Current issue
In press
Archive
About the Journal
Scope
Editorial Board
Indexed
Subscription
Contact
Publication fee
Editorial Policies
Peer Review Policy
For Reviewers
Research Ethics Policy
Plagiarism
Informed Consent Policy
Conflict of Interest Policy
Open Access Policy
Corrections, Retractions and Expressions of Concern
Advertising Policy
Instructions for Authors
News
New IMPACT FACTOR
Volume 70 Authors' Index
Volume 70 Reviewers' Index
Dietary recommendations during the COVID-19 pandemic. Statement of the Committee of Human Nutrition Science of the Polish Academy of Sciences
Our new CiteScore2020 from SCOPUS
June 2021 Issue has just been published
September 2021 issue has just been released
Volume 71's Reviewers Index
Our new Impact Factor and Cite Score
Our new CiteScore2022 from SCOPUS
September 2023 issue has just been published
December 2023 issue has just been published
March 2024 issue has just been published
Volume 73's Reviewers Index
June 2024 issue has just been published
September 2024 issue has just been published
December 2024 issue is now available on-line
Editorial Policies
Peer Review Policy
For Reviewers
Research Ethics Policy
Plagiarism
Informed Consent Policy
Conflict of Interest Policy
Open Access Policy
Corrections, Retractions and Expressions of Concern
Advertising Policy
News
New IMPACT FACTOR
Volume 70 Authors' Index
Volume 70 Reviewers' Index
Dietary recommendations during the COVID-19 pandemic. Statement of the Committee of Human Nutrition Science of the Polish Academy of Sciences
Our new CiteScore2020 from SCOPUS
June 2021 Issue has just been published
September 2021 issue has just been released
Volume 71's Reviewers Index
Our new Impact Factor and Cite Score
Our new CiteScore2022 from SCOPUS
September 2023 issue has just been published
December 2023 issue has just been published
March 2024 issue has just been published
Volume 73's Reviewers Index
June 2024 issue has just been published
September 2024 issue has just been published
December 2024 issue is now available on-line
ORIGINAL ARTICLE
Characteristic and Antimicrobial Resistance of Bacillus cereus Group Isolated from Food in Poland
1
Laboratory of Food Microbiology, Department of Food Safety, National Institute of Public Health NIH - National Research Institute, 24 Chocimska str, 00-791 Warsaw, Poland
Submission date: 2022-05-11
Final revision date: 2022-07-21
Acceptance date: 2022-08-08
Online publication date: 2022-09-05
Publication date: 2022-09-05
Corresponding author
Joanna Kowalska
Department of Food Safety, National Institute of Public Health NIH - National Research Institute, Chocimska, 00-791, Warsaw, Poland
Department of Food Safety, National Institute of Public Health NIH - National Research Institute, Chocimska, 00-791, Warsaw, Poland
Pol. J. Food Nutr. Sci. 2022;72(3):297-304
KEYWORDS
TOPICS
ABSTRACT
Bacillus cereus is a foodborne pathogen causing food safety issues due to the formation of difficult to eliminate spores and biofilms. The objective of this study was to investigate the occurrence of B. cereus (conducted as part of monitoring in 2017-2018) and the presence of a toxin gene in strains isolated from retail products (pastries/cakes; vegetables, spices, delicatessen products) in Poland, and to determine the susceptibility of these microorganisms to different antimicrobial agents. A total of 267 B. cereus isolates from food products were examined, of which 95.51% were found positive for the presence of at least one toxin gene, with the highest frequency of the nhe gene (91.39%). The hbl and cytK genes were detected in 53.56% and 44.19% of B. cereus strains, respectively. The lowest frequency was found for the ces gene (2.62%). The susceptibility of B. cereus isolates to 16 antimicrobials was investigated. Ampicillin and penicillin resistance was the most common resistance phenotype and was identified in 100% of the B. cereus isolates. In addition, the tested isolates exhibited resistance to: amoxicillin-clavulanic acid (96.25%), cephalothin (67.79%), ceftriaxone (64.42%), rifampicin (46.82%), trimethoprim-sulfamethoxazole (5.62%), quinupristin/dalfopristin (4.87%), chloramphenicol (3.75%), clindamycin (2.62%), teicoplanin (1.87%), erythromycin (1.87%), ciprofloxacin (0.75%), imipenem (0.75%), tetracycline (0.37%), and gentamicin (0.37%). The study results contribute to characterizing the diversity of B. cereus isolated from various food products in Poland and their impact on food safety and public health. This study delivers practical information on antibiotic resistance and the frequency of toxin genes among strains isolated from food.
FUNDING
This work was supported financially by NIPH-NIH (1/ZŚ/2017; 1/ZŚ/2018; BŻ-5/2019; 1FBBW/2021).
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
REFERENCES (50)
1.
Abdeen, E.E., Hussien, H., Hadad, G.A.E., Mousa, W.S. (2020). Prevalence of virulence determinants among Bacillus cereus isolated from milk products with potential public health concern. Pakistan Journal of Biological Sciences: PJBS, 23(3), 206–212. https://doi.org/10.3923/pjbs.2....
2.
Amin, W.F. (2018). Occurrence of Bacillus cereus in some milk-based desserts. Assiut Veterinary Medical Journal, 64(156), 41–46. https://doi.org/10.21608/avmj.....
3.
Berthold, A., Doroszkiewicz, B. (2009). Characteristics of Bacillus cereus emetic toxin. Medycyna Weterynaryjna, 65(1), 15-19 (in Polish; English abstract).
4.
Berthold-Pluta, A., Pluta, A., Garbowska, M., Stefańska, I. (2019). Prevalence and toxicity characterization of Bacillus cereus in food products from Poland. Foods, 8(7), art. no. 269. https://doi.org/10.3390/foods8....
5.
Bianco, A., Capozzi, L., Monno, M.R., Del Sambro, L., Manzulli, V., Pesole, G., Loconsole, D., Parisi, A. (2021). Characterization of Bacillus cereus group isolates from human bacteremia by whole-genome sequencing. Frontiers in Microbiology, 11, art. no. 599524. https://doi.org/10.3389/fmicb.....
6.
Borge, G.I.A., Skeie, M., Sørhaug, T., Langsrud, T., Granum, P.E. (2001). Growth and toxin profiles of Bacillus cereus isolated from different food sources. International Journal of Food Microbiology, 69(3), 237–246. https://doi.org/10.1016/S0168-....
7.
Brillard, J., Dupont, C., Berge, O., Dargaignaratz, C., Oriol-Gagnier, S., Doussan, C., Broussolle, V., Gillon, M., Clavel, T., Berard, A. (2015). The water cycle, a potential source of the bacterial pathogen Bacillus cereus. BioMed Research International, 2015(SI), art. no. 356928. https://doi.org/10.1155/2015/3....
8.
Carlin, F., Fricker, M., Pielaat, A., Heisterkamp, S., Shaheen, R., Salonen, M.S., Svensson, B., Nguyen-The, C., Ehling-Schulz, M. (2006). Emetic toxin-producing strains of Bacillus cereus show distinct characteristics within the Bacillus cereus group. International Journal of Food Microbiology, 109(1–2), 132–138. https://doi.org/10.1016/j.ijfo....
9.
CLSI. (2012) Clinical and Laboratory Standards Institute Performance standards for antimicrobial susceptibility testing: twenty-second informational supplement M100-S22. Clinical and Laboratory Standards Institute, Wayne, PA, USA.
10.
De Medts, R., Kolwijck, E., Corsten, M.F., Gòraj, B., Schouten, J. (2018). Bacillus cereus bacteraemia and cerebral lesions in two patients with haematological malignancies. Netherlands Journal of Critical Care, 26(6), 230-233.
11.
Dietrich, R., Jessberger, N., Ehling-Schulz, M., Märtlbauer, E., Granum, P.E. (2021). The food poisoning toxins of Bacillus cereus. Toxins, 13(2), art. no. 98. https://doi.org/10.3390/toxins....
12.
Drobniewski, F.A. (1993). Bacillus cereus and related species. Clinical Microbiology Reviews, 6(4), 324–338. https://doi.org/10.1128/CMR.6.....
13.
EFSA Panel on Contaminants in the Food Chain. (2016). Scientific opinion on the risks for public health related to the presence of Bacillus cereus and other Bacillus spp. including Bacillus thuringiensis in foodstuffs. EFSA Journal, 14(7), art. no. e04524. https://doi.org/10.2903/j.efsa....
14.
Ehling-Schulz, M., Guinebretiere, M.-H., Monthán, A., Berge, O., Fricker, M., Svensson, B. (2006). Toxin gene profiling of enterotoxic and emetic Bacillus cereus. FEMS Microbiology Letters, 260(2), 232–240. https://doi.org/10.1111/j.1574....
15.
Ehling-Schulz, M., Lereclus, D., Koehler, T.M. (2019). The Bacillus cereus group: Bacillus species with pathogenic potential. Chapter 55, In: V.A. Fischetti, R.P. Novick, J.J. Ferretti, D.A. Portnoy, M. Braunstein, J.I. Rood (Eds). Gram-Positive Pathogens, 3rd edition, ASM Press, Washington, DC, USA, pp. 875–902. https://doi.org/10.1128/978168....
16.
Ehling-Schulz, M., Vukov, N., Schulz, A., Shaheen, R., Andersson, M., Märtlbauer, E., Scherer, S. (2005). Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Applied and Environmental Microbiology, 71(1), 105–113. https://doi.org/10.1128/AEM.71....
17.
Faille, C., Tauveron, G., Le Gentil-Lelièvre, C., Slomianny, C. (2007). Occurrence of Bacillus cereus spores with a damaged exosporium: consequences on the spore adhesion on surfaces of food processing lines. Journal of Food Protection, 70(10), 2346–2353. https://doi.org/10.4315/0362-0....
18.
Fiedler, G., Schneider, C., Igbinosa, E.O., Kabisch, J., Brinks, E., Becker, B., Stoll, D.A., Cho, G.-S., Huch, M., Franz, C.M.A.P. (2019). Antibiotics resistance and toxin profiles of Bacillus cereus-group isolates from fresh vegetables from German retail markets. BMC Microbiology, 19, art. no. 250. https://doi.org/10.1186/s12866....
19.
Gao, T., Ding, Y., Wu, Q., Wang, J., Zhang, J., Yu, S., Wu, H. (2018). Prevalence, virulence genes, antimicrobial susceptibility, and genetic diversity of Bacillus cereus isolated from pasteurized milk in China. Frontiers in Microbiology, 9, art. no. 533. https://doi.org/10.3389/fmicb.....
20.
Gdoura-Ben Amor, M., Siala, M., Zayani, M., Grosset, N., Smaoui, S., Messadi-Akrout, F., Baron, F., Jan, S., Gautier, M., Gdoura, R. (2018). Isolation, identification, prevalence, and genetic diversity of Bacillus cereus group bacteria from different foodstuffs in Tunisia. Frontiers in Microbiology, 9, art. no. 447. https://doi.org/10.3389/fmicb.....
21.
Glasset, B., Herbin, S., Guillier, L., Cadel-Six, S., Vignaud, M.-L., Grout, J., Pairaud, S., Michel, V., Hennekinne, J.-A., Ramarao, N., Brisabois, A. (2016). Bacillus cereus-induced food-borne outbreaks in France, 2007 to 2014: epidemiology and genetic characterisation. Eurosurveillance, 21(48), art. no. 30413. https://doi.org/10.2807/1560-7....
22.
Guinebretière, M.-H., Broussolle, V., Nguyen-The, Ch. (2002). Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. Journal of Clinical Microbiology, 40(8), 3053–3056. https://doi.org/10.1128/JCM.40....
23.
György, É., Laslo, É., Antal, M., András, C.D. (2021). Antibiotic resistance pattern of the allochthonous bacteria isolated from commercially available spices. Food Science Nutrition, 9(8), 4550-4560. https://doi.org/10.1002/fsn3.2....
24.
Hansen, B.M., Hendriksen, N.B. (2001). Detection of enterotoxic Bacillus cereus and Bacillus thuringiensis strains by PCR analysis. Applied and Environmental Microbiology, 67(1), 185–189. https://doi.org/10.1128/AEM.67....
25.
Hansen, B.M., Leser, T.D., Hendriksen, N.B. (2001). Polymerase chain reaction assay for the detection of Bacillus cereus group cells. FEMS Microbiology Letters, 202(2), 209–213. https://doi.org/10.1111/j.1574....
26.
Hardy, S.P., Lund, T., Granum, P.E. (2001). CytK toxin of Bacillus cereus forms pores in planar lipid bilayers and is cytotoxic to intestinal epithelia. FEMS Microbiology Letters, 197(1), 47–51. https://doi.org/10.1111/j.1574....
27.
Juneja, V.K., Golden, C.E., Mishra, A., Harrison, M.A., Mohr, T.B. (2019). Predictive model for growth of Bacillus cereus at temperatures applicable to cooling of cooked pasta. Journal of Food Science, 84(3), 590–598. https://doi.org/10.1111/1750-3....
28.
Kong, L., Yu, S., Yuan, X., Li, C., Yu, P., Wang, J., Guo, H., Wu, S., Ye. Q., Lei, T., Yang, X., Zhang, Y., Wei, X., Zeng, H., Zhang, J., Wu, Q., Ding, Y. (2021). An investigation on the occurrence and molecular characterization of Bacillus cereus in meat and meat products in China. Foodborne Pathogens and Disease, 18(5), 306-314. https://doi.org/10.1089/fpd.20....
29.
Li, D., Lin, R., Xu, Y., Chen, Q., Deng, F., Deng, Y., Wen, J. (2021). Cereulide exposure caused cytopathogenic damages of liver and kidney in mice. International Journal of Molecular Sciences, 22(17), art. no. 9148. https://doi.org/10.3390/ijms22....
30.
Lindbäck, T., Fagerlund, A., Rødland, M.S., Granum, P.E. (2004). Characterization of the Bacillus cereus Nhe enterotoxin. Microbiology, 150(12), 3959–3967. https://doi.org/10.1099/mic.0.....
31.
Marxen, S., Stark, T.D., Rütschle, A., Lücking, G., Frenzel, E., Scherer, S., Ehling-Schulz, M., Hofmann, T. (2015). Depsipeptide intermediates interrogate proposed biosynthesis of cereulide, the emetic toxin of Bacillus cereus. Scientific Reports, 5, art. no. 10637. https://doi.org/10.1038/srep10....
32.
Messelhäußer, U., Ehling-Schulz, M. (2018). Bacillus cereus — a multifaceted opportunistic pathogen. Current Clinical Microbiology Reports, 5, 120-125. https://doi.org/10.1007/s40588....
33.
N’guessan, E., Bakayoko, S., Cisse, M., Dalie, W., Sindic, M. (2019). Prevalence of Bacillus cereus and emetic strains detection from Ivory Coast local flours. Agronomie Africaine, 8(1), 151–159.
34.
Organji, S.R., Abulreesh, H.H., Elbanna, K., Osman, G.E.H., Khider, M. (2015). Occurrence and characterization of toxigenic Bacillus cereus in food and infant feces. Asian Pacific Journal of Tropical Biomedicine, 5(7), 515-520. https://doi.org/10.1016/j.apjt....
35.
Owusu-Kwarteng, J., Wuni, A., Akabanda, F., Tano-Debrah, K., Jespersen, L. (2017). Prevalence, virulence factor genes and antibiotic resistance of Bacillus cereus sensu lato isolated from dairy farms and traditional dairy products. BMC Microbiology, 17, art. no. 65. https://doi.org/10.1186/s12866....
36.
Park, K.M., Kim, H.J., Jeong, M., Koo, M. (2020). Enterotoxin genes, antibiotic susceptibility, and biofilm formation of low-temperature-tolerant Bacillus cereus isolated from green leaf lettuce in the cold chain. Foods, 9(3), art. no. 249. https://doi.org/10.3390/foods9....
37.
PN EN ISO 7932:2005 (2005). Food and feed microbiology - Horizontal method for the enumeration of presumptive Bacillus cereus - Colony enumeration method at 30oC.
38.
Priest, F.G., Kaji, D.A., Rosato, Y.B., Canhos, V.P. (1994). Characterization of Bacillus thuringiensis and related bacteria by ribosomal RNA gene restriction fragment length polymorphisms. Microbiology, 140(5), 1015–1022. https://doi.org/10.1099/135008....
39.
Proroga, Y.T.R., Capuano, F., Castellano, S., Giordano, A., Mancusi, A., Delibato, E., Dumontet, S., Pasquale, V. (2019). Occurrence and toxin gene profile of Bacillus cereus in dairy products. Journal of Microbiology, Biotechnology and Food Sciences, 9(1), 58–62. https://doi.org/10.15414/jmbfs....
40.
Rajkovic, A., Uyttendaele, M., Vermeulen, A., Andjelkovic, M., Fitz-James, I., In ‘t Veld, P., Denon, Q., Verhe, R., Debevere, J. (2008). Heat resistance of Bacillus cereus emetic toxin, cereulide. Letters in Applied Microbiology, 46(5), 536–541. https://doi.org/10.1111/j.1472....
41.
Raymond, B., Wyres, K.L., Sheppard, S.K., Ellis, R.J., Bonsall, M.B. (2010). Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field. PLoS Pathogens, 6(5), art. no. e1000905. https://doi.org/10.1371/journa....
42.
Ribeiro, R.L., Bastos, M.O., Blanz, A.M., da Rocha, J.A., de Oliveira Velasco, N.A., de Oliveira Marre, A.T., Martins, I.S. (2022). Subacute infective endocarditis caused by Bacillus cereus in a patient with Systemic Lupus Erythematosus. The Journal of Infection in Developing Countries, 16(4), 733-736. https://doi.org/10.3855/jidc.1....
43.
Rossi, G.A.M., Aguilar, C.E.G., Silva, H.O., Vidal, A.M.C. (2018). Bacillus cereus group: genetic aspects related to food safety and dairy processing. Arquivos Do Instituto Biológico, 85(1-7), art no. e0232017. https://doi.org/10.1590/1808-1....
44.
Rodrigo, D., Rosell, C.M., Martinez, A. (2021). Risk of Bacillus cereus in relation to rice and derivatives. Foods, 10(2), art. no. 302. https://doi.org/10.3390/foods1....
45.
Rouzeau-Szynalski, K., Stollewerk, K., Messelhaeusser, U., Ehling-Schulz, M. (2020). Why be serious about emetic Bacillus cereus: Cereulide production and industrial challenges. Food Microbiology, 85, art. no. 103279. https://doi.org/10.1016/j.fm.2....
46.
Schoeni, J.L., Lee Wong, A.C. (2005). Bacillus cereus food poisoning and its toxins. Journal of Food Protection, 68(3), 636–648. https://doi.org/10.4315/0362-0....
47.
Shah, M.M., Miringu, G., Wada, A., Kaneko, S., Ichinose, Y. (2019). Case report: Bacillus pumilus–caused bacteremia in a patient with food poisoning. The American Journal of Tropical Medicine and Hygiene, 100(3), 688-690. https://doi.org/10.4269/ajtmh.....
48.
Yibar, A., Cetinkaya, F., Soyutemiz, E., Yaman, G. (2017). Prevalence, enterotoxin production and antibiotic resistance of Bacillus cereus isolated from milk and cheese. Kafkas Universitesi Veteriner Fakultesi Dergisi Journal, 23(4), 635-642. https://doi.org/10.9775/kvfd.2....
49.
Yu, S., Yu, P., Wang, J., Li, C., Guo, H., Liu, C., Kong, L., Yu, L., Wu, S., Lei, T., Chen, M., Zeng, H., Pang, R., Zhang, Y., Wei, X., Zhang, J., Wu, Q., Ding, Y. (2020). A study on prevalence and characterization of Bacillus cereus in ready-to-eat foods in China. Frontiers in Microbiology, 10, art. no. 3043. https://doi.org/10.3389/fmicb.....
50.
Zhao, S., Chen, J., Fei, P., Feng, H., Wang, Y., Ali, M.A., Li, S., Jing, H., Yang, W. (2020). Prevalence, molecular characterization, and antibiotic susceptibility of Bacillus cereus isolated from dairy products in China. Journal of Dairy Science, 103(5), 3994–4001. https://doi.org/10.3168/jds.20....
CITATIONS (4):
1.
Characterization of Antioxidant and Antimicrobial Activity and Phenolic Compound Profile of Extracts from Seeds of Different Vitis Species
Luisa Pozzo, Teresa Grande, Andrea Raffaelli, Vincenzo Longo, Stanisław Weidner, Ryszard Amarowicz, Magdalena Karamać
Molecules
Luisa Pozzo, Teresa Grande, Andrea Raffaelli, Vincenzo Longo, Stanisław Weidner, Ryszard Amarowicz, Magdalena Karamać
Molecules
2.
Prevalence and genomic characterization of the Bacillus cereus group strains contamination in food products in Southern China
Zhiwei Zheng, Lianwei Ye, Wenguang Xiong, Qiao Hu, Kaichao Chen, Ruanyang Sun, Sheng Chen
Science of The Total Environment
Zhiwei Zheng, Lianwei Ye, Wenguang Xiong, Qiao Hu, Kaichao Chen, Ruanyang Sun, Sheng Chen
Science of The Total Environment
3.
Characterization of the Bacillus cereus Group Isolated from Ready-to-Eat Foods in Poland by Whole-Genome Sequencing
Joanna Kowalska, Elżbieta Maćkiw, Dorota Korsak, Jacek Postupolski
Foods
Joanna Kowalska, Elżbieta Maćkiw, Dorota Korsak, Jacek Postupolski
Foods
4.
Organic vs. Conventional Milk: Uncovering the Link to Antibiotic Resistance in Bacillus cereus sensu lato
Marek Bartoszewicz, Urszula Czyżewska, Monika Zambrzycka, Izabela Święcicka
International Journal of Molecular Sciences
Marek Bartoszewicz, Urszula Czyżewska, Monika Zambrzycka, Izabela Święcicka
International Journal of Molecular Sciences
Share
RELATED ARTICLE
| eISSN: | 2083-6007 |
| ISSN: | 1230-0322 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
