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Microchimica Acta

, 186:114 | Cite as

Nanomaterial-based optical and electrochemical techniques for detection of methicillin-resistant Staphylococcus aureus: a review

  • Atal A. S. Gill
  • Sima Singh
  • Neeta Thapliyal
  • Rajshekhar KarpoormathEmail author
Review Article

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is responsible for a number of life-threatening complications in humans. Mutations in the genetic sequence of S. aureus due to the presence of certain genes results in resistance against β-lactamases. Thus, there is an urgent need for developing highly sensitive techniques for the early detection of MRSA to counter the rise in resistant strains. This review (142 refs.) extensively covers literature reports on nanomaterial-based optical and electrochemical sensors from the year 1983 to date, with particularly emphasis on recent advances in electrochemical sensing (such as voltammetry and impedimetric) and optical sensing (such as colorimetry and fluorometry) techniques. Among the electrochemical methods, various nanomaterials were employed for the modification of electrodes. Whereas, in optical assays, formats such as enzyme linked immunosorbent assay, lateral flow assays or in optical fiber systems are common. In addition, novel sensing platforms are reported by applying advanced nanomaterials which include gold nanoparticles, nanotitania, graphene, graphene-oxide, cadmium telluride and related quantum dots, nanocomposites, upconversion nanoparticles and bacteriophages. Finally, closing remarks and an outlook conclude the review.

Graphical abstract

Schematic of the diversity of nanomaterial-based methods for detection of methicillin-resistant Staphylococcus aureus (MRSA). AuNPs: gold nanoparticles; QDs: quantum dots; PVL: Panton-Valentine leukocidin; mecA gene: mec-gene complex encoding methicillin resistance

Keywords

Methicillin-resistant Staphylococcus aureus (MRSA) Biosensors Nanomaterials Electrochemical sensing Luminescence-based techniques Polymerase chain reaction (PCR) 

Notes

Acknowledgments

The authors would like to thank the College of Health Sciences, University of Kwazulu-Natal (UKZN), Nanotechnology platform-UKZN and the National Research Foundation of South Africa (NRF-SA) for funding (Grant No.103728 and 112079).

Compliance with ethical standards

The author(s) declare that they have no competing interests.

References

  1. 1.
    Akhtar N (2010) Hospital acquired infections in a medical intensive care unit. J College Physic Surgeons-Pakistan 20(6):386–390Google Scholar
  2. 2.
    Yang Y, Hu Z, Shang W, Hu Q, Zhu J, Yang J, Peng H, Zhang X, Liu H, Cong Y, Li S, Hu X, Zhou R, Rao X (2017) Molecular and phenotypic characterization revealed high prevalence of multidrug-resistant methicillin-susceptible Staphylococcus aureus in Chongqing, Southwestern China. Microb Drug Resist 23:241–246PubMedGoogle Scholar
  3. 3.
    Campoccia D, Montanaro L, Arciola CR (2006) The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 27:2331–2339PubMedGoogle Scholar
  4. 4.
    Parmar A, Lakshminarayanan R, Iyer A, Mayandi V, Goh ETL, Lloyd DG, Madder A (2018) Design and syntheses of highly potent Teixobactin analogues against Staphylococcus aureus, methicillin-resistant Staphylococcus aureus (MRSA), and vancomycin-resistant enterococci (VRE) in vitro and in vivo. J Med Chem 61(5):2009–2017.  https://doi.org/10.1021/acs.jmedchem.7b01634 CrossRefPubMedGoogle Scholar
  5. 5.
    Kanafani ZA, Fowler VG (2009) Evans’ infections of humans: staphylococcal infections. In: Brachman P, Abrutyn E (eds) Bacterial infections of humans. Springer, BostonGoogle Scholar
  6. 6.
    Furukawa S, Kuchma SL, O’Toole GA (2006) Keeping their options open: acute versus persistent infections. J Bacteriol 188(4):1211–1217.  https://doi.org/10.1128/JB.188.4.1211-1217.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Levy SB, Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10:S122–S129PubMedGoogle Scholar
  8. 8.
    Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. Jama 298(15):1763–1771PubMedGoogle Scholar
  9. 9.
    Herber OR, Schnepp W, Rieger MA (2007) A systematic review on the impact of leg ulceration on patients' quality of life. Health Qual Life Outcomes 5(1):44PubMedPubMedCentralGoogle Scholar
  10. 10.
    Kuehnert MJ, Hill HA, Kupronis BA, Tokars JI, Solomon SL, Jernigan DB (2005) Methicillin-resistant-Staphylococcus aureus hospitalizations. United States. Emerg Infect Dis 11:868–872PubMedGoogle Scholar
  11. 11.
    Yoshikawa TT, Bradley SF (2002) Staphylococcus aureus infections and antibiotic resistance in older adults. Clin Infect Dis 34(2):211–216Google Scholar
  12. 12.
    Jones ME, Draghi DC, Thornsberry C, Karlowsky JA, Sahm DF, Wenzel RP (2004) Emerging resistance among bacterial pathogens in the intensive care unit—a European and North American Surveillance study (2000–2002). Ann Clin Microbiol Antimicrob 29:3–14Google Scholar
  13. 13.
    Nathwani D, Morgan M, Masterton RG, Dryden M, Cookson BD, French G, Lewis D, British Society for Antimicrobial Chemotherapy Working Party on Community-onset MRSA Infections (2008) Guidelines for UK practice for the diagnosis and management of methicillin-resistant Staphylococcus aureus (MRSA) infections presenting in the community. J Antimicrob Chemother 61(5):976–94Google Scholar
  14. 14.
    Palavecino E (2004) Community-acquired methicillin-resistant Staphylococcus aureus infections. Clin Lab Med 24:403–418PubMedGoogle Scholar
  15. 15.
    Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM, O'Brien FG, Coombs GW, Pearman JW, Tenover FC, Kapi M, Tiensasitorn C, Ito T, Hiramatsu K (2002) Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40:4289–4294PubMedPubMedCentralGoogle Scholar
  16. 16.
    Strimbu K, Tavel JA (2010) What are biomarkers? Curr Opin HIV AIDS 5(6):463–466PubMedPubMedCentralGoogle Scholar
  17. 17.
    International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53:4961–4967.  https://doi.org/10.1128/AAC.00579-09 CrossRefGoogle Scholar
  18. 18.
    Munita JM, Arias CA (2016) Mechanisms of antibiotic resistance. Microbiol Spectr 4(2).  https://doi.org/10.1128/microbiolspec.VMBF-0016-2015
  19. 19.
    Szmiegielski S, Prevost G, Monteil H (1999) Leukocidal toxins of staphylococci. Zentralbl Bakteriol 289(2):185–201.  https://doi.org/10.1016/S0934-8840(99)80105-4 CrossRefGoogle Scholar
  20. 20.
    Kaneko J, Kamio Y (2004) Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: structures, pore-forming mechanism, and organization of the genes. Biosci Biotechnol Biochem 68(5):981–1003.  https://doi.org/10.1271/bbb.68.981 CrossRefPubMedGoogle Scholar
  21. 21.
    Goering RV, McDougal LK, Fosheim GE, Bonnstetter KK, Wolter DJ, Tenover FC (2007) Epidemiologic distribution of the arginine catabolic mobile element among selected methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates. J Clin Microbiol 45(6):1981–1984.  https://doi.org/10.1128/JCM.00273-07 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Takadama S, Nakaminami H, Sato A, Shoshi M, Fujii T, Noguchi N (2018) Dissemination of Panton-valentine leukocidin-positive methicillin-resistant Staphylococcus aureus USA300 clone in multiple hospitals in Tokyo. Japan Clin Microbiol Infect 24:1211.e1–1211.e7.  https://doi.org/10.1016/j.cmi.2018.02.012 CrossRefGoogle Scholar
  23. 23.
    Ellington MJ, Yearwood L, Ganner M, East C, Kearns AM (2008) Distribution of the ACME-arcA gene among methicillin-resistant Staphylococcus aureus from England and Wales. J Antimicrob Chemother 61:73–77.  https://doi.org/10.1093/jac/dkm422 CrossRefPubMedGoogle Scholar
  24. 24.
    Paul SK, Ghosh S, Kawaguchiya M, Urushibara N, Hossain MA, Ahmed S, Mahmud C, Jilani MSA, Haq JA, Ahmed AA, Kobayashi N (2014) Detection and genetic characterization of PVL-positive ST8-MRSA-IVa and exfoliative toxin D-positive European CA-MRSA-like ST1931 (CC80) MRSA-Iva strains in Bangladesh. Microb Drug Resist 20(4):325–336.  https://doi.org/10.1089/mdr.2013.0153 CrossRefPubMedGoogle Scholar
  25. 25.
    Chadwick SG, Prasad A, Smith WL, Mordechai E, Adelson ME, Gygax SE (2013) Detection of epidemic USA300 community-associated methicillin-resistant Staphylococcus aureus strains by use of a single allele-specific PCR assay targeting a novel polymorphism of Staphylococcus aureus pbp3. J Clin Microbiol 51(8):2541–2550.  https://doi.org/10.1128/JCM.00417-13 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Cho IH, Irudayaraj J (2013) In-situ Immuno-gold nanoparticle network ELISA biosensors for pathogen detection. Int J Food Microbiol 164(1):70–75PubMedGoogle Scholar
  27. 27.
    Yu H, Zhao G, Dou W (2015) Simultaneous detection of pathogenic Bacteria using agglutination test based on colored silica nanoparticles. Curr Pharm Biotechnol 16(8):716–723PubMedGoogle Scholar
  28. 28.
    Onori M, Coltella L, Mancinelli L, Argentieri M, Menichella D, Villani A, Grandin A, Valentini D, Raponi M, Russo C (2014) Evaluation of a multiplex PCR assay for simultaneous detection of bacterial and viral Enteropathogens in stool samples of Paediatric patients. Diagn Microbiol Infect Dis 79(2):149–154PubMedGoogle Scholar
  29. 29.
    Sheu DS, Wang YT, Lee CY (2000) Rapid detection of poly hydroxy alkanoate-accumulating bacteria isolated from the environment by Colony PCR. Microbiology 146(8):2019–2025PubMedGoogle Scholar
  30. 30.
    Oblath EA, Henley WH, Alarie JP, Ramsey JM (2013) A microfluidic Chip integrating DNA extraction and real-time PCR for the detection of Bacteria in saliva. Lab Chip 13(7):1325–1332PubMedPubMedCentralGoogle Scholar
  31. 31.
    Yuen JWM, Chung TWK, Loke AY (2015) Methicillin-resistant Staphylococcus aureus (MRSA) contamination in bedside surfaces of a hospital Ward and the potential effectiveness of enhanced disinfection with an antimicrobial polymer surfactant. Int J Environ Res Public Health 12:3026–3041PubMedPubMedCentralGoogle Scholar
  32. 32.
    Silbert S, Kubasek C, Uy D, Widen R (2014) Comparison of ESwab with traditional swabs for detection of methicillin-resistant Staphylococcus aureus using two different walk-away commercial real-time PCR methods. J Clin Microbiol 52:2641–2643PubMedPubMedCentralGoogle Scholar
  33. 33.
    Hombach H, Maurer FP, Pfiffner T, Böttger EC, Furrer R (2015) Standardization of operator-dependent variables affecting precision and accuracy of the disk diffusion method for antibiotic susceptibility test. J Clin Microbiol 53:3864–3869PubMedPubMedCentralGoogle Scholar
  34. 34.
    Shin JH, Kim EC, Kim S, Koh EH, Lee DH, Koo SH, Cho JH, Kim JS, Ryoo NH (2013) A multicentre study about pattern and organisms isolated in follow-up blood cultures. Ann Clin Microbiol 16(1):8–12Google Scholar
  35. 35.
    Robotham JV, Graves N, Cookson BD, Barnett AG, Wilson JA, Edgeworth JD, Batra R, Cuthbertson BH, Cooper BS (2011) Screening, isolation, and decolonisation strategies in the control of meticillin resistant Staphylococcus aureus in intensive care units: cost effectiveness evaluation. Bmj 343:d5694PubMedPubMedCentralGoogle Scholar
  36. 36.
    Stürenburg E (2009) Rapid detection of methicillin-resistant Staphylococcus aureus directly from clinical samples: methods, effectiveness and cost considerations. Ger Med Sci 7.  https://doi.org/10.3205/000065
  37. 37.
    Matsui H, Hanaki H, Inoue M, Akama H, Nakae T, Sunakawa K, Omura S (2011) Development of an immunochromatographic strip for simple detection of penicillin-binding protein 2a. Clin Vaccine Immunol 18:248–253PubMedGoogle Scholar
  38. 38.
    Liu Y, Lord H, Maciążek-Jurczyk M, Jolly S, Hussain MA, Pawliszyn J (2014) (2014) development of an immunoaffinity solid phase microextraction method for the identification of pencillin binding protein 2a. J Chromatogr A 1364:64–73PubMedGoogle Scholar
  39. 39.
    Kumar SM et al (2008) Current trends in rapid diagnostics for methicillin-resistant Staphylococcus aureus and Glycopeptide-resistant enterococcus species. J Clin Microbiol 46:1577–1587Google Scholar
  40. 40.
    Coia JE, Duckworth GJ, Edwards DI, Farrington M, Fry C, Humphreys H, Mallaghan C, Tucker DR, Joint Working Party of the British Society of Antimicrobial Chemotherapy, Hospital Infection Society, Infection Control Nurses Association (2006) Guidelines for the control and prevention of methicillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities. J Hosp Infect 63(suppl 1):S1–S44PubMedGoogle Scholar
  41. 41.
    Ellem JA, Olma T, O’Sullivan MVN (2015) Rapid detection of methicillin-resistant Staphylococcus aureus and methicillin-Susceptible S. aureus directly from positive blood cultures by use of the BD max staph SR assay. J Clin Microbiol 53:3900–3904PubMedPubMedCentralGoogle Scholar
  42. 42.
    Warnke P, Frickmann H, Ottl P, Podbielski A (2014) Nasal screening for MRSA: different swabs – different results. PLoS One 9:e111627PubMedPubMedCentralGoogle Scholar
  43. 43.
    Holtfreter S, Grumann D, Balau V, Barwich A, Kolata J, Goehler A, Weiss S, Holtfreter B, Bauerfeind SS, Döring P, Friebe E, Haasler N, Henselin K, Kühn K, Nowotny S, Radke D, Schulz K, Schulz SR, Trübe P, Vu CH, Walther B, Westphal S, Cuny C, Witte W, Völzke H, Grabe HJ, Kocher T, Steinmetz I, Bröker BM (2016) Molecular epidemiology of Staphylococcus aureus in the general population in Northeast Germany-results of the Study of Health in Pomerania (SHIP-TREND-0). J Clin Microbiol 54(11):2774–2785.  https://doi.org/10.1128/JCM.00312-16 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Faron ML, Buchan BW, Vismara C, Lacchini C, Bielli A, Gesu G, Liebregts T, van Bree A, Jansz A, Soucy G, Korver J, Ledeboer NA (2016) Automated scoring of chromogenic Media for the Detection of MRSA using the WASPLab image analysis software. J Clin Microbiol 54:620–624PubMedPubMedCentralGoogle Scholar
  45. 45.
    Rajendran R, Rayman G (2014) Point-of-care blood glucose testing for diabetes Care in Hospitalized Patients: an evidence-based review. J Diabetes Sci Technol 8(6):1081–1090PubMedPubMedCentralGoogle Scholar
  46. 46.
    Warnke P, Devide A, Weise M, Frickmann H, Schwarz NG, Schäffler H, Ottl P, Podbielski A (2016) Utilizing moist or dry swabs for the sampling of nasal MRSA carriers? An in vivo and in vitro Study. PLoS One 11(9):e0163073PubMedPubMedCentralGoogle Scholar
  47. 47.
    Pinchuk IV, Beswick EJ, Reyes VE (2010) Staphyloccocus enterotoxins. Toxins (Basel) 2(8):2177–2197Google Scholar
  48. 48.
    Wu S, Duan N, Gu H, Hao L, Ye H, Gong W, Wang Z (2016) A review of the methods for detection of staphylococcus aureus enterotoxins. Toxins (Basel) 8(7):E176.  https://doi.org/10.3390/toxins8070176 CrossRefGoogle Scholar
  49. 49.
    Poil MA, Rivera VR, Neal D (2002) Sensitive and specific colorimetric ELISAS for Staphylococcus aureus enterotoxins A and B in urine buffer. Toxicon 40(12):1723–1726Google Scholar
  50. 50.
    Templeman LA, King KD, Anderson GP, Ligler FS (1996) Quantitating staphylococcal enterotoxin B in diverse media using a portable fiber-optic biosensor. Anal Biochem 233:50–57Google Scholar
  51. 51.
    Goldman ER, Anderson GP, Tran PT, Mattoussi H, Charles PT, Mauro JM (2002) Conjugation of luminescent quantum dots with antibodies using an engineered adaptor protein to provide new reagents for fluorimmunoassays. Anal Chem 74(4):841–847PubMedGoogle Scholar
  52. 52.
    Poojary NS, Ramlal S, Urs RM, Sripathy MH, Batra HV (2014) Application of monoclonal antibodies generated against Panton-Valentine Leukocidin (PVL-S) toxin for specific identification of community acquired methicillin resistance Staphylococcus aureus. Microbiol Res 169(12):924–930.  https://doi.org/10.1016/j.micres.2014.05.002 CrossRefPubMedGoogle Scholar
  53. 53.
    Prevost G, Cribier B, Couppié P, Petiau P, Supersac G, Finck-Barbançon V, Monteil H, Piemont Y (1995) Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect Immun 63(10):4121–4129PubMedPubMedCentralGoogle Scholar
  54. 54.
    Malhotra-Kumar S, Haccuria K, Michiels M, Ieven M, Poyart C, Hryniewicz W, Goossens H, MOSAR WP2 Study Team (2008) Current trends in rapid diagnostics for methicillin-resistant Staphylococcus aureus and glycopeptide-resistant enterococcus species. J Clin Microbiol 46(5):1577–187aPubMedPubMedCentralGoogle Scholar
  55. 55.
    Nijhuis RH, van Maarseveen NM, van Hannen EJ, van Zwet AA, Mascini EM (2014) A rapid and high-throughput screening approach for methicillin-resistant Staphylococcus aureus based on the combination of two different real-time PCR assays. J Clin Microbiol 52(8):2861–2867PubMedPubMedCentralGoogle Scholar
  56. 56.
    Liu Y, Zhang J, Ji Y (2016) PCR-based approaches for the detection of clinical methicillin-resistant Staphylococcus aureus. Open Microbiol J 10:45–56PubMedPubMedCentralGoogle Scholar
  57. 57.
    Toleman MS, Reuter S, Coll F, Harrison EM, Blane B, Brown NM, Török ME, Parkhill J, Peacock SJ (2016) Systematic surveillance detects multiple silent introductions and household transmission of methicillin-resistant Staphylococcus aureus USA300 in the East of England. J Infect Dis 214(3):447–453PubMedPubMedCentralGoogle Scholar
  58. 58.
    Shen F, Davydova EK, Du W, Kreutz JE, Piepenburg O, Ismagilov RF (2011) Digital isothermal quantification of nucleic acids via simultaneous chemical initiation of recombinase polymerase amplification reactions on SlipChip. Anal Chem 83(9):3533–3540PubMedPubMedCentralGoogle Scholar
  59. 59.
    Calderwood MS (2015) Editorial commentary: duration of colonization with methicillin-resistant Staphylococcus aureus: a question with many answers. Clin Infect Dis 60(10):1497–1499PubMedPubMedCentralGoogle Scholar
  60. 60.
    Xu J, Wang Y, Hu S (2017) Nanocomposites of graphene and graphene oxides: synthesis, molecular functionalization and application in electrochemical sensors and biosensors. A review. Microchim Acta 184(1):1–44.  https://doi.org/10.1007/s00604-016-2007-0 CrossRefGoogle Scholar
  61. 61.
    Liu Y, Yu J (2016) Oriented immobilization of proteins on solid supports for use in biosensors and biochips: a review. Microchim Acta 183(1):1–19.  https://doi.org/10.1007/s00604-015-1623-4 CrossRefGoogle Scholar
  62. 62.
    Xu S (2012) Electromechanical biosensors for pathogen detection. Microchim Acta 178:245–260.  https://doi.org/10.1007/s00604-012-0831-4 CrossRefGoogle Scholar
  63. 63.
    Zhong Z, Gao X, Gao R, Jia L (2018) Selective capture and sensitive fluorometric determination of Pseudomonas aeruginosa by using aptamer modified magnetic nanoparticles. Microchim Acta 185:377.  https://doi.org/10.1007/s00604-018-2914-3 CrossRefGoogle Scholar
  64. 64.
    Shoaie N, Forouzandeh M, Omidfar K (2018) Voltammetric determination of the Escherichia coli DNA using a screen-printed carbon electrode modified with polyaniline and gold nanoparticles. Microchim Acta 185:217.  https://doi.org/10.1007/s00604-018-2749-y CrossRefGoogle Scholar
  65. 65.
    Liu AZZ, Bodapati S, Teed R, Vaithilingam S, Khuri-Yakub BT, Chen X, Dai H, Gambhir SS (2010) Ultrahigh sensitivity carbon nanotube agents for photoacoustic molecular imaging in living mice. Nano Lett 10:2168–2172PubMedPubMedCentralGoogle Scholar
  66. 66.
    Strayer AL, Ocsoy I, Tan W, Jones J, Paret M (2016) Low concentrations of a silver-based nanocomposite to manage bacterial spot of tomato in the greenhouse. Plant Dis 100(7):1460–1465PubMedGoogle Scholar
  67. 67.
    Colvin VL (2004) The potential environmental impact of engineered nanomaterials. Nat Biotechnol 22(6):760Google Scholar
  68. 68.
    Huang PJJ, Liu J (2013) Separation of short single- and double-stranded DNA based on their adsorption kinetics difference on graphene oxide. Nanomaterials (Basel) 3(2):221–228Google Scholar
  69. 69.
    Mandal SS, Navratna V, Sharma P, Gopal B, Bhattacharyya AJ (2014) Titania nanotube-modified screen-printed carbon electrodes enhance the sensitivity in the electrochemical detection of proteins. Bioelectrochemistry 98:46–52PubMedGoogle Scholar
  70. 70.
    Watanabe K, Kuwata N, Sakamoto H, Amano Y, Satomura T, Suye S-I (2015) A smart DNA sensing system for detecting methicillin-resistant Staphylococcus aureus using modified nanoparticle probes. Biosens Bioelectron 67:419–423PubMedGoogle Scholar
  71. 71.
    Xu L, Liang W, Wen Y, Wang L, Yang X, Ren S, Jia N, Zuo X, Liu G (2017) An ultrasensitive electrochemical biosensor for the detection of mecA gene in methicillin-resistant Staphylococcus aureus. Biosens Bioelectron 99:424–430PubMedGoogle Scholar
  72. 72.
    Cihalova K, Hegerova D, Dostalova S, Jelinkova P, Krejcova L, Milosavljevic V, Krizkova S, Kopelab P, Adam V (2016) Particle-based immunochemical separation of methicillin resistant Staphylococcus aureus with indirect electrochemical detection of labelling oligonucleotides. Anal Methods 8:5123–5128Google Scholar
  73. 73.
    Wang Z, Zhang J, Chen P, Zhou X, Yang Y, Wu S, Niu L, Han Y, Wang L, Chen P, Boey F, Zhang Q, Liedberg B, Zhang H (2011) Label-free, electrochemical detection of methicillin-resistant staphylococcus aureus DNA with reduced graphene oxide-modified electrodes. Biosens Bioelectron 26:3881–3886PubMedGoogle Scholar
  74. 74.
    Yang Z, Wang Y, Zhang D (2017) A novel multifunctional electrochemical platform for simultaneous detection, elimination, and inactivation of pathogenic bacteria based on the Vancomycin-functionalised AgNPs/3D-ZnO nanorod arrays. Biosens Bioelectron 98:248–253.  https://doi.org/10.1016/j.bios.2017.06.058 CrossRefPubMedGoogle Scholar
  75. 75.
    Liu M, Xiang H, Hua E, Wang L, Jing X, Cao X, Sheng S, Xie G (2014) Ultrasensitive electrochemical biosensor for the detection of the mecA gene sequence in methicillin resistant strains of Staphylococcus aureus employing gold nanoparticles. Anal Lett 47(4):579–591Google Scholar
  76. 76.
    Antuña-Jiménez D, Díaz-Díaz G, Blanco-López MC, M. Lobo-Castañón J, Miranda-Ordieres AJ, Tuñón-Blanco P (2012) Chapter 1 - Molecularly imprinted electrochemical sensors: past, present, and future. Molecularly Imprinted Sensors, Pages 1–34Google Scholar
  77. 77.
    Faulkner LR, Bard AJ (2001) Electrochemical methods: fundamentals and applications, vol 2. Wiley, New York, p 482Google Scholar
  78. 78.
    Xia F, White RJ, Zuo X, Patterson A, Xiao Y, Kang D, Gong X, Plaxco KW, Heeger AJ (2010) An electrochemical super Sandwich assay for sensitive and selective DNA detection in complex matrices. J Am Chem Soc 132:14346–14348PubMedPubMedCentralGoogle Scholar
  79. 79.
    Louis R, Krause MS (2002) Theory of square wave voltammetry. Anal Chem 41(11):1362–1365.  https://doi.org/10.1021/ac60280a005 CrossRefGoogle Scholar
  80. 80.
    Chen A, Shah B (2013) Electrochemical sensing and biosensing based on square wave voltammetry. Anal Methods 5(9):2158–2173Google Scholar
  81. 81.
    Osteryoung JG, Osteryoung RA (1985) Instrumentation. Anal Chem 57(1):101–110Google Scholar
  82. 82.
    Macdonald JR (1992) Impedance spectroscopy. Ann Biomed Eng 20(3):289–305PubMedGoogle Scholar
  83. 83.
    Al-syadi AM, Yousef ES, El-Desoky MM, Al-Assiri MS (2013) Impedance spectroscopy of V2O5–Bi2O3–BaTiO3 glass–ceramics. Solid State Sci 26:72–82.  https://doi.org/10.1016/j.solidstatesciences.2013.10.002 CrossRefGoogle Scholar
  84. 84.
    Hernández S, Tortello M, Sacco A, Quaglio M, Meyer T, Bianco S (2014) New transparent laser-drilled fluorine-doped tin oxide covered quartz electrodes for photo-electrochemical water splitting. Electrochim Acta 131:184–194Google Scholar
  85. 85.
    Lanfredi S, Saia PS, Lebullenger R, Hernandes AC (2002) Electric conductivity and relaxation in fluoride, fluorophosphate and phosphate glasses: analysis by impedance spectroscopy. Solid State Ionics 146:329–339Google Scholar
  86. 86.
    Rubinson JF, Kayinamura YP (2009) Charge transport in conducting polymers: insights from impedance spectroscopy. Chem Soc Rev 38:3339–3347PubMedGoogle Scholar
  87. 87.
    Stassi S, Sacco A, Canavese G (2014) Impedance spectroscopy analysis of the tunneling conduction mechanism in piezoresistive composites. J Phys D: Appl Phys A 47:345306Google Scholar
  88. 88.
    Scrosati B, Croce F, Persi L (2000) Impedance spectroscopy study of PEO-based nanocomposite polymer electrolytes. J Electrochem Soc 147:1718–1721Google Scholar
  89. 89.
    Pollard R, Comte T (1989) Determination of transport properties for solid electrolytes from the impedance of thin layer cells. J Electrochem Soc 136:3734–3748Google Scholar
  90. 90.
    Robertson B, Tribollet B, Deslouis C (1988) Measurement of diffusion coefficients by DC and EHD electrochemical methods. J Electrochem Soc 135:2279–2284Google Scholar
  91. 91.
    Bousse L, Bergveld P (1983) On the impedance of the silicon dioxide/electrolyte interface. J Electroanal Chem Interfacial Electrochem 152:25–39Google Scholar
  92. 92.
    Roy SK, Orazem ME (2007) Error analysis of the impedance response of PEM fuel cells. J Electrochem Soc 154:B883–B891Google Scholar
  93. 93.
    Costamagna P, Costa P, Antonucci V (1998) Micro-modelling of solid oxide fuel cell electrodes. Electrochim Acta 43:375–394Google Scholar
  94. 94.
    Hidalgo D, Sacco A, Hernández S, Tommasi T (2015) Electrochemical and impedance characterization of microbial fuel cells based on 2D and 3D anodic electrodes working with seawater microorganisms under continuous operation. Bioresour Technol 195:139–146PubMedGoogle Scholar
  95. 95.
    Kumar S, Singh PK, Chilana GS (2009) Study of silicon solar cell at different intensities of illumination and wavelengths using impedance spectroscopy. Sol Energy Mater Sol Cells 93:1881–1884Google Scholar
  96. 96.
    Halme J, Vahermaa P, Miettunen K, Lund P (2010) Device physics of dye solar cells. Adv Mater 22:E210–E234PubMedGoogle Scholar
  97. 97.
    Cui N, Luo JL (2000) An AC impedance study of self-discharge mechanism of nickel–metal hydride (Ni–MH) battery using Mg2Ni-type hydrogen storage alloy anode. Electrochim Acta 45:3973–3981Google Scholar
  98. 98.
    Sun Y-K, Kim D-W, Choi Y-M (1999) Synthesis and characterization of spinel LiMn2−xNixO4 for lithium/polymer battery applications. J Power Sources 79:231–237Google Scholar
  99. 99.
    Lamberti A, Garino N, Sacco A, Bianco S, Chiodoni A, Gerbaldi C (2015) As-grown vertically aligned amorphous TiO2 nanotube arrays as high-rate Li-based microbattery anodes with improved long-term performance. Electrochim Acta 151:222–229Google Scholar
  100. 100.
    Templier V, Roupioz Y (2017) On the challenges of detecting whole Staphylococcus aureus cells with biosensors. J Appl Microbiol 123(5):1056–1067.  https://doi.org/10.1111/jam.13510 CrossRefPubMedGoogle Scholar
  101. 101.
    Scholz F (2013) Electroanalytical methods: guide to experiments and applications. Springer, Berlin, Heidelberg, p 109Google Scholar
  102. 102.
    Eduardo L, Joaquín G, Ángela M (2014) Recent advances on the theory of pulse techniques: a mini review. Electrochem Commun 43:25–30.  https://doi.org/10.1016/j.elecom.2014.03.004 CrossRefGoogle Scholar
  103. 103.
    Armada PG, Losada J, Vicente-Pérez S (1996) Cation analysis scheme by differential pulse polarography. J Chem Educ 73(6):544.  https://doi.org/10.1021/ed073p544 CrossRefGoogle Scholar
  104. 104.
    Wolfbeis OS (2002) Fiber-optic chemical sensors. Anal Chem 74(12):2663–2678PubMedGoogle Scholar
  105. 105.
    Cámara C, Moreno MC, Orellana G (1991) Chemical sensing with Fiberoptic devices. In: Biosensors with Fiberoptics, pp 29–84Google Scholar
  106. 106.
    Lübbers DW (1992) Fluorescence based chemical sensors. In: Advances in biosensors, vol 2. JAI Press, New York, pp 215–260Google Scholar
  107. 107.
    Strohsahl CM, Miller BL, Krauss TD (2009) Detection of methicillin-resistant Staphylococcus aureus (MRSA) using the NanoLantern™ Biosensor. Proceedings Volume 7167, Frontiers in Pathogen Detection: From Nanosensors to Systems; 71670S.  https://doi.org/10.1117/12.808872
  108. 108.
    Cihalova K, Hegerova D, Jimenez AM, Milosavljevic V, Kudr J, Skalickova S, Hynek D, Kopel P, Vaculovicova M, Adam V (2016) Antibody-free detection of infectious bacteria using quantum dots-based barcode assay. J Pharm Biomed Anal 134:325–332.  https://doi.org/10.1016/j.jpba.2016.10.025 CrossRefPubMedGoogle Scholar
  109. 109.
    Chan PH, Chen YC (2012) Human serum albumin stabilized gold nanoclusters as selective luminescent probes for Staphylococcus aureus and methicillin-resistant Staphylococcus aureus. Anal Chem 84(21):8952–8956PubMedGoogle Scholar
  110. 110.
    Zhao Z, Yan R, Yi X, Li J, Rao J, Guo Z, Yang Y, Li W, Li YQ, Chen C (2017) Bacteria-activated Theranostic Nanoprobes against methicillin-resistant Staphylococcus aureus infection. ACS Nano 11(5):4428–4438PubMedGoogle Scholar
  111. 111.
    Liu J, Cheng J, Zhang Y (2013) Upconversion nanoparticle based LRET system for sensitive detection of MRSA DNA sequence. Biosens Bioelectron 43:252–256PubMedGoogle Scholar
  112. 112.
    Ning Y, Gao Q, Zhang X, Wei K, Chen L (2016) A graphene oxide–based sensing platform for the determination of methicillin-resistant Staphylococcus aureus based on Strand-displacement polymerization recycling and synchronous fluorescent signal amplification. J Biomol Screen 21(8):851–857PubMedGoogle Scholar
  113. 113.
    Ning Y, Zou L, Gao Q, Hu J, Lu F (2018) Graphene oxide-based fluorometric determination of methicillin-resistant Staphylococcus aureus by using target-triggered chain reaction and deoxyribonuclease-assisted recycling. Mikrochim Acta 185(3):183.  https://doi.org/10.1007/s00604-018-2702-0 CrossRefPubMedGoogle Scholar
  114. 114.
    Fan Z, Kanchanapally R, Ray PC (2013) Hybrid graphene oxide based ultrasensitive SERS probe for label-free biosensing. J Phys Chem Lett 4(21):3813–3818Google Scholar
  115. 115.
    Storhoff JJ, Lucas AD, Garimella V, Bao YP, Müller UR (2004) Homogeneous detection of unamplified genomic DNA sequences based on colorimetric scatter of gold nanoparticle probes. Nat Biotechnol 22(7):883–887PubMedPubMedCentralGoogle Scholar
  116. 116.
    Ocsoy I, Yusufbeyoglu S, Yılmaz V, McLamore ES, Ildız N, Ulgen A (2017) DNA aptamer functionalized gold nanostructures for molecular recognition and photothermal inactivation of methicillin-resistant Staphylococcus aureus. Colloids Surf B: Biointerfaces 159:16–22.  https://doi.org/10.1016/j.colsurfb.2017.07.056 CrossRefPubMedGoogle Scholar
  117. 117.
    Abd-El-Hady H, El-Said W, El-Enbaawy M, Salah Eldin TA (2014) Preparation of mecA biosensor based on gold nanoparticles to determine methicillin resistant Staphylococcus aureus (MRSA) strains from human and animals. IOSR-JAVS 7(8):64–71Google Scholar
  118. 118.
    Chan WS, Tang BS, Boost MV, Chow C, Leung PH (2014) Detection of methicillin-resistant Staphylococcus aureus using a gold nanoparticle-based colorimetric polymerase chain reaction assay. Biosens Bioelectron 53:105–111.  https://doi.org/10.1016/j.bios.2013.09.027 CrossRefPubMedGoogle Scholar
  119. 119.
    Suaifan GARY, Alhogail S, Zourob M (2017) Rapid and low-cost biosensor for the detection of Staphylococcus aureus. Biosens Bioelectron 90:230–237.  https://doi.org/10.1016/j.bios.2016.11.047 CrossRefPubMedGoogle Scholar
  120. 120.
    Tawil N, Sacher E, Mandeville R, Meunier M (2012) Surface plasmon resonance detection of E. coli and methicillin-resistant S. aureus using bacteriophages. Biosens Bioelectron 37(1):24–29PubMedGoogle Scholar
  121. 121.
    Nawattanapaiboon K, Kiatpathomchai W, Santanirand P, Vongsakulyanon A, Amarit R, Somboonkaew A, Sutapun B, Srikhirin T (2015) SPR-DNA array for detection of methicillin-resistant Staphylococcus aureus (MRSA)in combination with loop-mediated isothermal amplification. Biosens Bioelectron 74:335–340PubMedGoogle Scholar
  122. 122.
    Chung HJ, Castro CM, Im H, Lee H, Weissleder R (2013) A magneto-DNA nanoparticle system for rapid detection and phenotyping of bacteria. Nat Biotechnol 8(5):369–375.  https://doi.org/10.1038/nnano.2013.70 CrossRefGoogle Scholar
  123. 123.
    Hiremath N, Guntupalli R, Vodyanoy V, Chin BA, Park MK (2015) Detection of methicillin-resistant Staphylococcus aureus using novellytic phage-based magnetoelastic biosensors. Sensors Actuators B Chem 210:129–136.  https://doi.org/10.1016/j.snb.2014.12.083 CrossRefGoogle Scholar
  124. 124.
    Bandara AB, Zuo Z, Ramachandran S, Ritter A, Heflin JR, Inzana TJ (2015) Detection of methicillin-resistant staphylococci by biosensor assay consisting of nanoscale films on optical fiber long-period gratings. Biosens Bioelectron 70:433–440.  https://doi.org/10.1016/j.bios.2015.03.041 CrossRefPubMedGoogle Scholar
  125. 125.
    Yang AK, Lu H, Wu SY, Kwok HC, Ho HP, Yu S, Cheung AK, Kong SK (2013) Detection of Panton-Valentine Leukocidin DNA from methicillin-resistant Staphylococcus aureus by resistive pulse sensing and loop-mediated isothermal amplification with gold nanoparticles. Anal Chim Acta 782:46–53.  https://doi.org/10.1016/j.aca.2013.04.004 CrossRefPubMedGoogle Scholar
  126. 126.
    Wang CH, Lien KY, Wu JJ, Lee GB (2011) A magnetic bead-based assay for the rapid detection of methicillin-resistant Staphylococcus aureus by using a microfluidic system with integrated loop-mediated isothermal amplification. Lab Chip 11(8):1521–1531.  https://doi.org/10.1039/c0lc00430h CrossRefPubMedGoogle Scholar
  127. 127.
    Zhang H, Ma L, Hua MZ, Wang S, Lu X (2016) Rapid detection of methicillin-resistant Staphylococcus aureus in pork using a nucleic acid-based lateral flow immunoassay. Int J Food Microbiol 243.  https://doi.org/10.1016/j.ijfoodmicro.2016.12.003
  128. 128.
    Wang Y, Yan W, Fu S, Hu S, Wang Y, Xu J, Ye C (2018) Multiple cross displacement amplification coupled with nanoparticles-based lateral flow biosensor for detection of Staphylococcus aureus and identification of methicillin-Resistant S. aureus. Front Microbiol 9:907.  https://doi.org/10.3389/fmicb.2018.00907 CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Ramakrishnan R, Buckingham W, Domanus M, Gieser L, Klein K, Kunkel G, Prokhorova A, Riccelli PV (2004) Sensitive assay for identification of methicillin-resistant Staphylococcus aureus, based on direct detection of genomic DNA by use of gold nanoparticle probes, (Nanosphere, Inc., Northbrook, IL 60062; * author for correspondence). Abstracts of Oak Ridge Posters. Clin Chem 50(10):1949–1952PubMedGoogle Scholar
  130. 130.
    Brédas JL, Norton JE, Cornil J, Coropceanu V (2009) Molecular understanding of organic solar cells: the challenges. Acc Chem Res 42(11):1691–1699.  https://doi.org/10.1021/ar900099h CrossRefPubMedGoogle Scholar
  131. 131.
    Zhang CY, Johnson LW (2006) Quantum dot-based fluorescence resonance energy transfer with improved FRET efficiency in capillary flows. Anal Chem 78:5532–5537PubMedGoogle Scholar
  132. 132.
    Xu X, Li H, Hasan D, Ruoff RS, Wang AX, Fan DL (2013) Near-field enhanced Plasmonic-magnetic bifunctional nanotubes for single cell bioanalysis. Adv Funct Mater 23(35):4332–4338.  https://doi.org/10.1002/adfm.201203822 CrossRefGoogle Scholar
  133. 133.
    Blackie EJ, Le Ru EC, Etchegoin PG (2009) Single-molecule surface-enhanced Raman spectroscopy of nonresonant molecules. J Am Chem Soc 131(40):14466–14472.  https://doi.org/10.1021/ja905319w CrossRefPubMedGoogle Scholar
  134. 134.
    Nie S, Emory SR (1997) Probing single molecules and single nanoparticles by surface-enhanced Raman scattering. Science 275(5303):1102–1106.  https://doi.org/10.1126/science.275.5303.1102 CrossRefPubMedGoogle Scholar
  135. 135.
    Huh YS, Chung AJ, Erickson D (2009) Surface enhanced Raman spectroscopy and its application to molecular and cellular analysis. Microfluid Nanofluid 6:285–297Google Scholar
  136. 136.
    Germain ME, Knapp MJ (2009) Optical explosives detection: from color changes to fluorescence turn-on. Chem Soc Rev 38(9):2543–2555PubMedGoogle Scholar
  137. 137.
    Ghosh SK, Pal T (2007) Interparticle coupling effect on the surface plasmon resonance of gold nanoparticles: from theory to applications. Chem Rev 107(11):4797–4862PubMedGoogle Scholar
  138. 138.
    Erlich HA (1989) Polymerase chain reaction. J Clin Immunol 9(6):437–447PubMedGoogle Scholar
  139. 139.
    Rajamani M, Johney J, Ragunathan R (2017) Detection of mecA gene associated with methicillin resistant Staphylococcus aureus and its alternatives using nanoparticles and chia seeds. Int J Med Res Health Sci 6(11):67–75Google Scholar
  140. 140.
    Chin CD, Linder V, Sia SK (2012) Commercialization of microfluidic point-of-care diagnostic devices. Lab Chip 12:2118–2134.  https://doi.org/10.1039/c2lc21204h CrossRefPubMedGoogle Scholar
  141. 141.
    WHO. Antimicrobial resistance - fact sheet No 194, updated on April 2015. Available from: http://www.who.int/mediacentre/factsheets/fs194/en/
  142. 142.
    Roca I, Akova M, Baquero F, Carlet J, Cavaleri M, Coenen S, Cohen J, Findlay D, Gyssens I, Heure OE, Kahlmeter G, Kruse H, Laxminarayan R, Liébana E, López-Cerero L, MacGowan A, Martins M, Rodríguez-Baño J, Rolain JM, Segovia C, Sigauque B, Tacconelli E, Wellington E, Vila J (2015) The global threat of antimicrobial resistance: science for intervention. New Microbes New Infect 6:22–29PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Atal A. S. Gill
    • 1
  • Sima Singh
    • 1
  • Neeta Thapliyal
    • 2
  • Rajshekhar Karpoormath
    • 1
    Email author
  1. 1.Department of Pharmaceutical Chemistry, College of Health SciencesUniversity of KwaZulu-NatalDurbanSouth Africa
  2. 2.Department of Applied ScienceWomen Institute of TechnologyDehradunIndia

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