Skip to main content

Development of rapid dipstick assay for food pathogens, Salmonella, by optimized parameters

Journal of Food Science and Technology volume 56, pages 140–148 (2019)Cite this article

Abstract

Salmonella is among the very important pathogens threating the human and animal health. Rapid and easy detection of these pathogens is crucial. In this context, antibody (Ab) based lateral flow assays (LFAs) which are simple immunochromatographic point of care test kits were developed by gold nanoparticles (GNPs) as labelling agent for Salmonella detection. For that purpose some critical parameters such as reagent concentrations on the capture zones, conjugate concentrations and ideal membrane type needed for LFAs for whole cell detection were tested for naked eye analysis. Therefore, prepared LFAs were applied to the live and heat inactivated cells when they were used alone or included in different bacterial mixtures. Among the test platforms, membrane 180 (M180) was found as an ideal membrane and 36 nm GNPs showed highly good labelling in the developed LFAs. Diluted conjugates and low concentrations of reagents affected the test signal negatively. Salmonella was detected in different bacterial mixtures, selectively in 4–5 min. The best recognized species by used Ab were S. enteritidis and S. infantis. 5 × 105S. typhimurium cells were also determined as a limit of detection of this study with mentioned parameters.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Alves J, Niguma NH, Oliveira TC (2015) Detection of Salmonella spp. in eight complex food matrices using polymerase chain reaction assay. J Food Saf 35:453–457

    Article  CAS  Google Scholar 

  • Ang GY, Yu CY, Yean CY (2012) Ambient temperature detection of PCR amplicons with a novel sequence-specific nucleic acid lateral flow biosensor. Biosens Bioelectron 38:151–156

    Article  CAS  PubMed  Google Scholar 

  • BVL (Bundesamt für Verbraucherschutz und Lebensmittelsicherheit) (1996) Position statement of the ZKBS on classifying Salmonella typhimurium LT2 strains and Salmonella typhimurium strains with stable mutations in aroA, galE or cya and crp genes as recipient organisms in genetic engineering operations. Ref. No: 6790-10-42

  • Cam D, Oktem HA (2017) Optimizations needed for lateral flow assay for rapid detection of pathogenic E. coli. Turk J Biol 41:954–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandler J, Gurmin T, Robinson N (2000) The place of gold in rapid tests. IVD Technol 6:37–49

    Google Scholar 

  • Choi DH, Lee SK, Oh YK, Bae BW, Lee SD, Kim S, Shin YB, Kim MG (2010) A dual gold nanoparticle conjugate-based lateral flow assay (LFA) method for the analysis of troponin I. Biosens Bioelectron 25:1999–2002

    Article  CAS  PubMed  Google Scholar 

  • Cogan TA, Humphrey TJ (2003) The rise and fall of Salmonella enteritidis in the UK. J Appl Microbiol 94:114–119

    Article  Google Scholar 

  • D’Souza DH, Critzer FJ, Golden DA (2009) Real-time reverse-transcriptase polymerase chain reaction for the rapid detection of Salmonella using inv A primers. Foodborne Pathog Dis 6:1097–1106

    Article  CAS  PubMed  Google Scholar 

  • Du XJ, Zhou TJ, Li P, Wang S (2017) A rapid Salmonella detection method involving thermophilic helicase-dependent amplification and a lateral flow assay. Mol Cell Probes 34:37–44

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • ECDC (2016). Salmonellosis—annual epidemiological report 2016 (2014 data). Annual epidemiological report on communicable diseases in Europe

  • Englebienne P (2000) Immune and receptor assays in theory and practice. CRC Press, New York, pp 233–234

    Google Scholar 

  • Goncagül G, Günaydin E, Carli KT (2005) Prevalence of Salmonella serogroups in chicken meat. Turk J Vet Anim Sci 29:103–106

    Google Scholar 

  • He Y, Zhang S, Zhang X, Baloda M, Gurung AS, Xu H, Zhang X, Liu G (2011) Ultrasensitive nucleic acid biosensor based on enzyme–gold nanoparticle dual label and lateral flow strip biosensor. Biosens Bioelectron 26:2018–2024

    Article  CAS  PubMed  Google Scholar 

  • Jain PK, Lee KS, El-Sayed IH, El-Sayed MA (2006) Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine. Phys Chem B 110:7238–7248

    Article  CAS  Google Scholar 

  • Kim G, Moon JH, Moh CY, Lim JG (2015) A microfluidic nano-biosensor for the detection of pathogenic Salmonella. Biosens Bioelectron 67:243–247

    Article  CAS  PubMed  Google Scholar 

  • Kimling J, Maier M, Okenve B, Kotaidis V, Ballot H, Plech A (2006) Turkevich method for gold nanoparticle synthesis revisited. J Phys Chem B 110:15700–15707

    Article  CAS  PubMed  Google Scholar 

  • Laderman EI, Whitworth E, Dumaual E, Jones M, Hudak A, Hogrefe W, Carney J, Groen J (2008) Rapid, sensitive, and specific lateral-flow immunochromatographic point-of-care device for detection of herpes simplex virus type 2-specific immunoglobulin G antibodies in serum and whole blood. Clin Vaccine Immunol 15:159–163

    Article  CAS  PubMed  Google Scholar 

  • Liu CC, Yeung CY, Chen PH, Yeh MK, Hou SY (2013) Salmonella detection using 16S ribosomal DNA/RNA probe-gold nanoparticles and lateral flow immunoassay. Food Chem 141:2526–2532

    Article  CAS  PubMed  Google Scholar 

  • 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 100:7016–7025

    Article  CAS  Google Scholar 

  • Lou S, Ye JY, Li KQ, Wu A (2012) A gold nanoparticle-based immunochromatographic assay: the influence of nanoparticulate size. Analyst 137:1174–1181

    Article  CAS  PubMed  Google Scholar 

  • Mikawa AY, Santos SAT, Kenfe FR, da Silva FH, da Costa PI (2009) Development of a rapid one-step immunochromatographic assay for HCV core antigen detection. J Virol Methods 158:160–164

    Article  CAS  PubMed  Google Scholar 

  • Moongkarndi P, Rodpai E, Kanarat S (2011) Evaluation of an immunochromatographic assay for rapid detection of Salmonella enterica serovars Typhimurium and Enteritidis. J Vet Diagn Invest 23:797–801

    Article  PubMed  Google Scholar 

  • Nara S, Tripathi V, Singh H, Shrivastav TG (2010) Colloidal gold probe based rapid immunochromatographic strip assay for cortisol. Anal Chim Acta 682:66–71

    Article  CAS  PubMed  Google Scholar 

  • O’Farrell B (2009) Evolution in lateral flow—based immunoassay systems. In: Lateral flow immunoassay. pp 1–33, Humana Press, New York

  • Olsen SJ, Bishop R, Brenner FW, Roels TH, Bean N, Tauxe RV, Slutsker L (2001) The changing epidemiology of Salmonella: trends in serotypes isolated from humans in the United States, 1987–1997. J Infect Dis 183:753–761

    Article  CAS  PubMed  Google Scholar 

  • Oral R, Sümer S, Can D, Tiraş Ü, Yener H (1995) Yenidoğan Ünitesinde Salmonella Typhimurium Salgını. Turkiye Klinikleri J Pediatr 4:50–55

    Google Scholar 

  • Preechakasedkit P, Pinwattana K, Dungchai W, Siangproh W, Chaicumpa W, Tongtawe P, Chailapakul O (2012) Development of a one-step immunochromatographic strip test using gold nanoparticles for the rapid detection of Salmonella typhi in human serum. Biosens Bioelectron 31:562–566

    Article  CAS  PubMed  Google Scholar 

  • Rosi NL, Giljohann DA, Thaxton CS, Lytton-Jean AK, Han MS, Mirkin CA (2006) Oligonucleotide-modified gold nanoparticles for intracellular gene regulation. Science 312:1027–1030

    Article  CAS  PubMed  Google Scholar 

  • Safenkova IV, Zherdev AV, Dzantiev BB (2010) Correlation between the composition of multivalent antibody conjugates with colloidal gold nanoparticles and their affinity. J Immunol Methods 357:17–25

    Article  CAS  PubMed  Google Scholar 

  • Sapparapu G (2003) Development of immunological reagents for detecting Salmonella Enterica serovar Typhimurium (Master of Science dissertation, University of Florida)

  • Shen G, Shen G, Yu R (2007) Au nanoparticle network-type thin films formed via mixed assembling and cross-linking route for biosensor application: quartz crystal microbalance study. Anal Biochem 365:1–6

    Article  CAS  PubMed  Google Scholar 

  • Shin JH, Hong J, Go H, Park J, Kong M, Ryu S, Kim KP, Roh E, Park JK (2018) Multiplexed detection of Foodborne pathogens from contaminated lettuces using a handheld multistep lateral flow assay device. J Agric Food Chem 66:290–297

    Article  CAS  PubMed  Google Scholar 

  • Singh J, Sharma S, Nara S (2015) Evaluation of gold nanoparticle based lateral flow assays for diagnosis of enterobacteriaceae members in food and water. Food Chem 170:470–483

    Article  CAS  PubMed  Google Scholar 

  • Sperling RA, Gil PR, Zhang F, Zanella M, Parak WJ (2008) Biological applications of gold nanoparticles. Chem Soc Rev 37:1896–1908

    Article  CAS  PubMed  Google Scholar 

  • Stone GG, Oberst RD, Hays MP, McVey S, Galland JC, Curtiss R, Kelly SM, Chengappa MM (1995) Detection of Salmonella typhimurium from rectal swabs of experimentally infected beagles by short cultivation and PCR-hybridization. J Clin Microbiol 33:1292–1295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Verwey EJW, Overbeek JTG (1948) The free energy of a double layer system. Theory of the stability of lyophobic colloids. Elsevier, New York, p 51

    Google Scholar 

  • Voetsch AC, Van Gilder TJ, Angulo FJ, Farley MM, Shallow S, Marcus R, Tauxe RV (2004) Emerging infections program FoodNet working group. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 38:127–134

    Article  Google Scholar 

  • Wen CY, Hu J, Zhang ZL, Tian ZQ, Ou GP, Liao YL, Li Y, Xie M, Sun ZY, Pang DW (2013) One-step sensitive detection of Salmonella typhimurium by coupling magnetic capture and fluorescence identification with functional nanospheres. Anal Chem 85:1223–1230

    Article  CAS  PubMed  Google Scholar 

  • Yuan J, Tao Z, Yu Y, Ma X, Xia Y, Wang L, Wang Z (2014) A visual detection method for Salmonella typhimurium based on aptamer recognition and nanogold labeling. Food Control 37:188–192

    Article  CAS  Google Scholar 

  • Zhang S, Huang TS, Bridgman R, Weese J (2006) Development and characterization of monoclonal and polyclonal antibodies against Salmonella enterica Typhimurium for biosensor detection. J Food Sci 71:M100–M104

    Article  CAS  Google Scholar 

  • Zhao Y, Jiang X, Qu Y, Pan R, Pang X, Jiang Y, Man C (2017) Salmonella detection in powdered dairy products using a novel molecular tool. J Dairy Sci 100:3480–3496

    Article  CAS  PubMed  Google Scholar 

  • Zuo P, Li X, Dominguez DC, Ye BC (2013) A PDMS/paper/glass hybrid microfluidic biochip integrated with aptamer-functionalized graphene oxide nano-biosensors for one-step multiplexed pathogen detection. Lab Chip 13:3921–3928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the Faculty Development Program (ÖYP-BAP-08-11-DPT-2011K121010), and Scientific and Technological Research Council of Turkey (TÜBİTAK-TEYDEB) projects funded to Nanobiz Nanobiotechnological Systems R&D Limited. The authors acknowledge to Ankara University Faculty of Veterinary Medicine for bacterial samples and Dr. Ceren Berkman for help.

Author information

Affiliations

  1. Department of Biological Sciences, Middle East Technical University, 06800, Ankara, Turkey

    Dilek Çam & Hüseyin Avni Öktem

  2. Department of Biology, Çankırı Karatekin University, 18100, Çankırı, Turkey

    Dilek Çam

  3. NANOBIZ TECHNOLOGY INC., Gallium Block No: 27/218, METU Technopolis, 06800, Ankara, Turkey

    Hüseyin Avni Öktem

Authors
  1. Dilek Çam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hüseyin Avni Öktem
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dilek Çam.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Çam, D., Öktem, H.A. Development of rapid dipstick assay for food pathogens, Salmonella, by optimized parameters. J Food Sci Technol 56, 140–148 (2019). https://doi.org/10.1007/s13197-018-3467-5

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-018-3467-5

Keywords

  • Lateral flow assay
  • Salmonella
  • Gold nanoparticles
  • Whole cell detection