Ammonium Sensing Patch with Ultrawide Linear Range and Eliminated Interference for Universal Body Fluids Analysis
Corresponding Author: Yuanjing Lin
Nano-Micro Letters,
Vol. 17 (2025), Article Number: 92
Abstract
Ammonium level in body fluids serves as one of the critical biomarkers for healthcare, especially those relative to liver diseases. The continuous and real-time monitoring in both invasive and non-invasive manners is highly desired, while the ammonium concentrations vary largely in different body fluids. Besides, the sensing reliability based on ion-selective biosensors can be significantly interfered by potassium ions. To tackle these challenges, a flexible and biocompatible sensing patch for wireless ammonium level sensing was reported with an ultrawide linear range for universal body fluids including blood, tears, saliva, sweat and urine. The as-prepared biocompatible sensors deliver a reliable sensitivity of 58.7 mV decade−1 in the range of 1–100 mM and a desirable selectivity coefficient of 0.11 in the interference of potassium ions, attributed to the cross-calibration within the sensors array. The sensor’s biocompatibility was validated by the cell growth on the sensor surface (> 80%), hemolysis rates (< 5%), negligible cellular inflammatory responses and weight changes of the mice with implanted sensors. Such biocompatible sensors with ultrawide linear range and desirable selectivity open up new possibility of highly compatible biomarker analysis via different body fluids in versatile approaches.
Highlights:
1 The as-prepared sensors can detect NH4+ in the body fluids with a high sensitivity of 58.7 mV decade−1 and an ultrawide detection range of 1–100 mM.
2 The biocompatible sensors exhibit desirable biocompatibility and minimal toxicity for continuous and long-term monitoring.
3 The average detection error of the integrated and wireless biosensing patch was 13.2%, and body fluid detection accuracy is improved by more than 18% after cross-calibration.
Keywords
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- Z. Liang, C.E. Wilson, B. Teng, S.C. Kinnamon, E.R. Liman, The proton channel OTOP1 is a sensor for the taste of ammonium chloride. Nat. Commun. 14, 6194 (2023). https://doi.org/10.1038/s41467-023-41637-4
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- R. Das, F. Moradi, H. Heidari, Biointegrated and wirelessly powered implantable brain devices: a review. IEEE Trans. Biomed. Circuits Syst. 14, 343–358 (2020). https://doi.org/10.1109/TBCAS.2020.2966920
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References
Z. Liang, C.E. Wilson, B. Teng, S.C. Kinnamon, E.R. Liman, The proton channel OTOP1 is a sensor for the taste of ammonium chloride. Nat. Commun. 14, 6194 (2023). https://doi.org/10.1038/s41467-023-41637-4
W. Lv, J. Yang, Q. Xu, J.A.-A. Mehrez, J. Shi et al., Wide-range and high-accuracy wireless sensor with self-humidity compensation for real-time ammonia monitoring. Nat. Commun. 15, 6936 (2024). https://doi.org/10.1038/s41467-024-51279-9
Y. Yu, J. Nassar, C. Xu, J. Min, Y. Yang et al., Biofuel-powered soft electronic skin with multiplexed and wireless sensing for human-machine interfaces. Sci. Robot. 5, eaaz7946 (2020). https://doi.org/10.1126/scirobotics.aaz7946
M. Mallet, V. Desplats, C. Bouzbib, P. Sultanik, I. Alioua et al., Blood ammonia in patients with chronic liver diseases: A better defined role in clinical practice. Anal. Biochem. 657, 114873 (2022). https://doi.org/10.1016/j.ab.2022.114873
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D.L. Ramada, J. de Vries, J. Vollenbroek, N. Noor, O. ter Beek et al., Portable, wearable and implantable artificial kidney systems: needs, opportunities and challenges. Nat. Rev. Nephrol. 19, 481–490 (2023). https://doi.org/10.1038/s41581-023-00726-9
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T.H. Tranah, M.P. Ballester, J.A. Carbonell-Asins, J. Ampuero, G. Alexandrino et al., Plasma ammonia levels predict hospitalisation with liver-related complications and mortality in clinically stable outpatients with cirrhosis. J. Hepatol. 77, 1554–1563 (2022). https://doi.org/10.1016/j.jhep.2022.07.014
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H. Seethapathy, A.Z. Fenves, Pathophysiology and management of hyperammonemia in organ transplant patients. Am. J. Kidney Dis. 74, 390–398 (2019). https://doi.org/10.1053/j.ajkd.2019.03.419
Y.Y. Jin, P. Singh, H.J. Chung, S.T. Hong, Blood ammonia as a possible etiological agent for Alzheimer’s disease. Nutrients 10, 564 (2018). https://doi.org/10.3390/nu10050564
V. Massafra, A. Milona, H.R. Vos, R.J.J. Ramos, J. Gerrits et al., Farnesoid X receptor activation promotes hepatic amino acid catabolism and ammonium clearance in mice. Gastroenterology 152, 1462-1476.e10 (2017). https://doi.org/10.1053/j.gastro.2017.01.014
M.M. Adeva, G. Souto, N. Blanco, C. Donapetry, Ammonium metabolism in humans. Metabolism 61, 1495–1511 (2012). https://doi.org/10.1016/j.metabol.2012.07.007
H.Y.Y. Nyein, M. Bariya, B. Tran, C.H. Ahn, B.J. Brown et al., A wearable patch for continuous analysis of thermoregulatory sweat at rest. Nat. Commun. 12, 1823 (2021). https://doi.org/10.1038/s41467-021-22109-z
L. Salvigni, P.D. Nayak, A. Koklu, D. Arcangeli, J. Uribe et al., Reconfiguration of organic electrochemical transistors for high-accuracy potentiometric sensing. Nat. Commun. 15, 6499 (2024). https://doi.org/10.1038/s41467-024-50792-1
E. Shirzaei Sani, C. Xu, C. Wang, Y. Song, J. Min et al., A stretchable wireless wearable bioelectronic system for multiplexed monitoring and combination treatment of infected chronic wounds. Sci. Adv. 9, eadf7388 (2023). https://doi.org/10.1126/sciadv.adf7388
T.R. Veltman, C.J. Tsai, N. Gomez-Ospina, M.W. Kanan, G. Chu, Point-of-care analysis of blood ammonia with a gas-phase sensor. ACS Sens. 5, 2415–2421 (2020). https://doi.org/10.1021/acssensors.0c00480
X. Ma, Z. Jiang, Y. Lin, Flexible energy storage devices for wearable bioelectronics. J. Semicond. 42(10), 101602 (2021). https://doi.org/10.1088/1674-4926/42/10/101602
S.N.A.B.M. Nashruddin, F.H.M. Salleh, A.A.M. Raub, Early detection of kidney problems through voltammetry, potentiometry, amperometry, and impedance electrochemical techniques: a comprehensive review. Measurement 230, 114475 (2024). https://doi.org/10.1016/j.measurement.2024.114475
Y. Shi, Z. Zhang, Q. Huang, Y. Lin, Z. Zheng, Wearable sweat biosensors on textiles for health monitoring. J. Semicond. 44, 021601 (2023). https://doi.org/10.1088/1674-4926/44/2/021601
L.R. Jaishi, J. Yu, W. Ding, F. Tsow, X. Xian, A novel colorimetric tuning fork sensor for ammonia monitoring. Sens. Actuat. B Chem. 405, 135342 (2024). https://doi.org/10.1016/j.snb.2024.135342
D. Li, X. Xu, Z. Li, T. Wang, C. Wang, Detection methods of ammonia nitrogen in water: a review. Trac Trends Anal. Chem. 127, 115890 (2020). https://doi.org/10.1016/j.trac.2020.115890
Q. Hua, G. Shen, A wearable sweat patch for non-invasive and wireless monitoring inflammatory status. J. Semicond. 44, 100401 (2023). https://doi.org/10.1088/1674-4926/44/10/100401
Z. Shi, P. Deng, L.-A. Zhou, M. Jin, F. Fang et al., Wireless and battery-free wearable biosensing of riboflavin in sweat for precision nutrition. Biosens. Bioelectron. 251, 116136 (2024). https://doi.org/10.1016/j.bios.2024.116136
W. Quan, J. Shi, M. Zeng, W. Lv, X. Chen et al., Highly sensitive ammonia gas sensors at room temperature based on the catalytic mechanism of N, C coordinated Ni single-atom active center. Nano-Micro Lett. 16, 277 (2024). https://doi.org/10.1007/s40820-024-01484-4
Y. Luo, M.R. Abidian, J.-H. Ahn, D. Akinwande, A.M. Andrews et al., Technology roadmap for flexible sensors. ACS Nano 17, 5211–5295 (2023). https://doi.org/10.1021/acsnano.2c12606
I.D. Weiner, J.W. Verlander, Ammonia transporters and their role in acid-base balance. Physiol. Rev. 97, 465–494 (2017). https://doi.org/10.1152/physrev.00011.2016
L. Xu, L. Zhong, Y. Tang, T. Han, S. Liu et al., Beyond nonactin: potentiometric ammonium ion sensing based on ion-selective membrane-free Prussian blue analogue transducers. Anal. Chem. 94, 10487–10496 (2022). https://doi.org/10.1021/acs.analchem.2c01765
R.J. Barsotti, Measurement of ammonia in blood. J. Pediatr. 138, S11–S20 (2001). https://doi.org/10.1067/mpd.2001.111832
E. Bakker, E. Pretsch, P. Bühlmann, Selectivity of potentiometric ion sensors. Anal. Chem. 72, 1127–1133 (2000). https://doi.org/10.1021/ac991146n
F. Fuhrmann, W. Seichter, M. Mazik, Selective recognition of ammonium over potassium ion with acyclic receptor molecules bearing 3, 4, 5-trialkylpyrazolyl groups. Organic Mater. 4, 61–72 (2022). https://doi.org/10.1055/a-1896-6890
M. Cuartero, N. Colozza, B.M. Fernández-Pérez, G.A. Crespo, Why ammonium detection is particularly challenging but insightful with ionophore-based potentiometric sensors - an overview of the progress in the last 20 years. Analyst 145, 3188–3210 (2020). https://doi.org/10.1039/d0an00327a
Y. Shi, K. Zhou, X. Ma, L. Huang, X. Hu et al., Washable textile biosensors enabled by nanostructured oxides with fast ion diffusion. Device 2, 100503 (2024). https://doi.org/10.1016/j.device.2024.100503
K. Zhou, R. Ding, X. Ma, Y. Lin, Printable and flexible integrated sensing systems for wireless healthcare. Nanoscale 16, 7264–7286 (2024). https://doi.org/10.1039/d3nr06099c
R. Das, F. Moradi, H. Heidari, Biointegrated and wirelessly powered implantable brain devices: a review. IEEE Trans. Biomed. Circuits Syst. 14, 343–358 (2020). https://doi.org/10.1109/TBCAS.2020.2966920
C. Li, C. Guo, V. Fitzpatrick, A. Ibrahim, M.J. Zwierstra et al., Design of biodegradable, implantable devices towards clinical translation. Nat. Rev. Mater. 5, 61–81 (2019). https://doi.org/10.1038/s41578-019-0150-z
K. Nan, K. Wong, D. Li, B. Ying, J.C. McRae et al., An ingestible, battery-free, tissue-adhering robotic interface for non-invasive and chronic electrostimulation of the gut. Nat. Commun. 15, 6749 (2024). https://doi.org/10.1038/s41467-024-51102-5
L. Crawford, M. Wyatt, J. Bryers, B. Ratner, Biocompatibility evolves: phenomenology to toxicology to regeneration. Adv. Healthc. Mater. 10, e2002153 (2021). https://doi.org/10.1002/adhm.202002153
Y. Liu, H. Jia, H. Sun, S. Jia, Z. Yang et al., A high-density 1, 024-channel probe for brain-wide recordings in non-human Primates. Nat. Neurosci. 27, 1620–1631 (2024). https://doi.org/10.1038/s41593-024-01692-6
X. Ma, P. Wang, L. Huang, R. Ding, K. Zhou et al., A monolithically integrated in-textile wristband for wireless epidermal biosensing. Sci. Adv. 9, eadj2763 (2023). https://doi.org/10.1126/sciadv.adj2763
P. Wang, X. Ma, Z. Lin, F. Chen, Z. Chen et al., Well-defined in-textile photolithography towards permeable textile electronics. Nat. Commun. 15, 887 (2024). https://doi.org/10.1038/s41467-024-45287-y
J. Zhou, S. Zhou, P. Fan, X. Li, Y. Ying et al., Implantable electrochemical microsensors for in vivo monitoring of animal physiological information. Nano-Micro Lett. 16, 49 (2023). https://doi.org/10.1007/s40820-023-01274-4
R. Athavale, N. Pankratova, C. Dinkel, E. Bakker, B. Wehrli et al., Fast potentiometric CO2 sensor for high-resolution in situ measurements in fresh water systems. Environ. Sci. Technol. 52, 11259–11266 (2018). https://doi.org/10.1021/acs.est.8b02969
S.K. Berezin, Valinomycin as a classical anionophore: mechanism and ion selectivity. J. Membr. Biol. 248, 713–726 (2015). https://doi.org/10.1007/s00232-015-9784-y
M. Weber, H. Steinle, S. Golombek, L. Hann, C. Schlensak et al., Blood-contacting biomaterials: in vitro evaluation of the hemocompatibility. Front. Bioeng. Biotechnol. 6, 99 (2018). https://doi.org/10.3389/fbioe.2018.00099
B. Martínez-Haya, J.R. Avilés-Moreno, F. Gámez, G. Berden, J. Oomens, Preferential host-guest coordination of nonactin with ammonium and hydroxylammonium. J. Chem. Phys. 149, 225101 (2018). https://doi.org/10.1063/1.5049956
J.R. Avilés-Moreno, F. Gámez, G. Berden, J. Oomens, B. Martínez-Haya, Inclusion complexes of the macrocycle nonactin with benchmark protonated amines: Aniline and serine. Phys. Chem. Chem. Phys. 24, 8422–8431 (2022). https://doi.org/10.1039/d2cp00264g
L.A. Cynober, Plasma amino acid levels with a note on membrane transport: characteristics, regulation, and metabolic significance. Nutrition 18, 761–766 (2002). https://doi.org/10.1016/s0899-9007(02)00780-3