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Autonomous Sweat Extraction and Analysis Applied to Cystic Fibrosis and Glucose Monitoring Using a Fully Integrated Wearable Platform

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Autonomous Sweat Extraction and Analysis Applied to Cystic Fibrosis and Glucose Monitoring Using a Fully Integrated Wearable Platform Autonomous sweat extraction and analysis applied to cystic fibrosis and glucose monitoring using a fully integrated wearable platform Sam Emaminejada,b,c,d,1,2, Wei Gaob,c,d,1, Eric Wub, Zoe A. Daviese, Hnin Yin Yin Nyeinb,c,d, Samyuktha Challaa,f, Sean P. Ryane, Hossain M. Fahadb,c,d, Kevin Chenb,c,d, Ziba Shahparb,c,d, Salmonn Talebia,f, Carlos Millaf,3, Ali Javeyb,c,d,3, and Ronald W. Davisa,3 aStanford Genome Technology Center, Stanford School of Medicine, Palo Alto, CA 94304; bDepartment of Electrical Engineering and Computer Sciences, University of California, Berkeley, CA 94720; cBerkeley Sensor and Actuator Center, University of California, Berkeley, CA 94720; dMaterials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720; eThe Stanford Cystic Fibrosis Center, Center for Excellence in Pulmonary Biology, Stanford School of Medicine, Palo Alto, CA 94305; and fDepartment of Electrical Engineering, Stanford University, Stanford, CA 94305 Contributed by Ronald W. Davis, February 14, 2017 (sent for review December 15, 2016; reviewed by Maneesh Jain and Andre Marziali) Perspiration-based wearable biosensors facilitate continuous moni- to limit our ability to capitalize on this noninvasive and rich source toring of individuals’ health states with real-time and molecular-level of information for broad population monitoring. A wearable and insight. The inherent inaccessibility of sweat in sedentary individuals miniaturized iontophoresis interface is an excellent solution to in large volume (≥10 μL) for on-demand and in situ analysis has overcome this barrier. The iontophoresis process involves delivery limited our ability to capitalize on this noninvasive and rich source of stimulating agonists to the sweat glands with the aid of an of information. A wearable and miniaturized iontophoresis interface electrical current. The challenge remains in devising an ionto- is an excellent solution to overcome this barrier. The iontophoresis phoresis interface that can extract and deliver sufficient amount of process involves delivery of stimulating agonists to the sweat glands sweat to the sensor surface for robust sensing, without electrode with the aid of an electrical current. The challenge remains in de- corrosion and burning/causing discomfort in subjects. vising an iontophoresis interface that can extract sufficient amount Iontophoresis is currently a widely used method to stimulate of sweat for robust sensing, without electrode corrosion and burn- local sweat secretion at a selected site (21). The conventional ing/causing discomfort in subjects. Here, we overcame this challenge procedure involves stimulation, collection, and analysis all in sep- through realizing an electrochemically enhanced iontophoresis inter- arate steps, which not only requires extensive manual sample face, integrated in a wearable sweat analysis platform. This interface handling steps, but also fails to provide real-time insight into the can be programmed to induce sweat with various secretion profiles secretion process. Despite the technological shortcomings, sweat for real-time analysis, a capability which can be exploited to advance analysis has shown great potential for a variety of clinical and our knowledge of the sweat gland physiology and the secretion physiological applications. For example, the sweat chloride level in process. To demonstrate the clinical value of our platform, human iontophoresis-extracted sweat sample is currently considered the subject studies were performed in the context of the cystic fibrosis diagnosis and preliminary investigation of the blood/sweat glucose Significance correlation. With our platform, we detected the elevated sweat elec- trolyte content of cystic fibrosis patients compared with that of The inherent inaccessibility of sweat in sedentary individuals in healthy control subjects. Furthermore, our results indicate that oral large volume (≥10 μL) for on-demand and in situ analysis has glucose consumption in the fasting state is followed by increased limited our ability to capitalize on this noninvasive and rich source glucose levels in both sweat and blood. Our solution opens the of information. Through devising an electrochemically enhanced, possibility for a broad range of noninvasive diagnostic and general programmable, and miniaturized iontophoresis interface, in- population health monitoring applications. tegrated in a wearable sensing platform, we demonstrated a method for periodic sweat extraction and in situ analysis. The wearable | biosensors | noninvasive | iontophoresis | system can be programmed to induce sweat with various secre- personalized medicine tion profiles, which in combination with the in situ analysis ca- pability allow us to gain real-time insight into the sweat-secretion earable biosensors have received considerable attention and gland physiology. To demonstrate the clinical value of our owing to their great promise for a wide range of clinical and platform, human subject studies were performed in the context W ENGINEERING physiological applications (1–10). Despite significant progress of the cystic fibrosis diagnosis and preliminary investigation of made in printed and flexible biosensors in the field, a majority of the blood/sweat glucose correlation. wearable devices focus on monitoring of physical activity or se- lected electrophysiological parameters, providing only limited in- Author contributions: S.E., W.G., C.M., A.J., and R.W.D. designed research; S.E., W.G., formation regarding physiological changes of complex homeostatic E.W., Z.A.D., H.Y.Y.N., S.C., S.P.R., H.M.F., K.C., Z.S., S.T., C.M., A.J., and R.W.D. performed – research; S.E., W.G., E.W., C.M., A.J., and R.W.D. contributed new reagents/analytic tools; responses (4 10). Wearable chemical sensors offer great oppor- S.E., W.G., E.W., C.M., A.J., and R.W.D. analyzed data; and S.E., W.G., E.W., C.M., A.J., and tunities for collecting physiological information at the molecular R.W.D. wrote the paper. level (3, 9–19). Recently research advances have resulted in a va- Reviewers: M.J., Cirina; and A.M., University of British Columbia. PHYSIOLOGY riety of wearable sweat sensors that can be used for real-time The authors declare no conflict of interest. analysis of sweat biomarkers including electrolytes, metabolites, Freely available online through the PNAS open access option. and heavy metals (11–20). We recently demonstrated a fully in- 1S.E. and W.G. contributed equally to this work. tegrated wearable sensing system for real-time monitoring of 2Present address: Department of Electrical Engineering, University of California, Los An- multiple analytes in human perspiration during physical exercise geles, CA 90095. which allows accurate measurement of sweat analytes through 3To whom correspondence may be addressed. Email: [email protected], ajavey@ signal processing and calibration (16). berkeley.edu, or [email protected]. The inherent inaccessibility of sweat in sedentary individuals in This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. large volume (≥10 μL) for on-demand and in situ analysis remains 1073/pnas.1701740114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1701740114 PNAS | May 2, 2017 | vol. 114 | no. 18 | 4625–4630 Downloaded by guest on October 1, 2021 gold standard for screening cystic fibrosis (CF), a genetic chronic This system implements a wirelessly programmable iontophoresis disease that affects lungs and digestive system (21–23). A strong capability to induce sweat with different excretion rate profiles and correlation between blood and sweat ethanol concentrations has at periodic time intervals. Through integration of sensing electrodes been reported which could enable continuous blood-alcohol mon- on the same substrate as that of the iontophoresis electrodes, the induced sweat can be analyzed on-site immediately. The sensors are itoring by sweat analysis (24, 25). In a recent work, real-time sweat + − ethanol monitoring using a wearable tattoo-based iontophoretic- capable of quantifying sweat Na ,Cl , and glucose, with high sen- biosensing system has been developed (20). Sweat extracted from sitivity in the physiologically relevant ranges of interest. As shown in iontophoresis has also been shown to contain glucose levels that can Fig. 1, our platform consists of an electrode array, containing the sweat induction and sensing electrodes, integrated with a wireless accurately reflect blood glucose (26). flexible printed circuit board (FPCB). The independent function- Here, we devised an electrochemically enhanced iontophoresis ality of the individual sensors and the iontophoresis process is interface which can extract sufficient sweat volume for robust preserved through electrically decoupling the switchable sweat analysis without causing discomfort in patients. This interface can sensing and sweat induction modes of operation (Fig. 1C). be programmed to induce sweat periodically with various secretion The electrodes were patterned on a mechanically flexible poly- profiles. Hence, it can be used to gain an unprecedented insight ethylene terephthalate (PET) substrate to form a stable sensor–skin into the secretion process to advance the state of the science and contact (Fig. 1B). The sweat induction electrodes interface the skin our knowledge of the sweat gland physiology. Accordingly, we in- with a thin layer of agonist agent hydrogel in between. To electri- tegrated this capability to demonstrate a fully integrated and au- cally
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