Abstract
Graphene has emerged as a champion material for a variety of applications cutting across multiple disciplines in science and engineering. Graphene and its derivatives have displayed huge potential as a biosensing material due to their unique physicochemical properties, good electrical conductivity, optical properties, biocompatibility, ease of functionalization, and flexibility. Their widespread use in making biosensors has opened up new possibilities for early diagnosis of life-threatening diseases and real-time health monitoring. Following an introduction and discussion on the significance of fabrication protocols and assembly, this review is intended to assess why graphene is suitable to build better biosensors, the working of existing biosensing schemes and their current status toward commercialization for wearable diagnostic and prognostic devices. We believe this review will provide a critical insight for harnessing graphene as a suitable biosensor for the clinical diagnostics, its future prospects and challenges ahead.
Similar content being viewed by others
References
S.P. Mohanty and E. Kougianos: Biosensors: A tutorial review. IEEE Potentials 25(2), 35 (2006).
A. Darwish and A.E. Hassanien: Wearable and implantable wireless sensor network solutions for healthcare monitoring. Sensors 11(6), 5561 (2011).
P. Mehrotra: Biosensors and their applications—A review. J. Oral. Biol. Craniofac. Res. 6(2), 153 (2016).
S. Wang, T. Chinnasamy, M.A. Lifson, F. Inci, and U. Demirci: Flexible substrate-based devices for point-of-care diagnostics. Trends Biotechnol. 34(11), 909 (2016).
S.A. Soper and A. Rasooly: Cancer: A global concern that demands new detection technologies. Analyst 141(2), 367 (2016).
S. Gs, A. Cv, and B.B. Mathew: Biosensors: A modern day achievement. J. Instrum. Technol. 2(1), 26 (2014).
A. Nehra and K. Pal Singh: Current trends in nanomaterial embedded field effect transistor-based biosensor. Biosens. Bioelectron. 74, 731 (2015).
M. Holzinger, A. Le Goff, and S. Cosnier: Nanomaterials for biosensing applications: A review. Front. Chem. 2 (2014), doi: https://doi.org/10.3389/fchem.2014.00063.
A.B. Chinen, C.M. Guan, J.R. Ferrer, S.N. Barnaby, T.J. Merkel, and C.A. Mirkin: Nanoparticle probes for the detection of cancer biomarkers, cells, and tissues by fluorescence. Chem. Rev. 115(19), 10530 (2015).
N. Yang, X. Chen, T. Ren, P. Zhang, and D. Yang: Carbon nanotube based biosensors. Sens. Actuators, B 207(Part A), 690 (2015).
T-T. Tran and A. Mulchandani: Carbon nanotubes and graphene nano field-effect transistor-based biosensors. TrAC, Trends Anal. Chem. 79, 222 (2016).
A.B. Kaul: Two-dimensional layered materials: Structure, properties, and prospects for device applications. J. Mater. Res. 29(3), 348 (2014).
A.K. Geim and K.S. Novoselov: The rise of graphene. Nat. Mater. 6(3), 183 (2007).
A.C. Ferrari, F. Bonaccorso, V. Fal’ko, K.S. Novoselov, S. Roche, P. Bøggild, S. Borini, F.H.L. Koppens, V. Palermo, N. Pugno, J.A. Garrido, R. Sordan, A. Bianco, L. Ballerini, M. Prato, E. Lidorikis, J. Kivioja, C. Marinelli, T. Ryhänen, A. Morpurgo, J.N. Coleman, V. Nicolosi, L. Colombo, A. Fert, M. Garcia-Hernandez, A. Bachtold, G.F. Schneider, F. Guinea, C. Dekker, M. Barbone, Z. Sun, C. Galiotis, A.N. Grigorenko, G. Konstantatos, A. Kis, M. Katsnelson, L. Vandersypen, A. Loiseau, V. Morandi, D. Neumaier, E. Treossi, V. Pellegrini, M. Polini, A. Tredicucci, G.M. Williams, B.H. Hong, J-H. Ahn, J.M. Kim, H. Zirath, B.J. van Wees, H. van der Zant, L. Occhipinti, A.D. Matteo, I.A. Kinloch, T. Seyller, E. Quesnel, X. Feng, K. Teo, N. Rupesinghe, P. Hakonen, S.R.T. Neil, Q. Tannock, T. Löfwander, and J. Kinaret: Science and technology roadmap for graphene, related two-dimensional crystals, and hybrid systems. Nanoscale 7(11), 4598 (2015).
L. Feng, L. Wu, and X. Qu: New horizons for diagnostics and therapeutic applications of graphene and graphene oxide. Adv. Mater. 25(2), 168 (2013).
D. Sharma, S. Kanchi, M.I. Sabela, and K. Bisetty: Insight into the biosensing of graphene oxide: Present and future prospects. Arabian J. Chem. 9(2), 238 (2016).
C.S. Park, H. Yoon, and O.S. Kwon: Graphene-based nanoelectronic biosensors. J. Ind. Eng. Chem. 38, 13 (2016).
D. Du, Y. Yang, and Y. Lin: Graphene-based materials for biosensing and bioimaging. MRS Bull. 37(12), 1290 (2012).
N. Celik, W. Balachandran, and N. Manivannan: Graphene-based biosensors: Methods, analysis and future perspectives. IET Circ. Device. Syst. 9(6), 434 (2015).
E. Morales-Narváez, L. Baptista-Pires, A. Zamora-Gálvez, and A. Merkoçi: Graphene-based biosensors: Going simple. Adv. Mater. 29(7) (2016), doi: https://doi.org/10.1002/adma.201604905.
S.M.A. Cruz, A.F. Girão, G. Gonçalves, and P.A.A.P. Marques: Graphene: The missing piece for cancer diagnosis?Sensors 16(1), E137 (2016).
M. Pumera: Graphene in biosensing. Mater. Today 14(7–8), 308 (2011).
J. Lee, J. Kim, S. Kim, and D-H. Min: Biosensors based on graphene oxide and its biomedical application. Adv. Drug Delivery Rev. 105(Part B), 275 (2016).
Y. Liu, X. Dong, and P. Chen: Biological and chemical sensors based on graphene materials. Chem. Soc. Rev. 41(6), 2283 (2012).
X. Zhu, Y. Liu, P. Li, Z. Nie, and J. Li: Applications of graphene and its derivatives in intracellular biosensing and bioimaging. Analyst 141(15), 4541 (2016).
L.C. Clark and C. Lyons: Electrode systems for continuous monitoring in cardiovascular surgery. Ann. N. Y. Acad. Sci. 102(1), 29 (1962).
P. Pandey, M. Datta, and B.D. Malhotra: Prospects of nanomaterials in biosensors. Anal. Lett. 41(2), 159 (2008).
P. Malik, V. Katyal, V. Malik, A. Asatkar, G. Inwati, and T.K. Mukherjee: Nanobiosensors: Concepts and variations. Int. Scholarly Res. Not. 2013, e327435 (2013).
E. Juanola-Feliu, P.L. Miribel-Català, C. Páez Avilés, J. Colomer-Farrarons, M. González-Piñero, and J. Samitier: Design of a customized multipurpose nano-enabled implantable system for in vivo theranostics. Sensors 14(10), 19275 (2014).
E. Ghafar-Zadeh: Wireless integrated biosensors for point-of-care diagnostic applications. Sensors 15(2), 3236 (2015).
K.S. Novoselov, A.K. Geim, S.V. Morozov, D. Jiang, Y. Zhang, S.V. Dubonos, I.V. Grigorieva, and A.A. Firsov: Electric field effect in atomically thin carbon films. Science 306(5696), 666 (2004).
A.H. Castro Neto, F. Guinea, N.M.R. Peres, K.S. Novoselov, and A.K. Geim: The electronic properties of graphene. Rev. Mod. Phys. 81(1), 109 (2009).
E. Morales-Narváez and A. Merkoçi: Graphene oxide as an optical biosensing platform. Adv. Mater. 24(25), 3298 (2012).
R.R. Nair, W.C. Ren, R. Jalil, I. Riaz, V.G. Kravets, L. Britnell, P. Blake, F. Schedin, A.S. Mayorov, S. Yuan, M.I. Katsnelson, H.M. Cheng, W. Strupinski, L.G. Bulusheva, A.V. Okotrub, I.V. Grigorieva, A.N. Grigorenko, K.S. Novoselov, and A.K. Geim: Fluorographene: Two dimensional counterpart of teflon. Small 6(24), 2877 (2010).
J. Yao, Y. Sun, M. Yang, and Y. Duan: Chemistry, physics and biology of graphene-based nanomaterials: New horizons for sensing, imaging and medicine. J. Mater. Chem. 22(29), 14313 (2012).
X.T. Zheng, A. Ananthanarayanan, K.Q. Luo, and P. Chen: Glowing graphene quantum dots and carbon dots: Properties, syntheses, and biological applications. Small 11(14), 1620 (2015).
M. Nurunnabi, K. Parvez, M. Nafiujjaman, V. Revuri, H.A. Khan, X. Feng, and Y. Lee: Bioapplication of graphene oxide derivatives: Drug/gene delivery, imaging, polymeric modification, toxicology, therapeutics and challenges. RSC Adv. 5(52), 42141 (2015).
V. Urbanová, F. Karlický, A. Matěj, F. Šembera, Z. Janoušek, J.A. Perman, V. Ranc, K. Čépe, J. Michl, M. Otyepka, and R. Zbořil: Fluorinated graphenes as advanced biosensors—Effect of fluorine coverage on electron transfer properties and adsorption of biomolecules. Nanoscale 8(24), 12134 (2016).
P. Avouris: Graphene: Electronic and photonic properties and devices. Nano Lett. 10(11), 4285 (2010).
Y. Zhu, S. Murali, W. Cai, X. Li, J.W. Suk, J.R. Potts, and R.S. Ruoff: Graphene and graphene oxide: Synthesis, properties, and applications. Adv. Mater. 22(35), 3906 (2010).
N.O. Weiss, H. Zhou, L. Liao, Y. Liu, S. Jiang, Y. Huang, and X. Duan: Graphene: An emerging electronic material. Adv. Mater. 24(43), 5782 (2012).
X. Du, I. Skachko, A. Barker, and E.Y. Andrei: Approaching ballistic transport in suspended graphene. Nat. Nanotechnol. 3(8), 491 (2008).
K.I. Bolotin, K.J. Sikes, Z. Jiang, M. Klima, G. Fudenberg, J. Hone, P. Kim, and H.L. Stormer: Ultrahigh electron mobility in suspended graphene. Solid State Commun. 146(9–10), 351 (2008).
S.V. Morozov, K.S. Novoselov, M.I. Katsnelson, F. Schedin, D.C. Elias, J.A. Jaszczak, and A.K. Geim: Giant intrinsic carrier mobilities in graphene and its bilayer. Phys. Rev. Lett. 100(1), 016602 (2008).
V. Georgakilas, J.N. Tiwari, K.C. Kemp, J.A. Perman, A.B. Bourlinos, K.S. Kim, and R. Zboril: Noncovalent functionalization of graphene and graphene oxide for energy materials, biosensing, catalytic, and biomedical applications. Chem. Rev. 116(9), 5464 (2016).
V. Georgakilas, M. Otyepka, A.B. Bourlinos, V. Chandra, N. Kim, K.C. Kemp, P. Hobza, R. Zboril, and K.S. Kim: Functionalization of graphene: Covalent and non-covalent approaches, derivatives and applications. Chem. Rev. 112(11), 6156 (2012).
C.K. Chua and M. Pumera: Covalent chemistry on graphene. Chem. Soc. Rev. 42(8), 3222 (2013).
M. Mandal, A. Maitra, T. Das, and C.K. Das: Graphene and related two-dimensional materials. In Graphene Materials: Fundamentals and Emerging Applications, A. Tiwari and M. Syväjärvi, eds. (John Wiley & Sons, Inc., Hoboken, 2015); pp. 3–23.
M.J. Allen, V.C. Tung, and R.B. Kaner: Honeycomb carbon: A review of graphene. Chem. Rev. 110(1), 132 (2010).
Y. Wang, Z. Li, J. Wang, J. Li, and Y. Lin: Graphene and graphene oxide: Biofunctionalization and applications in biotechnology. Trends Biotechnol. 29(5), 205 (2011).
K. Yang, Y. Li, X. Tan, R. Peng, and Z. Liu: Behavior and toxicity of graphene and its functionalized derivatives in biological systems. Small 9(9–10), 1492 (2013).
A. Bianco: Graphene: Safe or toxic? The two faces of the medal. Angew. Chem., Int. Ed. 52(19), 4986 (2013).
L. Ou, B. Song, H. Liang, J. Liu, X. Feng, B. Deng, T. Sun, and L. Shao: Toxicity of graphene-family nanoparticles: A general review of the origins and mechanisms. Part. Fibre Toxicol. 13, 57 (2016).
M. Pelin, L. Fusco, V. León, C. Martín, A. Criado, S. Sosa, E. Vázquez, A. Tubaro, and M. Prato: Differential cytotoxic effects of graphene and graphene oxide on skin keratinocytes. Sci. Rep. 7, 40572 (2017).
K. Wang, J. Ruan, H. Song, J. Zhang, Y. Wo, S. Guo, and D. Cui: Biocompatibility of graphene oxide. Nanoscale Res. Lett. 6(1), 8 (2010).
A. Schinwald, F.A. Murphy, A. Jones, W. MacNee, and K. Donaldson: Graphene-based nanoplatelets: A new risk to the respiratory system as a consequence of their unusual aerodynamic properties. ACS Nano 6(1), 736 (2012).
J-H. Liu, S-T. Yang, H. Wang, Y. Chang, A. Cao, and Y. Liu: Effect of size and dose on the biodistribution of graphene oxide in mice. Nanomedicine 7(12), 1801 (2012).
X. Guo and N. Mei: Assessment of the toxic potential of graphene family nanomaterials. J. Food Drug Anal. 22(1), 105 (2014).
M. Xu, J. Zhu, F. Wang, Y. Xiong, Y. Wu, Q. Wang, J. Weng, Z. Zhang, W. Chen, and S. Liu: Improved in vitro and in vivo biocompatibility of graphene oxide through surface modification: Poly(acrylic acid)-functionalization is superior to PEGylation. ACS Nano 10(3), 3267 (2016).
N.R. Jacobsen, G. Pojana, P. White, P. Møller, C.A. Cohn, K.S. Korsholm, U. Vogel, A. Marcomini, S. Loft, and H. Wallin: Genotoxicity, cytotoxicity, and reactive oxygen species induced by single-walled carbon nanotubes and C(60) fullerenes in the FE1-Mutatrade markMouse lung epithelial cells. Environ. Mol. Mutagen. 49(6), 476 (2008).
S. Bengtson, K. Kling, A.M. Madsen, A.W. Noergaard, N.R. Jacobsen, P.A. Clausen, B. Alonso, A. Pesquera, A. Zurutuza, R. Ramos, H. Okuno, J. Dijon, H. Wallin, and U. Vogel: No cytotoxicity or genotoxicity of graphene and graphene oxide in murine lung epithelial FE1 cells in vitro. Environ. Mol. Mutagen. 57(6), 469 (2016).
K. Yang, J. Wan, S. Zhang, B. Tian, Y. Zhang, and Z. Liu: The influence of surface chemistry and size of nanoscale graphene oxide on photothermal therapy of cancer using ultra-low laser power. Biomaterials 33(7), 2206 (2012).
N. Morimoto, T. Kubo, and Y. Nishina: Tailoring the oxygen content of graphite and reduced graphene oxide for specific applications. Sci. Rep. 6, 21715 (2016).
W. Choi, I. Lahiri, R. Seelaboyina, and Y.S. Kang: Synthesis of graphene and its applications: A review. Crit. Rev. Solid State Mater. Sci. 35(1), 52 (2010).
M. Pumera: Electrochemistry of graphene: New horizons for sensing and energy storage. Chem. Rec. 9(4), 211 (2009).
R.S. Edwards and K.S. Coleman: Graphene synthesis: Relationship to applications. Nanoscale 5(1), 38 (2012).
F. Bonaccorso, A. Lombardo, T. Hasan, Z. Sun, L. Colombo, and A.C. Ferrari: Production and processing of graphene and 2d crystals. Mater. Today 15(12), 564 (2012).
D. Wei and Y. Liu: Controllable synthesis of graphene and its applications. Adv. Mater. 22(30), 3225 (2010).
R.Y.N. Gengler, K. Spyrou, and P. Rudolf: A roadmap to high quality chemically prepared graphene. J. Phys. D: Appl. Phys. 43(37), 374015 (2010).
H. Gao and H. Duan: 2D and 3D graphene materials: Preparation and bioelectrochemical applications. Biosens. Bioelectron. 65, 404 (2015).
S. Pei and H-M. Cheng: The reduction of graphene oxide. Carbon 50(9), 3210 (2012).
S. Thakur and N. Karak: Alternative methods and nature-based reagents for the reduction of graphene oxide: A review. Carbon 94, 224 (2015).
S.R. Dhakate, N. Chauhan, S. Sharma, J. Tawale, S. Singh, P.D. Sahare, and R.B. Mathur: An approach to produce single and double layer graphene from re-exfoliation of expanded graphite. Carbon 49(6), 1946 (2011).
S.R. Dhakate, N. Chauhan, S. Sharma, and R.B. Mathur: The production of multi-layer graphene nanoribbons from thermally reduced unzipped multi-walled carbon nanotubes. Carbon 49(13), 4170 (2011).
N. Mishra, J. Boeckl, N. Motta, and F. Iacopi: Graphene growth on silicon carbide: A review. Phys. Status Solidi A 213(9), 2277 (2016).
Y. Zhang, L. Zhang, and C. Zhou: Review of chemical vapor deposition of graphene and related applications. Acc. Chem. Res. 46(10), 2329 (2013).
J.J. Richardson, M. Björnmalm, and F. Caruso: Technology-driven layer-by-layer assembly of nanofilms. Science 348(6233), aaa2491 (2015).
Z. Matharu, A.J. Bandodkar, V. Gupta, and B.D. Malhotra: Fundamentals and application of ordered molecular assemblies to affinity biosensing. Chem. Soc. Rev. 41(3), 1363 (2012).
G. Zeng, Y. Xing, J. Gao, Z. Wang, and X. Zhang: Unconventional layer-by-layer assembly of graphene multilayer films for enzyme-based glucose and maltose biosensing. Langmuir 26(18), 15022 (2010).
J.S. Park, S.M. Cho, W-J. Kim, J. Park, and P.J. Yoo: Fabrication of graphene thin films based on layer-by-layer self-assembly of functionalized graphene nanosheets. ACS Appl. Mater. Interfaces 3(2), 360 (2011).
T. Lee, S.H. Min, M. Gu, Y.K. Jung, W. Lee, J.U. Lee, D.G. Seong, and B-S. Kim: Layer-by-layer assembly for graphene-based multilayer nanocomposites: Synthesis and applications. Chem. Mater. 27(11), 3785 (2015).
L.J. Cote, F. Kim, and J. Huang: Langmuir–Blodgett assembly of graphite oxide single layers. J. Am. Chem. Soc. 131(3), 1043 (2009).
B.G. Choi, H. Park, T.J. Park, M.H. Yang, J.S. Kim, S-Y. Jang, N.S. Heo, S.Y. Lee, J. Kong, and W.H. Hong: Solution chemistry of self-assembled graphene nanohybrids for high-performance flexible biosensors. ACS Nano 4(5), 2910 (2010).
J. Tian, P-X. Yuan, D. Shan, S-N. Ding, G-Y. Zhang, and X-J. Zhang: Biosensing platform based on graphene oxide via self-assembly induced by synergic interactions. Anal. Biochem. 460, 16 (2014).
J-J. Shao, W. Lv, and Q-H. Yang: Self-assembly of graphene oxide at interfaces. Adv. Mater. 26(32), 5586 (2014).
N. Chauhan, V. Palaninathan, S. Raveendran, A.C. Poulose, Y. Nakajima, T. Hasumura, T. Uchida, T. Hanajiri, T. Maekawa, and D.S. Kumar: N2-plasma-assisted one-step alignment and patterning of graphene oxide on a SiO2/Si substrate via the Langmuir–Blodgett technique. Adv. Mater. Interfaces 2(5) (2015), doi: https://doi.org/10.1002/admi.201400515.
D. Rodrigo, O. Limaj, D. Janner, D. Etezadi, F.J.G. de Abajo, V. Pruneri, and H. Altug: Mid-infrared plasmonic biosensing with graphene. Science 349(6244), 165 (2015).
B. Zribi, J-M. Castro-Arias, D. Decanini, N. Gogneau, D. Dragoe, A. Cattoni, A. Ouerghi, H. Korri-Youssoufi, and A-M. Haghiri-Gosnet: Large area graphene nanomesh: An artificial platform for edge-electrochemical biosensing at the sub-attomolar level. Nanoscale 8(34), 15479 (2016).
M.G. Santonicola, M.G. Coscia, M. Sirilli, and S. Laurenzi: Nanomaterial-based biosensors for a real-time detection of biological damage by UV light. In Conf. Proc. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. (IEEE Eng. Med. Biol. Soc. Annu. Conf. 2015, 2015); p. 4391.
M.S. Artiles, C.S. Rout, and T.S. Fisher: Graphene-based hybrid materials and devices for biosensing. Adv. Drug Delivery Rev. 63(14–15), 1352 (2011).
Z. Dong, D. Wang, X. Liu, X. Pei, L. Chen, and J. Jin: Bio-inspired surface-functionalization of graphene oxide for the adsorption of organic dyes and heavy metal ions with a superhigh capacity. J. Mater. Chem. A 2(14), 5034 (2014).
L. Wang, J.A. Jackman, W.B. Ng, and N-J. Cho: Flexible, graphene-coated biocomposite for highly sensitive, real-time molecular detection. Adv. Funct. Mater. 26(47), 8623 (2016).
S. Liu and X. Guo: Carbon nanomaterials field-effect-transistor-based biosensors. NPG Asia Mater. 4(8), e23 (2012).
Y. Ohno, K. Maehashi, and K. Matsumoto: Front. Graphene Carbon Nanotub., K. Matsumoto, ed. (Springer, Japan, 2015); pp. 91–103.
S. Okamoto, Y. Ohno, K. Maehashi, K. Inoue, and K. Matsumoto: Immunosensors based on graphene field-effect transistors fabricated using antigen-binding fragment. Jpn. J. Appl. Phys. 51(6S), 06FD08 (2012).
G. Saltzgaber, P. Wojcik, T. Sharf, M.R. Leyden, J.L. Wardini, C.A. Heist, A.A. Adenuga, V.T. Remcho, and E.D. Minot: Scalable graphene field-effect sensors for specific protein detection. Nanotechnology 24(35), 355502 (2013).
S. Viswanathan, T.N. Narayanan, K. Aran, K.D. Fink, J. Paredes, P.M. Ajayan, S. Filipek, P. Miszta, H.C. Tekin, F. Inci, U. Demirci, P. Li, K.I. Bolotin, D. Liepmann, and V. Renugopalakrishanan: Graphene–protein field effect biosensors: Glucose sensing. Mater. Today 18(9), 513 (2015).
Y. Yang, X. Yang, X. Zou, S. Wu, D. Wan, A. Cao, L. Liao, Q. Yuan, and X. Duan: Ultrafine graphene nanomesh with large on/off ratio for high-performance flexible biosensors. Adv. Funct. Mater. (2016), doi: https://doi.org/10.1002/adfm.201604096.
N. Mohanty and V. Berry: Graphene-based single-bacterium resolution biodevice and DNA transistor: Interfacing graphene derivatives with nanoscale and microscale biocomponents. Nano Lett. 8(12), 4469 (2008).
Y.H. Kwak, D.S. Choi, Y.N. Kim, H. Kim, D.H. Yoon, S-S. Ahn, J-W. Yang, W.S. Yang, and S. Seo: Flexible glucose sensor using CVD-grown graphene-based field effect transistor. Biosens. Bioelectron. 37(1), 82 (2012).
A. Kakatkar, T.S. Abhilash, R.D. Alba, J.M. Parpia, and H.G. Craighead: Detection of DNA and poly-l-lysine using CVD graphene-channel FET biosensors. Nanotechnology 26(12), 125502 (2015).
N.S. Green and M.L. Norton: Interactions of DNA with graphene and sensing applications of graphene field-effect transistor devices: A review. Anal. Chim. Acta 853, 127 (2015).
M. Zhang, C. Liao, C.H. Mak, P. You, C.L. Mak, and F. Yan: Highly sensitive glucose sensors based on enzyme-modified whole-graphene solution-gated transistors. Sci. Rep. 5, 8311 (2015).
Y. Huang, X. Dong, Y. Liu, L-J. Li, and P. Chen: Graphene-based biosensors for detection of bacteria and their metabolic activities. J. Mater. Chem. 21(33), 12358 (2011).
S.S. Varghese, S.H. Varghese, S. Swaminathan, K.K. Singh, and V. Mittal: Two-dimensional materials for sensing: Graphene and beyond. Electronics 4(3), 651 (2015).
X. You and J.J. Pak: 2013 Transducers Eurosensors XXVII 17th Int. Conf. Solid-State Sens. Actuators Microsyst. (TRANSDUCERS EUROSENSORS XXVII, 2013); pp. 2443–2446.
O.S. Kwon, H.S. Song, S.J. Park, S.H. Lee, J.H. An, J.W. Park, H. Yang, H. Yoon, J. Bae, T.H. Park, and J. Jang: An ultrasensitive, selective, multiplexed superbioelectronic nose that mimics the human sense of smell. Nano Lett. 15(10), 6559 (2015).
S. Myung, A. Solanki, C. Kim, J. Park, K.S. Kim, and K-B. Lee: Graphene-encapsulated nanoparticle-based biosensor for the selective detection of cancer biomarkers. Adv. Mater. 23(19), 2221 (2011).
S.M. Yoo and S.Y. Lee: Optical biosensors for the detection of pathogenic microorganisms. Trends Biotechnol. 34(1), 7 (2016).
M.Y. Berezin and S. Achilefu: Fluorescence lifetime measurements and biological imaging. Chem. Rev. 110(5), 2641 (2010).
K.P. Loh, Q. Bao, G. Eda, and M. Chhowalla: Graphene oxide as a chemically tunable platform for optical applications. Nat. Chem. 2(12), 1015 (2010).
G. Eda, Y-Y. Lin, C. Mattevi, H. Yamaguchi, H-A. Chen, I-S. Chen, C-W. Chen, and M. Chhowalla: Blue photoluminescence from chemically derived graphene oxide. Adv. Mater. 22(4), 505 (2010).
J. Shang, L. Ma, J. Li, W. Ai, T. Yu, and G.G. Gurzadyan: The origin of fluorescence from graphene oxide. Sci. Rep. 2, 792 (2012).
R.P. Choudhary, S. Shukla, K. Vaibhav, P.B. Pawar, and S. Saxena: Optical properties of few layered graphene quantum dots. Mater. Res. Express 2(9), 95024 (2015).
J. Wang, S. Cao, Y. Ding, F. Ma, W. Lu, and M. Sun: Theoretical investigations of optical origins of fluorescent graphene quantum dots. Sci. Rep. 6, 24850 (2016).
J.A. McGuire: Growth and optical properties of colloidal graphene quantum dots. Phys. Status Solidi RRL 10(1), 91 (2016).
X-P. He and H. Tian: Photoluminescence architectures for disease diagnosis: From graphene to thin-layer transition metal dichalcogenides and oxides. Small 12(2), 144 (2016).
R. Romero-Aburto, T.N. Narayanan, Y. Nagaoka, T. Hasumura, T.M. Mitcham, T. Fukuda, P.J. Cox, R.R. Bouchard, T. Maekawa, D.S. Kumar, S.V. Torti, S.A. Mani, and P.M. Ajayan: Fluorinated graphene oxide; A new multimodal material for biological applications. Adv. Mater. 25(39), 5632 (2013).
T.D. Martins, A.C.C. Ribeiro, H.S. de Camargo, P.A. da C. Filho, H.P.M. Cavalcante, and D.L. Dias: New Insights on Optical Biosensors: Techniques, Construction and Application (InTech, Rijeka, 2013).
Z. Wang, H. Zeng, and L. Sun: Graphene quantum dots: Versatile photoluminescence for energy, biomedical, and environmental applications. J. Mater. Chem. C 3(6), 1157 (2015).
R. Xie, Z. Wang, W. Zhou, Y. Liu, L. Fan, Y. Li, and X. Li: Graphene quantum dots as smart probes for biosensing. Anal. Methods 8(20), 4001 (2016).
C. Zhu, D. Du, and Y. Lin: Graphene and graphene-like 2D materials for optical biosensing and bioimaging: A review. 2D Mater. 2(3), 32004 (2015).
H. Chang, L. Tang, Y. Wang, J. Jiang, and J. Li: Graphene fluorescence resonance energy transfer aptasensor for the thrombin detection. Anal. Chem. 82(6), 2341 (2010).
Y. Wang, L. Tang, Z. Li, Y. Lin, and J. Li: In situ simultaneous monitoring of ATP and GTP using a graphene oxide nanosheet-based sensing platform in living cells. Nat. Protoc. 9(8), 1944 (2014).
S. He, B. Song, D. Li, C. Zhu, W. Qi, Y. Wen, L. Wang, S. Song, H. Fang, and C. Fan: A graphene nanoprobe for rapid, sensitive, and multicolor fluorescent DNA analysis. Adv. Funct. Mater. 20(3), 453 (2010).
E. Morales-Narváez, T. Naghdi, E. Zor, and A. Merkoçi: Photoluminescent lateral-flow immunoassay revealed by graphene oxide: Highly sensitive paper-based pathogen detection. Anal. Chem. 87(16), 8573 (2015).
C-Y. Poon, Q. Li, J. Zhang, Z. Li, C. Dong, A.W-M. Lee, W-H. Chan, and H-W. Li: FRET-based modified graphene quantum dots for direct trypsin quantification in urine. Anal. Chim. Acta 917, 64 (2016).
Q. Wu, Y. Sun, P. Ma, D. Zhang, S. Li, X. Wang, and D. Song: Gold nanostar-enhanced surface plasmon resonance biosensor based on carboxyl-functionalized graphene oxide. Anal. Chim. Acta 913, 137 (2016).
D. Du, Z. Zou, Y. Shin, J. Wang, H. Wu, M.H. Engelhard, J. Liu, I.A. Aksay, and Y. Lin: Sensitive immunosensor for cancer biomarker based on dual signal amplification strategy of graphene sheets and multienzyme functionalized carbon nanospheres. Anal. Chem. 82(7), 2989 (2010).
B. Liang, L. Fang, G. Yang, Y. Hu, X. Guo, and X. Ye: Direct electron transfer glucose biosensor based on glucose oxidase self-assembled on electrochemically reduced carboxyl graphene. Biosens. Bioelectron. 43, 131 (2013).
Q. Wu, Y. Hou, M. Zhang, X. Hou, L. Xu, N. Wang, J. Wang, and W. Huang: Amperometric cholesterol biosensor based on zinc oxide films on a silver nanowire–graphene oxide modified electrode. Anal. Methods 8(8), 1806 (2016).
H. Lee, T.K. Choi, Y.B. Lee, H.R. Cho, R. Ghaffari, L. Wang, H.J. Choi, T.D. Chung, N. Lu, T. Hyeon, S.H. Choi, and D-H. Kim: A graphene-based electrochemical device with thermoresponsive microneedles for diabetes monitoring and therapy. Nat. Nanotechnol. 11(6), 566 (2016).
Q. Gong, Y. Wang, and H. Yang: A sensitive impedimetric DNA biosensor for the determination of the HIV gene based on graphene-Nafion composite film. Biosens. Bioelectron. 89(Pt 1), 565 (2017).
S. Ge, L. Zhang, Y. Zhang, H. Liu, J. Huang, M. Yan, and J. Yu: Electrochemical K-562 cells sensor based on origami paper device for point-of-care testing. Talanta 145, 12 (2015).
F. Tehrani, L. Reiner, and B. Bavarian: Rapid prototyping of a high sensitivity graphene based glucose sensor strip. PLoS One 10(12), e0145036 (2015).
J. Kailashiya, N. Singh, S.K. Singh, V. Agrawal, and D. Dash: Graphene oxide-based biosensor for detection of platelet-derived microparticles: A potential tool for thrombus risk identification. Biosens. Bioelectron. 65, 274 (2015).
M. Zhu, C. Zeng, and J. Ye: Graphene-modified carbon fiber microelectrode for the detection of dopamine in mice hippocampus tissue. Electroanalysis 23(4), 907 (2011).
H. Gu, Y. Yu, X. Liu, B. Ni, T. Zhou, and G. Shi: Layer-by-layer self-assembly of functionalized graphene nanoplates for glucose sensing in vivo integrated with on-line microdialysis system. Biosens. Bioelectron. 32(1), 118 (2012).
M. Arvand and N. Ghodsi: A voltammetric sensor based on graphene-modified electrode for the determination of trace amounts of l-dopa in mouse brain extract and pharmaceuticals. J. Solid State Electrochem. 17(3), 775 (2013).
H. Gu, Y. Yang, X. Zhou, T. Zhou, and G. Shi: Online electrochemical method for continuous and simultaneous monitoring of glucose and l-lactate in vivo with graphene hybrids as the electrocatalyst. J. Electroanal. Chem. 730, 41 (2014).
K. Manibalan, V. Mani, C-H. Huang, S-T. Huang, and P-C. Chang: A new electrochemical substrate for rapid and sensitive in vivo monitoring of β-galactosidase gene expressions. Analyst 140(17), 6040 (2015).
T-C. Liu, M-C. Chuang, C-Y. Chu, W-C. Huang, H-Y. Lai, C-T. Wang, W-L. Chu, S-Y. Chen, and Y-Y. Chen: Implantable graphene-based neural electrode interfaces for electrophysiology and neurochemistry in in vivo hyperacute stroke model. ACS Appl. Mater. Interfaces 8(1), 187 (2016).
X. Wang, Q. Li, J. Xu, S. Wu, T. Xiao, J. Hao, P. Yu, and L. Mao: Rational design of bioelectrochemically multifunctional film with oxidase, ferrocene, and graphene oxide for development of in vivo electrochemical biosensors. Anal. Chem. 88(11), 5885 (2016).
S. Kumar, S. Kumar, S. Srivastava, B.K. Yadav, S.H. Lee, J.G. Sharma, D.C. Doval, and B.D. Malhotra: Reduced graphene oxide modified smart conducting paper for cancer biosensor. Biosens. Bioelectron. 73, 114 (2015).
B. Derkus: Applying the miniaturization technologies for biosensor design. Biosens. Bioelectron. 79, 901 (2016).
J.P. Lafleur, A. Jönsson, S. Senkbeil, and J.P. Kutter: Recent advances in lab-on-a-chip for biosensing applications. Biosens. Bioelectron. 76, 213 (2016).
P.K. Ang, A. Li, M. Jaiswal, Y. Wang, H.W. Hou, J.T.L. Thong, C.T. Lim, and K.P. Loh: Flow sensing of single cell by graphene transistor in a microfluidic channel. Nano Lett. 11(12), 5240 (2011).
L. Cao, L. Cheng, Z. Zhang, Y. Wang, X. Zhang, H. Chen, B. Liu, S. Zhang, and J. Kong: Visual and high-throughput detection of cancer cells using a graphene oxide-based FRET aptasensing microfluidic chip. Lab Chip 12(22), 4864 (2012).
H.J. Yoon, T.H. Kim, Z. Zhang, E. Azizi, T.M. Pham, C. Paoletti, J. Lin, N. Ramnath, M.S. Wicha, D.F. Hayes, D.M. Simeone, and S. Nagrath: Sensitive capture of circulating tumour cells by functionalized graphene oxide nanosheets. Nat. Nanotechnol. 8(10), 735 (2013).
K. ul Hasan, M.H. Asif, M.U. Hassan, M.O. Sandberg, O. Nur, M. Willander, S. Fagerholm, and P. Strålfors: A miniature graphene-based biosensor for intracellular glucose measurements. Electrochim. Acta 174, 574 (2015).
F. Liu, Y. Piao, J.S. Choi, and T.S. Seo: Three-dimensional graphene micropillar based electrochemical sensor for phenol detection. Biosens. Bioelectron. 50, 387 (2013).
H.J. Yoon, A. Shanker, Y. Wang, M. Kozminsky, Q. Jin, N. Palanisamy, M.L. Burness, E. Azizi, D.M. Simeone, M.S. Wicha, J. Kim, and S. Nagrath: Tunable thermal-sensitive polymer–graphene oxide composite for efficient capture and release of viable circulating tumor cells. Adv. Mater. 28(24), 4891 (2016).
M.S. Mannoor, H. Tao, J.D. Clayton, A. Sengupta, D.L. Kaplan, R.R. Naik, N. Verma, F.G. Omenetto, and M.C. McAlpine: Graphene-based wireless bacteria detection on tooth enamel. Nat. Commun. 3, 763 (2012).
A.Y. Zhu, F. Yi, J.C. Reed, H. Zhu, and E. Cubukcu: Optoelectromechanical multimodal biosensor with graphene active region. Nano Lett. 14(10), 5641 (2014).
P. Li, B. Zhang, and T. Cui: Towards intrinsic graphene biosensor: A label-free, suspended single crystalline graphene sensor for multiplex lung cancer tumor markers detection. Biosens. Bioelectron. 72, 168 (2015).
T-Y. Chen, P.T.K. Loan, C-L. Hsu, Y-H. Lee, J. Tse-Wei Wang, K-H. Wei, C-T. Lin, and L-J. Li: Label-free detection of DNA hybridization using transistors based on CVD grown graphene. Biosens. Bioelectron. 41, 103 (2013).
S. Mao, K. Yu, J. Chang, D.A. Steeber, L.E. Ocola, and J. Chen: Direct growth of vertically-oriented graphene for field-effect transistor biosensor. Sci. Rep. 3, 1696 (2013).
C. Yu, X. Chang, J. Liu, L. Ding, J. Peng, and Y. Fang: Creation of reduced graphene oxide based field effect transistors and their utilization in the detection and discrimination of nucleoside triphosphates. ACS Appl. Mater. Interfaces 7(20), 10718 (2015).
J.H. An, S.J. Park, O.S. Kwon, J. Bae, and J. Jang: High-performance flexible graphene aptasensor for mercury detection in mussels. ACS Nano 7(12), 10563 (2013).
L. He, Q. Wang, D. Mandler, M. Li, R. Boukherroub, and S. Szunerits: Detection of folic acid protein in human serum using reduced graphene oxide electrodes modified by folic-acid. Biosens. Bioelectron. 75, 389 (2016).
C-W. Lin, K-C. Wei, S. Liao, C-Y. Huang, C-L. Sun, P-J. Wu, Y-J. Lu, H-W. Yang, and C-C.M. Ma: A reusable magnetic graphene oxide-modified biosensor for vascular endothelial growth factor detection in cancer diagnosis. Biosens. Bioelectron. 67, 431 (2015).
H.D. Jang, S.K. Kim, H. Chang, and J-W. Choi: 3D label-free prostate specific antigen (PSA) immunosensor based on graphene–gold composites. Biosens. Bioelectron. 63, 546 (2015).
T. Hu, L. Zhang, W. Wen, X. Zhang, and S. Wang: Enzyme catalytic amplification of miRNA-155 detection with graphene quantum dot-based electrochemical biosensor. Biosens. Bioelectron. 77, 451 (2016).
Z. Fan, J. Wang, Y. Nie, L. Ren, B. Liu, and G. Liu: Metal-organic frameworks/graphene oxide composite: A new enzymatic immobilization carrier for hydrogen peroxide biosensors. J. Electrochem. Soc. 163(3), B32 (2016).
F. Liu, Y. Zhang, J. Yu, S. Wang, S. Ge, and X. Song: Application of ZnO/graphene and S6 aptamers for sensitive photoelectrochemical detection of SK-BR-3 breast cancer cells based on a disposable indium tin oxide device. Biosens. Bioelectron. 51, 413 (2014).
L. Baptista-Pires, B. Pérez-López, C.C. Mayorga-Martinez, E. Morales-Narváez, N. Domingo, M.J. Esplandiu, F. Alzina, C.M.S. Torres, and A. Merkoçi: Electrocatalytic tuning of biosensing response through electrostatic or hydrophobic enzyme–graphene oxide interactions. Biosens. Bioelectron. 61, 655 (2014).
S. Kurbanoglu, L. Rivas, S.A. Ozkan, and A. Merkoçi: Electrochemically reduced graphene and iridium oxide nanoparticles for inhibition-based angiotensin-converting enzyme inhibitor detection. Biosens. Bioelectron. 88, 122 (2017).
Z. Wang, P. Huang, A. Bhirde, A. Jin, Y. Ma, G. Niu, N. Neamati, and X. Chen: A nanoscale graphene oxide–peptide biosensor for real-time specific biomarker detection on the cell surface. Chem. Commun. 48(78), 9768 (2012).
M. Singh, M. Holzinger, M. Tabrizian, S. Winters, N.C. Berner, S. Cosnier, and G.S. Duesberg: Noncovalently functionalized monolayer graphene for sensitivity enhancement of surface plasmon resonance immunosensors. J. Am. Chem. Soc. 137(8), 2800 (2015).
Q. Zhao, Y. Zhou, Y. Li, W. Gu, Q. Zhang, and J. Liu: Luminescent iridium(III) complex labeled DNA for graphene oxide-based biosensors. Anal. Chem. 88(3), 1892 (2016).
J.S. Lee, H-A. Joung, M-G. Kim, and C.B. Park: Graphene-based chemiluminescence resonance energy transfer for homogeneous immunoassay. ACS Nano 6(4), 2978 (2012).
J.H. Jung, D.S. Cheon, F. Liu, K.B. Lee, and T.S. Seo: A graphene oxide based immuno-biosensor for pathogen detection. Angew. Chem., Int. Ed. 49(33), 5708 (2010).
Y.V. Stebunov, O.A. Aftenieva, A.V. Arsenin, and V.S. Volkov: Highly sensitive and selective sensor chips with graphene-oxide linking layer. ACS Appl. Mater. Interfaces 7(39), 21727 (2015).
ACKNOWLEDGMENTS
The authors would like to acknowledge their sincere gratitude to the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan for the financial support under the program of the strategic research foundation at private universities S1101017, organized by the MEXT, Japan.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chauhan, N., Maekawa, T. & Kumar, D.N.S. Graphene based biosensors—Accelerating medical diagnostics to new-dimensions. Journal of Materials Research 32, 2860–2882 (2017). https://doi.org/10.1557/jmr.2017.91
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1557/jmr.2017.91