Advances in Rapid Detection Methods for Foodborne Pathogens

Xihong  Zhao; Chii-Wann  Lin; Jun  Wang; Deog Hwan  Oh

doi:10.4014/jmb.1310.10013

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Review

Advances in Rapid Detection Methods for Foodborne Pathogens

Xihong Zhao ^{1, 2, 3}, Chii-Wann Lin ³, Jun Wang ² and Deog Hwan Oh ^2*

¹Key Laboratory for Green Chemical Process of Ministry of Education, School of Chemical Engineering and Pharmacy, Wuhan Institute of Technology, Wuhan 430073, China, ²Department of Food Science and Biotechnology and Institute of Bioscience and Biotechnology, Kangwon National University, Chuncheon 200701, Republic of Korea, ³Institute of Biomedical Engineering, National Taiwan University, Taipei 10617, Taiwan

Received: October 7, 2013; Accepted: December 22, 2013

J. Microbiol. Biotechnol. 2014; 24(3): 297-312

Published March 28, 2014 https://doi.org/10.4014/jmb.1310.10013

Abstract

Food safety is increasingly becoming an important public health issue, as foodborne diseases present a widespread and growing public health problem in both developed and developing countries. The rapid and precise monitoring and detection of foodborne pathogens are some of the most effective ways to control and prevent human foodborne infections. Traditional microbiological detection and identification methods for foodborne pathogens are well known to be time consuming and laborious as they are increasingly being perceived as insufficient to meet the demands of rapid food testing. Recently, various kinds of rapid detection, identification, and monitoring methods have been developed for foodborne pathogens, including nucleic-acid-based methods, immunological methods, and biosensor-based methods, etc. This article reviews the principles, characteristics, and applications of recent rapid detection methods for foodborne pathogens.

Keywords

foodborne pathogen, rapid detection, nucleic acid based methods, immunological methods, biosensor based methods

References

Abbas A, Linman MJ, Cheng QA. 2011. New trends in instrumental design for surface plasmon resonance-based biosensors. Biosens. Bioelectron. 26: 1815-1824.
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.
Asiello PJ, Baeumner AJ. 2011. Miniaturized isothermal nucleic acid amplification, a review. Lab. Chip 11: 14201430.
Baeumner AJ, Cohen RN, Miksic V, Min J. 2003. RNA biosensor for the rapid detection of viable Escherichia coli in drinking water. Biosens. Bioelectron. 18: 405-413.
Bolton FJ, Fritz E, Poynton S, Jensen T. 2000. Rapid enzyme-linked immunoassay for detection of Salmonella in food and feed products: performance testing program. J. AOAC Int. 83: 299-303.
Campbell GA, Mutharasan R. 2006. Piezoelectric-excited millimeter-sized cantilever (PEMC) sensors detect Bacillus anthracis at 300 spores/ml. Biosens. Bioelectron. 21: 16841692.
Cao W, S u M, Z hang S . 2010. Rap id and s ensitive DNA target detection using enzyme amplified electrochemical detection based on microchip. Electrophoresis 31: 659-665.
CDC 2011. CDC Estimates of Foodborne Illness in the United States. [Online.] http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html
Chamberlain JS, Gibbs RA, Ranier JE, Nguyen PN, Caskey CT. 1988. Deletion screening of the Duchenne muscular dystrophy locus via multiplex DNA amplification. Nucleic Acids Res. 16: 11141-11156.
Chen HM, Lin CW. 2007. Hydrogel-coated streptavidin piezoelectric biosensors and applications to selective detection of Strep-Tag displaying cells. Biotechnol. Prog. 23: 741-748.
Chen HT, Zhang J, Sun DH, Ma LN, Liu XT, Cai XP, Liu YS. 2008. Development of reverse transcription loopmediated isothermal amplification for rapid detection of H9 avian influenza virus. J. Virol. Methods 151: 200-203.
Chen J, Ma XY, Yuan YW, Zhang W. 2011. Sensitive and rapid detection of Alicyclobacillus acidoterrestris u sing loop mediated isothermal amplification. J. Sci. Food Agric. 91:1070-1074.
Chen SY, Wang F, Beaulieu JC, Stein RE, Ge BL. 2011. Rapid detection of viable salmonellae in produce by coupling propidium monoazide with loop-mediated isothermal amplification. Appl. Environ. Microbiol. 77: 4008-4016.
Chen ZG. 2008. Conductometric immunosensors for the detection of staphylococcal enterotoxin B based bioelectrocalytic reaction on micro-comb electrodes. Bioproc. Biosyst. Eng. 31: 345-350.
Chuang TL, Wei SC, Lee SY, Lin CW. 2012. A polycarbonate based surface plasmon resonance sensing cartridge for high sensitivity HBV loop-mediated isothermal amplification. Biosens. Bioelectron. 32: 89-95.
Churruca E, Girbau C, Martinez I, Mateo E, Alonso R, Fernandez-Astorga A. 2007. Detection of Campylobacter jejuni and Campylobacter coli in chicken meat samples by real-time nucleic acid sequence-based amplification with molecular beacons. Int. J. Food Microbiol. 117: 85-90.
Compton J. 1991. Nucleic acid sequence-based amplification. Nature 350: 91-92.
de Boer E, Beumer RR. 1999. Methodology for detection and typing of foodborne microorganisms. Int. J. Food Microbiol. 50: 119-130.
DeCory TR, Durst RA, Zimmerman SJ, Garringer LA, Paluca G, DeCory HH, Montagna RA. 2005. Development of an immunomagnetic bead-immunoliposome fluorescence assay for rapid detection of Escherichia coli O157:H7 in aqueous samples and comparison of the assay with a standard microbiological method. Appl. Environ. Microbiol. 71: 1856-1864.
Delmulle BS, De Saeger SM, Sibanda L, Barna-Vetro I, Van Peteghem CH. 2005. Development of an immunoassaybased lateral flow dipstick for the rapid detection of aflatoxin B1 in pig feed. J. Agric. Food Chem. 53: 3364-3368.
Derzelle S, Grine A, Madic J, de Garam CP, Vingadassalon N, Dilasser F, et al. 2011. A quantitative PCR assay for the detection and quantification of Shiga toxin-producing Escherichia coli (STEC) in minced beef and dairy products. Int. J. Food Microbiol. 151: 44-51.
Dey D, Goswami T. 2011. Optical Biosensors: A revolution towards quantum nanoscale electronics device fabrication. J. Biomed. Biotechnol. 2011: 348218.
Dongyou L. 2010. Molecular Detection of Foodborne Pathogens. CRC Press, Boca Raton.
Dwivedi HP, Jaykus LA. 2011. Detection of pathogens in foods: the current state-of-the-art and future directions. Crit. Rev. Microbiol. 37: 40-63.
Feng P. 1997. Impact of molecular biology on the detection of foodborne pathogens. Mol. Biotechnol. 7: 267-278.
Foley SL, Grant K. 2007. Molecular techniques of detection and discrimination of foodborne pathogens and their toxins, p. 485-510. In Simjee S (ed.). Infectious Disease: Foodborne Diseases. Humana Press Inc, Totowa, NJ.
Fusco V, Quero GM, Morea M, Blaiotta G, Visconti A. 2011. Rapid and reliable identification of Staphylococcus aureus harbouring the enterotoxin gene cluster (egc) and quantitative detection in raw milk by real time PCR. Int. J. Food Microbiol. 144: 528-537.
Fykse EM, Skogan G, Davies W, Olsen JS, Blatny JM. 2007. Detection of Vibrio cholerae by real-time nucleic acid sequence-based amplification. Appl. Environ. Microbiol. 73:1457-1466.
Gill P, Ghaemi A. 2008. Nucleic acid isothermal amplification technologies: a review. Nucleosides Nucleotides Nucleic Acids 27: 224-243.
Gill P, Ramezani R, Amiri MVP, Ghaemi A, Hashempour T, Eshraghi N, et al. 2006. Enzyme-linked immunosorbent assay of nucleic acid sequence-based amplification for molecular detection of M-tuberculosis. Biochem. Biophys. Res. Commun. 347: 1151-1157.
Gizeli E, Lowe CR. 1996. Immunosensors. Curr. Opin. Biotechnol. 7: 66-71.
Gomez P, Pagnon M, Egea-Cortines M, Artes F, Weiss J. 2010. A fast molecular nondestructive protocol for evaluating aerobic bacterial load on fresh-cut lettuce. Food Sci. Technol. Int. 16: 409-415.
Grothaus GD, Bandla M, Currier T, Giroux R, Jenkins GR, Lipp M, et al. 2006. Immunoassay as an analytical tool in agricultural biotechnology. J. AOAC Int. 89: 913-928.
Guatelli JC, Whitfield KM, Kwoh DY, Barringer KJ, Richman DD, Gingeras TR. 1990. Isothermal, in vitro amplification of nucleic acids by a multienzyme reaction modeled after retroviral replication. Proc. Natl. Acad. Sci. USA 87: 7797.
Hahm BK, Bhunia AK. 2006. Effect of environmental stresses on antibody-based detection of Escherichia coli O157:H7, Salmonella enterica serotype Enteritidis and Listeria monocytogenes. J. Appl. Microbiol. 100: 1017-1027.
Hahn MA, Keng PC, Krauss TD. 2008. Flow cytometric analysis to detect pathogens in bacterial cell mixtures using semiconductor quantum dots. Anal. Chem. 80: 864872.
Hill WE. 1996. The polymerase chain reaction: applications for the detection of foodborne pathogens. Crit. Rev. Food Sci. Nutr. 36: 123-173.
Ikeda S, Takabe K, Inagaki M, Funakoshi N, Suzuki K. 2007. Detection of gene point mutation in paraffin sections using in situ loop-mediated isothermal amplification. Pathol. Int. 57: 594-599.
Iseki H, Alhassan A, Ohta N, Thekisoe OMM, Yokoyama N, Inoue N, et al. 2007. Development of a multiplex loopmediated isothermal amplification (mLAMP) method for the simultaneous detection of bovine Babesia p arasites. J. Microbiol. Methods 71: 281-287.
Jasson V, Jacxsens L, Luning P, Rajkovic A, Uyttendaele M. 2010. Alternative microbial methods: an overview and selection criteria. Food Microbiol. 27: 710-730.
Jung BY, Jung S C, K weon C H. 2 005. D evelop ment o f a rapid immunochromatographic strip for detection of Escherichia coli O157. J. Food Prot. 68: 2140-2143.
Kawasaki S, Fratamico PM, Horikoshi N, Okada Y, Takeshita K, Sameshima T, Kawamoto S. 2009. Evaluation of a multiplex PCR system for simultaneous detection of Salmonella spp., listeria monocytogenes, and Escherichia coli O157:H7 in foods and in food subjected to freezing. Foodborne Pathog. Dis. 6: 81-89.
Kawasaki S, Horikoshi N, Okada Y, Takeshita K, Sameshima T, Kawamoto S. 2005. Multiplex PCR for simultaneous detection of Salmonella spp., Listeria monocytogenes, and Escherichia coli O 157:H7 i n meat s amp les. J. Food Prot. 68:551-556.
Kim HJ, Lee HJ, Lee KH, Cho JC. 2012. Simultaneous detection of pathogenic Vibrio species using multiplex realtime PCR. Food Control 23: 491-498.
Kong RY, Lee SK, Law TW, Law SH, Wu RS. 2002. Rapid detection of six types of bacterial pathogens in marine waters by multiplex PCR. Water Res. 36: 2802-2812.
Lan YB, Wang SZ, Yin YG, Hoffmann WC, Zheng XZ. 2008. Using a surface plasmon resonance biosensor for rapid detection of Salmonella Typhimurium in chicken carcass. J. Bionic Eng. 5: 239-246.
Laura A, Gilda D, Claudio B, Cristina G, Gianfranco G. 2011. A lateral flow immunoassay for measuring ochratoxin A: development of a single system for maize, wheat and durum wheat. Food Control 22: 1965-1970.
Lazcka O, Del Campo FJ, Munoz FX. 2007. Pathogen detection: A perspective of traditional methods and biosensors. Biosens. Bioelectron. 22: 1205-1217.
Lee JY, Deininger RA. 2004. Detection of E. coli in beach water within 1 hour using immunomagnetic separation and ATP bioluminescence. Luminescence 19: 31-36.
Leonard P, Hearty S, Brennan J, Dunne L, Quinn J, Chakraborty T, O’Kennedy R. 2003. Advances in biosensors for detection of pathogens in food and water. Enzyme Microb. Technol. 32: 3-13.
Li Y, Cheng P, Gong JH, Fang LC, Deng J, Liang WB, Zheng JS. 2012. Amperometric immunosensor for the detection of Escherichia coli O157:H7 in food specimens. Anal. Biochem. 421: 227-233.
Li Y, Mustapha A. 2004. Simultaneous detection of Escherichia coli O157:H7, Salmonella, and Shigella in apple cider and produce by a multiplex PCR. J. Food Prot. 67: 2733.
Lin WS, Cheng CM, Van KT. 2010. A quantitative PCR assay for rapid detection of Shigella species in fresh produce. J. Food Prot. 73: 221-233.
Lin YH, Chen SH, Chuang YC, Lu YC, Shen TY, Chang CA, Lin CS. 2008. Disposable amperometric immunosensing strips fabricated by Au nanoparticles-modified screenprinted carbon electrodes for the detection of foodborne pathogen Escherichia coli O157:H7. Biosens Bioelectron. 23:1832-1837.
Liu Y, Chuang CK, Chen WJ. 2009. In situ reversetranscription loop-mediated isothermal amplification (in situ RT-LAMP) for detection of Japanese encephalitis viral RNA in host cells. J. Clin. Virol. 46: 49-54.
Loens K, Beck T, Goossens H, Ursi D, Overdijk M, Sillekens P, Ieven M. 2006. Development of conventional and real-time nucleic acid sequence-based amplification assays for detection of Chlamydophila pneumoniae in respiratory specimens. J. Clin. Microbiol. 44: 1241-1244.
Louie AS, Marenchic IG, Whelan RH. 1998. A fieldable modular biosensor for use in detection of foodborne pathogens. Field Anal. Chem. Technol. 2: 371-377.
Luo XL, Xu JJ, Zhao W, Chen HY. 2004. Glucose biosensor based on E NFET d op ed w ith SiO2 nanoparticles. Sensors Actuat B Chem. 97: 249-255.
Magliulo M, Simoni P, Guardigli M, Michelini E, Luciani M, Lelli R, Roda A. 2007. A rapid multiplexed chemiluminescent immunoassay for the detection of Escherichia coli O157:H7, Yersinia enterocolitica, Salmonella typhimurium, and Listeria monocytogenes pathogen bacteria. J. A g ric. F ood C hem. 55:4933-4939.
Mandal PK, Biswas AK, Choi K, Pal U. 2011. Methods for rapid detection of foodborne pathogens: an overview. Am. J. Food Technol. 6: 87-102.
Martinon A, Wilkinson MG. 2011. Selection of optimal primer sets for use in a duplex sybr green-based, real-time polymerase chain reaction protocol for the detection of listeria monocytogenes and staphyloccocus aureus in foods. J. Food Saf. 31: 297-312.
Maruyama F, Kenzaka T, Yamaguchi N, Tani K, Nasu M. 2003. Detection of bacteria carrying the stx2 gene by in situ loop-mediated isothermal amplification. Appl. Environ. Microbiol. 69: 5023-5028.
McEgan R, Fu TJ, Warriner K. 2009. Concentration and detection of Salmonella in mung bean sprout spent irrigation water by use of tangential flow filtration coupled with an amperometric flowthrough enzyme-linked immunosorbent assay. J. Food Prot. 72: 591-600.
Meeusen CA, Alocilja EC, Osburn WN. 2005. Detection of E. coli O157:H7 using a miniaturized surface plasmon resonance biosensor. Trans. ASAE 48: 2409-2416.
Min J, Baeumner AJ. 2002. Highly sensitive and specific detection of viable Escherichia coli in drinking water. Anal. Biochem. 303: 186-193.
Mukhopadhyay A, Mukhopadhyay UK. 2007. Novel multiplex PCR approaches for the simultaneous detection of human pathogens: Escherichia coli O157:H7 and Listeria monocytogenes. J. Microbiol. Methods 68: 193-200.
Muldoon MT, Teaney G, Li J, Onisk DV, Stave JW. 2007. Bacteriophage-based enrichment coupled to immunochromatographic strip-based detection for the determination of Salmonella in meat and poultry. J. Food Prot. 70: 2235-2242.
Nam HM, Srinivasan V, Gillespie BE, Murinda SE, Oliver SP. 2005. Application of SYBR green real-time PCR assay for specific detection of Salmonella s p p .in d airy f arm environmental samples. Int. J. Food Microbiol. 102: 161-171.
Nemoto J, Ikedo M, Kojima T, Momoda T, Konuma H, Hara-Kudo Y. 2011. Development and evaluation of a loop-mediated isothermal amplification assay for rapid and sensitive detection of Vibrio parahaemolyticus. J. Food Prot. 74: 1462-1467.
Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T. 2000. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. 28:E63.
Ohtsuka K, Tanaka M, Ohtsuka T, Takatori K, Hara-Kudo Y. 2010. Comparison of detection methods for Escherichia coli O157 in beef livers and carcasses. Foodborne Pathog. Dis. 7: 1563-1567.
Oliver SP, Jayarao BM, Almeida RA. 2005. Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog. Dis. 2: 115-129.
Ong KG, Zeng KF, Yang XP, Shankar K, Ruan CM, Grimes CA. 2006. Quantification of multiple bioagents with wireless, remote-query magnetoelastic microsensors. IEEE Sensors J. 6: 514-523.
Pal S, Ying W, Alocilja EC, Downes FP. 2008. Sensitivity and specificity performance of a direct-charge transfer biosensor for detecting Bacillus cereus in selected food matrices Biosys Eng. 99: 461-468.
Park YS, Lee SR, Kim YG. 2006. Detection of Escherichia coli O157:H7, Salmonella spp., Staphylococcus aureus and Listeria monocytogenes in kimchi by multiplex polymerase chain reaction (mPCR). J. Microbiol. 44: 92-97.
Pedrero M, Campuzano S, Pingarron JM. 2009. Electroanalytical sensors and devices for multiplexed detection of foodborne pathogen microorganisms. Sensors 9: 5503-5520.
Planche T, Aghaizu A, Holliman R, Riley P, Poloniecki J, Breathnach A, Krishna S. 2008. Diagnosis of Clostridium difficile infection by toxin detection kits: a systematic review. Lancet Infect. Dis. 8: 777-784.
Posthuma-Trump ie GA, K orf J, v an Amerongen A . 2009. Lateral flow (immuno) assay: its strengths, weaknesses, opportunities and threats. A literature survey. Anal. Bioanal. Chem. 393: 569-582.
Qiao YM, Guo YC, Zhang XE, Zhou YF, Zhang ZP, Wei HP, et al. 2007. Loop-mediated isothermal amplification for rapid detection of Bacillus anthracis spores. Biotechnol. Lett. 29: 1939-1946.
Rahman S, Lipert RJ, Porter MD. 2006. Rapid screening of pathogenic bacteria using solid phase concentration and diffuse reflectance spectroscopy. Anal. Chim. Acta 569: 8390.
Rao VK, Rai GP, Agarwal GS, Suresh S. 2005. Amperometric immunosensor for detection of antibodies of Salmonella Typhi in patient serum. Anal. Chim. Acta 531: 173-177.
Rasooly A, Herold KE. 2006. Biosensors for the analysis of food- and waterborne pathogens and their toxins. J. AOAC Int. 89: 873-883.
Rodriguez-Lazaro D, Jofre A, Aymerich T, Hugas M, Pla M. 2004. Rapid quantitative detection of Listeria monocytogenes in meat products by real-time PCR. Appl. Environ. Microbiol. 70: 6299-6301.
Rosebrough SF, Hartley DF. 1996. Biochemical modification of streptavidin and avidin: in vitro and in vivo analysis. J. Nucl. Med. 37: 1380-1384.
Salmain M, Ghasemi M, Boujday S, Spadavecchia J, Techer C, Val F, et al. 2011. Piezoelectric immunosensor for direct and rapid detection of staphylococcal enterotoxin A (SEA) at the ng level. Biosens. Bioelectron. 29: 140-144.
Sankaran S, Panigrahi S, Mallik S. 2011. Olfactory receptor based piezoelectric biosensors for detection of alcohols related to food safety applications. Sensors Actuat B Chem. 155: 8-18.
Schlosser G, Kacer P, Kuzma M, Szilagyi Z, Sorrentino A, Manzo C, et al. 2007. Coupling immunomagnetic separation on magnetic beads with matrix-assisted laser desorption ionization-time of flight mass spectrometry for detection of staphylococcal enterotoxin B. Appl. Environ. Microbiol. 73:6945-6952.
Seki M, Yamashita Y, Torigoe H, Tsuda H, Sato S, Maeno M. 2005. Loop-mediated isothermal amplification method targeting the lytA gene for detection of Streptococcus pneumoniae. J. Clin. Microbiol. 43: 1581-1586.
Seo KH, Brackett RE, Hartman NF, Campbell DP. 1999. Development of a rapid response biosensor for detection of Salmonella typhimurium. J. Food Prot. 62: 431-437.
Sharma H, Mutharasan R. 2013. Review of biosensors for foodborne pathogens and toxins. Sensors Actuat. B Chem. 183: 535-549.
Shi XM, Long F, Suo B. 2010. Molecular methods for the detection and characterization of foodborne pathogens. Pure Appl. Chem. 82: 69-79.
Si CY, Ye ZZ, Wang YX, Gai L, Wang JP, Ying YB. 2011. Rapid detection of Escherichia coli O157:H7 using surface plasmon resonance (SPR) biosensor. Spectrosc. Spectral Anal. 31: 2598-2601.
Simpkins SA, Chan AB, Hays J , Pop ping B, Cook N. 2 000. An RNA transcription-based amplification technique (NASBA) for the detection of viable Salmonella enterica. Lett. Appl. Microbiol. 30: 75-79.
Singh C, Agarwal GS, Rai GP, Singh L, Rao VK. 2005. Specific detection of Salmonella T yp hi u sing renewable amperometric immunosensor. Electroanalysis 17: 2062-2067.
Song TY, Toma C, Nakasone N, Iwanaga M. 2005. Sensitive and rapid detection of Shigella and enteroinvasive Escherichia coli by a loop-mediated isothermal amplification method. FEMS Microbiol. Lett. 243: 259-263.
Spangler BD, Wilkinson EA, Murphy JT, Tyler BJ. 2001. Comparison of the Spreeta (R) surface plasmon resonance sensor and a quartz crystal microbalance for detection of Escherichia coli heat-labile enterotoxin. Anal. Chim. Acta 444:149-161.
Stevens KA, Jaykus LA. 2004. Bacterial separation and concentration from complex sample matrices: a review. Crit. Rev. Microbiol. 30: 7-24.
Tokarskyy O, Marshall DL. 2008. Immunosensors for rapid detection of Escherichia coli O157 : H7-perspectives for use in the meat processing industry. Food Microbiol. 25: 1-12.
Tsaloglou MN, Bahi MM, Waugh EM, Morgan H, Mowlem M. 2011. On-chip real-time nucleic acid sequence-based amplification for RNA detection and amplification. Anal. Methods 3: 2127-2133.
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.
Vernozy-Rozand C, Mazuy-Cruchaudet C, Bavai C, Richard Y. 2004. Comparison of three immunological methods for detecting staphylococcal enterotoxins from food. Lett. Appl. Microbiol. 39: 490-494.
Verstraete K, Robyn J, Del-Favero J, De Rijk P, Joris MA, Herman L, et al. 2012. Evaluation of a multiplex-PCR detection in combination with an isolation method for STEC O26, O103, O111, O145 and sorbitol fermenting O157 in food. Food Microbiol. 29: 49-55.
Vo-Dinh T, Griffin G, Stokes DL, Wintenberg A. 2003. Multi-functional biochip for medical diagnostics and pathogen detection. Sensors Actuat B Chem. 90: 104-111.
Wang CH, Lien KY, Wu JJ, Lee GB. 2011. A magnetic bead-based assay for the rapid detection of methicillinresistant Staphylococcus aureus by using a microfluidic system with integrated loop-mediated isothermal amplification. Lab. Chip 11: 1521-1531.
Wang DG, Wang YZ, Wang JH, Zhang XW, Xiao FG. 2011. Rapid detection of viable Listeria monocytogenes in raw milk using loop-mediated isothermal amplification with the aid of ethidium monoazide. Milchwissenschaft Milk Sci. Int. 66: 426-429.
Wang LX, Li Y, Mustapha A. 2007. Rapid and simultaneous quantitation of Escherichia coli O157:H7, Salmonella, and Shigella in ground beef by multiplex realtime PCR and immunomagnetic separation. J. Food Prot. 70:1366-1372.
Wang YX, Ye ZZ, Si CY, Ying YB. 2011. Subtractive inhibition assay for the detection of E. coli O157:H7 using surface plasmon resonance. Sensors 11: 2728-2739.
Waswa J, Irudayaraj J, DebRoy C. 2007. Direct detection of E. coli O157:H7 in selected food systems by a surface plasmon resonance biosensor. LWT Food Sci. Technol. 40: 187-192.
Waswa JW, Debroy C, Irudayaraj J. 2006. Rapid detection of Salmonella enteritidis and Escherichia coli using surface plasmon resonance biosensor. J. Food Process Eng. 29: 373-385.
World Health Organization. 2007. Food safety and foodborne illness. [Online.] http://www.who.int/mediacentre/factsheets/fs237/en/
Wu VCH, Chen SH, Lin CS. 2007. Real-time detection of Escherichia coli O157:H7 sequences using a circulating-flow system of quartz crystal microbalance. Biosens. Bioelectron. 22: 2967-2975.
Yamazaki W, Ishibashi M, Kawahara R, Inoue K. 2008. Development of a loop-mediated isothermal amplification assay for sensitive and rapid detection of Vibrio parahaemolyticus. BMC Microbiol. 8.
Yamazaki W, Kumeda Y, Uemura R, Misawa N. 2011. Evaluation of a loop-mediated isothermal amplification assay for rapid and simple detection of Vibrio parahaemolyticus in naturally contaminated seafood samples. Food Microbiol. 28:1238-1241.
Yang H, Ma XY, Zhang XZ, Wang Y, Zhang W. 2011. Development and evaluation of a loop-mediated isothermal amplification assay for the rapid detection of Staphylococcus aureus in food. Eur. Food Res. Technol. 232: 769-776.
Yang L, Bashir R. 2008. Electrical/electrochemical impedance for rapid detection of foodborne pathogenic bacteria. Biotechnol. Adv. 26: 135-150.
Ye YX, Wang B, Huang F, Song YS, Yan H, Alam MJ, et al. 2011. Application of in situ loop-mediated isothermal amplification method for detection of Salmonella in foods. Food Control 22: 438-444.
Yoo JH, Choi SM, Choi JH, Kwon EY, Park C, Shin WS. 2008. Construction of internal control for the quantitative assay of Aspergillus fumigatus using real-time nucleic acid sequence-based amplification. Diagn. Microbiol. Infect. Dis. 60: 121-124.
Zhao XH, Li YM, Wang L, You LJ, Xu ZB, Li L, et al. 2010. Development and application of a loop-mediated isothermal amplification method on rapid detection Escherichia coli O157 strains from food samples. Mol. Biol. Rep. 37: 21832188.
Zhao XH, Wang L, Chu J, Li YY, Li YM, Xu ZB, et al. 2010. Development and application of a rapid and simple loopmediated isothermal amplification method for food-borne Salmonella detection. Food Sci. Biotechnol. 19: 1655-1659.
Zhao XH, Wang L, Chu J, Li YY, Li YM, Xu ZB, et al. 2010. Rapid detection of Vibrio parahaemolyticus strains and virulent factors by loop-mediated isothermal amplification assays. Food Sci. Biotechnol. 19: 1191-1197.
Zhao XH, Wang L, Li YM, Xu ZB, Li L, He XW, et al. 2011. Development and application of a loop-mediated isothermal amplification method on rapid detection of Pseudomonas aeruginosa strains. World J. Microbiol. Biotechnol. 27: 181-184.

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Article

Review

J. Microbiol. Biotechnol. 2014; 24(3): 297-312

Published online March 28, 2014 https://doi.org/10.4014/jmb.1310.10013

Advances in Rapid Detection Methods for Foodborne Pathogens

Xihong Zhao ^{1, 2, 3}, Chii-Wann Lin ³, Jun Wang ² and Deog Hwan Oh ^2*

¹Key Laboratory for Green Chemical Process of Ministry of Education, School of Chemical Engineering and Pharmacy, Wuhan Institute of Technology, Wuhan 430073, China, ²Department of Food Science and Biotechnology and Institute of Bioscience and Biotechnology, Kangwon National University, Chuncheon 200701, Republic of Korea, ³Institute of Biomedical Engineering, National Taiwan University, Taipei 10617, Taiwan

Received: October 7, 2013; Accepted: December 22, 2013

Abstract

Food safety is increasingly becoming an important public health issue, as foodborne diseases
present a widespread and growing public health problem in both developed and developing
countries. The rapid and precise monitoring and detection of foodborne pathogens are some of
the most effective ways to control and prevent human foodborne infections. Traditional
microbiological detection and identification methods for foodborne pathogens are well known
to be time consuming and laborious as they are increasingly being perceived as insufficient to
meet the demands of rapid food testing. Recently, various kinds of rapid detection,
identification, and monitoring methods have been developed for foodborne pathogens,
including nucleic-acid-based methods, immunological methods, and biosensor-based
methods, etc. This article reviews the principles, characteristics, and applications of recent
rapid detection methods for foodborne pathogens.

Keywords: foodborne pathogen, rapid detection, nucleic acid based methods, immunological methods, biosensor based methods

Abstract

References

Abbas A, Linman MJ, Cheng QA. 2011. New trends in instrumental design for surface plasmon resonance-based biosensors. Biosens. Bioelectron. 26: 1815-1824.
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.
Asiello PJ, Baeumner AJ. 2011. Miniaturized isothermal nucleic acid amplification, a review. Lab. Chip 11: 14201430.
Baeumner AJ, Cohen RN, Miksic V, Min J. 2003. RNA biosensor for the rapid detection of viable Escherichia coli in drinking water. Biosens. Bioelectron. 18: 405-413.
Bolton FJ, Fritz E, Poynton S, Jensen T. 2000. Rapid enzyme-linked immunoassay for detection of Salmonella in food and feed products: performance testing program. J. AOAC Int. 83: 299-303.
Campbell GA, Mutharasan R. 2006. Piezoelectric-excited millimeter-sized cantilever (PEMC) sensors detect Bacillus anthracis at 300 spores/ml. Biosens. Bioelectron. 21: 16841692.
Cao W, S u M, Z hang S . 2010. Rap id and s ensitive DNA target detection using enzyme amplified electrochemical detection based on microchip. Electrophoresis 31: 659-665.
CDC 2011. CDC Estimates of Foodborne Illness in the United States. [Online.] http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html
Chamberlain JS, Gibbs RA, Ranier JE, Nguyen PN, Caskey CT. 1988. Deletion screening of the Duchenne muscular dystrophy locus via multiplex DNA amplification. Nucleic Acids Res. 16: 11141-11156.
Chen HM, Lin CW. 2007. Hydrogel-coated streptavidin piezoelectric biosensors and applications to selective detection of Strep-Tag displaying cells. Biotechnol. Prog. 23: 741-748.
Chen HT, Zhang J, Sun DH, Ma LN, Liu XT, Cai XP, Liu YS. 2008. Development of reverse transcription loopmediated isothermal amplification for rapid detection of H9 avian influenza virus. J. Virol. Methods 151: 200-203.
Chen J, Ma XY, Yuan YW, Zhang W. 2011. Sensitive and rapid detection of Alicyclobacillus acidoterrestris u sing loop mediated isothermal amplification. J. Sci. Food Agric. 91:1070-1074.
Chen SY, Wang F, Beaulieu JC, Stein RE, Ge BL. 2011. Rapid detection of viable salmonellae in produce by coupling propidium monoazide with loop-mediated isothermal amplification. Appl. Environ. Microbiol. 77: 4008-4016.
Chen ZG. 2008. Conductometric immunosensors for the detection of staphylococcal enterotoxin B based bioelectrocalytic reaction on micro-comb electrodes. Bioproc. Biosyst. Eng. 31: 345-350.
Chuang TL, Wei SC, Lee SY, Lin CW. 2012. A polycarbonate based surface plasmon resonance sensing cartridge for high sensitivity HBV loop-mediated isothermal amplification. Biosens. Bioelectron. 32: 89-95.
Churruca E, Girbau C, Martinez I, Mateo E, Alonso R, Fernandez-Astorga A. 2007. Detection of Campylobacter jejuni and Campylobacter coli in chicken meat samples by real-time nucleic acid sequence-based amplification with molecular beacons. Int. J. Food Microbiol. 117: 85-90.
Compton J. 1991. Nucleic acid sequence-based amplification. Nature 350: 91-92.
de Boer E, Beumer RR. 1999. Methodology for detection and typing of foodborne microorganisms. Int. J. Food Microbiol. 50: 119-130.
DeCory TR, Durst RA, Zimmerman SJ, Garringer LA, Paluca G, DeCory HH, Montagna RA. 2005. Development of an immunomagnetic bead-immunoliposome fluorescence assay for rapid detection of Escherichia coli O157:H7 in aqueous samples and comparison of the assay with a standard microbiological method. Appl. Environ. Microbiol. 71: 1856-1864.
Delmulle BS, De Saeger SM, Sibanda L, Barna-Vetro I, Van Peteghem CH. 2005. Development of an immunoassaybased lateral flow dipstick for the rapid detection of aflatoxin B1 in pig feed. J. Agric. Food Chem. 53: 3364-3368.
Derzelle S, Grine A, Madic J, de Garam CP, Vingadassalon N, Dilasser F, et al. 2011. A quantitative PCR assay for the detection and quantification of Shiga toxin-producing Escherichia coli (STEC) in minced beef and dairy products. Int. J. Food Microbiol. 151: 44-51.
Dey D, Goswami T. 2011. Optical Biosensors: A revolution towards quantum nanoscale electronics device fabrication. J. Biomed. Biotechnol. 2011: 348218.
Dongyou L. 2010. Molecular Detection of Foodborne Pathogens. CRC Press, Boca Raton.
Dwivedi HP, Jaykus LA. 2011. Detection of pathogens in foods: the current state-of-the-art and future directions. Crit. Rev. Microbiol. 37: 40-63.
Feng P. 1997. Impact of molecular biology on the detection of foodborne pathogens. Mol. Biotechnol. 7: 267-278.
Foley SL, Grant K. 2007. Molecular techniques of detection and discrimination of foodborne pathogens and their toxins, p. 485-510. In Simjee S (ed.). Infectious Disease: Foodborne Diseases. Humana Press Inc, Totowa, NJ.
Fusco V, Quero GM, Morea M, Blaiotta G, Visconti A. 2011. Rapid and reliable identification of Staphylococcus aureus harbouring the enterotoxin gene cluster (egc) and quantitative detection in raw milk by real time PCR. Int. J. Food Microbiol. 144: 528-537.
Fykse EM, Skogan G, Davies W, Olsen JS, Blatny JM. 2007. Detection of Vibrio cholerae by real-time nucleic acid sequence-based amplification. Appl. Environ. Microbiol. 73:1457-1466.
Gill P, Ghaemi A. 2008. Nucleic acid isothermal amplification technologies: a review. Nucleosides Nucleotides Nucleic Acids 27: 224-243.
Gill P, Ramezani R, Amiri MVP, Ghaemi A, Hashempour T, Eshraghi N, et al. 2006. Enzyme-linked immunosorbent assay of nucleic acid sequence-based amplification for molecular detection of M-tuberculosis. Biochem. Biophys. Res. Commun. 347: 1151-1157.
Gizeli E, Lowe CR. 1996. Immunosensors. Curr. Opin. Biotechnol. 7: 66-71.
Gomez P, Pagnon M, Egea-Cortines M, Artes F, Weiss J. 2010. A fast molecular nondestructive protocol for evaluating aerobic bacterial load on fresh-cut lettuce. Food Sci. Technol. Int. 16: 409-415.
Grothaus GD, Bandla M, Currier T, Giroux R, Jenkins GR, Lipp M, et al. 2006. Immunoassay as an analytical tool in agricultural biotechnology. J. AOAC Int. 89: 913-928.
Guatelli JC, Whitfield KM, Kwoh DY, Barringer KJ, Richman DD, Gingeras TR. 1990. Isothermal, in vitro amplification of nucleic acids by a multienzyme reaction modeled after retroviral replication. Proc. Natl. Acad. Sci. USA 87: 7797.
Hahm BK, Bhunia AK. 2006. Effect of environmental stresses on antibody-based detection of Escherichia coli O157:H7, Salmonella enterica serotype Enteritidis and Listeria monocytogenes. J. Appl. Microbiol. 100: 1017-1027.
Hahn MA, Keng PC, Krauss TD. 2008. Flow cytometric analysis to detect pathogens in bacterial cell mixtures using semiconductor quantum dots. Anal. Chem. 80: 864872.
Hill WE. 1996. The polymerase chain reaction: applications for the detection of foodborne pathogens. Crit. Rev. Food Sci. Nutr. 36: 123-173.
Ikeda S, Takabe K, Inagaki M, Funakoshi N, Suzuki K. 2007. Detection of gene point mutation in paraffin sections using in situ loop-mediated isothermal amplification. Pathol. Int. 57: 594-599.
Iseki H, Alhassan A, Ohta N, Thekisoe OMM, Yokoyama N, Inoue N, et al. 2007. Development of a multiplex loopmediated isothermal amplification (mLAMP) method for the simultaneous detection of bovine Babesia p arasites. J. Microbiol. Methods 71: 281-287.
Jasson V, Jacxsens L, Luning P, Rajkovic A, Uyttendaele M. 2010. Alternative microbial methods: an overview and selection criteria. Food Microbiol. 27: 710-730.
Jung BY, Jung S C, K weon C H. 2 005. D evelop ment o f a rapid immunochromatographic strip for detection of Escherichia coli O157. J. Food Prot. 68: 2140-2143.
Kawasaki S, Fratamico PM, Horikoshi N, Okada Y, Takeshita K, Sameshima T, Kawamoto S. 2009. Evaluation of a multiplex PCR system for simultaneous detection of Salmonella spp., listeria monocytogenes, and Escherichia coli O157:H7 in foods and in food subjected to freezing. Foodborne Pathog. Dis. 6: 81-89.
Kawasaki S, Horikoshi N, Okada Y, Takeshita K, Sameshima T, Kawamoto S. 2005. Multiplex PCR for simultaneous detection of Salmonella spp., Listeria monocytogenes, and Escherichia coli O 157:H7 i n meat s amp les. J. Food Prot. 68:551-556.
Kim HJ, Lee HJ, Lee KH, Cho JC. 2012. Simultaneous detection of pathogenic Vibrio species using multiplex realtime PCR. Food Control 23: 491-498.
Kong RY, Lee SK, Law TW, Law SH, Wu RS. 2002. Rapid detection of six types of bacterial pathogens in marine waters by multiplex PCR. Water Res. 36: 2802-2812.
Lan YB, Wang SZ, Yin YG, Hoffmann WC, Zheng XZ. 2008. Using a surface plasmon resonance biosensor for rapid detection of Salmonella Typhimurium in chicken carcass. J. Bionic Eng. 5: 239-246.
Laura A, Gilda D, Claudio B, Cristina G, Gianfranco G. 2011. A lateral flow immunoassay for measuring ochratoxin A: development of a single system for maize, wheat and durum wheat. Food Control 22: 1965-1970.
Lazcka O, Del Campo FJ, Munoz FX. 2007. Pathogen detection: A perspective of traditional methods and biosensors. Biosens. Bioelectron. 22: 1205-1217.
Lee JY, Deininger RA. 2004. Detection of E. coli in beach water within 1 hour using immunomagnetic separation and ATP bioluminescence. Luminescence 19: 31-36.
Leonard P, Hearty S, Brennan J, Dunne L, Quinn J, Chakraborty T, O’Kennedy R. 2003. Advances in biosensors for detection of pathogens in food and water. Enzyme Microb. Technol. 32: 3-13.
Li Y, Cheng P, Gong JH, Fang LC, Deng J, Liang WB, Zheng JS. 2012. Amperometric immunosensor for the detection of Escherichia coli O157:H7 in food specimens. Anal. Biochem. 421: 227-233.
Li Y, Mustapha A. 2004. Simultaneous detection of Escherichia coli O157:H7, Salmonella, and Shigella in apple cider and produce by a multiplex PCR. J. Food Prot. 67: 2733.
Lin WS, Cheng CM, Van KT. 2010. A quantitative PCR assay for rapid detection of Shigella species in fresh produce. J. Food Prot. 73: 221-233.
Lin YH, Chen SH, Chuang YC, Lu YC, Shen TY, Chang CA, Lin CS. 2008. Disposable amperometric immunosensing strips fabricated by Au nanoparticles-modified screenprinted carbon electrodes for the detection of foodborne pathogen Escherichia coli O157:H7. Biosens Bioelectron. 23:1832-1837.
Liu Y, Chuang CK, Chen WJ. 2009. In situ reversetranscription loop-mediated isothermal amplification (in situ RT-LAMP) for detection of Japanese encephalitis viral RNA in host cells. J. Clin. Virol. 46: 49-54.
Loens K, Beck T, Goossens H, Ursi D, Overdijk M, Sillekens P, Ieven M. 2006. Development of conventional and real-time nucleic acid sequence-based amplification assays for detection of Chlamydophila pneumoniae in respiratory specimens. J. Clin. Microbiol. 44: 1241-1244.
Louie AS, Marenchic IG, Whelan RH. 1998. A fieldable modular biosensor for use in detection of foodborne pathogens. Field Anal. Chem. Technol. 2: 371-377.
Luo XL, Xu JJ, Zhao W, Chen HY. 2004. Glucose biosensor based on E NFET d op ed w ith SiO2 nanoparticles. Sensors Actuat B Chem. 97: 249-255.
Magliulo M, Simoni P, Guardigli M, Michelini E, Luciani M, Lelli R, Roda A. 2007. A rapid multiplexed chemiluminescent immunoassay for the detection of Escherichia coli O157:H7, Yersinia enterocolitica, Salmonella typhimurium, and Listeria monocytogenes pathogen bacteria. J. A g ric. F ood C hem. 55:4933-4939.
Mandal PK, Biswas AK, Choi K, Pal U. 2011. Methods for rapid detection of foodborne pathogens: an overview. Am. J. Food Technol. 6: 87-102.
Martinon A, Wilkinson MG. 2011. Selection of optimal primer sets for use in a duplex sybr green-based, real-time polymerase chain reaction protocol for the detection of listeria monocytogenes and staphyloccocus aureus in foods. J. Food Saf. 31: 297-312.
Maruyama F, Kenzaka T, Yamaguchi N, Tani K, Nasu M. 2003. Detection of bacteria carrying the stx2 gene by in situ loop-mediated isothermal amplification. Appl. Environ. Microbiol. 69: 5023-5028.
McEgan R, Fu TJ, Warriner K. 2009. Concentration and detection of Salmonella in mung bean sprout spent irrigation water by use of tangential flow filtration coupled with an amperometric flowthrough enzyme-linked immunosorbent assay. J. Food Prot. 72: 591-600.
Meeusen CA, Alocilja EC, Osburn WN. 2005. Detection of E. coli O157:H7 using a miniaturized surface plasmon resonance biosensor. Trans. ASAE 48: 2409-2416.
Min J, Baeumner AJ. 2002. Highly sensitive and specific detection of viable Escherichia coli in drinking water. Anal. Biochem. 303: 186-193.
Mukhopadhyay A, Mukhopadhyay UK. 2007. Novel multiplex PCR approaches for the simultaneous detection of human pathogens: Escherichia coli O157:H7 and Listeria monocytogenes. J. Microbiol. Methods 68: 193-200.
Muldoon MT, Teaney G, Li J, Onisk DV, Stave JW. 2007. Bacteriophage-based enrichment coupled to immunochromatographic strip-based detection for the determination of Salmonella in meat and poultry. J. Food Prot. 70: 2235-2242.
Nam HM, Srinivasan V, Gillespie BE, Murinda SE, Oliver SP. 2005. Application of SYBR green real-time PCR assay for specific detection of Salmonella s p p .in d airy f arm environmental samples. Int. J. Food Microbiol. 102: 161-171.
Nemoto J, Ikedo M, Kojima T, Momoda T, Konuma H, Hara-Kudo Y. 2011. Development and evaluation of a loop-mediated isothermal amplification assay for rapid and sensitive detection of Vibrio parahaemolyticus. J. Food Prot. 74: 1462-1467.
Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T. 2000. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. 28:E63.
Ohtsuka K, Tanaka M, Ohtsuka T, Takatori K, Hara-Kudo Y. 2010. Comparison of detection methods for Escherichia coli O157 in beef livers and carcasses. Foodborne Pathog. Dis. 7: 1563-1567.
Oliver SP, Jayarao BM, Almeida RA. 2005. Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog. Dis. 2: 115-129.
Ong KG, Zeng KF, Yang XP, Shankar K, Ruan CM, Grimes CA. 2006. Quantification of multiple bioagents with wireless, remote-query magnetoelastic microsensors. IEEE Sensors J. 6: 514-523.
Pal S, Ying W, Alocilja EC, Downes FP. 2008. Sensitivity and specificity performance of a direct-charge transfer biosensor for detecting Bacillus cereus in selected food matrices Biosys Eng. 99: 461-468.
Park YS, Lee SR, Kim YG. 2006. Detection of Escherichia coli O157:H7, Salmonella spp., Staphylococcus aureus and Listeria monocytogenes in kimchi by multiplex polymerase chain reaction (mPCR). J. Microbiol. 44: 92-97.
Pedrero M, Campuzano S, Pingarron JM. 2009. Electroanalytical sensors and devices for multiplexed detection of foodborne pathogen microorganisms. Sensors 9: 5503-5520.
Planche T, Aghaizu A, Holliman R, Riley P, Poloniecki J, Breathnach A, Krishna S. 2008. Diagnosis of Clostridium difficile infection by toxin detection kits: a systematic review. Lancet Infect. Dis. 8: 777-784.
Posthuma-Trump ie GA, K orf J, v an Amerongen A . 2009. Lateral flow (immuno) assay: its strengths, weaknesses, opportunities and threats. A literature survey. Anal. Bioanal. Chem. 393: 569-582.
Qiao YM, Guo YC, Zhang XE, Zhou YF, Zhang ZP, Wei HP, et al. 2007. Loop-mediated isothermal amplification for rapid detection of Bacillus anthracis spores. Biotechnol. Lett. 29: 1939-1946.
Rahman S, Lipert RJ, Porter MD. 2006. Rapid screening of pathogenic bacteria using solid phase concentration and diffuse reflectance spectroscopy. Anal. Chim. Acta 569: 8390.
Rao VK, Rai GP, Agarwal GS, Suresh S. 2005. Amperometric immunosensor for detection of antibodies of Salmonella Typhi in patient serum. Anal. Chim. Acta 531: 173-177.
Rasooly A, Herold KE. 2006. Biosensors for the analysis of food- and waterborne pathogens and their toxins. J. AOAC Int. 89: 873-883.
Rodriguez-Lazaro D, Jofre A, Aymerich T, Hugas M, Pla M. 2004. Rapid quantitative detection of Listeria monocytogenes in meat products by real-time PCR. Appl. Environ. Microbiol. 70: 6299-6301.
Rosebrough SF, Hartley DF. 1996. Biochemical modification of streptavidin and avidin: in vitro and in vivo analysis. J. Nucl. Med. 37: 1380-1384.
Salmain M, Ghasemi M, Boujday S, Spadavecchia J, Techer C, Val F, et al. 2011. Piezoelectric immunosensor for direct and rapid detection of staphylococcal enterotoxin A (SEA) at the ng level. Biosens. Bioelectron. 29: 140-144.
Sankaran S, Panigrahi S, Mallik S. 2011. Olfactory receptor based piezoelectric biosensors for detection of alcohols related to food safety applications. Sensors Actuat B Chem. 155: 8-18.
Schlosser G, Kacer P, Kuzma M, Szilagyi Z, Sorrentino A, Manzo C, et al. 2007. Coupling immunomagnetic separation on magnetic beads with matrix-assisted laser desorption ionization-time of flight mass spectrometry for detection of staphylococcal enterotoxin B. Appl. Environ. Microbiol. 73:6945-6952.
Seki M, Yamashita Y, Torigoe H, Tsuda H, Sato S, Maeno M. 2005. Loop-mediated isothermal amplification method targeting the lytA gene for detection of Streptococcus pneumoniae. J. Clin. Microbiol. 43: 1581-1586.
Seo KH, Brackett RE, Hartman NF, Campbell DP. 1999. Development of a rapid response biosensor for detection of Salmonella typhimurium. J. Food Prot. 62: 431-437.
Sharma H, Mutharasan R. 2013. Review of biosensors for foodborne pathogens and toxins. Sensors Actuat. B Chem. 183: 535-549.
Shi XM, Long F, Suo B. 2010. Molecular methods for the detection and characterization of foodborne pathogens. Pure Appl. Chem. 82: 69-79.
Si CY, Ye ZZ, Wang YX, Gai L, Wang JP, Ying YB. 2011. Rapid detection of Escherichia coli O157:H7 using surface plasmon resonance (SPR) biosensor. Spectrosc. Spectral Anal. 31: 2598-2601.
Simpkins SA, Chan AB, Hays J , Pop ping B, Cook N. 2 000. An RNA transcription-based amplification technique (NASBA) for the detection of viable Salmonella enterica. Lett. Appl. Microbiol. 30: 75-79.
Singh C, Agarwal GS, Rai GP, Singh L, Rao VK. 2005. Specific detection of Salmonella T yp hi u sing renewable amperometric immunosensor. Electroanalysis 17: 2062-2067.
Song TY, Toma C, Nakasone N, Iwanaga M. 2005. Sensitive and rapid detection of Shigella and enteroinvasive Escherichia coli by a loop-mediated isothermal amplification method. FEMS Microbiol. Lett. 243: 259-263.
Spangler BD, Wilkinson EA, Murphy JT, Tyler BJ. 2001. Comparison of the Spreeta (R) surface plasmon resonance sensor and a quartz crystal microbalance for detection of Escherichia coli heat-labile enterotoxin. Anal. Chim. Acta 444:149-161.
Stevens KA, Jaykus LA. 2004. Bacterial separation and concentration from complex sample matrices: a review. Crit. Rev. Microbiol. 30: 7-24.
Tokarskyy O, Marshall DL. 2008. Immunosensors for rapid detection of Escherichia coli O157 : H7-perspectives for use in the meat processing industry. Food Microbiol. 25: 1-12.
Tsaloglou MN, Bahi MM, Waugh EM, Morgan H, Mowlem M. 2011. On-chip real-time nucleic acid sequence-based amplification for RNA detection and amplification. Anal. Methods 3: 2127-2133.
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.
Vernozy-Rozand C, Mazuy-Cruchaudet C, Bavai C, Richard Y. 2004. Comparison of three immunological methods for detecting staphylococcal enterotoxins from food. Lett. Appl. Microbiol. 39: 490-494.
Verstraete K, Robyn J, Del-Favero J, De Rijk P, Joris MA, Herman L, et al. 2012. Evaluation of a multiplex-PCR detection in combination with an isolation method for STEC O26, O103, O111, O145 and sorbitol fermenting O157 in food. Food Microbiol. 29: 49-55.
Vo-Dinh T, Griffin G, Stokes DL, Wintenberg A. 2003. Multi-functional biochip for medical diagnostics and pathogen detection. Sensors Actuat B Chem. 90: 104-111.
Wang CH, Lien KY, Wu JJ, Lee GB. 2011. A magnetic bead-based assay for the rapid detection of methicillinresistant Staphylococcus aureus by using a microfluidic system with integrated loop-mediated isothermal amplification. Lab. Chip 11: 1521-1531.
Wang DG, Wang YZ, Wang JH, Zhang XW, Xiao FG. 2011. Rapid detection of viable Listeria monocytogenes in raw milk using loop-mediated isothermal amplification with the aid of ethidium monoazide. Milchwissenschaft Milk Sci. Int. 66: 426-429.
Wang LX, Li Y, Mustapha A. 2007. Rapid and simultaneous quantitation of Escherichia coli O157:H7, Salmonella, and Shigella in ground beef by multiplex realtime PCR and immunomagnetic separation. J. Food Prot. 70:1366-1372.
Wang YX, Ye ZZ, Si CY, Ying YB. 2011. Subtractive inhibition assay for the detection of E. coli O157:H7 using surface plasmon resonance. Sensors 11: 2728-2739.
Waswa J, Irudayaraj J, DebRoy C. 2007. Direct detection of E. coli O157:H7 in selected food systems by a surface plasmon resonance biosensor. LWT Food Sci. Technol. 40: 187-192.
Waswa JW, Debroy C, Irudayaraj J. 2006. Rapid detection of Salmonella enteritidis and Escherichia coli using surface plasmon resonance biosensor. J. Food Process Eng. 29: 373-385.
World Health Organization. 2007. Food safety and foodborne illness. [Online.] http://www.who.int/mediacentre/factsheets/fs237/en/
Wu VCH, Chen SH, Lin CS. 2007. Real-time detection of Escherichia coli O157:H7 sequences using a circulating-flow system of quartz crystal microbalance. Biosens. Bioelectron. 22: 2967-2975.
Yamazaki W, Ishibashi M, Kawahara R, Inoue K. 2008. Development of a loop-mediated isothermal amplification assay for sensitive and rapid detection of Vibrio parahaemolyticus. BMC Microbiol. 8.
Yamazaki W, Kumeda Y, Uemura R, Misawa N. 2011. Evaluation of a loop-mediated isothermal amplification assay for rapid and simple detection of Vibrio parahaemolyticus in naturally contaminated seafood samples. Food Microbiol. 28:1238-1241.
Yang H, Ma XY, Zhang XZ, Wang Y, Zhang W. 2011. Development and evaluation of a loop-mediated isothermal amplification assay for the rapid detection of Staphylococcus aureus in food. Eur. Food Res. Technol. 232: 769-776.
Yang L, Bashir R. 2008. Electrical/electrochemical impedance for rapid detection of foodborne pathogenic bacteria. Biotechnol. Adv. 26: 135-150.
Ye YX, Wang B, Huang F, Song YS, Yan H, Alam MJ, et al. 2011. Application of in situ loop-mediated isothermal amplification method for detection of Salmonella in foods. Food Control 22: 438-444.
Yoo JH, Choi SM, Choi JH, Kwon EY, Park C, Shin WS. 2008. Construction of internal control for the quantitative assay of Aspergillus fumigatus using real-time nucleic acid sequence-based amplification. Diagn. Microbiol. Infect. Dis. 60: 121-124.
Zhao XH, Li YM, Wang L, You LJ, Xu ZB, Li L, et al. 2010. Development and application of a loop-mediated isothermal amplification method on rapid detection Escherichia coli O157 strains from food samples. Mol. Biol. Rep. 37: 21832188.
Zhao XH, Wang L, Chu J, Li YY, Li YM, Xu ZB, et al. 2010. Development and application of a rapid and simple loopmediated isothermal amplification method for food-borne Salmonella detection. Food Sci. Biotechnol. 19: 1655-1659.
Zhao XH, Wang L, Chu J, Li YY, Li YM, Xu ZB, et al. 2010. Rapid detection of Vibrio parahaemolyticus strains and virulent factors by loop-mediated isothermal amplification assays. Food Sci. Biotechnol. 19: 1191-1197.
Zhao XH, Wang L, Li YM, Xu ZB, Li L, He XW, et al. 2011. Development and application of a loop-mediated isothermal amplification method on rapid detection of Pseudomonas aeruginosa strains. World J. Microbiol. Biotechnol. 27: 181-184.