Abstract
Pathogen detection is a critical point for the identification and the prevention of problems related to food safety. Failures at detecting contaminations in food may cause outbreaks with drastic consequences to public health. In spite of the real need for obtaining analytical results in the shortest time possible, conventional methods may take several days to produce a diagnosis. Salmonella spp. is the major cause of foodborne diseases worldwide and its absence is a requirement of the health authorities. Biosensors are bioelectronic devices, comprising bioreceptor molecules and transducer elements, able to detect analytes (chemical and/or biological species) rapidly and quantitatively. Electrochemical immunosensors use antibody molecules as bioreceptors and an electrochemical transducer. These devices have been widely used for pathogen detection at low cost. There are four main techniques for electrochemical immunosensors: amperometric, impedimetric, conductometric, and potentiometric. Almost all types of immunosensors are applicable to Salmonella detection. This article reviews the developments and the applications of electrochemical immunosensors for Salmonella detection, particularly the advantages of each specific technique. Immunosensors serve as exciting alternatives to conventional methods, allowing “real-time” and multiple analyses that are essential characteristics for pathogen detection and much desired in health and safety control in the food industry.
Similar content being viewed by others
References
Afonso A, Perez-Lopes B, Faria RC, Mattoso L, Hernandez-Herrero M, Roig-Sagues A, Maltez-Da CM, Merkoci A (2013) Electrochemical detection of Salmonella using gold nanoparticles. Biosens Bioelectron 40:121–126
Alonso-Lomillo MA, Domínguez-Renedo O, Arcos-Martínez MJ (2010) Screen-printed biosensors in microbiology; a review. Talanta 82:1629–1636
Anandan V, Gangadharan R, Zhang G (2009) Role of SAM chain length in enhancing the sensitivity of nanopillar modified electrodes for glucose detection. Sensors 9:1295–1305
Andrews WH, Jacobson A, Hammack T (2015) Food and Drug Administration. Bacteriological Analytical Manual (BAM). Chapter 5 Salmonella Available at: http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070149. htm (accessed 06.01.16)
Arora P, Sindhu A, Dilbaghi N, Chaudhury A (2011) Biosensors as innovative tools for the detection of food borne pathogens. Biosens Bioelectron 28:1–12
Babacan S, Pirarnik P, Letcher S, Rand AG (2000) Evaluation of antibody immobilization methods for piezoelectric biosensor application. Biosens Bioelectron 15:615–621
Bally M, Voros J (2009) Nanoscale labels: nanoparticles and liposomes in the development of high-performance biosensors. Nanomed 4:447–467
Brandão D, Liébana S, Campoy S, Cortés P, Alegret S, Pividori MI (2013) Electrochemical magneto-immunosensing of Salmonella based on nano and micro-sized magnetic particles. J Phys: Conf Series 421(012020):1–7
Brzeska M, Panhorst M, Kamp PB, Schotter J, Reiss G, Pühler A, Becker A, Brückl H (2004) Detection and manipulation of biomolecules by magnetic carriers. J Biotechnol 112:25–33
Burcu BE, Kemal SM (2015) Applications of electrochemical immunosensors for early clinical diagnostics. Talanta 132:162–174
Canbaz MÇ, Sezgintürk MK (2014) Fabrication of a highly sensitive disposable immunosensor based on indium tin oxide substrates for cancer biomarker detection. Anal Biochem 446:9–18
Cao Y, Sun X, Guo Y, Zhao W, Wang X (2015) An electrochemical immunosensor based on interdigitated array microelectrode for the detection of chlorpyrifos. Bioprocess Biosyst Eng 38:307–313
Centers for Disease Control and Prevention (2012) Pathogens causing US foodborne illnesses, hospitalizations, and deaths, 2000–2008 http://www.cdc.gov/foodborneburden/PDFs/pathogens-complete-list-01-12.pdf. Accessed 10 December 2015
Chumyim P, Rijiravanich P, Somasundrum M, Surareungchai W (2014) Detection of Salmonella enterica serovar Typhimurium in milk sample using electrochemical immunoassay and enzyme amplified labeling. Int Conf Agric Environ Biol Sci (AEBS-2014) Phuket (Thailand) 24–25
Clark LC Jr, Lyons C (1962) Electrode systems for continuous monitoring in cardiovascular surgery. Am NY Acad Sci 31:29–45
Coen MC, Lehmann R, Groning P, Bielmann M, Galli C, Schlapbach L (2001) Adsorption and bioactivity of protein A on silicon surfaces studies by AFM and XPS. J Colloid Interf Sci 233:180–189
Croci L, Delibato E, Volpe G, Palleschi G (2001) A rapid electro-chemical ELISA for the detection of Salmonella in meat samples. Anal Lett 34:2597–2607
Delibato E, Volpe G, Stangalini D, De Medici D, Moscone D, Palleschi G (2006) Development of SYBR-green real-time PCR and a multichannel electrochemical immunosensor for specific detection of Salmonella enterica. Anal Lett 39:1611–1625
Derkus B, Kc E, Mazi H, Emregul E, Yumak T, Sinag A (2014) Protein a immunosensor for the detection of immunoglobulin G by impedance spectroscopy. Bioprocess Biosyst Eng 37:965–976
Dev Das R, Roychaudhuri C, Maju S, Das S, Saha H (2009) Macroporous silicone based simple and eficiente trapping platform for electrical detection of Salmonella Typhimurium pathogens. Biosens Bioelectron 24:3215–3222
Dill K, Stanker LH, Young CR (1999) Detection of Salmonella in poultry using a silicon chip-based biosensor. J Biochem Biophys Methods 41:61–67
Dominguez-Benetton X, Srikanth S, Satyawali Y, Vanbroekhoven K, Pant D (2013) Enzymatic electrosynthesis: an overview on the progress in enzyme-electrodes for the production of electricity, fuels and chemicals. J Microb Biochem Technol S6:007. doi:10.4172/1948-5948. S6-007
Dong J, Xu M, Maa Q, Ai S, Zhao H (2013) A label-free electrochemical impedance immunosensor based on AuNPs/PAMAM-MWCNT-Chi nanocomposite modified glassy carbon electrode for detection of Salmonella Typhimurium in milk. Food Chem 141:1980–1986
European Food Safety Agency (2014) EFSA explains zoonotic diseases—Salmonella. http://www.efsa.europa.eu/en/search/doc/factsheetsalmonella.pdf. Accessed 20 October 2015
Feng P (2010) Rapid methods for detecting foodborne pathogens. In: Food and Drug Administration. Bacteriological Analytical Manual (BAM). Appendix 1. Available at: http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070149.htm (accessed 06.12.14)
Ferreira NS, Sales MGF (2014) Disposable immunosensor using a simple method for oriented antibody immobilization for label free real time detection of an oxidative stress biomarker implicated in cancer diseases. Biosens Bioelectron 53:193–199
Food and Drug Administration (2012) Bad bug book, foodborne pathogenic microorganisms and natural toxins. Second edition. [Salmonella species, pp. 9–13]
Freitas M, Viswanathan S, Nouws H, Oliveira M, Delerue-Matos C (2014) Iron oxide/gold core/shell nanomagnetic probes and CdS biolabels for amplified electrochemical immunosensing of Salmonella Typhimurium. Biosens Bioelectron 51:195–200
Gehring AG, Crawford CG, Mazenko RS, Van Houten LJ, Brewster JD (1996) Enzyme-linked immunomagnetic electrochemical detection of Salmonella Typhimurium. J Immunol Methods 195:15–25
Gil ES, Mello GR (2010) Electrochemical biosensors in pharmaceutical analysis. Braz J Pharm Sci 46:375–391
Hayes JJ, Kennmore M, Badley A, Cullen DC (1998) AFM study of antibody adsorption to polystylene microtitre plates. Nanobiotechnol 4:141–151
Holford TRJ, Davis F, Higson SPJ (2012) Recent trends in antibody based sensors. Biosens Bioelectron 34:12–24
Hu CM, Dou W, Zhao G (2014) Enzyme immunosensor based on gold nanoparticles electroposition and streptavidin-biotin system for detection of S. Pullorum & S. Gallinarum. Electrochim Acta 117:239–245
Jaffrezic-Renault N, Dzyadevych SV (2008) Conductometric microbiosensors for environmental monitoring. Sens 8:2569–2588
Kaur J, Singh KV, Schmid AH, Varshney GC, Suri R, Raje M (2004) Atomic force spectrsocpy-based study of antibody pesticide interactions for characterization of immunosensor surface. Biosens Bioelectron 20:284–293
Kim S, Choi SJ (2014) A lipid-based method for the preparation of a piezoelectric DNA biosensor. Anal Biochem 458:1–3
Kim G-H, Rand AG, Letcher SV (2003) Impedance characterization of a piezoelectric immunosensor part II: Salmonella Typhimurium detection using magnetic enhancement. Biosens Bioelectron 18:91–99
Kirsch J, Siltanen C, Zhou Q, Revzin A, Simonian A (2013) Biosensor technology: recent advances in threat agent detection and medicine. Chem Soc Rev 42:8733–8768
Lawrence AJ, Moores GR (1972) Conductimetry in enzyme studies. European J Biochem 24:538–546
Lee W, Oh B-K, Bae YM, Paek S-H, Lee WH, Choi J-W (2003) Fabrication of self-assembled protein A monolayer and its application as an immunosensor. Biosens Bioelectron 19:185–192
Lee K-M, Runyon M, Herrman TJ, Hsieh J, Phillips R (2015) Review of Salmonella detection and identification methods: aspects of rapid emergency response and food safety. Food Control 47:264–276
Liébana S, Lermo A, Alegret S, Pividori MI, Campoy S, Cortés MP (2009) Rapid detection of Salmonella in milk by electrochemical magneto-immunosensing. Biosens Bioelectron 25:510–513
Liu Y, Che Y, Li Y (2001) Rapid detection of Salmonella Typhimurium using immunomagnetic separation and immuno-optical sensing method. Sens Actuators: B Chem 72:214–218
Liu X, Wang X, Zhang J, Feng H, Liu X, Wong DKY (2012) Detection of estradiol at an electrochemical immunosensor with a Cu UPD| DTBP-Protein G scaffold. Biosens Bioelectron 35:56–62
Ma X, Jiang Y, Jia F, Chen J, Wang Z, Yu Y (2014) An aptamer-based electrochemical biosensor for the detection of Salmonella. J Microbiol Methods 98:94–98
Mantzila AG, Maipa V, Prodromidis MI (2008) Development of a faradaic impedimetric immunosensor for the detection of Salmonella Typhimurium in milk. Anal Chem 80:1169–1175
Margot H, Stephan R, Mahony E, Iversen C (2013) Comparison of rapid cultural methods for the detection of Salmonella species. International J Food Microbiol 163:47
Martín-Yerga D, González-García MB, Costa-García A (2013) Biosensor array based on the in situ detection of quantum dots as electrochemical label. Sens Actuators: B Chem 182:184–189
Meyer MHF, Hartmann M, Krause H-J, Blankenstein G, Mueller-Chorus B, Oster J, Miethe P, Keusgen M (2007) CRP determination based on a novel magnetic biosensor. Biosens Bioelectron 22:973–979
Morales MD, Serra B, Guzmán-Vázquez de Prada A, Reviejo AJ, Pingarrón JM (2007) An electrochemical method for simultaneous detection and identification of Escherichia coli, Staphylococcus aureus and Salmonella Choleraesuis using a glucose oxidase-peroxidase composite biosensor. Analyst 132:572–578
Mortari A, Lorenzelli L (2014) Recent sensing technologies for pathogen detection in milk: a review. Biosens Bioelectron 60:8–21
Muhammad-Tahir Z, Alocilja EC (2003) A conductometric biosensor for biosecurity. Biosens Bioelectron 18:813–819
Murugaiyan S, Ramasamy R, Gopal N (2014) Biosensors in clinical chemistry: an overview. Adv Biomed Res 3:67
Nandakumar S, Woolard SN, Yuan D, Rouse BT, Kumaraguru U (2008) Natural killer cells as novel helpers in anti-herpes simplex virus immune response. J Virol 82:10820–10831
Nandakumar V, Bishop D, Alonas E, Labelle J, Joshi L, Alford TI (2011) A low- cost electrochemical biosensor for rapid bacterial detection. IEEE Sensors J 11:210–216
Nguyen P-D, Tran TB, Nguyen DTX, Min J (2014) Magnetic silica nanotube-assisted impedimetric immunosensor for the separation and label-free detection of Salmonella Typhimurium. Sens Actuators: B. Chemical 197:314–320
Niraj MMGASP (2012) Histamine biosensor: a review. Int J Pharm Sci Res 3:4158–4168
Olsen EV, Pathirana ST, Samoylov AM, Barbaree JM, Chin BA, Neely WC, Vodyanoy V (2003) Specific and selective biosensor for Salmonella and its detection in the environment. J Micorbiol Methods 53:273–285
Özel RE, Ispas C, Ganesana M, Leiter JC, Andreescu S (2014) Glutamate oxidase biosensor based on mixed ceria and titania nanoparticles for the detection of glutamate in hypoxic environments. Biosens Bioelectron 52:397–402
Park I-S, Kim W-Y, Kim N (2000) Operational characteristics of an antibody-immobilized QCM system detecting Salmonella spp. Biosens Bioelectron 15:167–172
Pathirana ST, Barbaree J, Chin BA, Hartell MG, Neely WC (2000) Rapid and sensitive biosensor for Salmonella. Biosens Bioelectron 15:135–144
Pimenta-Martins MG, Furtado RF, Heneine LG, Dias RS, Morges MF, Alves CR (2012) Development of an amperometric immunosensor for detection of Staphylococcal enterotoxin type A in cheese. J Microbiol Methods 91:138–143
Pohanka M, Skládal P (2008) Electrochemical biosensors—principles and applications. J Appl Biomed 6:57–64
Pournaras AV, Koraki T, Prodromidis MI (2008) Development of an impedimetric immunosensor based on electropolymerized polytyramine films for the direct detection of Salmonella Typhimurium in pure cultures of type strains and inoculated real samples. Anal Chim Acta 624:301–307
Prashar D (2012) Self assembled monolayers—a review. Int J Chem Tech Res 4:258–265
Prodromidis MI (2010) Impedimetric immunosensors—a review. Electrochim Acta 55:4227–4233
Prusak-Sochaczewski E, Luong JTT, Guilbault GG (1990) Development of a piezoelectric immunosensor for the detection of Salmonella Typhimurium. Enzyme Microbiol Technol 12:173–177
Purvis D, Leonardova O, Farmakovsky D, Cherkasov V (2003). An ultrasensitive and stable potentiometric immunosensor. Biosens and Bioelectron 18:1385–1390
Qureshi A, Gurbuz Y, Niazi JH (2012) Biosensors for cardiac biomarkers detection: a review.(Report). Sens Actuators: B Chem 171:62–76
Ricci F, Adornetto G, Palleschi G (2012) A review of experimental aspects of electrochemical immunosensors. Electrochim Acta 84:74–83
Rickert J, Gopel W, Beck W, Jung G, Heiduschka P (1996) A ‘mixed’ self- assembled monolayer for an impedimetric immunosensor. Biosens Bioelectron 11:757–768
Salam F, Tothill IE (2009) Detection of Salmonella Typhimurium using an electrochemical immunosensor. Biosens Bioelectron 24:2630–2636
Saleem M (2013) Biosensors a promising future in measurements. IOP Conf. Series: Mater Sci Eng 51(012012):1–10
Si S-H, Li X, Fung Y-S, Zhu D-R (2001) Rapid detection of Salmonella Enteritidis by piezoelectric immunosensor. Microchem J 68:21–27
Sibai A, Elamri K, Barbier D, Zaffrezic-Renault N, Souteyrand E (1996) Analysis of the polymer-antibody-antigen interaction in a capacitive immunosensor by FTIR difference spectroscopy. Sens actuators: B Chem 31:125–130
Singh R, Mukherjee MD, Sumana G, Gupta RK, Sood S, Malhotra BD (2014) Biosensors for pathogen detection: a smart approach towards clinical diagnosis. Sens actuators: B Chem 197:385–404
Skládal P, Kovar D, Krajicek V, Siskova P, Pribyl J, Svabenska E (2013) Electrochemical immunosensors for detection of microorganisms. Int J Electrochem Sci 8:1635–1649
Soto AMG, Jaffari SA, Bone S (2001) Characterisation and optimization of AC conductometric biosensor. Biosens Bioelectron 16:23–29
Su L, Jia W, Hou C, Lei Y (2011) Microbial biosensors: a review. Biosens and Bioelectron 26:1788–1799
Vashist SK, Zheng D, Al-Rubeaan K, Luong JHT, Sheu F-S (2011) Advances in carbon nanotube based electrochemical sensors for bioanalytical applications. Biotechnol Adv 29:169–188
Velusamy V, Arshak K, Korostynska O, Oliwa K, Adley C (2010) An overview of foodborne pathogen detection: in the perspective of biosensors. Biotechnol Adv 28:232–254
Vidal JC, Bonel L, Ezquerra A, Hernandez S, Bertolin JR, Cubel C, Castillo JR (2013) Electrochemical affinity biosensors for detection of mycotoxins: a review. Biosens Bioelectron 49:146–158
Vilarino N, Fonfria ES, Louzao MC, Botana LM (2009) Use of biosensors as alternatives to current regulatory methods for marine biotoxins. Sens 9(11):9414
Vo-Dihn T, Tromberg GD, Griffin KR, Ambrose MJ, Sepaniak MJ, Gardenhire EM (1987) Antibody-based fiber ptics biosensor for the carcinogen benzo (a) pyrene. Appl Spectro Sci 41:735–738
Wang J (2005) Nanomaterial based electrochemical biosensors. Analyst 130:421–426
Wang Y, Ye Z, Ying Y (2012) New trends in impedimetric biosensors for the detection of foodborne pathogenic bacteria. Sensors 12:3449–3471
Wong YYNG, Ng MH, Si SH, Yao SZ, Fung YS (2002) Immunosensor for the differentiation and detection of Salmonella species based on quartz crystal microbalance. Biosens Bioelectron 17:676–684
Yang G-J, Huang J-L, Meng W-J, Shen M, Jiao X-A (2009) A reusable capacitive immunosensor for detection of Salmonella spp. based on grafted ethylene diamine and self-assembled gold nanoparticle monolayers. Anal Chim Acta 647:159–166
Zhao Y, Zheng Y, Kong R, Xia L, Qu F (2016) Ultrasensitive electrochemical immunosensor based on horseradish peroxidase (HRP)-loaded silica-poly (acrylic acid) brushes for protein biomarker detection. Biosens Bioelectron 75:383–388
Zhu D, Yan Y, Lei P, Shen B, Cheng W, Ju H, Ding SJ (2014) A novel electrochemical sensing strategy for rapid and ultrasensitive detection of Salmonella by rolling circle amplification and DNA-AuNPs probe. Anal Chim Acta 846:44–50
Acknowledgments
The authors acknowledge the financial support of the CNPq (Award number: 475174/2012-7) and CAPES Brazilian agencies. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Melo, A.M.A., Alexandre, D.L., Furtado, R.F. et al. Electrochemical immunosensors for Salmonella detection in food. Appl Microbiol Biotechnol 100, 5301–5312 (2016). https://doi.org/10.1007/s00253-016-7548-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-016-7548-y