Advertisement

Development of a Capture ELISA for Rapid Detection of Salmonella enterica in Food Samples

  • Tiziana Di Febo
  • Maria Schirone
  • Pierina Visciano
  • Ottavio Portanti
  • Gisella Armillotta
  • Tiziana Persiani
  • Elisabetta Di Giannatale
  • Manuela Tittarelli
  • Mirella Luciani
Article

Abstract

In this study, an immunology-based assay that employed specific monoclonal antibodies binding with somatic or flagella antigens of Salmonella enterica subsp. enterica was performed. As this pathogen is one of the most important bacterial species responsible for foodborne outbreaks, its detection in food by rapid and easy methods is properly suitable. After a first screening by indirect ELISA, three monoclonal antibodies (1B6D9, 1B6C11, 1D12F11) versus S. enterica subsp. enterica serovar Typhimurium ATCC 14028 (whole antigen) and another one (4E6F11) versus S. enterica flagellin were further characterized by immunoblotting and mass spectrometry analysis. Then, a total of 84 food samples (dairy products, meat, pasta and flour, eggs, and animal feed) were analyzed by both the official method ISO 6579:2002 and S. enterica capture ELISA. For the standardization of the last method, the specific monoclonal antibody 4E6F11 was selected. The developed Salmonella capture ELISA showed a significant agreement with the official method (ISO 6579:2002). Relative sensitivity, specificity, and accuracy were 100%, 81.0%, and 90.5%, respectively. Therefore, this assay could represent a valid alternative to conventional methods able to detect this pathogen in food.

Keywords

Salmonella enterica Monoclonal antibodies Capture ELISA Food 

Notes

Compliance with Ethical Standards

Conflict of Interest

Tiziana Di Febo declares that she has no conflict of interest. Maria Schirone declares that she has no conflict of interest. Pierina Visciano declares that she has no conflict of interest. Ottavio Portanti declares that he has no conflict of interest. Gisella Armillotta declares that she has no conflict of interest. Tiziana Persiani declares that she has no conflict of interest. Elisabetta Di Giannatale declares that she has no conflict of interest. Manuela Tittarelli declares that she has no conflict of interest. Mirella Luciani declares that she has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed Consent

Not applicable.

References

  1. Abdelhaseib MU, Singh AK, Bailey M, Singh M, El-Khateib T, Bhunia AK (2016) Fiber optic and light scattering sensors: complimentary approaches to rapid detection of Salmonella enterica in food samples. Food Control 61:135–145CrossRefGoogle Scholar
  2. Andino A, Hanning I (2015) Salmonella enterica: survival, colonization and virulence differences among serovars. Sci World J 2015:520179CrossRefGoogle Scholar
  3. Aribam SD, Ogawa Y, Matsui H, Hirota J, Okamura M, Akiba M, Shimoji Y, Eguchi M (2015) Monoclonal antibody-based competitive enzyme-linked immunosorbent assay to detect antibodies to O:4 Salmonella in the sera of livestock and poultry. J Microbiol Meth 108:1–3CrossRefGoogle Scholar
  4. Bell RL, Jarvis KG, Ottesen AR, McFarland AA, Brown EW (2016) Recent and emerging innovations in Salmonella detection: a food and environmental perspective. Microb Biotechnol 9:279–292CrossRefGoogle Scholar
  5. Bonardi S, Alpigiani I, Bruini I, Barilli E, Brindani F, Morganti M, Cavallini P, Bolzoni L, Pongolini S (2016) Detection of Salmonella enterica in pigs at slaughter and comparison with human isolates in Italy. Int J Food Microbiol 218:44–50CrossRefGoogle Scholar
  6. Brown AC, Grass JE, Richardson LC, Nisler AR, Bicknese AS, Gould LH (2017) Antimicrobial resistance in Salmonella that caused foodborne disease outbreaks: United States, 2003-2012. Epidemiol Infect 145(4):766–774CrossRefGoogle Scholar
  7. EFSA, European Food Safety Authority, and ECDC, European Centre for Disease Prevention and Control (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 15(12):5077Google Scholar
  8. Fardsanei F, Soltan Dallal MM, Douraghi M, Zahraei Salehi T, Mahmoodi M, Memariani H, Nikkhahi F (2017) Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype Enteritidis isolated from meats and eggs. Microb Pathog 107:451–456CrossRefGoogle Scholar
  9. García-Fierro R, Montero I, Bances M, Gonzáles-Hevia MA, Rodicio MR (2016) Antimicrobial drug resistance and molecular typing of Salmonella enterica serovar risen from different sources. Microb Drug Resist 22(3):211–217CrossRefGoogle Scholar
  10. Gopinath S, Carden S, Monack D (2012) Shedding light on Salmonella carriers. Trends Microbiol 20(7):320–327CrossRefGoogle Scholar
  11. Hiriart Y, Serradell MDLA, Martínez A, Sampaolesi S, Maciel GD, Chabalgoity JA et al (2013) Generation and selection of anti-flagellin monoclonal antibodies useful for serotyping Salmonella enterica. SpringerPlus 2(640):1–9Google Scholar
  12. Ho YN, Tsai HC, Hsu BM, Chiou CS (2018) The association of Salmonella enterica from aquatic environmental and clinical samples in Taiwan. Sci Total Environ 624:106–113CrossRefGoogle Scholar
  13. Ibrahim GF, Fleet GH, Lyons MJ, Walker RA (1985) Method for the isolation of highly purified Salmonella flagellins. J Clin Microbiol 22(6):1040–1044PubMedPubMedCentralGoogle Scholar
  14. ISO, International Organization for Standardization (2002) ISO 6579:2002. Microbiology of food and animal feeding stuffs - horizontal method for the detection of Salmonella spp, 4th EditionGoogle Scholar
  15. Kang MS, Oh JY, Kwon YK, Lee DY, Jeong OM, Choi BK, Youn SY, Jeon BW, Lee HJ, Lee HS (2017) Public health significance of major genotypes of Salmonella enterica serovar Enteritidis present in both human and chicken isolates in Korea. Res Vet Sci 112:125–131CrossRefGoogle Scholar
  16. Karoonuthaisiri N, Charlermroj R, Teerapornpuntakit J, Kumpoosiri M, Himananto O, Grant IR, Gajanandana O, Elliott CT (2015) Bead array for Listeria monocytogenes detection using specific monoclonal antibodies. Food Control 47:462–471CrossRefGoogle Scholar
  17. Kore K, Asrade B, Demissie K, Aragaw K (2017) Characterization of Salmonella isolated from apparently healthy slaughtered cattle and retail beef in Hawassa, southern Ethiopia. Prev Vet Med 147:11–16CrossRefGoogle Scholar
  18. Lamas M, Miranda JM, Regal P, Vásquez B, Franco CM, Cepeda A (2018) A comprehensive review of non-enterica subspecies of Salmonella enterica. Microbiol Res 206:60–73CrossRefGoogle Scholar
  19. Lee KM, 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 47:264–276CrossRefGoogle Scholar
  20. Luciani M, Schirone M, Portanti O, Visciano P, Armillotta G, Tofalo R, Suzzi G, Sonsini L, di Febo T (2018) Development of a rapid method for the detection of Yersinia enterocolitica serotype O:8 from food. Food Microbiol 73:85–92CrossRefGoogle Scholar
  21. Luo Y, Yi W, Yao Y, Zhu N, Qin P (2018) Characteristic diversity and antimicrobial resistance of Salmonella gastroenteritis. J Infect Chemother 24:251–255CrossRefGoogle Scholar
  22. 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):127–137CrossRefGoogle Scholar
  23. Nakane PK, Kawaoi A (1974) Peroxidase-labeled antibody. A new method of conjugation. J Histochem Cytochem 22:1084–1091CrossRefGoogle Scholar
  24. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75(17):4646–4658CrossRefGoogle Scholar
  25. Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using stage tips. Nat Protoc 2(8):1896–1906CrossRefGoogle Scholar
  26. Ronholm J, Zhang Z, Cao X, Lin M (2011) Monoclonal antibodies to lipopolysaccharide antigens of Salmonella enterica serotype typhimurium DT104. Hybridoma 30(1):43–52CrossRefGoogle Scholar
  27. Schneid ADS, Lüdtke CB, Diel C, Aleixo JAG (2005) Production and characterization of monoclonal antibodies for the detection of Salmonella enterica in chicken meat. Braz J Microbiol 36:163–169CrossRefGoogle Scholar
  28. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68(5):850–858CrossRefGoogle Scholar
  29. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1(6):2856–2860CrossRefGoogle Scholar
  30. Soffientini P, Bachi A (2016) STAGE-diging: a novel in-gel digestion processing for proteomics samples. J Proteome 140:48–54CrossRefGoogle Scholar
  31. Tindall BJ, Grimont PAD, Garrity GM, Euzéby P (2005) Nomenclature and taxonomy of the genus Salmonella. Int J Syst Evol Microbiol 55:521–524CrossRefGoogle Scholar
  32. Wang H, Jiang Y, Liu X, Qian W, Xu X, Zhou G (2016) Behavior variability of Salmonella enterica isolates from meat-related sources. LWT Food Sci Technol 73:375–382CrossRefGoogle Scholar
  33. Zaki S, Abd-El-Haleem D, El-Helow E, Mustafa M (2009) Molecular and biochemical diagnosis of Salmonella in wastewater. J Appl Sci Environ Manag 13(2):83–92Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Tiziana Di Febo
    • 1
  • Maria Schirone
    • 2
  • Pierina Visciano
    • 2
  • Ottavio Portanti
    • 1
  • Gisella Armillotta
    • 1
  • Tiziana Persiani
    • 1
  • Elisabetta Di Giannatale
    • 1
  • Manuela Tittarelli
    • 1
  • Mirella Luciani
    • 1
  1. 1.Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise “G. Caporale”TeramoItaly
  2. 2.Faculty of Bioscience and Technology for Food, Agriculture and EnvironmentUniversity of TeramoTeramoItaly

Personalised recommendations