Survival of Escherichia coli O157, Salmonella Enteritidis, Bacillus cereus and Clostridium botulinum in non-alcoholic beers
DOI:
https://doi.org/10.58430/jib.v130i4.61Keywords:
non-alcoholic beer, pathogens, Salmonella, Escherichia coli, heat resistance, yeastAbstract
Why was the work done: To (i) determine whether microbial pathogens were present in packaged alcohol-free and low alcohol beers, (ii) to assess whether pathogens can survive or grow in non-alcoholic beers, and (iii) to determine the impact of pH and bitterness on their growth and survival of pathogens in alcohol-free beer.
How was the work done: : 50 alcohol-free and low alcohol beers, available in the UK, were screened for pathogens and analysed for ABV, pH and bitterness (IBU). One of the alcohol-free beers (with the lowest IBU) was adjusted to 25 and 50 IBU and pH 3.8, 4.2, 4.6 and 4.9. Challenge testing of these beers was performed with Escherichia coli O157, Salmonella Enteritidis, Bacillus cereus and Clostridium botulinum. In addition, the heat resistance (D60 value) of the pathogens, spoilage bacteria and Saccharomyces cerevisiae ascospores in these beers was determined.
What are the main findings: Salmonella, E. coli, Enterobacteriaceae, Bacillus cereus and sulphite reducing clostridia were not found in any of the 50 beers. However, two emerging opportunistic pathogens (Cupriavidus gilardii and Sphingomonas paucimobilis) were found in the low alcohol keg beers. None of the pathogens used in this study could grow in the alcohol-free beer at low pH (pH 3.8). E. coli O157 was unable to grow at pH 4.2 but could grow at pH 4.6 but only with reduced levels of carbon dioxide and increased oxygen. Salmonella Enteritidis was able to grow at pH 4.2 and 4.6 but also with reduced levels of CO2 and increased O2. Although Bacillus cereus and C. botulinum were unable to grow in any of the tested conditions, both pathogens were able to survive. Survival and/or growth of the microorganisms was impacted by pH; bitterness had no effect.
Why is the work important: Salmonella Enteritidis and E. coli O157 only grew in alcohol free beer at a higher pH (4.2 and 4.6 for Salmonella and 4.6 for E. coli) together with with reduced levels of CO2 and increased O2. This suggests that packaged beer with appreciable levels of carbon dioxide and negligible levels of oxygen will not support the growth of pathogens. However, draught alcohol free beer may be vulnerable to pathogens.
Downloads
References
Billah MM, Rahman MS. 2024. Salmonella in the environment: A review on ecology, antimicrobial resistance, seafood contaminations, and human health implications. J Hazard Mater 13:1-12. DOI: https://doi.org/10.1016/j.hazadv.2024.100407
Brown KL, Martinez A. 1992. The heat resistance of spores of Clostridium botulinum 213B heated at 121-130°C in acidified mushroom extract. J Food Prot 55:913-915. DOI: https://doi.org/10.4315/0362-028X-55.11.913
Bucher O, Holley RA, Ahmed R, Tabor H, Nadon C, Ng LK, D'aoust JY. 2007. Occurrence and characterization of Salmonella from chicken nuggets, strips, and pelleted broiler feed. J Food Prot 70:2251-2258. DOI: https://doi.org/10.4315/0362-028X-70.10.2251
Center for Disease Control. 2024. Listeria (Listeriosis).
Cobo M, Charles-Vegdahl A, Kirkpatrick K, Worobo R. 2023. Survival of foodborne pathogens in low and monalcoholic craft beer. J Food Prot 86:1-5. DOI: https://doi.org/10.1016/j.jfp.2023.100183
Ehling-Schulz M, Lereclus D, Koehler TM. 2019. The Bacillus cereus Group: Bacillus species with pathogenic potential. Microbiol Spectr 7:10.1128/microbiolspec.gpp3-0032-2018 DOI: https://doi.org/10.1128/microbiolspec.GPP3-0032-2018
Eu. D-GFC. 2024. Rapid Alert System for Food and Feed (RASFF).
FDA. 2012. Bad Bug Book, Handbook of Foodborne Pathogenic Microorganisms and Natural Toxins. Second Edition.
Gaglio R, Francesca N, Di Gerlando R, Mahony J, De Martino S, Stucchi C, Moschetti G, Settanni L. 2017. Enteric bacteria of food ice and their survival in alcoholic beverages and soft drinks. Food Microbiol 67:17-22. DOI: https://doi.org/10.1016/j.fm.2017.04.020
Gandhi M, Chikindas ML. 2007. Listeria: A foodborne pathogen that knows how to survive. Int J Food Microbiol 113:1-15. DOI: https://doi.org/10.1016/j.ijfoodmicro.2006.07.008
Jevons AJ, Quain DE. 2022. Identification of spoilage microflora in draught beer using culture‐dependent methods. J Appl Micro 133:3728-3740. DOI: https://doi.org/10.1111/jam.15810
Johnson EA, Bradshaw M. 2001. Clostridium botulinum and its neurotoxins: a metabolic and cellular perspective. Toxicon 39:1703-1722. DOI: https://doi.org/10.1016/S0041-0101(01)00157-X
Johnson EA, Haas GJ. 2001. Antimicrobial activity of hops extract against Clostridium botulinum, Clostridium difficile and Helicobacter pylori. United States patent application. Patent No 6251461
Jones G. 2012. A Guide to Microorganisms and their Control - Guideline 68, Campden BRI.
Kim HJ, Song WJ. 2023. Inactivation of E. coli O157:H7 in foods by emerging technologies: a review. Lett Appl Microbiol 76:1-25. DOI: https://doi.org/10.1093/lambio/ovac007
Kim SA, Kim NH, Lee SH, Hwang IG, Rhee MS. 2014. Survival of foodborne pathogenic bacteria (Bacillus cereus, E. coli O157:H7, Salmonella enterica serovar Typhimurium, Staphylococcus aureus, and Listeria monocytogenes) and Bacillus cereus spores in fermented alcoholic beverages (beer and refined rice wine). J Food Prot 77:419-426. DOI: https://doi.org/10.4315/0362-028X.JFP-13-234
King JS, Mabbitt LA. 2009. Preservation of raw milk by the addition of carbon dioxide. J Dairy Res 49:439-447. DOI: https://doi.org/10.1017/S0022029900022573
Kobayashi T, Nakamura I, Fujita H, Tsukimori A, Sato A, Fukushima S, Ohkusu K, Matsumoto T. 2016. First case report of infection due to Cupriavidus gilardii in a patient without immunodeficiency: a case report. BMC Infect Dis 16:493. DOI: https://doi.org/10.1186/s12879-016-1838-y
Koskinen R, Ali-Vehmas T, Kampfer P, Laurikkala M, Tsitko I, Kostyal E, Atroshi F, Salkinoja-Salonen M. 2000. Characterization of Sphingomonas isolates from Finnish and Swedish drinking water distribution systems. J Appl Microbiol 89:687-696. DOI: https://doi.org/10.1046/j.1365-2672.2000.01167.x
Lacoursiere A, Thompson BG, Kole MM, Ward D, Gerson DF. 1986. Effects of carbon dioxide concentration on anaerobic fermentations of E. coli. Appl Microbiol Biotechnol 23:404-406. DOI: https://doi.org/10.1007/BF00257042
Logan NA. 2012. Bacillus and relatives in foodborne illness. J Appl Microbiol 112:417-429. DOI: https://doi.org/10.1111/j.1365-2672.2011.05204.x
Loss CR, Hotchkiss JH. 2002. Effect of dissolved carbon dioxide on thermal inactivation of microorganisms in milk. J Food Prot 65:1924-1929. DOI: https://doi.org/10.4315/0362-028X-65.12.1924
Majowicz SE, Scallan E, Jones-Bitton A, Sargeant JM, Stapleton J, Angulo FJ, Yeung DH, Kirk MD. 2014. Global incidence of human Shiga toxin-producing E. coli infections and deaths: a systematic review and knowledge synthesis. Foodborne Pathog Dis 11:447-455. DOI: https://doi.org/10.1089/fpd.2013.1704
Martin JD, Werner BG, Hotchkiss JH. 2003. Effects of carbon dioxide on bacterial growth parameters in milk as measured by conductivity. J Dairy Sci 86:1932-1940. DOI: https://doi.org/10.3168/jds.S0022-0302(03)73780-1
McDowell R, Sands E, Friedman H. 2024. Bacillus cereus. Treasure Island (FL), (online book). StatPearls Publishing.
Menz G, Aldred P, Vriesekoop F. 2011. Growth and survival of foodborne pathogens in beer. J Food Prot 74:1670-1675. DOI: https://doi.org/10.4315/0362-028X.JFP-10-546
Menz G, Vriesekoop F, Zarei M, Zhu B, Aldred P. 2010. The growth and survival of food-borne pathogens in sweet and fermenting brewers' wort. Int J Food Microbiol 140:19-25. DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.02.018
Michino H, Araki K, Minami S, Takaya S, Sakai N, Miyazaki M, Ono A, Yanagawa H. 1999. Massive outbreak of E. coli O157 H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol 150:787-796. DOI: https://doi.org/10.1093/oxfordjournals.aje.a010082
Midura T, Gerber M, Wood R, Leonard AR. 1970. Outbreak of food poisoning caused by Bacillus cereus. Public Health Rep 85:45-48. DOI: https://doi.org/10.2307/4593779
Munford ARG, Alvarenga VO, Do Prado-Silva L, Crucello A, Campagnollo FB, Chaves RD, Oteiza JM, Sant'ana AS. 2017. Sporeforming bacteria in beer: Occurrence, diversity, presence of hop resistance genes and fate in alcohol-free and lager beers. Food Control 81:126-136. DOI: https://doi.org/10.1016/j.foodcont.2017.06.003
Ng H, Bayne HG, Garibaldi JA. 1969. Heat resistance of Salmonella: the uniqueness of Salmonella Senftenberg 775W. Appl Microbiol 17:78-82. DOI: https://doi.org/10.1128/am.17.1.78-82.1969
Quain DE. 2021. The enhanced susceptibility of alcohol-free and low alcohol beers to microbiological spoilage: implications for draught dispense. J Inst Brew 127:406-416. DOI: https://doi.org/10.1002/jib.670
Rachon G, Raleigh CP, Pawlowsky K. 2021. Heat resistance of yeast ascospores and their utilisation for the validation of pasteurisation processes for beers. J Inst Brew 127:149-159. DOI: https://doi.org/10.1002/jib.646
Rachon G, Rice CJ, Pawlowsky K, Raleigh CP. 2018. Challenging the assumptions around the pasteurisation requirements of beer spoilage bacteria. J Inst Brew 124:443-449. DOI: https://doi.org/10.1002/jib.520
Rawson AM, Dempster AW, Humphreys CM, Minton NP. 2023. Pathogenicity and virulence of Clostridium botulinum. Virulence 14:1-28. DOI: https://doi.org/10.1080/21505594.2023.2205251
Rój E, Tadić VM, Mišić D, Žižović I, Arsić I, Dobrzyńska-Inger A, Kostrzewa D. 2015. Supercritical carbon dioxide hops extracts with antimicrobial properties. Open Chem 13:1157-1171. DOI: https://doi.org/10.1515/chem-2015-0131
Ruiz C, Mccarley A, Espejo ML, Cooper KK, Harmon DE. 2019. Comparative genomics reveals a well-conserved intrinsic resistome in the emerging multidrug-resistant pathogen Cupriavidus gilardii. mSphere 4:1-15. DOI: https://doi.org/10.1128/mSphere.00631-19
Ryan MP, Adley CC. 2010. Sphingomonas paucimobilis: a persistent Gram-negative nosocomial infectious organism. J Hosp Infect 75:153-157. DOI: https://doi.org/10.1016/j.jhin.2010.03.007
Taylor AJ, Gilbert RJ. 1975. Bacillus cereus food poisoning: a provisional serotyping scheme. J Med Microbiol 8:543-550. DOI: https://doi.org/10.1099/00222615-8-4-543
Tiwari A, Nagalli S. 2024. Clostridium botulinum. Treasure Island (FL), (online book). StatPearls Publishing.
Wells JG, Davis BR, Wachsmuth IK, Riley LW, Remis RS, Sokolow R, Morris GK. 1983. Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare E. coli serotype. J Clin Microbiol 18:512-520. DOI: https://doi.org/10.1128/jcm.18.3.512-520.1983
Wentz TG, Yao K, Schill KM, Reddy NR, Skinner GE, Morrissey TR, Wang Y, Muruvanda T, Manickam G, Pillai CA, Thirunavukkarasu N, Hoffmann M, Hammack TS, Brown EW, Allard MW, Sharma SK. 2018. Closed genome sequence of Clostridium botulinum strain CFSAN064329 (62A). Genome Announc 6:10.1128/genomea.00528-18. DOI: https://doi.org/10.1128/genomeA.00528-18
WHO. 2018. Salmonella (non-typhoidal).
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Journal of the Institute of Brewing
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
This is an open access article which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed or built upon in any way.
Permission will be required if the proposed reuse is not covered by the terms of the License. In this event, email the Editor in Chief - david.quain@ibd.org.uk - with details of your request.