Reduction of Bacillus cereus on table eggshells through disinfection with quaternary ammonium salts, ethanol, and ultraviolet radiation

  • Joel Reyes-Roldan Universidad Autónoma de Guerrero. Facultad de Ciencias Químico Biológicas. Laboratorio de Investigación en Patometabolismo Microbiano. Chilpancingo de Los Bravo-Guerrero https://orcid.org/0009-0000-0287-9184
  • María Cristina Santiago-Dionisio Universidad Autónoma de Guerrero. Facultad de Ciencias Químico Biológicas. Laboratorio de Investigación en Análisis Microbiológicos. Chilpancingo de Los Bravo-Guerrero. México https://orcid.org/0000-0001-5187-665X
  • Salvador Muñoz-Barrios Universidad Autónoma de Guerrero. Facultad de Ciencias Naturales. Laboratorio de Investigación en Inmunología y Microbiología. Las Petaquillas-Guerrero. México https://orcid.org/0000-0002-4821-5356
  • Arturo Ramírez-Peralta Universidad Autónoma de Guerrero. Facultad de Ciencias Químico Biológicas. Laboratorio de Investigación en Patometabolismo Microbiano. Chilpancingo de Los Bravo-Guerrero. México http://orcid.org/0000-0002-7037-6412
DOI: https://doi.org/10.56903/kasmera.535108
Keywords: Bacillus cereus, eggs, disinfectant

Abstract

This study observed a decrease in log10 CFU/mL of B. cereus after applying quaternary ammonium salts, indicating residual activity. Additionally, exposing whole eggs to UV radiation for 5 minutes reduced the microbial growth of B. cereus.

Author Biography

Arturo Ramírez-Peralta, Universidad Autónoma de Guerrero. Facultad de Ciencias Químico Biológicas. Laboratorio de Investigación en Patometabolismo Microbiano. Chilpancingo de Los Bravo-Guerrero. México

Químico biólogo parasitólogo de formación, maestría y doctorado en ciencias biomédicas con orientación en microbiología por la Universidad Autónoma de Guerrero, México, con estancia doctoral en la “University of Connecticut” en Connecticut, USA; durante dos años.
Actualmente, profesor investigador en la Universidad Autónoma de Guerrero, Sistema Nacional de Investigadores nivel I, miembro de las academias de Seminario de Investigación, Microbiología y biotecnología; de la Universidad Autónoma de Guerrero. Con publicaciones en revistas internacionales arbitradas y en congresos nacionales e internacionales. Revisor de revistas indexadas y arbitradas.

References

Carrillo S, Ríos VH, Calvo C, Carranco ME, Casas M, Pérez-Gil F. n-3 Fatty acid content in eggs laid by hens fed with marine algae and sardine oil and stored at different times and temperatures. J Appl Phycol [Internet]. 2012;24(3):593-9. Disponible en: https://doi.org/10.1007/s10811-011-9777-x. DOI: 10.1007/s10811-011-9777-x

Fraeye I, Bruneel C, Lemahieu C, Buyse J, Muylaert K, Foubert I. Dietary enrichment of eggs with omega-3 fatty acids: A review. Food Res Int [Internet]. 2012;48(2):961-9. Disponible en: https://www.sciencedirect.com/science/article/pii/S0963996912001226 DOI: 10.1016/j.foodres.2012.03.014

Mendoza Rodríguez YY, Brambila Paz J de J, Arana Coronado JJ, Sangerman- Jarquín DM, Molina Gómez JN. El mercado de huevo en México: tendencia hacia la diferenciación en su consumo. Rev Mex Ciencias Agrícolas [Internet]. 2017;7(6):1455-66. Disponible en: https://cienciasagricolas.inifap.gob.mx/index.php/agricolas/article/view/206 DOI: 10.29312/remexca.v7i6.206

Al-Ajeeli MN, Taylor TM, Alvarado CZ, Coufal CD. Comparison of eggshell surface sanitization technologies and impacts on consumer acceptability. Poult Sci [Internet]. 2016;95(5):1191-7. Disponible en: https://www.sciencedirect.com/science/article/pii/S003257911931836X DOI: 10.3382/ps/pew014 PMID 26944973

Howard ZR, O’Bryan CA, Crandall PG, Ricke SC. Salmonella Enteritidis in shell eggs: Current issues and prospects for control. Food Res Int [Internet]. 2012;45(2):755-64. Disponible en: https://www.sciencedirect.com/science/article/pii/S0963996911002602 DOI: 10.1016/j.foodres.2011.04.030

Kone AZ, Jan S, Le Marechal C, Grosset N, Gautier M, Puterflam J, et al. Identifying risk factors for eggshell contamination by Bacillus cereus group bacteria in French laying farms. Br Poult Sci [Internet]. 2013;54(3):298-305. Disponible en: https://www.tandfonline.com/doi/10.1080/00071668.2013.783900?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub%20%200pubmed# DOI: 10.1080/00071668.2013.783900 PMID 23650940

Chaemsanit S, Akbar A, Anal AK. Isolation of total aerobic and pathogenic bacteria from table eggs and its contents. Food Appl Biosci J [Internet]. 2017;3(1):1-9. Disponible en: https://li01.tci-thaijo.org/index.php/fabjournal/article/view/78102 DOI: 10.14456/fabj.2015.1

Enosi Tuipulotu D, Mathur A, Ngo C, Man SM. Bacillus cereus: Epidemiology, Virulence Factors, and Host–Pathogen Interactions. Trends Microbiol [Internet]. 2021;29(5):458-71. Disponible en: https://doi.org/10.1016/j.tim.2020.09.003 DOI: 10.1016/j.tim.2020.09.003 PMID 33004259

Duport C, Jobin M, Schmitt P. Adaptation in Bacillus cereus: From Stress to Disease. Front Microbiol [Internet]. 2016;7. Disponible en: https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2016.01550 DOI: 10.3389/fmicb.2016.01550 PMID 27757102 PMCID PMC504791

Cruz-Facundo IM, Adame-Gómez R, Vences-Velázquez A, Rodríguez-Bataz E, Muñoz-Barrios S, Pérez-Oláis JH, et al. Bacillus cereus in Eggshell: Enterotoxigenic Profiles and Biofilm Production. Brazilian J Poult Sci [Internet]. 2022;24(2). Disponible en: https://www.scielo.br/j/rbca/a/Cbw3bLmQ48n78TjYBBnTBYg/?lang=en DOI: 10.1590/1806-9061-2021-1535

Latimer GW Jr, editor. Official Methods of Analysis of AOAC INTERNATIONAL [Internet]. 22.a ed. New York: Oxford University Press; 2023. Disponible en: https://academic.oup.com/aoac-publications/book/45491

Davies R, Breslin M. Observations on Salmonella contamination of commercial laying farms before and after cleaning and disinfection. Vet Rec [Internet]. 2003;152(10):283–7. Disponible en: http://dx.doi.org/10.1136/vr.152.10.283 DOI: 10.1136/vr.152.10.283 PMID 12650470

Bermudez-Aguirre D, Niemira BA. A review on egg pasteurization and disinfection: Traditional and novel processing technologies. Compr Rev Food Sci Food Saf [Internet]. 2023;22(2):756–84. Disponible en: http://dx.doi.org/10.1111/1541-4337.13088 DOI: 10.1111/1541-4337.13088 PMID 36537903

Dórea FC, Cole DJ, Hofacre C, Zamperini K, Mathis D, Doyle MP, et al. Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations. Appl Environ Microbiol [Internet]. 2010;76(23):7820–5. Disponible en: http://dx.doi.org/10.1128/AEM.01320-10 DOI: 10.1128/AEM.01320-10 PMID 20889797 PMCID PMC2988591

Messens W, Grijspeerdt K, De Reu K, De Ketelaere B, Mertens K, Bamelis F, et al. Eggshell penetration of various types of hens’ eggs by Salmonella enterica serovar Enteritidis. J Food Prot [Internet]. 2007;70(3):623–8. Disponible en: http://dx.doi.org/10.4315/0362-028x-70.3.623 DOI: 10.4315/0362-028x-70.3.623 PMID 17388050

Abdoli B, Khoshtaghaza MH, Ghomi H, Torshizi MAK, Mehdizadeh SA, Pishkar G, et al. Cold atmospheric pressure air plasma jet disinfection of table eggs: Inactivation of Salmonella enterica, cuticle integrity and egg quality. Int J Food Microbiol [Internet]. 2024;410(110474):110474. Disponible en: http://dx.doi.org/10.1016/j.ijfoodmicro.2023.110474. DOI: 10.1016/j.ijfoodmicro.2023.110474 PMID 37984215

Chung H, Kim H, Myeong D, Kim S, Choe N-H. Effect of chlorine dioxide gas application to egg surface: Microbial reduction effect, quality of eggs, and hatchability. Korean J Food Sci Anim Resour [Internet]. 2018;38(3):487–97. Disponible en: http://dx.doi.org/10.5851/kosfa.2018.38.3.487 DOI: 10.5851/kosfa.2018.38.3.487 PMID 30018493 PMCID PMC6048379

Davies RH, Breslin M. Investigation of Salmonella contamination and disinfection in farm egg-packing plants. J Appl Microbiol [Internet]. 2003;94(2):191–6. Disponible en: http://dx.doi.org/10.1046/j.1365-2672.2003.01817.x. DOI: 10.1046/j.1365-2672.2003.01817.x PMID 12534810 PMCID PMC6048379

Medina-Gudiño J, Rivera-Garcia A, Santos-Ferro L, Ramirez-Orejel JC, Agredano-Moreno LT, Jimenez-Garcia LF, et al. Analysis of Neutral Electrolyzed Water anti-bacterial activity on contaminated eggshells with Salmonella enterica or Escherichia coli. Int J Food Microbiol [Internet]. 2020;320(108538):108538. Disponible en: http://dx.doi.org/10.1016/j.ijfoodmicro.2020.108538 DOI: 10.1016/j.ijfoodmicro.2020.108538 PMID 32004824

Rivera-Garcia A, Santos-Ferro L, Ramirez-Orejel JC, Agredano-Moreno LT, Jimenez-Garcia LF, Paez-Esquiliano D, et al. The effect of neutral electrolyzed water as a disinfectant of eggshells artificially contaminated with Listeria monocytogenes. Food Sci Nutr [Internet]. 2019;7(7):2252–60. Disponible en: http://dx.doi.org/10.1002/fsn3.1053 DOI: 10.1002/fsn3.1053 PMID 31367353 PMCID PMC6657710

Vinayananda CO, Fairoze N, Madhavaprasad CB, Byregowda SM, Nagaraj CS, Bagalkot P, et al. Studies on occurrence, characterisation and decontamination of emerging pathogenic Escherichia coli (STEC, ETEC and EIEC) in table eggs. Br Poult Sci [Internet]. 2017;58(6):664–72. Disponible en: http://dx.doi.org/10.1080/00071668.2017.1373387 DOI: 10.1080/00071668.2017.1373387 PMID 28881144

Obłąk E, Futoma-Kołoch B, Wieczyńska A. Biological activity of quaternary ammonium salts and resistance of microorganisms to these compounds. World J Microbiol Biotechnol [Internet]. 2021;37(2):22. Disponible en: http://dx.doi.org/10.1007/s11274-020-02978-0 DOI: 10.1007/s11274-020-02978-0 PMID 33428020

Ghosh S, Ramirez-Peralta A, Gaidamakova E, Zhang P, Li Y-Q, Daly MJ, et al. Effects of Mn levels on resistance of Bacillus megaterium spores to heat, radiation and hydrogen peroxide: Effects of Mn levels on B. megaterium spore resistance. J Appl Microbiol [Internet]. 2011;111(3):663–70. Disponible en: http://dx.doi.org/10.1111/j.1365-2672.2011.05095.x DOI: 10.1111/j.1365-2672.2011.05095.x PMID 21714839

Rutala WA, Gergen MF, Sickbert-Bennett EE, Anderson DJ, Weber DJ, CDC Prevention Epicenters Program. Antimicrobial activity of a continuously active disinfectant against healthcare pathogens. Infect Control Hosp Epidemiol [Internet]. 2019;40(11):1284–6. Disponible en: http://dx.doi.org/10.1017/ice.2019.260 DOI: 10.1017/ice.2019.260 PMID 31556367

Published
2025-10-09
How to Cite
1.
Reyes-Roldan J, Santiago-Dionisio MC, Muñoz-Barrios S, Ramírez-Peralta A. Reduction of Bacillus cereus on table eggshells through disinfection with quaternary ammonium salts, ethanol, and ultraviolet radiation. Kasmera [Internet]. 2025Oct.9 [cited 2025Oct.30];53:e5335108. Available from: https://produccioncientifica.luz.edu.ve/index.php/kasmera/article/view/35108
Issue
Vol. 53 (2025)
Section
Original Articles

Copyright (c) 2025 Joel Reyes-Roldan, María Cristina Santiago-Dionisio, Salvador Muñoz-Barrios, Arturo Ramírez-Peralta

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

 

Kasmera journal is registered under a Creative Commons an Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0), available at: https://creativecommons.org/licenses/by-nc-sa/4.0/deed.en; which guarantees the freedom to share-copy and redistribute the material in any medium or format and adapt-remix, transform and build from the material, provided that the name of the authors, the Department of Infectious and Tropical Diseases, Zulia´s University and Kasmera Journal, you must also provide a link to the original document and indicate if changes have been made.

The Department of Infectious and Tropical Diseases, University of Zulia and Kasmera Journal do not retain the rights to published manuscript and the contents are the sole responsibility of the authors, who retain their moral, intellectual, privacy and publicity rights. The guarantee on the intervention of the manuscript (revision, correction of style, translation, layout) and its subsequent dissemination is granted through a license of use and not through a transfer of rights, which represents the Kasmera Journal and Department Infectious Diseases, University of Zulia are exempt from any liability that may arise from ethical misconduct by the authors.

Kasmera is considered a green SHERPA/RoMEO journal, that is, it allows self-archiving of both the pre-print (draft of a manuscript) and the post-print (the corrected and peer-reviewed version) and even the final version (layout as it will be published in the journal) both in personal repositories and in institutional and databases.