coupling effect of triboelectric generation with electrostatic induction, triboelectric nanogenerators (TENGs) have gained prominence as an effective way to harness the human body’s mechanical energy to power wearable sensors and devices. Numerous animal-, plant- ,and human-inspired morphologies and structures are discussed, along with the corresponding suitable friction material used in the TENG device for higher output and better sensing performance. Solid–solid and liquid–solid TENGs are also discussed in some detail, and the authors provide a forward-looking perspective on the existing challenges for deploying TENGs in multifunctional biosensing for remote healthcare applications. Over the past 2–3 years, with the world battling the fierce outbreak of the COVID-19 pandemic, there has been a tremendous medical need for rapid testing and diagnostics to screen for pathogenic infections at the population level. Toward this goal, nanotechnology-based electrochemical approaches (26) have been growing in popularity, owing to their high sensitivity, low cost of testing, and rapid turnaround. Apropos to the pandemic era, Lissel and colleagues have designed (27) an organic field-effect transistor based on a stretchable triblock copolymer platform, for detection of the SARS-CoV-2 antigen as well as antibodies against the S1 protein. The OFET sensor showed a wide range of detection from 0.1 fg/mL to 1 μg/mL, with rapid test results in under 20 min. With favorable mechanical properties such as the ability to be stretched up to 90% without cracking, this low-cost biosensor can be potentially adapted to be incorporated into garments, lab-on-a-mask, as well as on-skin diagnostic platforms, offering dual functionality for detecting the virus antigen (active infection sensing) as well as presence of antibodies against the virus (immune surveillance). Two-dimensional nanomaterials such as graphene and its derivatives, transition metal dichalcogenides (TMDs, in the form of MX2, where M = Mo, W, Sn, Hf, etc. and X = S, Se, Te) and MXenes (in the form of Mn+1XnTx, n = 1–3, where M = Ti, Ta, Nb, Mo, Zr, Cr, etc. and X = C and/or N, and Tx represents the terminal groups OH, F, or O) are another emerging area of interest for biochemical sensing applications, owing to their unique planar structure and ability to be functionalized using bioinspired techniques, such as mussel-inspired polydopamine surface coatings (28) on graphene quantum dots for optical imaging. In this issue, Chen and co-workers describe (29) the fabrication of an annealed (30) graphene oxide (aGO)-based biosensor, which uses the effect of redistribution of the oxygen functional groups (31) to achieve enhanced bonding of a DNA probe on the GO nanosheet. Using this annealing technique, the authors have reported an enhancement factor of ∼19.6× for the aGO probes, compared to untreated GO, with the added benefit of higher stability of the aGO probes against fluorescence quenching under laser confocal microscopy. One of the most widely deployed applications of wearable devices such as the Apple Watch and other fitness sensors is for regular physiological monitoring of health signals, including step counting, sleep tracking, women’s health monitoring, and blood oxygen measurements, to name a few. With the global rise in the incidence of both adult and childhood obesity, the ability to identify obesity markers at an early stage is of utmost importance. Toward this goal, Nurunnabi and co-workers have developed (32) an impedimetric sensing platform for the selective detection of leptin, a hormone partially implicated in the obesity epidemic via the leptin resistance pathway. The LepSens device was shown to have a linear detection range from 500 fg/mL to 50 ng/mL, with a limit of detection ∼185 fg/mL, which makes it capable of detecting physiological levels of Lep in human plasma (∼20–100 ng/mL for healthy-obese individuals). With good sensitivity, high selectivity, and experimental stability and reproducibility, this biosensor platform could be potentially developed as a point-of-care diagnostic for measuring leptin levels in blood, for mitigating obesity. Finally, we conclude this issue with a deep dive into the world of point-of-care testing of cancer, in a review article by Quadir and colleagues. (33) The authors discuss the core design principles of wearable diagnostics for biosensors (WDBs) using bioinspiration, followed by the advances in disease signal detection and amplification. Advanced manufacturing processes, which allow for conformal devices to match the human anatomy are investigated, followed by the coupling of material properties to pathophysiological process to identify the hallmarks of cancer using WDBs. Beyond the diagnostic realm, the authors also discuss several new multiomics platforms for myriad applications of bioinspired sensors in cancer imaging, surgery, genetic mapping, and high-throughput noninvasive monitoring, to name a few. The authors also tabulate a diverse list of FDA-approved WDB sensors, devices, and detection kits used for biomedical applications. With the rapid advances in soft materials, sensing technologies, conformable structures, power generation systems, and wireless communication protocols as illustrated in Figure 2, multifunctional wearable systems that can be designed to mimic natural materials and shapes have seen exponential growth over the past few years, with a few biointegrated devices already available in the commercial market. (34) Taken together, we believe that the future is bright for emerging on-body, self-powered, machine learning-augmented bioinspired sensors for continuous monitoring, prevention, and early diagnosis of health conditions, with the goal of empowering individuals with real-time personalized data to lead a healthy life. Figure 2. An overview of the innovation drivers powering the next-generation wearable devices and biosensors. Top image reproduced from ref (35). Available under a CC BY-NC 4.0 license. Bottom right image reproduced with permission from ref (36). Copyright 2016 Elsevier. Bottom left image reprinted with permission. Image courtesy of Graham Rowlands, Raytheon BBN Technologies. Created with BioRender.com. N.M.B. wrote the manuscript. M.R. and M.N. edited, revised, and provided feedback on the manuscript. This article references 36 other publications. This article has not yet been cited by other publications. Figure 1. Key ideas and concepts discussed in this Special Issue on Bioinspired Materials for Wearable Diagnostics and Biosensors. Figure 2. An overview of the innovation drivers powering the next-generation wearable devices and biosensors. Top image reproduced from ref (35). Available under a CC BY-NC 4.0 license. Bottom right image reproduced with permission from ref (36). Copyright 2016 Elsevier. Bottom left image reprinted with permission. Image courtesy of Graham Rowlands, Raytheon BBN Technologies. Created with BioRender.com. This article references 36 other publications.
更新日期：2023-05-08
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