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Immuno- and nucleic acid-based current technique for Salmonella detection in food

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Abstract

Salmonella is a major cause of foodborne illness throughout the world and has resulted in a serious of public health issues over the past decades. The conventional culture methods for Salmonella detection are laborious and time-consuming; thus a variety of new methods have been developed to enable rapid detection. Among them, immuno- and nucleic acid-based methods are fast developing because the advancing of molecular science provides more target antibodies and genes for Salmonella detection. These new targets might enable a lower detection limit and higher sensitivity/specificity and, therefore shorten the detection period while ensuring the detection accuracy. This review emphasizes the effect of current immuno- and nucleic acid-based techniques for Salmonella detection. The target antibodies and target genes identified and applied during the latest research are also listed out as a reference. Besides, the main features of various immune- and nucleic acid-based techniques used for Salmonella detection in food are also summarized and compared. This review would provide the in-time and comprehensive guidance to achieve rapid and accurate detection of foodborne Salmonella.

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Abbreviations

16S-seq:

16S rRNA gene amplicon sequencing

BPW:

Buffered peptone water

CDC:

Centers for Disease Control and Prevention

CFU:

Colony forming unit

EFSA:

European Food Safety Authority

ELISA:

Enzyme-linked immunosorbent assay

EMA:

Ethidium monoazide

EU:

European Union

FDA:

Food and Drug Administration

IMS:

Immuneomagnetic separation

ISO:

International Organization of Standardization

LAMP:

Loop-mediated isothermal amplification

LB:

Lactose broth

LFIA:

Lateral flow immunoassays

LOD:

Limit of detection

mPCR:

Multiplex polymerase chain reaction

NASBA:

Nucleic acid sequence-based amplification

NGS:

Next generation sequencing

PCR:

Polymerase chain reaction

PMA:

Propidium monoazide

qPCR:

Quantitative PCR

RASFF:

Rapid Alert System for Food and Feed

RNA-seq:

RNA sequencing

RPA:

Recombinase polymerase amplification

UK:

United Kingdom

USA:

United States of America

USDA:

United States Department of Agriculture

VBNC:

Viable but not culturable

WHO:

World Health Organization

WGS:

Whole genome sequencing

References

  1. World Health Organization (2015) WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007–2015. https://apps.who.int/iris/bitstream/handle/10665/199350/9789241565165_eng.pdf. Accessed 25 Apr 2019

  2. World Health Organization (2018) Salmonella (non-typhoidal). https://www.who.int/en/news-room/fact-sheets/detail/Salmonella-(non-typhoidal). Accessed 25 Apr 2019

  3. Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM (2011) Global monitoring of Salmonella serovar distribution from the World Health Organization global foodborne infections network country data bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8(8):887–900. https://doi.org/10.1089/fpd.2010.0787

    Article  PubMed  Google Scholar 

  4. Centers for Disease Control and Prevention (2014) National enteric disease surveillance: Salmonella surveillance overview. https://www.cdc.gov/nationalsurveillance/pdfs/NationalSalmSurveillOverview_508.pdf. Accessed 25 Apr 2019

  5. Centers for Disease Control and Prevention (2017) Making food safer to eat. https://www.cdc.gov/vitalsigns/FoodSafety/index.html. Accessed 25 Apr 2019

  6. United States Department of Agriculture (2017) Cost of foodborne illness estimates for Salmonella (non-typhoidal). https://ers.usda.gov/data-products/cost-estimates-of-foodborne-illnesses.aspx. Accessed 25 Apr 2019

  7. United States Food and Drug Administration (2018) Bacteriological analytical manual (BAM) chapter 5: Salmonella. https://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070149.htm. Accessed 25 Apr 2019

  8. International Organization for Standardization (2017) Microbiology of the food chain—horizontal method for the detection, enumeration and serotyping of Salmonella—part 1: detection of Salmonella spp., vol ISO 6579-1:2017. Geneva, Switzerland. https://www.iso.org/standard/56712.html. Accessed 25 Apr 2019

  9. Lai W (2015) Novel strategies to enhance lateral flow immunoassay sensitivity for detecting foodborne pathogens. J Agric Food Chem 63(3):745–753. https://doi.org/10.1021/jf5046415

    Article  CAS  PubMed  Google Scholar 

  10. Zheng Q, Mikå-Krajnik M, Yang Y, Lee SM, Lee SC, Yuk HG (2016) Evaluation of real-time PCR coupled with immunomagnetic separation or centrifugation for the detection of healthy and sanitizer-injured Salmonella spp. on mung bean sprouts. Int J Food Microbiol 222:48–55. https://doi.org/10.1016/j.ijfoodmicro.2016.01.013

    Article  CAS  PubMed  Google Scholar 

  11. Rapid Alert System for Food and Feed (2019) The rapid alert system for food and feed (RASFF) portal. https://webgate.ec.europa.eu/rasff-window/portal/. Accessed 25 Apr 2019

  12. Centers for Disease Control and Prevention (2019) Reports of selected Salmonella outbreak investigations. https://www.cdc.gov/Salmonella/outbreaks.html. Accessed 25 Apr 2019

  13. European Food Safety Authority (2018) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J 16(12):1–262. https://doi.org/10.2903/j.efsa.2018.5500

    Article  CAS  Google Scholar 

  14. European Food Safety Authority (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 15(12):1–228. https://doi.org/10.2903/j.efsa.2017.5077

    Article  CAS  Google Scholar 

  15. Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D'Angelo M, Hurd S, Medus C, Cronquist A, Angulo FJ (2008) Salmonellosis outcomes differ substantially by serotype. J Infect Dis 198(1):109–114. https://doi.org/10.1086/588823

    Article  PubMed  Google Scholar 

  16. Park SH, Aydin M, Khatiwara A, Dolan MC, Gilmore DF, Bouldin JL, Ahn S, Ricke SC (2014) Current and emerging technologies for rapid detection and characterization of Salmonella in poultry and poultry products. Food Microbiol 38:250–262. https://doi.org/10.1016/j.fm.2013.10.002

    Article  CAS  PubMed  Google Scholar 

  17. Lee K-M, Runyon M, Herrman TJ, Phillips R, Hsieh J (2015) Review of Salmonella detection and identification methods: aspects of rapid emergency response and food safety. Food Control 47:264–276. https://doi.org/10.1016/j.foodcont.2014.07.011

    Article  Google Scholar 

  18. Maciorowski KG, Herrera P, Jones FT, Pillai SD, Ricke SC (2006) Cultural and immunological detection methods for Salmonella spp. in animal feeds—a review. Vet Res Commun 30(2):127–137. https://doi.org/10.1007/s11259-006-3221-8

    Article  CAS  PubMed  Google Scholar 

  19. Shi C, Singh P, Ranieri ML, Wiedmann M, Moreno Switt AI (2015) Molecular methods for serovar determination of Salmonella. Crit Rev Microbiol 41(3):309–325. https://doi.org/10.3109/1040841X.2013.837862

    Article  PubMed  Google Scholar 

  20. Law JW, Ab Mutalib NS, Chan KG, Lee LH (2014) Rapid methods for the detection of foodborne bacterial pathogens: principles, applications, advantages and limitations. Front Microbiol 5:770. https://doi.org/10.3389/fmicb.2014.00770

    Article  PubMed  Google Scholar 

  21. Wang H, Gill VS, Cheng CM, Gonzalezescalona N, Irvin KA, Zheng J, Bell RL, Jacobson AP, Hammack TS (2015) Evaluation and comparison of rapid methods for the detection of Salmonella in naturally contaminated pine nuts using different pre enrichment media. Food Microbiol 46:58–65. https://doi.org/10.1016/j.fm.2014.06.028

    Article  CAS  PubMed  Google Scholar 

  22. Hyeon JY, Hwang IG, Kwak HS, Park JS, Heo S, Choi IS, Park CK, Seo KH (2009) Evaluation of an automated ELISA (VIDAS(R)) and real-time PCR by comparing with a conventional culture method for the detection of Salmonella spp. in steamed pork and raw broccoli sprouts. Korean J Food Sci Anim Resour 29(4):506–512. https://doi.org/10.5851/kosfa.2009.29.4.506

    Article  Google Scholar 

  23. Jain S, Chattopadhyay S, Jackeray R, Abid CK, Kohli GS, Singh H (2012) Highly sensitive detection of Salmonella typhi using surface aminated polycarbonate membrane enhanced-ELISA. Biosens Bioelectron 31(1):37–43. https://doi.org/10.1016/j.bios.2011.09.031

    Article  CAS  PubMed  Google Scholar 

  24. Tuchinda K, Naknam B, Sunthornandh P, Kittikul C, Lawhavinit O (2011) Detection of Salmonella in food samples by dot-ELISA using polyclonal antibody. Kasetsart J (Nat Sci) 45(3):444–450

    Google Scholar 

  25. Chunglok W, Wuragil DK, Oaew S, Somasundrum M, Surareungchai W (2011) Immunoassay based on carbon nanotubes-enhanced ELISA for Salmonella enterica serovar Typhimurium. Biosens Bioelectron 26(8):3584–3589. https://doi.org/10.1016/j.bios.2011.02.005

    Article  CAS  PubMed  Google Scholar 

  26. Uyttendaele M, Vanwildemeersch K, Debevere J (2003) Evaluation of real-time PCR vs automated ELISA and a conventional culture method using a semi-solid medium for detection of Salmonella. Lett Appl Microbiol 37(5):386–391. https://doi.org/10.1046/j.1472-765X.2003.01415.x

    Article  CAS  PubMed  Google Scholar 

  27. Kumar R, Surendran PK, Thampuran N (2007) Evaluation of culture, ELISA and PCR assays for the detection of Salmonella in seafood. Lett Appl Microbiol 46(2):221–226. https://doi.org/10.1111/j.1472-765X.2007.02286.x

    Article  CAS  PubMed  Google Scholar 

  28. Eriksson E, Aspan A (2007) Comparison of culture, ELISA and PCR techniques for Salmonella detection in faecal samples for cattle, pig and poultry. BMC Vet Res 3(1):21–21. https://doi.org/10.1186/1746-6148-3-21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zhao X, Lin CW, Wang J, Oh DH (2014) Advances in rapid detection methods for foodborne pathogens. J Microbiol Biotechnol 24(3):297–312. https://doi.org/10.4014/jmb.1310.10013

    Article  CAS  PubMed  Google Scholar 

  30. Eltzov E, Guttel S, Adarina LYK, Sinawang PD, Ionescu RE, Marks RS (2015) Lateral flow immunoassays—from paper strip to smartphone technology. Electroanal 27(9):2116–2130. https://doi.org/10.1002/elan.201500237

    Article  CAS  Google Scholar 

  31. Chun P (2009) Colloidal gold and other labels for lateral flow immunoassays. In: Wong R, Tse H (eds) Lateral flow immunoassay. Humana Press, New Jersey, pp 1–19. https://doi.org/10.1007/978-1-59745-240-3_5

    Chapter  Google Scholar 

  32. Shin JH, Hong J, Go H, Park J, Kong M, Ryu S, Kim K, Roh E, Park JK (2017) Multiplexed detection of foodborne pathogens from contaminated lettuces using a handheld multistep lateral flow assay device. J Agric Food Chem 66(1):290–297. https://doi.org/10.1021/acs.jafc.7b03582

    Article  CAS  PubMed  Google Scholar 

  33. Rohde A, Hammerl JA, Boone I, Jansen W, Fohler S, Klein G, Dieckmann R, Al Dahouk S (2017) Overview of validated alternative methods for the detection of foodborne bacterial pathogens. Trends Food Sci Technol 62:113–118. https://doi.org/10.1016/j.tifs.2017.02.006

    Article  CAS  Google Scholar 

  34. Feldpausch E, Le QN, Viator R, Li L, Foti D, Mozola M, Biswas P, Rice J, Alles S (2016) Validation of the Reveal® 2.0 Group D1 Salmonella test for detection of Salmonella Enteritidis in raw shell eggs and poultry-associated matrixes. J AOAC Int 99(4):1017–1024. https://doi.org/10.5740/jaoacint.16-0125

    Article  CAS  PubMed  Google Scholar 

  35. Melo AM, Alexandre DL, Furtado RF, Borges MF, Figueiredo EA, Biswas A, Cheng HN, Alves CR (2016) Electrochemical immunosensors for Salmonella detection in food. Appl Microbiol Biotechnol 100(12):5301–5312. https://doi.org/10.1007/s00253-016-7548-y

    Article  CAS  PubMed  Google Scholar 

  36. Arora P, Sindhu A, Dilbaghi N, Chaudhury A (2011) Biosensors as innovative tools for the detection of food borne pathogens. Biosens Bioelectron 28(1):1–12. https://doi.org/10.1016/j.bios.2011.06.002

    Article  CAS  PubMed  Google Scholar 

  37. 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(2):232–254. https://doi.org/10.1016/j.biotechadv.2009.12.004

    Article  CAS  PubMed  Google Scholar 

  38. Lazcka O, Del Campo FJ, Munoz FX (2007) Pathogen detection: a perspective of traditional methods and biosensors. Biosens Bioelectron 22(7):1205–1217. https://doi.org/10.1016/j.bios.2006.06.036

    Article  CAS  PubMed  Google Scholar 

  39. Farka Z, Juřík T, Pastucha M, Skládal P (2016) Enzymatic precipitation enhanced surface plasmon resonance immunosensor for the detection of Salmonella in powdered milk. Anal Chem 88(23):11830–11836. https://doi.org/10.1021/acs.analchem.6b03511

    Article  CAS  PubMed  Google Scholar 

  40. Kim G, Moon JH, Moh CY, Lim JG (2015) A microfluidic nano-biosensor for the detection of pathogenic Salmonella. Biosens Bioelectron 67:243–247. https://doi.org/10.1016/j.bios.2014.08.023

    Article  CAS  PubMed  Google Scholar 

  41. Lu D, Pang G, Xie J (2017) A new phosphothreonine lyase electrochemical immunosensor for detecting Salmonella based on horseradish peroxidase/GNPs-thionine/chitosan. Biomed Microdevices 19(1):12. https://doi.org/10.1007/s10544-017-0149-4

    Article  CAS  PubMed  Google Scholar 

  42. Mutreja R, Jariyal M, Pathania P, Sharma A, Sahoo DK, Suri CR (2016) Novel surface antigen based impedimetric immunosensor for detection of Salmonella Typhimurium in water and juice samples. Biosens Bioelectron 85:707–713. https://doi.org/10.1016/j.bios.2016.05.079

    Article  CAS  PubMed  Google Scholar 

  43. Cinti S, Volpe G, Piermarini S, Delibato E, Palleschi G (2017) Electrochemical biosensors for rapid detection of foodborne Salmonella: a critical overview. Sensors 17(8):1910. https://doi.org/10.3390/s17081910

    Article  CAS  PubMed Central  Google Scholar 

  44. Su L, Jia W, Hou C, Lei Y (2011) Microbial biosensors: a review. Biosens Bioelectron 26(5):1788–1799. https://doi.org/10.1016/j.bios.2010.09.005

    Article  CAS  PubMed  Google Scholar 

  45. Keith M (1997) Evaluation of an automated enzyme-linked fluorescent immunoassay system for the detection of Salmonella in foods. J Food Protoc 60(6):682–685. https://doi.org/10.4315/0362-028X-60.6.682

    Article  Google Scholar 

  46. Chin WH, Sun Y, Høgberg J, Quyen TL, Engelsmann P, Wolff A, Bang DD (2017) Direct PCR—a rapid method for multiplexed detection of different serotypes of Salmonella in enriched pork meat samples. Mol Cell Probes 32:24–32. https://doi.org/10.1016/j.mcp.2016.11.004

    Article  CAS  PubMed  Google Scholar 

  47. Mercanoglu TB, Ben U, Aytac SA (2009) Rapid detection of Salmonella in milk by combined immunomagnetic separation-polymerase chain reaction assay. J Dairy Sci 92(6):2382–2388. https://doi.org/10.3168/jds.2008-1537

    Article  CAS  Google Scholar 

  48. Vinayaka AC, Ngo TA, Kant K, Engelsmann P, Dave VP, Shahbazi M-A, Wolff A, Bang DD (2019) Rapid detection of Salmonella enterica in food samples by a novel approach with combination of sample concentration and direct PCR. Biosensors Bioelectron 129:224–230. https://doi.org/10.1016/j.bios.2018.09.078

    Article  CAS  Google Scholar 

  49. Khan AB, Sahir KH, Ahmed M, Khan SI (2014) Rapid detection of Salmonella in food samples by polymerase chain reaction after a 10 h pre-enrichment. J Food Saf 34(1):79–86. https://doi.org/10.1111/jfs.12099

    Article  CAS  Google Scholar 

  50. Almeida MVd, Silva A, Nero LA (2014) Evaluation of target sequences for the polymerase chain reaction-based detection of Salmonella in artificially contaminated beef. Foodborne Pathog Dis 11(2):111–118. https://doi.org/10.1089/fpd.2013.1623

    Article  CAS  PubMed  Google Scholar 

  51. Albakri KAA (2015) Comparison between PCR and culture methods for detection of Salmonella Typhimurium from food and beverage. Donn J Food Sci Technol 1(2):006–016

    Google Scholar 

  52. Ganz K, Gill A (2013) Inhibition of polymerase chain reaction for the detection of Escherichia coli O157:H7 and Salmonella enterica on walnut kernels. Food Microbiol 35(1):15–20. https://doi.org/10.1016/j.fm.2013.02.002

    Article  CAS  PubMed  Google Scholar 

  53. Xiao L, Zhang Z, Sun X, Pan Y, Zhao Y (2015) Development of a quantitative real-time PCR assay for viable Salmonella spp. without enrichment. Food Control 57:185–189. https://doi.org/10.1016/j.foodcont.2015.03.050

    Article  CAS  Google Scholar 

  54. Malorny B, Huehn S, Dieckmann R, Krämer N, Helmuth R (2009) Polymerase chain reaction for the rapid detection and serovar identification of Salmonella in food and feeding stuff. Food Anal Methods 2(2):81–95. https://doi.org/10.1007/s12161-008-9057-9

    Article  Google Scholar 

  55. Medici DD, Croci L, Delibato E, Pasquale SD, Filetici E, Toti L (2003) Evaluation of DNA extraction methods for use in combination with SYBR Green I real-time PCR to detect Salmonella enterica serotype Enteritidis in poultry. Appl Environ Microbiol 69(6):3456–3461. https://doi.org/10.1128/aem.69.6.3456-3461.2003

    Article  PubMed  PubMed Central  Google Scholar 

  56. Espy MJ, Uhl JR, Sloan LM, Buckwalter SP, Jones MF, Vetter EA, Yao JDC, Wengenack NL, Rosenblatt JE, Cockerill FR (2006) Real-time PCR in clinical microbiology: applications for routine laboratory testing. Clin Mcrobiol Rev 19(1):165–256. https://doi.org/10.1128/CMR.19.1.165-256.2006

    Article  CAS  Google Scholar 

  57. Singh P, Mustapha A (2014) Development of a real-time PCR melt curve assay for simultaneous detection of virulent and antibiotic resistant Salmonella. Food Microbiol 44(6):6–14. https://doi.org/10.1016/j.fm.2014.04.014

    Article  CAS  PubMed  Google Scholar 

  58. Dmitric M, Vidanovic D, Matovic K, Sekler M, Saric L, Arsic M, Karabasil N (2017) In-house validation of real-time PCR methods for detecting the invA and ttr genes of Salmonella spp. in food. J Food Process Preserv 42(2):e13455. https://doi.org/10.1111/jfpp.13455

    Article  CAS  Google Scholar 

  59. Delibato E, Rodriguez-Lazaro D, Gianfranceschi M, Cesare AD, Comin D, Gattuso A, Hernandez M, Sonnessa M, Pasquali F, Sreter-Lancz Z (2014) European validation of real-time PCR method for detection of Salmonella spp. in pork meat. Int J Food Microbiol 184(4):134–138. https://doi.org/10.1016/j.ijfoodmicro.2014.01.005

    Article  CAS  PubMed  Google Scholar 

  60. Cossu A, Levin RE (2014) Rapid conventional PCR and real-time-qPCR detection of low numbers of Salmonella enterica from ground beef without enrichment. Food Biotechnol 28(2):96–105. https://doi.org/10.1080/08905436.2014.895946

    Article  CAS  Google Scholar 

  61. Tatavarthy A, Cannons A (2010) Real-time PCR detection of Salmonella species using a novel target: the outer membrane porin F gene (ompF). Lett Appl Microbiol 50(6):645–652. https://doi.org/10.1111/j.1472-765X.2010.02848.x

    Article  CAS  PubMed  Google Scholar 

  62. Mccabe EM, Burgess CM, O’Regan E, Mcguinness S, Barry T, Fanning S, Duffy G (2011) Development and evaluation of DNA and RNA real-time assays for food analysis using the hilA gene of Salmonella enterica subspecies enterica. Food Microbiol 28(3):447–456. https://doi.org/10.1016/j.fm.2010.10.012

    Article  CAS  PubMed  Google Scholar 

  63. Riyaz-Ul-Hassan S, Verma V, Qazi GN (2013) Real-time PCR-based rapid and culture-independent detection of Salmonella in dairy milk-addressing some core issues. Lett Appl Microbiol 56(4):275–282. https://doi.org/10.1111/lam.12046

    Article  CAS  PubMed  Google Scholar 

  64. Garima K, Tudor B, Bruce R, Stratton GS, Thomas NA, Alan C, Jeff H, Balakrishnan P (2016) Red seaweeds Sarcodiotheca gaudichaudii and Chondrus crispusdown regulate virulence factors of Salmonella Enteritidis and induce immune responses in Caenorhabditis elegans. Front Microbiol 7:421. https://doi.org/10.3389/fmicb.2016.00421

    Article  Google Scholar 

  65. Kim SA, Park SH, Lee SI, Ricke SC (2017) Development of a rapid method to quantify Salmonella Typhimurium using a combination of MPN with qPCR and a shortened time incubation. Food Microbiol 65:7–18. https://doi.org/10.1016/j.fm.2017.01.013

    Article  CAS  PubMed  Google Scholar 

  66. Hassena AB, Barkallah M, Fendri I, Grosset N, Neila IB, Gautier M, Gdoura R (2015) Real time PCR gene profiling and detection of Salmonella using a novel target: the siiA gene. J Microbiol Methods 109:9–15. https://doi.org/10.1016/j.mimet.2014.11.018

    Article  CAS  PubMed  Google Scholar 

  67. Margot H, Stephan R, Guarino S, Jagadeesan B, Chilton D, O'Mahony E, Iversen C (2013) Inclusivity, exclusivity and limit of detection of commercially available real-time PCR assays for the detection of Salmonella. Int J Food Microbiol 165(3):221–226. https://doi.org/10.1016/j.ijfoodmicro.2013.05.012

    Article  CAS  PubMed  Google Scholar 

  68. Wang L, Mustapha A (2010) EMA-real-time PCR as a reliable method for detection of viable Salmonella in chicken and eggs. J Food Sci 75(3):M134–M139. https://doi.org/10.1111/j.1750-3841.2010.01525.x

    Article  CAS  PubMed  Google Scholar 

  69. Nocker A, Cheung C, Camper A (2006) Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J Microbiol Methods 67(2):310–320. https://doi.org/10.1016/j.mimet.2006.04.015

    Article  CAS  PubMed  Google Scholar 

  70. Liang N, Dong J, Luo L, Li Y (2011) Detection of viable Salmonella in lettuce by propidium monoazide real-time PCR. J Food Sci 76(4):234–237. https://doi.org/10.1111/j.1750-3841.2011.02123.x

    Article  CAS  Google Scholar 

  71. Smpkins SA, Chan AB, Hays J, Pöpping B, Cook N (2000) An RNA transcription-based amplification technique (NASBA) for the detection of viable Salmonella enterica. Lett Appl Microbiol 30(1):75–79. https://doi.org/10.1046/j.1472-765x.2000.00670.x

    Article  Google Scholar 

  72. Gilbride K (2014) Molecular methods for the detection of waterborne pathogens. In: Bridle H (ed) Waterborne pathogens: detection methods and applications. Elsevier Science, Amsterdam, pp 231–290. https://doi.org/10.1016/B978-0-444-59543-0.00008-6

    Chapter  Google Scholar 

  73. Fakruddin M, Mazumdar RM, Chowdhury A, Mannan KSB (2012) Nucleic acid sequence based amplification (NASBA)-prospects and applications. Int J Life Sci Pharma Res 2(1):106–121

    CAS  Google Scholar 

  74. Kievs G, Johnl M (2007) Nucleic acid sequence-based amplification (NASBA) in molecular bacteriology: a procedural guide. J Rapid Methods Autom Microbiol 15(3):295–309. https://doi.org/10.1111/j.1745-4581.2007.00099.x

    Article  Google Scholar 

  75. Honsvall BK, Robertson LJ (2017) From research lab to standard environmental analysis tool: will NASBA make the leap? Water Res 109:389–397. https://doi.org/10.1016/j.watres.2016.11.052

    Article  CAS  PubMed  Google Scholar 

  76. Souii A, M’Hadheb-Gharbi MB, Gharbi J (2016) Nucleic acid-based biotechnologies for food–borne pathogen detection using routine time-intensive culture-based methods and fast molecular diagnostics. Food Sci Biotechnol 25(1):11–20. https://doi.org/10.1007/s10068-016-0002-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Mollasalehi H, Yazdanparast R (2013) An improved non-crosslinking gold nanoprobe-NASBA based on 16S rRNA for rapid discriminative bio-sensing of major salmonellosis pathogens. Biosens Bioelectron 47(17):231–236. https://doi.org/10.1016/j.bios.2013.03.012

    Article  CAS  PubMed  Google Scholar 

  78. Cook N, Ellison J, Kurdziel AS, Simpkins S, Hays JP (2002) A NASBA-based method to detect Salmonella enterica serotype Enteritidis strain PT4 in liquid whole egg. J Food Protoc 65(7):1177–1178. https://doi.org/10.4315/0362-028X-65.7.1177

    Article  CAS  Google Scholar 

  79. Saharan P, Khatri P, Dingolia S, Duhan JS, Gahlawat SK (2013) Rapid detection of viruses using loop-mediated isothermal amplification (LAMP): a review. In: Salar RK, Gahlawat SK, Siwach P, Duhan JS (eds) Biotechnology: prospects and applications. Springer India, New Delhi, pp 287–306

    Chapter  Google Scholar 

  80. Li Y, Fan P, Zhou S, Zhang L (2017) Loop-mediated isothermal amplification (LAMP): a novel rapid detection platform for pathogens. Microb Pathog 107:54–61. https://doi.org/10.1016/j.micpath.2017.03.016

    Article  CAS  PubMed  Google Scholar 

  81. Abdullah J, Saffie N, Sjasri FA, Husin A, Abdulrahman Z, Ismail A, Aziah I, Mohamed M (2014) Rapid detection of Salmonella typhi by loop-mediated isothermal amplification (LAMP) method. Braz J Microbiol 45(4):1385–1391. https://doi.org/10.1590/S1517-83822014000400032

    Article  CAS  PubMed  Google Scholar 

  82. Yang Q, Wang F, Jones KL, Meng J, Prinyawiwatkul W, Ge B (2015) Evaluation of loop-mediated isothermal amplification for the rapid, reliable, and robust detection of Salmonella in produce. Food Microbiol 46:485–493. https://doi.org/10.1016/j.fm.2014.09.011

    Article  CAS  PubMed  Google Scholar 

  83. Martzy R, Kolm C, Brunner K, Mach RL, Krska R, Šinkovec H, Sommer R, Farnleitner AH, Reischer GH (2017) A loop-mediated isothermal amplification (LAMP) assay for the rapid detection of Enterococcus spp. in water. Water Res 122:62–69. https://doi.org/10.1016/j.watres.2017.05.023

    Article  CAS  PubMed  Google Scholar 

  84. Ohtsuka K, Yanagawa K, Takatori K, Hara-Kudo Y (2005) Detection of Salmonella enterica in naturally contaminated liquid eggs by loop-mediated isothermal amplification, and characterization of Salmonella isolates. Appl Environ Microbiol 71(11):6730–6735. https://doi.org/10.1128/AEM.71.11.6730-6735.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Domesle KJ, Yang Q, Hammack TS, Ge B (2018) Validation of a Salmonella loop-mediated isothermal amplification assay in animal food. Int J Food Microbiol 264(2):63–76. https://doi.org/10.1016/j.ijfoodmicro.2017.10.020

    Article  CAS  PubMed  Google Scholar 

  86. Yang Q, Chen S, Ge B (2013) Detecting Salmonella serovars in shell eggs by loop-mediated isothermal amplification. J Food Protoc 76(10):1790–1796. https://doi.org/10.4315/0362-028X.JFP-13-140

    Article  CAS  Google Scholar 

  87. Ziros PG, Kokkinos PA, Papanotas K, Vantarakis A (2012) Loop-mediated isothermal amplification (LAMP) for the detection of Salmonella spp. isolated from different food types. J Microbiol Biotechnol Food Sci 2(1):152–161

    CAS  Google Scholar 

  88. Ravan H, Yazdanparast R (2012) Development of a new loop-mediated isothermal amplification assay for prt (rfbS) gene to improve the identification of Salmonella serogroup D. World J Microbiol Biotechnol 28(5):2101–2106. https://doi.org/10.1007/s11274-012-1014-5

    Article  CAS  PubMed  Google Scholar 

  89. Rathinasabapathi P (2017) Rapid detection of the flic-d gene of Salmonella typhi using loop-mediated isothermal amplification. Res J Biotechnol 12(7):7–10

    CAS  Google Scholar 

  90. Hu L, Ma LM, Zheng S, He X, Hammack TS, Brown EW, Zhang G (2018) Development of a novel loop-mediated isothermal amplification (LAMP) assay for the detection of Salmonella ser. Enteritidis from egg products. Food Control 88:190–197. https://doi.org/10.1016/j.foodcont.2018.01.006

    Article  CAS  Google Scholar 

  91. Liu N, Zou D, Dong D, Yang Z, Ao D, Liu W, Huang L (2017) Development of a multiplex loop-mediated isothermal amplification method for the simultaneous detection of Salmonella spp. and Vibrio parahaemolyticus. Sci Rep 7:45601. https://doi.org/10.1038/srep45601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Wu GP, Chen SH, Levin RE (2015) Application of ethidium bromide monoazide for quantification of viable and dead cells of Salmonella enterica by real-time loop-mediated isothermal amplification. J Microbiol Methods 117:41–48. https://doi.org/10.1016/j.mimet.2015.07.012

    Article  CAS  PubMed  Google Scholar 

  93. Fan F, Yan M, Du P, Chen C, Kan B (2015) Rapid and sensitive Salmonella typhi detection in blood and fecal samples using reverse transcription loop-mediated isothermal amplification. Foodborne Pathog Dis 12(9):778–786. https://doi.org/10.1089/fpd.2015.1950

    Article  CAS  PubMed  Google Scholar 

  94. Ye Y, Wang B, Huang F, Song Y, Yan H, Alam MJ, Yamasaki S, Shi L (2011) Application of in situ loop-mediated isothermal amplification method for detection of Salmonella in foods. Food Control 22(3–4):438–444. https://doi.org/10.1016/j.foodcont.2010.09.023

    Article  CAS  Google Scholar 

  95. Hsieh K, Patterson AS, Ferguson BS, Plaxco KW, Soh HT (2012) Rapid, sensitive, and quantitative detection of pathogenic DNA at the point of care through microfluidic electrochemical quantitative loop-mediated isothermal amplification. Angew Chem Int Ed 51(20):4896–4900. https://doi.org/10.1002/anie.201109115

    Article  CAS  Google Scholar 

  96. Lobato IM, O'Sullivan CK (2018) Recombinase polymerase amplification: basics, applications and recent advances. Trends Anal Chem 98:19–35. https://doi.org/10.1016/j.trac.2017.10.015

    Article  CAS  Google Scholar 

  97. Gao W, Huang H, Zhu P, Yan X, Fan J, Jiang J, Xu J (2018) Recombinase polymerase amplification combined with lateral flow dipstick for equipment-free detection of Salmonella in shellfish. Bioprocess Biosystems Eng 41(5):603–611. https://doi.org/10.1007/s00449-018-1895-2

    Article  CAS  Google Scholar 

  98. Piepenburg O, Williams CH, Stemple DL, Armes NA (2006) DNA detection using recombination proteins. PLoS Biol 4(7):e204. https://doi.org/10.1371/journal.pbio.0040204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Chen J, Liu X, Chen J, Guo Z, Wang J (2019) Development of a rapid test method for Salmonella enterica detection based on fluorescence probe-based recombinase polymerase amplification. Food Anal Methods. https://doi.org/10.1007/s12161-019-01526-3

    Article  Google Scholar 

  100. Liu HB, Zang YX, Du XJ, Li P, Wang S (2017) Development of an isothermal amplification-based assay for the rapid visual detection of Salmonella bacteria. J Dairy Sci 100(9):7016–7025. https://doi.org/10.3168/jds.2017-12566

    Article  CAS  PubMed  Google Scholar 

  101. Kim JY, Lee JL (2016) Rapid detection of Salmonella enterica serovar Enteritidis from eggs and chicken meat by real-time recombinase polymerase amplification in comparison with the two-step real-time PCR. J Food Saf 36(3):402–411. https://doi.org/10.1111/jfs.12261

    Article  CAS  Google Scholar 

  102. Choi G, Jung JH, Park BH, Oh SJ, Seo JH, Choi JS, Kim DH, Seo TS (2016) A centrifugal direct recombinase polymerase amplification (direct-RPA) microdevice for multiplex and real-time identification of food poisoning bacteria. Lab Chip 16(12):2309–2316. https://doi.org/10.1039/C6LC00329J

    Article  CAS  PubMed  Google Scholar 

  103. Dao TNT, Lee EY, Koo B, Jin CE, Lee TY, Shin Y (2018) A microfluidic enrichment platform with a recombinase polymerase amplification sensor for pathogen diagnosis. Anal Biochem 544:87–92. https://doi.org/10.1016/j.ab.2017.12.030

    Article  CAS  PubMed  Google Scholar 

  104. Kersting S, Rausch V, Bier FF, von Nickisch-Rosenegk M (2014) Multiplex isothermal solid-phase recombinase polymerase amplification for the specific and fast DNA-based detection of three bacterial pathogens. Microchim Acta 181(13):1715–1723. https://doi.org/10.1007/s00604-014-1198-5

    Article  CAS  Google Scholar 

  105. Gao W, Huang H, Zhang Y, Zhu P, Yan X, Fan J, Chen X (2017) Recombinase polymerase amplification-based assay for rapid detection of Listeria monocytogenes in food samples. Food Anal Methods 10(6):1972–1981. https://doi.org/10.1007/s12161-016-0775-0

    Article  Google Scholar 

  106. Yan L, Zhou J, Zheng Y, Gamson AS, Roembke BT, Nakayama S, Sintim HO (2014) Isothermal amplified detection of DNA and RNA. Mol Biosyst 10(5):970–1003. https://doi.org/10.1039/C3MB70304E

    Article  CAS  PubMed  Google Scholar 

  107. Santiago-Felipe S, Tortajada-Genaro LA, Morais S, Puchades R, Maquieira Á (2015) Isothermal DNA amplification strategies for duplex microorganism detection. Food Chem 174:509–515. https://doi.org/10.1016/j.foodchem.2014.11.080

    Article  CAS  PubMed  Google Scholar 

  108. Deng H, Gao Z (2015) Bioanalytical applications of isothermal nucleic acid amplification techniques. Anal Chim Acta 853:30–45. https://doi.org/10.1016/j.aca.2014.09.037

    Article  CAS  PubMed  Google Scholar 

  109. James A, Macdonald J (2015) Recombinase polymerase amplification: emergence as a critical molecular technology for rapid, low-resource diagnostics. Expert Rev Mol Diagn 15(11):1475–1489. https://doi.org/10.1586/14737159.2015.1090877

    Article  CAS  PubMed  Google Scholar 

  110. Liébana S, Brandao D, Alegret S, Pividori I (2014) Electrochemical immunosensors, genosensors and phagosensors for Salmonella detection. Anal Methods UK 6(22):8858–8873. https://doi.org/10.1039/c4ay01373e

    Article  Google Scholar 

  111. Song Y, Li W, Duan Y, Li Z, Deng L (2014) Nicking enzyme-assisted biosensor for Salmonella Enteritidis detection based on fluorescence resonance energy transfer. Biosens Bioelectron 55:400–404. https://doi.org/10.1016/j.bios.2013.12.053

    Article  CAS  PubMed  Google Scholar 

  112. Satisvar S, Gopinath SCB, Arshad MKM, Ong DV, Lakshmipriya T, Voon CH, Hashim U, Ruslinda AR, Chinni SV (2017) Comparative analysis of fliC gene from Salmonella enterica sub-species for biosensor probe design and phylogenetic tree construction. Songklanakarin J Sci Technol 39(3):373–381. https://doi.org/10.14456/sjst-psu.2017.41

    Article  CAS  Google Scholar 

  113. Das R, Sharma MK, Rao VK, Bhattacharya BK, Garg I, Venkatesh V, Upadhyay S (2014) An electrochemical genosensor for Salmonella typhi on gold nanoparticles-mercaptosilane modified screen printed electrode. J Biotechnol 188(3):9–16. https://doi.org/10.1016/j.jbiotec.2014.08.002

    Article  CAS  PubMed  Google Scholar 

  114. Mu J, Yang Y, Ding Y, Wang J, Li J, Du X, Chang D (2012) Detection of Salmonella Typhimurium (LT2) invA gene using PNA probe biosensor by electrochemical impedance. Asian J Chem 24(11):5357–5360. https://doi.org/10.1691/ph.2012.2626

    Article  CAS  Google Scholar 

  115. Oh SY, Heo NS, Shukla S, Cho HJ, Vilian A, Kim J, Lee SY, Han YK, Yoo SM, Huh YS (2017) Development of gold nanoparticle-aptamer-based LSPR sensing chips for the rapid detection of Salmonella Typhimurium in pork meat. Sci Rep 7(1):10130. https://doi.org/10.1038/s41598-017-10188-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Martínfernández B, Manzanarespalenzuela CL, López MS, Ns D, Lópezruiz B (2015) Electrochemical genosensors in food safety assessment. Crit Rev Food Sci Nutr 57(13):2758–2774. https://doi.org/10.1080/10408398.2015.1067597

    Article  CAS  Google Scholar 

  117. Ricke SC, Khatiwara A, Kwon YM (2013) Application of microarray analysis of foodborne Salmonella in poultry production: a review. Poult Sci 92(9):2243–2250. https://doi.org/10.3382/ps.2012-02740

    Article  CAS  PubMed  Google Scholar 

  118. Mcloughlin KS (2011) Microarrays for pathogen detection and analysis. Brief Funct Genom 10(6):342–353. https://doi.org/10.1093/bfgp/elr027

    Article  Google Scholar 

  119. Uttamchandani M, Jia LN, Ong BNZ, Moochhala S (2009) Applications of microarrays in pathogen detection and biodefence. Trends Biotechnol 27(1):53–61. https://doi.org/10.1016/j.tibtech.2008.09.004

    Article  CAS  PubMed  Google Scholar 

  120. Ojha S, Kostrzynska M (2008) Examination of animal and zoonotic pathogens using microarrays. Vet Res 39(1):4. https://doi.org/10.1051/vetres:2007042

    Article  CAS  PubMed  Google Scholar 

  121. Scaria J, Palaniappan RU, Chiu D, Phan JA, Ponnala L, Mcdonough P, Grohn YT, Porwollik S, Mcclelland M, Chiou CS (2008) Microarray for molecular typing of Salmonella enterica serovars. Mol Cell Probes 22(4):238–243. https://doi.org/10.1016/j.mcp.2008.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Zou W, Frye JG, Chang CW, Liu J, Cerniglia CE, Nayak R (2010) Microarray analysis of antimicrobial resistance genes in Salmonella enterica from preharvest poultry environment. J Appl Microbiol 107(3):906–914. https://doi.org/10.1111/j.1365-2672.2009.04270.x

    Article  CAS  Google Scholar 

  123. Zou W, Alkhaldi SF, Branham WS, Han T, Fuscoe JC, Han J, Foley SL, Xu J, Fang H, Cerniglia CE (2011) Microarray analysis of virulence gene profiles in Salmonella serovars from food/food animal environment. J Infect Dev Ctries 5(2):94–105. https://doi.org/10.3855/jidc.1396

    Article  CAS  PubMed  Google Scholar 

  124. Rasooly A, Herold KE (2008) Food microbial pathogen detection and analysis using DNA microarray technologies. Foodborne Pathog Dis 5(4):531. https://doi.org/10.1089/fpd.2008.0119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Meng gen MA, Wang HN, Yong YU, Zhang D, Liu SG (2007) Detection of antimicrobial resistance genes of pathogenic Salmonella from swine with DNA microarray. J Vet Diagn Investig 19(2):161–167. https://doi.org/10.1177/104063870701900204

    Article  Google Scholar 

  126. Figueiredo R, Card R, Nunes C, AbuOun M, Bagnall MC, Nunez J, Mendonca N, Anjum MF, da Silva GJ (2015) Virulence characterization of Salmonella enterica by a new microarray: detection and evaluation of the cytolethal distending toxin gene activity in the unusual host S. typhimurium. PLoS ONE 10(8):e0135010. https://doi.org/10.1371/journal.pone.0135010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Guo D, Liu B, Liu F, Cao B, Chen M, Hao X, Feng L, Wang L (2013) Development of a DNA microarray for molecular identification of all 46 Salmonella O serogroups. Appl Environ Microbiol 79(11):3392–3399. https://doi.org/10.1128/AEM.00225-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Huang A, Qiu Z, Jin M, Shen Z, Chen Z, Wang X, Li JW (2014) High-throughput detection of food-borne pathogenic bacteria using oligonucleotide microarray with quantum dots as fluorescent labels. Int J Food Microbiol 185:27–32. https://doi.org/10.1016/j.ijfoodmicro.2014.05.012

    Article  CAS  PubMed  Google Scholar 

  129. Ramirez-Castillo FY, Loera-Muro A, Jacques M, Garneau P, Avelar-Gonzalez FJ, Harel J, Guerrero-Barrera AL (2015) Waterborne pathogens: detection methods and challenges. Pathogens 4(2):307–334. https://doi.org/10.3390/pathogens4020307

    Article  PubMed  PubMed Central  Google Scholar 

  130. Mandal PK, Biswas AK, Choi K, Pal UK (2011) Methods for rapid detection of foodborne pathogens: an overview. Am J Food Technol 6(2):87–102. https://doi.org/10.3923/ajft.2011.87.102

    Article  Google Scholar 

  131. Ehrenreich A (2006) DNA microarray technology for the microbiologist: an overview. Appl Microbiol Biotechnol 73(2):255–273. https://doi.org/10.1007/s00253-006-0584-2

    Article  CAS  PubMed  Google Scholar 

  132. Severgnini M, Cremonesi P, Consolandi C, Bellis GD, Castiglioni B (2011) Advances in DNA microarray technology for the detection of foodborne pathogens. Food Bioprocess Technol 4(6):936–953. https://doi.org/10.1007/s11947-010-0430-5

    Article  Google Scholar 

  133. Koyuncu S, Andersson G, Vos P, Haggblom P (2011) DNA microarray for tracing Salmonella in the feed chain. Int J Food Microbiol 145(Suppl 1):S18–22. https://doi.org/10.1016/j.ijfoodmicro.2010.07.012

    Article  CAS  PubMed  Google Scholar 

  134. Reis-Filho JS (2009) Next-generation sequencing. Breast Cancer Res 11(Suppl 3):S12. https://doi.org/10.1186/bcr2431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Vasli N, Laporte J (2013) Impacts of massively parallel sequencing for genetic diagnosis of neuromuscular disorders. Acta Neuropathol 125(2):173–185. https://doi.org/10.1007/s00401-012-1072-7

    Article  CAS  PubMed  Google Scholar 

  136. Shendure J, Balasubramanian S, Church GM, Gilbert W, Rogers J, Schloss JA, Waterston RH (2017) DNA sequencing at 40: past, present and future. Nature 550(7676):345–353. https://doi.org/10.1038/nature24286

    Article  CAS  PubMed  Google Scholar 

  137. Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Gene 17(6):333–351. https://doi.org/10.1038/nrg.2016.49

    Article  CAS  Google Scholar 

  138. Deurenberg RH, Bathoorn E, Chlebowicz MA, Couto N, Ferdous M, Garcia-Cobos S, Kooistra-Smid AM, Raangs EC, Rosema S, Veloo AC, Zhou K, Friedrich AW, Rossen JW (2017) Application of next generation sequencing in clinical microbiology and infection prevention. J Biotechnol 243:16–24. https://doi.org/10.1016/j.jbiotec.2016.12.022

    Article  CAS  PubMed  Google Scholar 

  139. Frey KG, Bishop-Lilly KA (2015) Next-generation sequencing for pathogen detection and identification. In: Sails A, Tang YW (eds) Methods in microbiology, vol 42. Elsevier Science, Amsterdam, pp 525–554. https://doi.org/10.1016/bs.mim.2015.06.004

    Chapter  Google Scholar 

  140. Sekse C, Holst-Jensen A, Dobrindt U, Johannessen GS, Li W, Spilsberg B, Shi J (2017) High throughput sequencing for detection of foodborne pathogens. Front Microbiol 8:2029. https://doi.org/10.3389/fmicb.2017.02029

    Article  PubMed  PubMed Central  Google Scholar 

  141. Hindermann D, Gopinath G, Chase H, Negrete F, Althaus D, Zurfluh K, Tall BD, Stephan R, Nuesch-Inderbinen M (2017) Salmonella enterica serovar Infantis from food and human infections, Switzerland, 2010–2015: poultry-related multidrug resistant clones and an emerging ESBL producing clonal lineage. Front Microbiol 8:1322. https://doi.org/10.3389/fmicb.2017.01322

    Article  PubMed  PubMed Central  Google Scholar 

  142. Deng X, den Bakker HC, Hendriksen RS (2016) Genomic epidemiology: whole-genome-sequencing-powered surveillance and outbreak investigation of foodborne bacterial pathogens. Annu Rev Food Sci Technol 7:353–374. https://doi.org/10.1146/annurev-food-041715-033259

    Article  PubMed  Google Scholar 

  143. Loman NJ, Constantinidou C, Christner M et al (2013) A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of Shiga-toxigenic Escherichia coli O104:H4. JAMA 309(14):1502–1510. https://doi.org/10.1001/jama.2013.3231

    Article  CAS  PubMed  Google Scholar 

  144. Köser CU, Ellington MJ, Cartwright EJP, Gillespie SH, Brown NM, Farrington M, Holden MTG, Dougan G, Bentley SD, Parkhill J (2012) Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog 8(8):e1002824. https://doi.org/10.1371/journal.ppat.1002824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Didelot X, Bowden R, Wilson DJ, Peto TE, Crook DW (2012) Transforming clinical microbiology with bacterial genome sequencing. Nat Rev Genet 13(9):601–612. https://doi.org/10.1038/nrg3226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Inns T, Ashton PM, Herrera-Leon S, Lighthill J, Foulkes S, Jombart T, Rehman Y, Fox A, Dallman T, De Pinna E, Browning L, Coia JE, Edeghere O, Vivancos R (2017) Prospective use of whole genome sequencing (WGS) detected a multi-country outbreak of Salmonella Enteritidis. Epidemiol Infect 145(2):289–298. https://doi.org/10.1017/S0950268816001941

    Article  CAS  PubMed  Google Scholar 

  147. Nadon C, Van Walle I, Gerner-Smidt P, Campos J, Chinen I, Concepcion-Acevedo J, Gilpin B, Smith AM, Man Kam K, Perez E, Trees E, Kubota K, Takkinen J, Nielsen EM, Carleton H, Panel F-NE (2017) PulseNet International: vision for the implementation of whole genome sequencing (WGS) for global food-borne disease surveillance. Euro Surveill 22(23):30544. https://doi.org/10.2807/1560-7917.ES.2017.22.23.30544

    Article  PubMed  PubMed Central  Google Scholar 

  148. Ashton P, Nair S, Peters T, Tewolde R, Day M, Doumith M, Green J, Jenkins C, Underwood A, Arnold C, de Pinna E, Dallman T, Grant K (2015) Revolutionising public health reference microbiology using whole genome sequencing: Salmonella as an exemplar. bioRxiv. https://doi.org/10.1101/033225

    Article  Google Scholar 

  149. George T, Cindy B, Autumn G, John B, Ann W, Lina C, Crystal T, Rachel H, Virginia P, Luebbering L, Meller J, Perkins A, Ashley M, Jenell L (2017) Bacterial whole genome sequencing in investigation of Salmonella Oranienburg infection outbreak, Missouri, USA. Arch Clin Microbiol 08(04):59. https://doi.org/10.4172/1989-8436.100059

    Article  Google Scholar 

  150. Simon S, Trost E, Bender J, Fuchs S, Malorny B, Rabsch W, Prager R, Tietze E, Flieger A (2018) Evaluation of WGS based approaches for investigating a food-borne outbreak caused by Salmonella enterica serovar Derby in Germany. Food Microbiol 71:46–54. https://doi.org/10.1016/j.fm.2017.08.017

    Article  PubMed  Google Scholar 

  151. Taylor AJ, Lappi V, Wolfgang WJ, Lapierre P, Palumbo MJ, Medus C, Boxrud D (2015) Characterization of foodborne outbreaks of Salmonella enterica Serovar Enteritidis with whole-genome sequencing single nucleotide polymorphism-based analysis for surveillance and outbreak detection. J Clin Microbiol 53(10):3334–3340. https://doi.org/10.1128/JCM.01280-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Wuyts V, Denayer S, Roosens NH, Mattheus W, Bertrand S, Marchal K, Dierick K, De Keersmaecker SC (2015) Whole genome sequence analysis of Salmonella Enteritidis PT4 outbreaks from a national reference laboratory's viewpoint. PLOS Curr Outbreaks. https://doi.org/10.1371/currents.outbreaks.aa5372d90826e6cb0136ff66bb7a62fc

    Article  Google Scholar 

  153. Wilson MR, Brown E, Keys C, Strain E, Luo Y, Muruvanda T, Grim C, Jean-Gilles Beaubrun J, Jarvis K, Ewing L, Gopinath G, Hanes D, Allard MW, Musser S (2016) Whole genome DNA sequence analysis of Salmonella subspecies enterica serotype Tennessee obtained from related peanut butter foodborne outbreaks. PLoS ONE 11(6):e0146929. https://doi.org/10.1371/journal.pone.0146929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Agren EC, Wahlstrom H, Vesterlund-Carlson C, Lahti E, Melin L, Soderlund R (2016) Comparison of whole genome sequencing typing results and epidemiological contact information from outbreaks of Salmonella Dublin in Swedish cattle herds. Infect Ecol Epidemiol 6:31782. https://doi.org/10.3402/iee.v6.31782

    Article  PubMed  Google Scholar 

  155. Ebenezer V, Medlin LK, Ki JS (2012) Molecular detection, quantification, and diversity evaluation of microalgae. Mar Biotechnol 14(2):129–142. https://doi.org/10.1007/s10126-011-9427-y

    Article  CAS  Google Scholar 

  156. Deng X, Li Z, Zhang W (2012) Transcriptome sequencing of Salmonella enterica serovar Enteritidis under desiccation and starvation stress in peanut oil. Food Microbiol 30(1):311–315. https://doi.org/10.1016/j.fm.2011.11.001

    Article  CAS  PubMed  Google Scholar 

  157. Kroger C, Colgan A, Srikumar S, Handler K, Sivasankaran SK, Hammarlof DL, Canals R, Grissom JE, Conway T, Hokamp K, Hinton JC (2013) An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe 14(6):683–695. https://doi.org/10.1016/j.chom.2013.11.010

    Article  CAS  PubMed  Google Scholar 

  158. Razzauti M, Galan M, Bernard M, Maman S, Klopp C, Charbonnel N, Vayssiertaussat M, Eloit M, Cosson JF (2015) A comparison between transcriptome sequencing and 16S metagenomics for detection of bacterial pathogens in wildlife. PLoS Negl Trop Dis 9(8):e0003929. https://doi.org/10.1371/journal.pntd.0003929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Decuypere S, Meehan CJ, Van Puyvelde S, De Block T, Maltha J, Palpouguini L, Tahita M, Tinto H, Jacobs J, Deborggraeve S (2016) Diagnosis of bacterial bloodstream infections: a 16S metagenomics approach. PLoS Negl Trop Dis 10(2):e0004470. https://doi.org/10.1371/journal.pntd.0004470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Grim CJ, Daquigan N, Lusk Pfefer TS, Ottesen AR, White JR, Jarvis KG (2017) High-resolution microbiome profiling for detection and tracking of Salmonella enterica. Front Microbiol 8:1587. https://doi.org/10.3389/fmicb.2017.01587

    Article  PubMed  PubMed Central  Google Scholar 

  161. Jarvis KG, White JR, Grim CJ, Ewing L, Ottesen AR, Beaubrun JJ, Pettengill JB, Brown E, Hanes DE (2015) Cilantro microbiome before and after nonselective pre-enrichment for Salmonella using 16S rRNA and metagenomic sequencing. BMC Microbiol 15:160. https://doi.org/10.1186/s12866-015-0497-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Ottesen AR, Gonzalez A, Bell R, Arce C, Rideout S, Allard M, Evans P, Strain E, Musser S, Knight R (2013) Co-enriching microflora associated with culture based methods to detect Salmonella from tomato phyllosphere. PLoS ONE 8(9):e73079. https://doi.org/10.1371/journal.pone.0073079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Löfström C, Schelin J, Norling B, Vigre H, Hoorfar J, Rådström P (2011) Culture-independent quantification of Salmonella enterica in carcass gauze swabs by flotation prior to real-time PCR. Int J Food Microbiol 145(3):S103–S109. https://doi.org/10.1016/j.ijfoodmicro.2010.03.042

    Article  CAS  PubMed  Google Scholar 

  164. Giaccone V, Catellani P, Alberghini L (2012) Food as cause of human salmonellosis. In: Mahmoud BSM (ed) Salmonella—a dangerous foodborne pathogen. InTech Europe, Croatia, pp 47–67. https://doi.org/10.5772/30474

    Chapter  Google Scholar 

  165. Martin B, Garriga M, Aymerich T (2012) Pre-PCR treatments as a key factor on the probability of detection of Listeria monocytogenes and Salmonella in ready-to-eat meat products by real-time PCR. Food Control 27(1):163–169. https://doi.org/10.1016/j.foodcont.2012.03.010

    Article  CAS  Google Scholar 

  166. Zeinhom MMA, Wang Y, Sheng L, Du D, Li L, Zhu MJ, Lin Y (2017) Smart phone based immunosensor coupled with nanoflower signal amplification for rapid detection of Salmonella Enteritidis in milk, cheese and water. Sens Actuators B Chem 261:75–82. https://doi.org/10.1016/j.snb.2017.11.093

    Article  CAS  Google Scholar 

  167. Jarquin R, Hanning I, Ahn S, Ricke SC (2009) Development of rapid detection and genetic characterization of Salmonella in poultry breeder feeds. Sensors (Basel) 9(7):5308–5323. https://doi.org/10.3390/s90705308

    Article  CAS  Google Scholar 

  168. European Food Safety Authority (2014) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J 12(2):1–312. https://doi.org/10.2903/j.efsa.2014.3547

    Article  Google Scholar 

  169. European Food Safety Authority (2009) The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. EFSA J 7(1):1–350. https://doi.org/10.2903/j.efsa.2009.223r

    Article  Google Scholar 

  170. Liu J, Jiang J, An Z, Fan G, Liu L, Wang L (2012) A double antibody sandwich ELISA assay for the detection of Salmonella in food original samples. In: International conference on computer technology and science, Singapore, 2012. IACSIT Press, pp 471–476

  171. Moongkarndi P, Rodpai E, Kanarat S (2011) Evaluation of an immunochromatographic assay for rapid detection of Salmonellaenterica serovars Typhimurium and Enteritidis. J Vet Diagn Investig 23(4):797–801. https://doi.org/10.1177/1040638711408063

    Article  Google Scholar 

  172. Shukla S, Leem H, Lee JS, Kim M (2014) Immunochromatographic strip assay for the rapid and sensitive detection of Salmonella Typhimurium in artificially contaminated tomato samples. Can J Microbiol 60(6):399–406. https://doi.org/10.1139/cjm-2014-0223

    Article  CAS  PubMed  Google Scholar 

  173. Wang S, Zhang Y, An W, Wei Y, Liu N, Chen Y, Shuang S (2015) Magnetic relaxation switch immunosensor for the rapid detection of the foodborne pathogen Salmonella enterica in milk samples. Food Control 55:43–48. https://doi.org/10.1016/j.foodcont.2015.02.031

    Article  CAS  Google Scholar 

  174. Xu L, Liu Z, Li Y, Yin C, Hu Y, Xie X, Li Q, Jiao X (2018) A rapid method to identify Salmonella enterica serovar Gallinarum biovar Pullorum using a specific target gene ipaJ. Avian Pathol 47(3):1–20. https://doi.org/10.1080/03079457.2017.1412084

    Article  CAS  Google Scholar 

  175. Saeki EK, Alves J, Bonfante RC, Hirooka EY (2013) Multiplex PCR (mPCR) for the detection of Salmonella spp. and the differentiation of the Typhimurium and Enteritidis serovars in chicken meat. J Food Saf 33(1):25–29. https://doi.org/10.1111/jfs.12019

    Article  CAS  Google Scholar 

  176. Xiong D, Song L, Tao J, Zheng H, Zhou Z, Geng S, Pan Z, Jiao X (2017) An efficient multiplex PCR-based assay as a novel tool for accurate inter-serovar discrimination of Salmonella Enteritidis, S. Pullorum/Gallinarum and S. Dublin. Front Microbiol 8:420. https://doi.org/10.3389/fmicb.2017.00420

    Article  PubMed  PubMed Central  Google Scholar 

  177. Arunrut N, Kiatpathomchai W, Ananchaipattana C (2018) Multiplex PCR assay and lyophilization for detection of Salmonella spp., Staphylococcus aureus and Bacillus cereus in pork products. Food Sci Biotechnol 27(3):867–875. https://doi.org/10.1007/s10068-017-0286-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Hyeon JY, Deng X (2017) Rapid detection of Salmonella in raw chicken breast using real-time PCR combined with immunomagnetic separation and whole genome amplification. Food Microbiol 63:111–116. https://doi.org/10.1016/j.fm.2016.11.007

    Article  CAS  PubMed  Google Scholar 

  179. Jeong YS, Jung HK, Hong JH (2013) Multiplex real-time polymerase chain reaction for rapid detection of Staphylococcus aureus, Vibrio parahaemolyticus, and Salmonella Typhimurium in milk and kimbap. J Korean Soc Appl Biol Chem 56(6):715–721. https://doi.org/10.1007/s13765-013-3194-6

    Article  CAS  Google Scholar 

  180. Liu Y, Singh P, Mustapha A (2018) Multiplex high resolution melt-curve real-time PCR assay for reliable detection of Salmonella. Food Control 91:225–230. https://doi.org/10.1016/j.foodcont.2018.03.043

    Article  CAS  Google Scholar 

  181. Mollasalehi H, Yazdanparast R (2012) Non-crosslinking gold nanoprobes for detection of nucleic acid sequence-based amplification products. Anal Biochem 425(2):91–95. https://doi.org/10.1016/j.ab.2012.03.008

    Article  CAS  PubMed  Google Scholar 

  182. Li J, Zhai L, Bie X, Lu Z, Kong X, Yu Q, Lv F, Zhang C, Zhao H (2016) A novel visual loop-mediated isothermal amplification assay targeting gene62181533 for the detection of Salmonella spp. in foods. Food Control 60:230–236. https://doi.org/10.1016/j.foodcont.2015.07.036

    Article  CAS  Google Scholar 

  183. Wu GP, Levin RE (2015) Rapid and sensitive detection of Salmonella enterica ser. Enteritis retrieved from lettuce using a real-timeloop-mediated amplification isothermal assay without enrichment. Food Biotechnol 29(3):263–275. https://doi.org/10.1080/08905436.2015.1059767

    Article  CAS  Google Scholar 

  184. Zhu D, Yan Y, Lei P, Shen B, Cheng W, Ju H, Ding S (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(1):44–50. https://doi.org/10.1016/j.aca.2014.07.024

    Article  CAS  PubMed  Google Scholar 

  185. Zhang D, Yan Y, Li Q, Yu T, Cheng W, Wang L, Ju H, Ding S (2012) Label-free and high-sensitive detection of Salmonella using a surface plasmon resonance DNA-based biosensor. J Biotechnol 160(3–4):123–128. https://doi.org/10.1016/j.jbiotec.2012.03.024

    Article  CAS  PubMed  Google Scholar 

  186. Tortajada-Genaro LA, Rodrigo A, Hevia E, Mena S, Niñoles R, Maquieira Á (2015) Microarray on digital versatile disc for identification and genotyping of Salmonella and Campylobacter in meat products. Anal Bioanal Chem 407(24):7285–7294. https://doi.org/10.1007/s00216-015-8890-0

    Article  CAS  PubMed  Google Scholar 

  187. Day MR, Doumith M, Do Nascimento V, Nair S, Ashton PM, Jenkins C, Dallman TJ, Stevens FJ, Freedman J, Hopkins KL, Woodford N, De Pinna EM, Godbole G (2018) Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Salmonella enterica serovars Typhi and Paratyphi. J Antimicrob Chemother 73(2):365–372. https://doi.org/10.1093/jac/dkx379

    Article  CAS  PubMed  Google Scholar 

  188. Shah DH (2014) RNA sequencing reveals differences between the global transcriptomes of Salmonella enterica serovar Enteritidis strains with high and low pathogenicities. Appl Environ Microbiol 80(3):896–906. https://doi.org/10.1128/AEM.02740-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Dmitric M, Vidanovic D, Matovic K, Sekler M, Saric L, Arsic M, Karabasil N (2018) In-house validation of real-time PCR methods for detecting the INV A and TTR genes of Salmonella spp. in food. J Food Process Preserv 42(2):e13455. https://doi.org/10.1111/jfpp.13455

    Article  CAS  Google Scholar 

  190. Mollasalehi H, Yazdanparast R (2013) Development and evaluation of a novel nucleic acid sequence-based amplification method using one specific primer and one degenerate primer for simultaneous detection of Salmonella Enteritidis and Salmonella Typhimurium. Anal Chim Acta 770(7):169–174. https://doi.org/10.1016/j.aca.2013.01.053

    Article  CAS  PubMed  Google Scholar 

  191. Kokkinos PA, Ziros PG, Bellou M, Vantarakis A (2013) Loop-mediated isothermal amplification (LAMP) for the detection of Salmonella in food. Food Anal Methods 7(2):512–526. https://doi.org/10.1007/s12161-013-9748-8

    Article  Google Scholar 

  192. García T, Revenga-Parra M, Añorga L, Arana S, Pariente F, Lorenzo E (2012) Disposable DNA biosensor based on thin-film gold electrodes for selective Salmonella detection. Sens Actuators B Chem 161(1):1030–1037. https://doi.org/10.1016/j.snb.2011.12.002

    Article  CAS  Google Scholar 

  193. Valdés A, Ibáñez C, Simó C, García-Cañas V (2013) Recent transcriptomics advances and emerging applications in food science. TrAC Trends Anal Chem 52:142–154. https://doi.org/10.1016/j.trac.2013.06.014

    Article  CAS  Google Scholar 

  194. Oulas A, Pavloudi C, Polymenakou P, Pavlopoulos GA, Papanikolaou N, Kotoulas G, Arvanitidis C, Iliopoulos I (2015) Metagenomics: tools and insights for analyzing next-generation sequencing data derived from biodiversity studies. Bioinform Biol Insights 9:75–88. https://doi.org/10.4137/BBI.S12462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank the Research Foundation of the Projects of Science and Technology of Guangdong Province (Grant numbers 2015A020209121, 2015A030313425 and 2015A030310225), and the Project of Science and Technology of Guangzhou City (Grant number 201607010197) for financial support.

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Lin, L., Zheng, Q., Lin, J. et al. Immuno- and nucleic acid-based current technique for Salmonella detection in food. Eur Food Res Technol 246, 373–395 (2020). https://doi.org/10.1007/s00217-019-03423-9

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