Profiling of Bacillus cereus enterotoxigenic genes from retailed foods and detection of the nhe and hbl toxins with immunological assay
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Abstract
Bacillus cereus produces pore-forming toxins responsible for diarrhoea; therefore, rapidly detecting these toxins in food retailed for consumption is needed. The genomic DNA of 100 B. cereus isolates recovered from some retailed foods was extracted and used as a template for enterotoxin detection. The detection of genes of non-haemolyticnonhemolytic enterotoxin (nheA, nheB, nheC), hemolysin BL (hblA, hblC, hblD), entFM, cytK and bceT by the isolates was carried out with PCR using primers specific for the targeted genes, while the production of Nhe and Hbl enterotoxins in fifty of the randomly chosen isolates was detected with a Duopath Cereus Enterotoxin kit. Ninety-five percent of the isolates carried one or more components of the NHE complex, while 56% had one or more components of HBL. Sixteen out of the 100 isolates carried all the genes for NHE and HBL complex genes. The entFM, cytK and bceT genes were detected in 85%, 74% and 60% of B. cereus isolates, respectively. Starchy foods had the highest incidence of the HBL complex, while nheA and nheC occurred mostly in protein foods with 90% and 87% incidence, respectively. The immunological kit was able to detect the production of nonhemolytic enterotoxin (Nhe) in all the B. cereus isolates, while 28 B. cereus isolates produced hemolysin (hbl). Nineteen isolates that carried one or more genes encoding hbl did not produce the toxin. This study clearly showed that retailed foods sold in Ogun State, Nigeria, harbor B. cereus enterotoxigenic genes responsible for diarrhoea. These toxins can be rapidly detected in foods using both molecular and immunological methods.
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Keywords
B. cereus, Duopath cereus kit, Enterotoxins, hbl, nhe, PCR, Retailed foods
References
Abfalter, C.M., Schönauer, E., Ponnuraj, K., Huemer, M., Gadermaier, G., Regl, C., Briza, P., Ferreira, F., Huber, C.G., Brandstetter, H., Posselt, G. & Wessler, S. (2016). Cloning, purification and characterization of the collagenase ColA expressed by Bacillus cereus ATCC 14579. PloS one 2016, 11(9): e0162433. https://doi.org/10.1371/journal.pone.0162433
Adeleke, B.S., Ayangbenro, A.S. & Babalola, O.O. (2021). Genomic Analysis of Endophytic Bacillus cereus T4S and Its Plant Growth-Promoting Traits. Plants, 10(9), 1776. https://doi.org/10.3390/plants10091776.
Adesetan, T.O., Efuntoye, M.O. & Babalola, O.O. (2019). Biochemical characterization and antimicrobial susceptibility of Bacillus cereus isolates from some retailed foods in Ogun State, Nigeria. Journal of Microbiology, Biotechnology and Food Science, 9(3), 616-621. https://doi.org/10.15 414/jmbfs.2019/20.9.3.616-621.
Adesetan, T.O., Efuntoye, M.O. & Babalola, O.O. (2020). Genotypic Profiling of Bacillus cereus recovered from some retail foods in Ogun State, Nigeria and their Phylogenetic Relationship. International Journal of Microbiology 2020 (3):1-9. https://doi.org/10.1155/2020/3750948
Ankolekar, C., Rahmati, T. & Labbé, R. G. (2009). Detection of toxigenic Bacillus cereus and Bacillus thuringiensis spores in U.S. rice. International Journal of Food Microbiology, 128(3), 460-466. https://doi.org/10.1016/j.ijfoodmicro.2008.10.006
Asano, S-I., Nukumizu, Y., Bando, H., Iizuka, T. & Yamamoto, T. (1997). Cloning of novel enterotoxin genes from Bacillus cereus and Bacillus thuringiensis. Applied and Environmental Microbiology, 63(3), 1054-1057. https://doi.org/10.1128/AEM.63.3.1054-1057.1997
Ayangbenro, A.S. & Babalola, O. O. (2020). Genomic analysis of Bacillus cereusNWUAB01 and its heavy metal removal from polluted soil. Scientific Reports 10:19660. https://doi.org/10.1038/s41598-020-75170-x
Babalola, O.O., Aremu, B.R. & Ayangbenro, A. (2019). Draft genome sequence of heavy metal resistant Bacillus cereus NWUAB01. Microbiology Resource Announcements, 8(7), e01706-18. https://doi.org/10.1128/MRA.0 1706-18
Babalola, O. O., Adeleke, S.A. & Ayangbenro, A.S. (2021). Whole Genome Sequencing of Sunflower Root-Associated Bacillus cereus. Evolutionary Bioinformatics, 17: 1–6. https://doi.org/10.1177/11769343 211038948
Beecher, D. J. & Wong, A.C. (1994). Identification and analysis of the antigens detected by two commercial Bacillus cereus diarrheal enterotoxin immunoassay kits. Applied and Environmental Microbiology, 60(12), 4614-4616. https://doi.org/10.1128/aem.60.12.4614-4616.1994
Beecher, D. J., Schoeni, J. L. & Wong, A.C. (1995). Enterotoxic activity of hemolysin BL from Bacillus cereus. Infection and Immunity, 63(11), 4423-4428. https://doi.org/10.1128/IAI.63.11.4423-4428.1995
Boonchai, N., Asano, S.I., Bando, H. & Wiwat, C. (2008). Study on cytotoxicity and nucleotide sequences of enterotoxin FM of Bacillus cereus isolated from various food sources. Journal of the Medical Association of Thailand 91,1425-1432.
Cadot, C., Tran, S-L., Vignaud, M. L., De Buyser, M. L., Kolstø, A. B., Brisabois, A., Leredus, D., Guinebretiere, M.H. & Ramarao, N. (2010). InhA1, NprA, and HlyII as candidates for markers to differentiate pathogenic from nonpathogenic Bacillus cereus strains. Journal of Clinical Microbiology, 48(4), 1358-1365. https://doi.org/10.1128/JCM.02123-09
Carroll, L.M., Wiedmann, M., Mukherjee, M., Nicholas, D.C., Mingle, L.A., Dumas, N.B., Cole, J.A. & Kovac, J. (2019). Characterization of Emetic and Diarrheal Bacillus cereus Strains From a 2016 Foodborne Outbreak Using Whole-Genome Sequencing: Addressing the Microbiological, Epidemiological, and Bioinformatic Challenges. Frontiers in Microbiology 10:144. https://doi.org/10.3389/fmicb.2019.00144.
Chen, D., Li, Y., Lv, J., Liu, X., Gao, P., Zhen, G., Zhang, W., Wu, D., Jing, H., Li, Y., Zhao, Y., Ma, X., Ma, H. & Zhang, L. (2019). A foodborne outbreak of gastroenteritis caused by Norovirus and Bacillus cereus at a university in the Shunyi District of Beijing, China 2018: a retrospective cohort study. BMC Infectious Diseases, 19:910 https://doi.org/10.1186/s12879-019-4570-6.
Das, S., Surendran, P.K. & Thampuran, N. (2009). PCR-based detection of enterotoxigenic isolates of Bacillus cereus from tropical seafood. Indian Journal of Medical Research, 129, 316 - 320.
Delbrassine, L., Bottledoorn, N., Andjelkovic, M., Dierick, K. & Denayer, S. (2015). An Emetic Bacillus cereus outbreak in a Kindergarten: detection and quantification of critical levels of cereulide toxin. Foodborne Pathogens and Diseases, 12(1), 84 - 87. https://doi.org/10.1089/fdp.2014.1788
Dierick, K., Van Coillie, E., Swiecicka, I., Meyfroidt, G., Devlieger, H., Meulemans, A., Hoedemaekers, G., Fourie, L., Heyndrickx, M. & Mahillon, J. (2005). Fatal family outbreak of Bacillus cereus-associated food poisoning. Journal of Clinical Microbiology, 43(8), 4277-4279. https://doi.org/10.1128/JCM.43.8.4277-4279.2005
Dietrich, R., Moravek, M., Bürk, C., Granum, P. E. & Märtlbauer, E. (2005). Production and characterization of antibodies against each of the three subunits of the Bacillus cereus nonhemolytic enterotoxin complex. Applied and Environmental Microbiology, 71(12), 8214-8220. https://doi.org/10.1128/AEM.71.12.8214-8220.2005
EFSA (2005). Bacillus cereus and other Bacillus spp. in foodstuffs. EFSA Journal, 175, 1-48.
Ehling-Schulz, M., Fricker, M. & Scherer, S. (2004). Bacillus cereus, the causative agent of an emetic type of food-borne illness. Molecular Nutrition and Food Research, 48(7), 479-487.
Ehling-Schulz, M., Svensson, B., Guinebretiere, M. H, Lindbäck, T., Andersson, M., Schulz, A., Fricker, M., Christiansson, A., Granum, P.E. & Märtlbauer, E. (2005). Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains.
Microbiology, 151(1), 183-197. https://doi.org/10.1099/mic.0.27607-0
Ehling-Schulz, M., Fricker, M., Grallert, H., Rieck, P., Wagner, M. & Scherer, S. (2006). Cereulide synthetase gene cluster from emetic Bacillus cereus: structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1. BMC Microbiology, 6(1), 20. https://doi.org/10.1186/1471-2180-6-20
Ehling-Schulz, M., Lereclus, D. & Koehler, T.M. (2019). The Bacillus cereus group: Bacillus species with pathogenic potential. Microbiol. Spectr., 7(3),10. https://doi.org/10.1128/microbiolspec.GPP3-0032-2018
Frentzel, H., Kraushaar, B., Krause, G., Bodi, D., Wichmann-Schauer, H., Appel, B. & Mader, A. (2018). Phylogenetic and toxinogenic characteristics of Bacillus cereus group members isolated from spices and herbs. Food Control 83: 90–98. http://dx.doi.org/10.1016/j.foodc ont.20 16.12.022.
Gao, T., Ding, Y., Wu, Q., Wang, J., Zhang, J., Yu, S., Yu, P., Liu, C., Kong, L., Feng, Z., Chen, M., Wu, S., Zeng, H. & Wu, H. (2018). Prevalence, Virulence Genes, Antimicrobial Susceptibility, and Genetic Diversity of Bacillus cereus Isolated from Pasteurized Milk in China. Front. Microbiol. 9:533. doi: 10.3389/fmicb.2018.00533
Gdoura-Ben Amor, M., Jan, S., Baron, F., Grosset, N., Culot, A., Gdoura, R., Gautier, M. & Techer, C. (2019). Toxigenic potential and antimicrobial susceptibility of Bacillus cereus group bacteria isolated from Tunisian foodstuffs. BMC Microbiology 19:196. https://doi.org/10.1186/s12866-019-1571-y
Ghelardi, E., Celandroni, F., Salvetti, S., Barsotti, C., Baggiani, A. & Senesi, S. (2002).Identification and characterization of toxigenic Bacillus cereus isolates responsible for two food poisoning outbreaks. FEMS Microbiology Letters, 208, 129 - 134. https://doi.org/10.1111/j.1574-6968.20 02.tb11072.x
Granum, P. E., O’Sullivan, K. & Lund. T. (1999). The sequence of the nonhemoytic enterotoxin operon from Bacillus cereus. FEMS Microbiology Letters, 177: 225 -229 https://doi.org/10.1111/j.1574-6968.1999.tb13736.x
Guinebretière, M-H., Broussolle, V. & Nguyen-The, C. (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.40.8.3053-3056.2002
Guinebretière, M. H., Velge, P., Couvert, O., Carlin, F. & Debuyser, M-L. (2010). Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (groups I to VII) rather than species affiliation. Journal of Clinical Microbiology, 48(9), 3388-3391. https://doi.org/10.1128/JCM.00921-10
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/10.10.1128/AEM.67.1.185-189.2001
Heini, N., Stephan, R. & Johler, S. (2018). Toxin genes and cytotoxicity levels detected in Bacillus cereus isolates collected from cooked food products delivered by Swiss Army catering facilities. Italian Journal of Food Safety, 7:7323. https://doi.org/10.4081/ijfs.2018.7323.
Hoppe, I.J., Brandstetter, H. and Schonauer, E. (2021). Biochemical characterization of a collagenase from Bacillus cereus strain Q1. Scientific Reports, 11:4187. https://doi.rg/10.1038/s41598-021-83744-6
Hwang, J-Y & Park, J-H (2015). Characteristics of enterotoxin distribution, haemolysis, lecithinase, and starch hydrolysis of Bacillus cereus isolated from infant formulas and ready-to-eat foods. J. Dairy Sci. 98, 1–9. https://doi.org/10.3168/jds.2014-9042
Keisam, S., Tuikhar, N., Ahmed, G. & Jeyaram, K. (2019). Toxigenic and pathogenic Potential of enteric bacterial pathogens prevalent in the traditional fermented foods marketed in the Northeast region of India. International Journal of Food Microbiology, 296: 21-30. https://doi.org/10.1016/j.ijfoodmicro.2019.02.012.
Kotiranta, A., Lounatmaa, K. & Haapasalo, M. (2000). Epidemiology and pathogenesis of Bacillus cereus infections. Microbes and Infection, 2(2), 189-198. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.10.008
Krause, N., Moravek, M., Dietrich, R., Wehrle, E., Slaghuis, J. & Märtlbauer, E. (2010).Performance characteristics of the Duopath Cereus Enterotoxins assay for rapid detection of enterotoxinogenic Bacillus cereus strains. International Journal of Food Microbiology, 144(2), 322-326. http://doi.org/10.1016/j.ijfoodmicr o.2010.10.008.
Lapidus, A., Goltsman, E., Auger, S., Galleron, N., Ségurens, B., Dossat, C., Land, M., Broussolle, V., Brillard, J., Guinebretiere, M.H., Sanchis, V., Nguyen - The, C., Leredus, D., Richardson, P., Wincker, P., Weissenbach, J., Ehrlich, S.D. & Sorokin, A. (2008). Extending the Bacillus cereus group genomics to putative food-borne pathogens of different toxicity. Chemico-Biological Interactions, 171(2), 236-249. https://doi.org/10.1016/j.cbi.2007.03.003
Li, F., Zuo, S., Yu, P., Zhou, B., Wang, L., Liu, C., Wei, H. & Xu, H. (2016). Distribution and expression of the enterotoxin genes of Bacillus cereus in food products from Jiangxi Province, China. Food Control 67: 155-162. http://dx.doi.org/10.1016/j.foodcont.2016.02.049.
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.0.27359-0
López, A. C., Minnaard, J., Pérez, P. F. & Alippi, A. M. (2015). A case of intoxication due to a highly cytotoxic Bacillus cereus strain isolated from cooked chicken. Food Microbiology, 46, 195-199. https://doi.org/10.1016/j.fm.2014.08.005
Lund, T., De Buyser, M-L. & Granum, P. E. (2000). A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Molecular Microbiology, 38(2), 254-261. https://doi.org/10.1046/j.1365-2958.2000.02147.x
Martinelli, D., Fortunato, F., Tafuri, S., Cozza, V., Chironna, M., Germinario, C., Pedalino, B. & Prato, R. (2013). Lessons from a birthday party: a Bacillus cereus outbreak, Bari, Italy, January 2012. Ann 1st Super Sanita 49 (4), 391 -394. https://doi.org/10.4415/ANN_13_04_12
Mantynen, V. & Lindstorm, K. (1998). A rapid PCR-based DNA test for enterotoxic Bacillus cereus. Applied Environmental Microbiology 64, 1634–1639. https://doi.org/1 0.1128/AEM.64.5.1634-1639.18
Moravek, M., Dietrich, R., Buerk, C., Broussolle, V., Guinebretiere, M. H., Granum, P. E., Nguyen – The, C. & Martlbauer, E. (2006). Determination of the toxic potential of Bacillus cereus isolates by quantitative enterotoxin analyses. FEMS Microbiology Letters, 257, 293–298. https://doi.org/10.1111/j.1574-6968.200 6.00185.x
Naranjo, M., Denayer, S., Bottledorm, N., Delbrassinne, L., Veys, J., Waegenaere, J., Sirtaine, N., Driesen, R.B., Sipido, K.R., Mahillon, J. & Dierick, K. (2011). SuddenDeath of a Young Adult Associated with Bacillus cereus Food Poisoning. Journal of Clinical Microbiology, 49(12), 4379 - 4381. https://doi.org/10.1128/JCM.05129-11
Ngamwongsatit, P., Buasri, W., Piamariyanon, P., Pulsrikam, C., Ohba, M. & Assavanig,A. (2008). Broad distribution of enterotoxin genes (hbl CA, nhe ABC, cyt K and ent FM) among Bacillus cereus as shown by novel primers. International Journal of Food Microbiology, 121, 352-356. https://doi.org/10.1016/j.ijfoodmicro.2007.11.013
Oda, M., Takahashi, M., Matsuno, T., Uoo, K., Nagahama, M. & Sakurai, J. (2010). Hemolysis induced by Bacillus cereus sphingomyelinase. Biochimica et Biophysica Acta 1798, 1073–1080. https://doi.org/10.1016/j.bbame m.2010.03.004
Oltuszak-Walczak, E. & Walczak, P. (2007). PCR-Based DNA tests for detection of Emetic Bacillus cereus strains producing cereulide. Polish Journal of Food and Nutrition Sciences, 57(3A), 101- 105.
Ouoba, L.I.I., Thorsen, L. & Varnam, A.H. (2008). Enterotoxins and emetic toxins production by Bacillus cereus and other species of Bacillus isolated from Soumbala and Bikalga, African alkaline fermented food condiments. International Journal of Food Microbiology 124, 224-230. https://doi.org/10.1016/j.ijfoodmicro.2008.03.026
Powell, D. (2015). 44 kids sickened: Ottawa Chinese food takeout fined in summer camp food poisoning. Available at www.barflog./2014/08/44-kids-sickened-ottawa-chinese food. Retrieved on 15th June 2016.
Rahmati, T. & Labbe, R. (2008). Levels and toxigenicity of Bacillus cereus and Clostridium perfringens from retail seafood. Journal of Food Protection 71,1178-1185. https://doi.org/10.4315/0362-028x-71.6.1178
Ranjbar, R. & Shahreza, M.H.S. (2017). Prevalence, antibiotic-resistance properties and enterotoxin gene profile of Bacillus cereus strains isolated from milk-based baby foods. Tropical Journal of Pharmaceutical Research, 16 (8): 1931-1937. http://dx.doi.org/10.4314/tjpr.v16i8.25.
Rosenquist, H., Smidt, L., Andersen, S.R., Jensen, G.B. & Wilcks, A. (2005). Occurrence and significance of Bacillus cereus and Bacillus thuringiensis in ready-to-eat food. FEMS Microbiology Letters, 250, 129-136. https://doi.org/10.1016/j.femsle.2005.06.054
Ryan, P. A., Macmillan, J.D. & Zilinskas, B.A. (1997). Molecular cloning and characterization of the genes encoding the L1 and L2 components hemolysin BL from Bacillus cereus. Journal of Bacteriology, 179, 2551 - 2556. https://doi.org/10.1128/jb.179.8.2551-2556.1997
Sastalla, I., Fattah, R., Coppage, N., Nandy, P., Crown, D., Pomerantsev, A. P. & Leppla, S. H. (2013). The Bacillus cereus Hbl and Nhe tripartite enterotoxin components assemble sequentially on the surface of target cells and are not interchangeable. PloS one, 8(10), e76955. https://doi.org/10.1371/journal.pon e.0076955
Scallan, E., Griffin, P.M., Angulo, F.J., Tauxe, R.V. & Hoekstra, R.M. (2011). Foodborne illness acquired in the United States–unspecified agents. Emerging Infectious Diseases. 17 (1), 16–22. https://doi.org/10.3201/eid170 1.091101p2
Schoeni, J. L. & Wong, A.C.L. (2005). Bacillus cereus food poisoning and its toxins. Journal of Food Protection, 68(3), 636-648. https://doi.org/10.4315/0362-028x-68.3.6 36
Schreiber, N., Hackl, G., Reisinger, A.C., Zollner-Schwetz, I., Eller, K., Schlagenhaufen, C., Pietzka, A., Czerwenka, C., Stark, T.D., Kranzler, M., Fickert, P., Eller, P. & Ehling-Schulz, M. (2022). Acute Liver Failure after Ingestion of Fried Rice Balls: A Case Series of Bacillus cereus Food Poisonings. Toxins 14, 12. https://doi.org/10.3390/ toxins14010012.
Senesi, S. & Ghelardi, E. (2010). Production, secretion and biological activity of Bacillus cereus enterotoxins. Toxins, 2(7), 1690-1703. https://doi.org/10.3390/toxins 2071690
Senesi, S., Salvetti, S., Celandroni, F. & Ghelardi, E. (2010). Features of Bacillus cereus swarm cells. Research in Microbiology, 161(9), 743-749. https://doi.org/10.1016/j.resmic.2010.10.007
Stensfor Arnesen, L. P., Fagerlund, A. & Granum, P. E. (2008). From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiology Reviews, 32(4), 579-606. https://doi.org/10.1111/j.1574-6976.2008.00112.x
Thirkell, C.E., Sloan-Gardner, T.S., Kaczmarek, M.C. and Polkinghorne, B. (2019). An outbreak of Bacillus cereus toxin-mediated emetic and diarrhoeal syndromes at a restaurant in Canberra, Australia 2018. Communicable Diseases Intelligence 43, 10. https://doi.org/10.33321/cdi.2019.43.40
Turnbull, P.C.B., Jackson, P. J., Hill, K. K., Keim, P., Kolstø, A.B. & Beecher, D. J. (2002). Longstanding Taxonomic Enigmas within the ‘Bacillus cereus group’ are on the Verge of being Resolved by Far‒reaching Molecular Developments: forecasts on the possible outcome by an ad hoc team. Applications and Systematics of Bacillus and Relatives, 23-36. https://doi.org/10.1002/97804706 9674 3.ch3
Yang, I.C., Shih, D.Y., Wang, J.Y. & Pani, T.M. (2007). Development of rapid real-time PCR and most-probable-number real-time PCR assays to quantify enterotoxigenic strains of the species in the Bacillus cereus group. Journal of Food Protection, 70, 2774–2781. https://doi.org/10.431 5/0362-028x-70.12.2774
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, 10:3043. doi: 10.3389/fmicb.2019.03043.
Adeleke, B.S., Ayangbenro, A.S. & Babalola, O.O. (2021). Genomic Analysis of Endophytic Bacillus cereus T4S and Its Plant Growth-Promoting Traits. Plants, 10(9), 1776. https://doi.org/10.3390/plants10091776.
Adesetan, T.O., Efuntoye, M.O. & Babalola, O.O. (2019). Biochemical characterization and antimicrobial susceptibility of Bacillus cereus isolates from some retailed foods in Ogun State, Nigeria. Journal of Microbiology, Biotechnology and Food Science, 9(3), 616-621. https://doi.org/10.15 414/jmbfs.2019/20.9.3.616-621.
Adesetan, T.O., Efuntoye, M.O. & Babalola, O.O. (2020). Genotypic Profiling of Bacillus cereus recovered from some retail foods in Ogun State, Nigeria and their Phylogenetic Relationship. International Journal of Microbiology 2020 (3):1-9. https://doi.org/10.1155/2020/3750948
Ankolekar, C., Rahmati, T. & Labbé, R. G. (2009). Detection of toxigenic Bacillus cereus and Bacillus thuringiensis spores in U.S. rice. International Journal of Food Microbiology, 128(3), 460-466. https://doi.org/10.1016/j.ijfoodmicro.2008.10.006
Asano, S-I., Nukumizu, Y., Bando, H., Iizuka, T. & Yamamoto, T. (1997). Cloning of novel enterotoxin genes from Bacillus cereus and Bacillus thuringiensis. Applied and Environmental Microbiology, 63(3), 1054-1057. https://doi.org/10.1128/AEM.63.3.1054-1057.1997
Ayangbenro, A.S. & Babalola, O. O. (2020). Genomic analysis of Bacillus cereusNWUAB01 and its heavy metal removal from polluted soil. Scientific Reports 10:19660. https://doi.org/10.1038/s41598-020-75170-x
Babalola, O.O., Aremu, B.R. & Ayangbenro, A. (2019). Draft genome sequence of heavy metal resistant Bacillus cereus NWUAB01. Microbiology Resource Announcements, 8(7), e01706-18. https://doi.org/10.1128/MRA.0 1706-18
Babalola, O. O., Adeleke, S.A. & Ayangbenro, A.S. (2021). Whole Genome Sequencing of Sunflower Root-Associated Bacillus cereus. Evolutionary Bioinformatics, 17: 1–6. https://doi.org/10.1177/11769343 211038948
Beecher, D. J. & Wong, A.C. (1994). Identification and analysis of the antigens detected by two commercial Bacillus cereus diarrheal enterotoxin immunoassay kits. Applied and Environmental Microbiology, 60(12), 4614-4616. https://doi.org/10.1128/aem.60.12.4614-4616.1994
Beecher, D. J., Schoeni, J. L. & Wong, A.C. (1995). Enterotoxic activity of hemolysin BL from Bacillus cereus. Infection and Immunity, 63(11), 4423-4428. https://doi.org/10.1128/IAI.63.11.4423-4428.1995
Boonchai, N., Asano, S.I., Bando, H. & Wiwat, C. (2008). Study on cytotoxicity and nucleotide sequences of enterotoxin FM of Bacillus cereus isolated from various food sources. Journal of the Medical Association of Thailand 91,1425-1432.
Cadot, C., Tran, S-L., Vignaud, M. L., De Buyser, M. L., Kolstø, A. B., Brisabois, A., Leredus, D., Guinebretiere, M.H. & Ramarao, N. (2010). InhA1, NprA, and HlyII as candidates for markers to differentiate pathogenic from nonpathogenic Bacillus cereus strains. Journal of Clinical Microbiology, 48(4), 1358-1365. https://doi.org/10.1128/JCM.02123-09
Carroll, L.M., Wiedmann, M., Mukherjee, M., Nicholas, D.C., Mingle, L.A., Dumas, N.B., Cole, J.A. & Kovac, J. (2019). Characterization of Emetic and Diarrheal Bacillus cereus Strains From a 2016 Foodborne Outbreak Using Whole-Genome Sequencing: Addressing the Microbiological, Epidemiological, and Bioinformatic Challenges. Frontiers in Microbiology 10:144. https://doi.org/10.3389/fmicb.2019.00144.
Chen, D., Li, Y., Lv, J., Liu, X., Gao, P., Zhen, G., Zhang, W., Wu, D., Jing, H., Li, Y., Zhao, Y., Ma, X., Ma, H. & Zhang, L. (2019). A foodborne outbreak of gastroenteritis caused by Norovirus and Bacillus cereus at a university in the Shunyi District of Beijing, China 2018: a retrospective cohort study. BMC Infectious Diseases, 19:910 https://doi.org/10.1186/s12879-019-4570-6.
Das, S., Surendran, P.K. & Thampuran, N. (2009). PCR-based detection of enterotoxigenic isolates of Bacillus cereus from tropical seafood. Indian Journal of Medical Research, 129, 316 - 320.
Delbrassine, L., Bottledoorn, N., Andjelkovic, M., Dierick, K. & Denayer, S. (2015). An Emetic Bacillus cereus outbreak in a Kindergarten: detection and quantification of critical levels of cereulide toxin. Foodborne Pathogens and Diseases, 12(1), 84 - 87. https://doi.org/10.1089/fdp.2014.1788
Dierick, K., Van Coillie, E., Swiecicka, I., Meyfroidt, G., Devlieger, H., Meulemans, A., Hoedemaekers, G., Fourie, L., Heyndrickx, M. & Mahillon, J. (2005). Fatal family outbreak of Bacillus cereus-associated food poisoning. Journal of Clinical Microbiology, 43(8), 4277-4279. https://doi.org/10.1128/JCM.43.8.4277-4279.2005
Dietrich, R., Moravek, M., Bürk, C., Granum, P. E. & Märtlbauer, E. (2005). Production and characterization of antibodies against each of the three subunits of the Bacillus cereus nonhemolytic enterotoxin complex. Applied and Environmental Microbiology, 71(12), 8214-8220. https://doi.org/10.1128/AEM.71.12.8214-8220.2005
EFSA (2005). Bacillus cereus and other Bacillus spp. in foodstuffs. EFSA Journal, 175, 1-48.
Ehling-Schulz, M., Fricker, M. & Scherer, S. (2004). Bacillus cereus, the causative agent of an emetic type of food-borne illness. Molecular Nutrition and Food Research, 48(7), 479-487.
Ehling-Schulz, M., Svensson, B., Guinebretiere, M. H, Lindbäck, T., Andersson, M., Schulz, A., Fricker, M., Christiansson, A., Granum, P.E. & Märtlbauer, E. (2005). Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains.
Microbiology, 151(1), 183-197. https://doi.org/10.1099/mic.0.27607-0
Ehling-Schulz, M., Fricker, M., Grallert, H., Rieck, P., Wagner, M. & Scherer, S. (2006). Cereulide synthetase gene cluster from emetic Bacillus cereus: structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1. BMC Microbiology, 6(1), 20. https://doi.org/10.1186/1471-2180-6-20
Ehling-Schulz, M., Lereclus, D. & Koehler, T.M. (2019). The Bacillus cereus group: Bacillus species with pathogenic potential. Microbiol. Spectr., 7(3),10. https://doi.org/10.1128/microbiolspec.GPP3-0032-2018
Frentzel, H., Kraushaar, B., Krause, G., Bodi, D., Wichmann-Schauer, H., Appel, B. & Mader, A. (2018). Phylogenetic and toxinogenic characteristics of Bacillus cereus group members isolated from spices and herbs. Food Control 83: 90–98. http://dx.doi.org/10.1016/j.foodc ont.20 16.12.022.
Gao, T., Ding, Y., Wu, Q., Wang, J., Zhang, J., Yu, S., Yu, P., Liu, C., Kong, L., Feng, Z., Chen, M., Wu, S., Zeng, H. & Wu, H. (2018). Prevalence, Virulence Genes, Antimicrobial Susceptibility, and Genetic Diversity of Bacillus cereus Isolated from Pasteurized Milk in China. Front. Microbiol. 9:533. doi: 10.3389/fmicb.2018.00533
Gdoura-Ben Amor, M., Jan, S., Baron, F., Grosset, N., Culot, A., Gdoura, R., Gautier, M. & Techer, C. (2019). Toxigenic potential and antimicrobial susceptibility of Bacillus cereus group bacteria isolated from Tunisian foodstuffs. BMC Microbiology 19:196. https://doi.org/10.1186/s12866-019-1571-y
Ghelardi, E., Celandroni, F., Salvetti, S., Barsotti, C., Baggiani, A. & Senesi, S. (2002).Identification and characterization of toxigenic Bacillus cereus isolates responsible for two food poisoning outbreaks. FEMS Microbiology Letters, 208, 129 - 134. https://doi.org/10.1111/j.1574-6968.20 02.tb11072.x
Granum, P. E., O’Sullivan, K. & Lund. T. (1999). The sequence of the nonhemoytic enterotoxin operon from Bacillus cereus. FEMS Microbiology Letters, 177: 225 -229 https://doi.org/10.1111/j.1574-6968.1999.tb13736.x
Guinebretière, M-H., Broussolle, V. & Nguyen-The, C. (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.40.8.3053-3056.2002
Guinebretière, M. H., Velge, P., Couvert, O., Carlin, F. & Debuyser, M-L. (2010). Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (groups I to VII) rather than species affiliation. Journal of Clinical Microbiology, 48(9), 3388-3391. https://doi.org/10.1128/JCM.00921-10
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/10.10.1128/AEM.67.1.185-189.2001
Heini, N., Stephan, R. & Johler, S. (2018). Toxin genes and cytotoxicity levels detected in Bacillus cereus isolates collected from cooked food products delivered by Swiss Army catering facilities. Italian Journal of Food Safety, 7:7323. https://doi.org/10.4081/ijfs.2018.7323.
Hoppe, I.J., Brandstetter, H. and Schonauer, E. (2021). Biochemical characterization of a collagenase from Bacillus cereus strain Q1. Scientific Reports, 11:4187. https://doi.rg/10.1038/s41598-021-83744-6
Hwang, J-Y & Park, J-H (2015). Characteristics of enterotoxin distribution, haemolysis, lecithinase, and starch hydrolysis of Bacillus cereus isolated from infant formulas and ready-to-eat foods. J. Dairy Sci. 98, 1–9. https://doi.org/10.3168/jds.2014-9042
Keisam, S., Tuikhar, N., Ahmed, G. & Jeyaram, K. (2019). Toxigenic and pathogenic Potential of enteric bacterial pathogens prevalent in the traditional fermented foods marketed in the Northeast region of India. International Journal of Food Microbiology, 296: 21-30. https://doi.org/10.1016/j.ijfoodmicro.2019.02.012.
Kotiranta, A., Lounatmaa, K. & Haapasalo, M. (2000). Epidemiology and pathogenesis of Bacillus cereus infections. Microbes and Infection, 2(2), 189-198. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.10.008
Krause, N., Moravek, M., Dietrich, R., Wehrle, E., Slaghuis, J. & Märtlbauer, E. (2010).Performance characteristics of the Duopath Cereus Enterotoxins assay for rapid detection of enterotoxinogenic Bacillus cereus strains. International Journal of Food Microbiology, 144(2), 322-326. http://doi.org/10.1016/j.ijfoodmicr o.2010.10.008.
Lapidus, A., Goltsman, E., Auger, S., Galleron, N., Ségurens, B., Dossat, C., Land, M., Broussolle, V., Brillard, J., Guinebretiere, M.H., Sanchis, V., Nguyen - The, C., Leredus, D., Richardson, P., Wincker, P., Weissenbach, J., Ehrlich, S.D. & Sorokin, A. (2008). Extending the Bacillus cereus group genomics to putative food-borne pathogens of different toxicity. Chemico-Biological Interactions, 171(2), 236-249. https://doi.org/10.1016/j.cbi.2007.03.003
Li, F., Zuo, S., Yu, P., Zhou, B., Wang, L., Liu, C., Wei, H. & Xu, H. (2016). Distribution and expression of the enterotoxin genes of Bacillus cereus in food products from Jiangxi Province, China. Food Control 67: 155-162. http://dx.doi.org/10.1016/j.foodcont.2016.02.049.
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.0.27359-0
López, A. C., Minnaard, J., Pérez, P. F. & Alippi, A. M. (2015). A case of intoxication due to a highly cytotoxic Bacillus cereus strain isolated from cooked chicken. Food Microbiology, 46, 195-199. https://doi.org/10.1016/j.fm.2014.08.005
Lund, T., De Buyser, M-L. & Granum, P. E. (2000). A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Molecular Microbiology, 38(2), 254-261. https://doi.org/10.1046/j.1365-2958.2000.02147.x
Martinelli, D., Fortunato, F., Tafuri, S., Cozza, V., Chironna, M., Germinario, C., Pedalino, B. & Prato, R. (2013). Lessons from a birthday party: a Bacillus cereus outbreak, Bari, Italy, January 2012. Ann 1st Super Sanita 49 (4), 391 -394. https://doi.org/10.4415/ANN_13_04_12
Mantynen, V. & Lindstorm, K. (1998). A rapid PCR-based DNA test for enterotoxic Bacillus cereus. Applied Environmental Microbiology 64, 1634–1639. https://doi.org/1 0.1128/AEM.64.5.1634-1639.18
Moravek, M., Dietrich, R., Buerk, C., Broussolle, V., Guinebretiere, M. H., Granum, P. E., Nguyen – The, C. & Martlbauer, E. (2006). Determination of the toxic potential of Bacillus cereus isolates by quantitative enterotoxin analyses. FEMS Microbiology Letters, 257, 293–298. https://doi.org/10.1111/j.1574-6968.200 6.00185.x
Naranjo, M., Denayer, S., Bottledorm, N., Delbrassinne, L., Veys, J., Waegenaere, J., Sirtaine, N., Driesen, R.B., Sipido, K.R., Mahillon, J. & Dierick, K. (2011). SuddenDeath of a Young Adult Associated with Bacillus cereus Food Poisoning. Journal of Clinical Microbiology, 49(12), 4379 - 4381. https://doi.org/10.1128/JCM.05129-11
Ngamwongsatit, P., Buasri, W., Piamariyanon, P., Pulsrikam, C., Ohba, M. & Assavanig,A. (2008). Broad distribution of enterotoxin genes (hbl CA, nhe ABC, cyt K and ent FM) among Bacillus cereus as shown by novel primers. International Journal of Food Microbiology, 121, 352-356. https://doi.org/10.1016/j.ijfoodmicro.2007.11.013
Oda, M., Takahashi, M., Matsuno, T., Uoo, K., Nagahama, M. & Sakurai, J. (2010). Hemolysis induced by Bacillus cereus sphingomyelinase. Biochimica et Biophysica Acta 1798, 1073–1080. https://doi.org/10.1016/j.bbame m.2010.03.004
Oltuszak-Walczak, E. & Walczak, P. (2007). PCR-Based DNA tests for detection of Emetic Bacillus cereus strains producing cereulide. Polish Journal of Food and Nutrition Sciences, 57(3A), 101- 105.
Ouoba, L.I.I., Thorsen, L. & Varnam, A.H. (2008). Enterotoxins and emetic toxins production by Bacillus cereus and other species of Bacillus isolated from Soumbala and Bikalga, African alkaline fermented food condiments. International Journal of Food Microbiology 124, 224-230. https://doi.org/10.1016/j.ijfoodmicro.2008.03.026
Powell, D. (2015). 44 kids sickened: Ottawa Chinese food takeout fined in summer camp food poisoning. Available at www.barflog./2014/08/44-kids-sickened-ottawa-chinese food. Retrieved on 15th June 2016.
Rahmati, T. & Labbe, R. (2008). Levels and toxigenicity of Bacillus cereus and Clostridium perfringens from retail seafood. Journal of Food Protection 71,1178-1185. https://doi.org/10.4315/0362-028x-71.6.1178
Ranjbar, R. & Shahreza, M.H.S. (2017). Prevalence, antibiotic-resistance properties and enterotoxin gene profile of Bacillus cereus strains isolated from milk-based baby foods. Tropical Journal of Pharmaceutical Research, 16 (8): 1931-1937. http://dx.doi.org/10.4314/tjpr.v16i8.25.
Rosenquist, H., Smidt, L., Andersen, S.R., Jensen, G.B. & Wilcks, A. (2005). Occurrence and significance of Bacillus cereus and Bacillus thuringiensis in ready-to-eat food. FEMS Microbiology Letters, 250, 129-136. https://doi.org/10.1016/j.femsle.2005.06.054
Ryan, P. A., Macmillan, J.D. & Zilinskas, B.A. (1997). Molecular cloning and characterization of the genes encoding the L1 and L2 components hemolysin BL from Bacillus cereus. Journal of Bacteriology, 179, 2551 - 2556. https://doi.org/10.1128/jb.179.8.2551-2556.1997
Sastalla, I., Fattah, R., Coppage, N., Nandy, P., Crown, D., Pomerantsev, A. P. & Leppla, S. H. (2013). The Bacillus cereus Hbl and Nhe tripartite enterotoxin components assemble sequentially on the surface of target cells and are not interchangeable. PloS one, 8(10), e76955. https://doi.org/10.1371/journal.pon e.0076955
Scallan, E., Griffin, P.M., Angulo, F.J., Tauxe, R.V. & Hoekstra, R.M. (2011). Foodborne illness acquired in the United States–unspecified agents. Emerging Infectious Diseases. 17 (1), 16–22. https://doi.org/10.3201/eid170 1.091101p2
Schoeni, J. L. & Wong, A.C.L. (2005). Bacillus cereus food poisoning and its toxins. Journal of Food Protection, 68(3), 636-648. https://doi.org/10.4315/0362-028x-68.3.6 36
Schreiber, N., Hackl, G., Reisinger, A.C., Zollner-Schwetz, I., Eller, K., Schlagenhaufen, C., Pietzka, A., Czerwenka, C., Stark, T.D., Kranzler, M., Fickert, P., Eller, P. & Ehling-Schulz, M. (2022). Acute Liver Failure after Ingestion of Fried Rice Balls: A Case Series of Bacillus cereus Food Poisonings. Toxins 14, 12. https://doi.org/10.3390/ toxins14010012.
Senesi, S. & Ghelardi, E. (2010). Production, secretion and biological activity of Bacillus cereus enterotoxins. Toxins, 2(7), 1690-1703. https://doi.org/10.3390/toxins 2071690
Senesi, S., Salvetti, S., Celandroni, F. & Ghelardi, E. (2010). Features of Bacillus cereus swarm cells. Research in Microbiology, 161(9), 743-749. https://doi.org/10.1016/j.resmic.2010.10.007
Stensfor Arnesen, L. P., Fagerlund, A. & Granum, P. E. (2008). From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiology Reviews, 32(4), 579-606. https://doi.org/10.1111/j.1574-6976.2008.00112.x
Thirkell, C.E., Sloan-Gardner, T.S., Kaczmarek, M.C. and Polkinghorne, B. (2019). An outbreak of Bacillus cereus toxin-mediated emetic and diarrhoeal syndromes at a restaurant in Canberra, Australia 2018. Communicable Diseases Intelligence 43, 10. https://doi.org/10.33321/cdi.2019.43.40
Turnbull, P.C.B., Jackson, P. J., Hill, K. K., Keim, P., Kolstø, A.B. & Beecher, D. J. (2002). Longstanding Taxonomic Enigmas within the ‘Bacillus cereus group’ are on the Verge of being Resolved by Far‒reaching Molecular Developments: forecasts on the possible outcome by an ad hoc team. Applications and Systematics of Bacillus and Relatives, 23-36. https://doi.org/10.1002/97804706 9674 3.ch3
Yang, I.C., Shih, D.Y., Wang, J.Y. & Pani, T.M. (2007). Development of rapid real-time PCR and most-probable-number real-time PCR assays to quantify enterotoxigenic strains of the species in the Bacillus cereus group. Journal of Food Protection, 70, 2774–2781. https://doi.org/10.431 5/0362-028x-70.12.2774
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, 10:3043. doi: 10.3389/fmicb.2019.03043.
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Profiling of Bacillus cereus enterotoxigenic genes from retailed foods and detection of the nhe and hbl toxins with immunological assay. (2022). Journal of Applied and Natural Science, 14(1), 254-267. https://doi.org/10.31018/jans.v14i1.3258
