Abstract
Food-borne diseases are widespread; one of the reasons is contamination with staphylococcal pathogens that can produce enterotoxins of the protein, causing numerous diseases in humans. The long-term stability of the toxins requires that the methods for foodstuff quality control be refined to prevent contamination with staphylococcal enterotoxins. We developed a bead-based multiplex assay for the simultaneous detection of three staphylococcal enterotoxins (staphylococcal enterotoxin A (SEA), staphylococcal enterotoxin B (SEB), staphylococcal enterotoxin H (SEH)) by flow cytometry. For detection, we used functional beads coupled with monoclonal capture antibodies, biotinylated monoclonal detection antibodies, and streptavidin conjugated to phycoerythrin. The linear ranges of detection of SEA, SEB, and SEH were 0.02–20 ng/mL, 0.2–30 ng/mL, and 0.2–20 ng/mL, respectively. Each toxin was specifically detected without cross-reactions. An efficient use of the developed method for the analysis of foodstuffs was reported.
Similar content being viewed by others
References
Balaban N, Rasooly A (2000) Staphylococcal enterotoxins. Int J Food Microbiol 61:1–10. https://doi.org/10.1016/s0168-1605(00)00377-9
BD Cytometric Bead Array: Multiplexed bead-based immunoassays (2012) http://static.bdbiosciences.com/documents/CBA_Brochure_Intl.pdf. Accessed May 29, 2019
Dai J, Wu S, Huang J, Wu Q, Zhang F, Zhang J, Wang J, Ding Y, Zhang S, Yang X, Lei T, Xue L, Wu H (2019) Prevalence and characterization of Staphylococcus aureus isolated from pasteurized milk in China. Front Microbiol 10:641. https://doi.org/10.3389/fmicb.2019.00641
Du X, Zang YX, Liu HB, Li P, Wang S (2018) Rapid detection of Staphylococcus aureus via recombinase polymerase amplification combined with lateral flow strip. Food Anal Methods 11:2296–2306. https://doi.org/10.1007/s12161-018-1200-7
Ferraz TPL, Fiuza MC, dos Santos MLA, Pontes de Carvalho L, Soares NM (2004) Comparison of six methods for the extraction of lipids from serum in terms of effectiveness and protein preservation. J Biochem Biophys Methods 58:187–193. https://doi.org/10.1016/j.jbbm.2003.10.008
Fujikawa H, Igarashi H (1988) Rapid latex agglutination test for detection of staphylococcal enterotoxins A to E that uses high-density latex particles. Appl Environ Microbiol 54:2345–2348 PMC204255
Fursova KK, Shchannikova MP, Loskutova IV, Shepelyakovskaya AO, Artem’eva OA, Nikanova DA, Zinovieva NA, Brovko FA, Laman AG, Boutanaev AM, Sokolov SL (2018) Exotoxin diversity of Staphylococcus aureus isolated from milk of cows with subclinical mastitis in Central Russia. J Dairy Sci 101:4325–4331. https://doi.org/10.3168/jds.2017-14074
Hait JM, Nguyen AT, Tallent SM (2018) Analysis of the VIDAS® staph enterotoxin III (SET3) for detection of staphylococcal enterotoxins G, H, and I in foods. AOAC Int 101:1482–1489. https://doi.org/10.5740/jaoacint.17-0501
Hennekinne JA, De Buyser ML, Dragacc S (2012) Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 36:815–836. https://doi.org/10.1111/j.1574-6976.2011.00311.x
Huang X, Aguilar ZP, Xu H, Lai W, Xiong Y (2016) Membrane-based lateral flow immunochromatographic strip with nanoparticles as reporters for detection: a review. Biosens Bioelectron 75:166–180. https://doi.org/10.1016/j.bios.2015.08.032
Jenko KL, Zhang Y, Kostenko Y, Fan Y, Garcia-Rodriguez C, Lou J, Marks JD, Varnum SM (2004) Development of an ELISA microarray assay for the sensitive and simultaneous detection of ten biodefense toxins. Analyst 130:5093–5102. https://doi.org/10.1039/c4an01270d
Kadariya J, Smith TC, Thapaliya D (2014) Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int 827965:9. https://doi.org/10.1155/2014/827965
Kerr DE, Bergfalk C, Feldsine PT, John L, Tallent S, Hammack T, Brodsky M (2019) Evaluation of the TRANSIA® PLATE staphylococcal enterotoxins kit for the detection of staphylococcal enterotoxins in selected foods. AOAC Int 102:497–507. https://doi.org/10.5740/jaoacint.18-0255
Koike H, Kanda M, Hayashi H, Matsushima Y, Ohba Y, Nakagawa Y, Nagano C, Sekimura K, Hirai A, Shindo T, Otsuka K, Kamiie J, Sasamoto T, Hashimoto T (2019) Quantification of staphylococcal enterotoxin type a in cow milk by using a stable isotope-labelled peptide via liquid chromatography-tandem mass spectrometry. Food Addit Contam Part A 36:1098–1108. https://doi.org/10.1080/19440049.2019.1615641
Letertre C, Perelle S, Dilasser F, Fach P (2003) Detection and genotyping by real-time PCR of the staphylococcal enterotoxin genes sea to sej. Mol Cell Probes 17:139–147. https://doi.org/10.1016/s0890-8508(03)00045-8
Liao F, Gu W, Yang Z, Mo Z, Fan L, Guo Y, Fu X, Xu W, Li C, Dai J (2018) Molecular characteristics of Staphylococcus aureus isolates from food surveillance in Southwest China. BMC Microbiol 18:91–99. https://doi.org/10.1186/s12866-018-1239-z
Liubavina IA, Brovko FA, Valiakina TI, Vertiev IV, Grishin EV (2014) Development of methods for rapid test of staphylococcal enterotoxin a in food. Bioorg Khim 40:186–195
Morandi S, Brasca M, Lodi R, Cremonesi P, Castiglioni B (2007) Detection of classical enterotoxins and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products. Vet Microbiol 124:66–72. https://doi.org/10.1016/j.vetmic.2007.03.014
Nguyen AT, Tallent SM (2018) From commensal to consumer: Staphylococcus aureus toxins, diseases, and detection methods. J AOAC Int 101:1127–1134. https://doi.org/10.5740/jaoacint.17-0366
Nia Y, Mutel I, Assere A, Lombard B, Auvray F, Hennekinne JA (2016) Review over a 3-year period of European Union proficiency tests for detection of staphylococcal enterotoxins in food matrices. Toxins 8:107. https://doi.org/10.3390/toxins8040107
Official Journal of the European Union (2005) Commission Regulation (EC) No 2073/2005 of 15 November 2005 on Microbiological Criteria for Foodstuffs. https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32005R2073&from=EN. Accessed May 29, 2019
Qu J, Xie H, Zhang S, Luo P, Guo P, Chen X, Ke Y, Zhuang J, Zhou F, Jiang W (2019) Multiplex flow cytometric immunoassays for high-throughput screening of multiple mycotoxin residues in milk. Food Anal Methods 12:877–886. https://doi.org/10.1007/s12161-018-01412-4
R-Biopharm Official European Screening Method (2009) Official European screening method for staphylococcal enterotoxins in food RIDASCREEN® SET total (96 tests). https://foodr-biopharmcom/wp-content/uploads/sites/2/2012/06/r4105_set_total_de_en_fr_17-08-09pdf. Accessed May 29, 2019
Rubina AY, Filippova MA, Feizkhanova GU, Shepeliakovskaya AO, Sidina EI, Boziev KM, Laman AG, Brovko FA, Vertiev YV, Zasedatelev AS, Grishin EV (2010) Simultaneous detection of seven staphylococcal enterotoxins: development of hydrogel biochips for analytical and practical application. Anal Chem 82:8881–8889. https://doi.org/10.1021/ac1016634
Rudenko NV, Karatovskaya AP, Noskov AN, Shepelyakovskaya AO, Shchannikova MP, Loskutova IV, Brovko FA (2018) Immunochemical assay with monoclonal antibodies for detection of staphylococcal enterotoxin H. J Food Drug Anal 26(2):741–750. https://doi.org/10.1016/j.jfda.2017.10.011
Russmann H (2003) Toxins. Biogenic substances and potential threat agents. Bundesgesundheitsbl Gesundheitsforsch Gesundheitsschutz 46:989–996. https://doi.org/10.1007/s00103-003-0716-0
Shylaja R, Murali HS, Batra HV, Bawa AS (2010) A novel multiplex PCR system for the detection of staphylococcal enterotoxin B, tsst, nuc and fem genes of Staphylococcus aureus in food system. J Food Saf 30:443–454. https://doi.org/10.1111/j.1745-4565.2010.00218.x
Thomas D, Chou S, Dauwalder O, Lina G (2007) Diversity in Staphylococcus aureus enterotoxins. Chem Immunol Allergy 93:24–41. https://doi.org/10.1159/000100856
Tonacini J, Stephan D, Vogel G, Avondet MA, Kalman F, Crovadore J, Lefort F, Schnyder B (2019) Intact Staphylococcus enterotoxin SEB from culture supernatant detected by MALDI-TOF mass spectrometry. Toxins 11. https://doi.org/10.3390/toxins11020101
Wakabayashi Y, Umeda K, Yonogi S, Nakamura H, Yamamoto K, Kumeda Y, Kawatsu K (2018) Staphylococcal food poisoning caused by Staphylococcus argenteus harboring staphylococcal enterotoxin genes. Int J Food Microbiol 265:23–29. https://doi.org/10.1016/j.ijfoodmicro.2017.10.022
Wang W, Liu L, Xu L, Kuang H, Zhu J, Xu C (2016) Gold-nanoparticle-based multiplexed immunochromatographic strip for simultaneous detection of staphylococcal enterotoxin A, B, C, D, and E. Part Part Syst Charact 33:388–395. https://doi.org/10.1002/ppsc.201500219
Wu S, Duan N, Gu H, Hao L, Ye H, Gong W, Wang Z (2016) A review of the methods for detection of Staphylococcus aureus enterotoxins. Toxins 8. https://doi.org/10.3390/toxins8070176
Funding
This study was supported by a state contract No АААА-А19-119050790041-1, project theme 0101-2019-0038.
Author information
Authors and Affiliations
Contributions
The authors whose names appear on the submission have contributed sufficiently to the scientific work and therefore share collective responsibility and accountability for the results.
Corresponding author
Ethics declarations
Conflict of Interest
Anna Shepelyakovskaya declares that she has no conflict of interest. Natalia Rudenko declares that she has no conflict of interest. Anna Karatovskaya declares that she has no conflict of interest. Margarita Shchannikova declares that she has no conflict of interest. Irina Shulcheva declares that she has no conflict of interest. Ksenia Fursova declares that she has no conflict of interest. Anna Zamyatina declares that she has no conflict of interest. Khanafi Boziev declares that he has no conflict of interest. Vladimir Oleinikov declares that he has no conflict of interest. Fedor Brovko declares that he has no conflict of interest.
Ethical Approval
This article does not contain any studies with human participants performed by any of the authors. Informed consent is not applicable.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The manuscript has not been published previously (partially or completely). The manuscript has not been submitted to more than one journal for simultaneous consideration.
Rights and permissions
About this article
Cite this article
Shepelyakovskaya, A., Rudenko, N., Karatovskaya, A. et al. Development of a Bead-Based Multiplex Assay for the Simultaneous Quantification of Three Staphylococcal Enterotoxins in Food by Flow Cytometry. Food Anal. Methods 13, 1202–1210 (2020). https://doi.org/10.1007/s12161-020-01736-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12161-020-01736-0