Assessment of the development of Staphylococcus aureus during the production of soro on a laboratory scale

Authors

DOI:

https://doi.org/10.33448/rsd-v11i10.22450

Keywords:

Whey; Evaporation; Crystallization; Drying; Biofilm.

Abstract

The aim of this study was to evaluate the multiplication of S. aureus during whey powder production in laboratory scale. Whey was inoculated with 106 CFU∙ mL-1 of the S. aureus mixed culture at the beginning of the processing and the persistence of the microorganism after pasteurization, vacuum evaporation and drying was evaluated. The recontamination of whey by biofilms was also evaluated. Population of 102 CFU∙mL-1 of S. aureus was found after vacuum evaporation. The microorganism was able to multiply in concentrated whey during the crystallization of lactose, which infers that it is possible to form a biofilm during this stage. Confocal microscopy analysis confirmed the presence of adhered cells after 4 h of process (103 CFU∙cm2). After 12 h of incubation, the number of adhered cells was approximately 105 CFU∙cm2. Sessile cells of S. aureus in stainless steel were able to return to the planktonic phase. After spray drying, it was verified that the S. aureus population in the powder was 103 CFU∙g-1. The results obtained in laboratory scale points to the need of quality assurance systems to control the steps of industrial whey powder production.

References

Allignet, J., Aubert, S., Keit, G. H., & Solh, N. E. (2001). Staphylococcus strains carry derminants known to be in volved in pathogenicity: a gene encoding an autolysin-binding fibronectin and the ica operon involved in biofilm formation. Infection and immunity, 69, 712-718. https://doi.org/10.1128/IAI.69.2.712-718.2001

Al- Nabulsi, A. A., Osaili, T. M., Abunaser, R. A., Olaimat, A. N., Ayyash, M., Al-Holy, M. A., Kadora, K. M., & Holley, R. A. (2020). Factors affecting the viability of Staphylococcus aureus and production of enterotoxin during processing and storage of white-brined cheese. Journal of Dairy Science, 103, 6869-6881. https://doi.org/10.3168/jds.2020-18158

Anunciação, L. L. C., Linardi, W. R., Carmo, L. S., & Bergdoll, M. S. (1994). Production of Staphylococcal Enterotoxin “A” In White Cheese. Brazilian journal of microbiology, 25, 68-71.

Asao, T., Kumeda, Y., Kawai, T., Shibata, T., Oda, H., Haruki, K., Nakazawa, H., & Kozaki, S. (2003). An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: 265 estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiology and Infection, 130, 33–40. https://doi.org/ 10.1017/s0950268802007951

Badini, K. B., Filho, A. N., Amaral, L. A., & Germano, P. M. L. (1996). Health risk due to the consumption of raw milk commercialized without due authorization. SciElo, 30, 6-12.

Boari, C. A., Alves, M. P., Tebaldi, V. M. R., Savian, T. V., & Piccoli, R. H. (2009). Biofilm formation by Aeromonas hydrophila and Staphylococcus aureus on stainless steel using milk and different conditions of cultivation, Food Science and Technology. 29, 886-895. https://doi.org/10.1590/S0101-20612009000400029

Borelli, B. M., Lacerda, IC. A., Brandão, L. R., Vianna, C. R., Ferreira, M. C., Gomes, F. C. O., Carmo, L. S., Heneine, L. G. D., & Rosa, C. A. (2011). Identification of Staphylococcus spp. isolated during the ripening process of a traditional Minas cheese. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 63, 481-487. https://doi.org/10.1590/S0102-09352011000200028

Brazil. (2019b). Ministério da Saúde. Agência Nacional de Vigilância Sanitária. Instrução normativa n° 60, de 23 de dezembro de 2019. Listas de padrões microbiológicos para alimentos prontos para oferta ao consumidor.

Careli, R. T., Andrade, N. J., Soares, N. F., Júnior, J. I. R., Rosado, S. M., Bernardes, P. C. (2009). The adherence of Pseudomonas fluorescens to marble, granite, synth ic polymers, and stainless steel. Food Science and Technology, 171 – 176. https://doi.org/10.1590/S0101-20612009000100026

Cardozo, M. V., N. Nespolo, T. C. Delfino, C. C. Almeida, L. J. L. Pizauro, M. K. Valmorbida, N. Pereira, & F. A. Ávila. (2021). Raw milk cheese as a potential infection source of pathogenic and toxigenic food born pathogens. Food Science and Technology (Campinas) 41, 355–358. https://doi.org/10.1590/fst.37919.

Cebrián, G., Condón, S., & Mañas, P. (2016). Influence of growth and treatment temperature on Staphylococcus aureus resistance to pulsed electric fields: Relationship with membrane fluidity. Innovative Food Science & Emerging Technolgies, 37,161 – 169. https://doi.org/10.1016/j.ifset.2016.08.011

Commission Regulation (EC) No 2073/2005 of 15 November 2005 on 277 microbiological criteria for foodstuffs. OJ L 338, 22/12/2005, 1-26.

Da Silva Cândido, T. J., A. C. da Silva, L. G. de Matos, M. da Silva do Nascimento, C. H. Camargo, R. Cobo Zanella, V. L. Mores Rall, and N. C. Cirone Silva. (2020). Enterotoxigenic potential and molecular typing of Staphylococcus sp. isolated from organic and conventional fresh Minas cheese in the state of São Paulo, Brazil. International Dairy Journal. 102,104605.https://doi.org/10.1016/j.idairyj.2019 .104605.

De Leon, C. M. C. G., F. G. C. Sousa, M. M. S. Saraiva, P. E. N. Givisiez, N. M. V. Silva, R. F. C. Vieira, & C. J. B. Oliveira. (2020). Equipment contact surfaces as sources of Staphylococcus carrying enterotoxin-encoding genes in goat milk dairy plants. International Dairy Journal.111,104827. https://doi.org/10.1016/j.idairyj.2020 .104827.

Feitosa, A. C., Rosimeire, M. R., Edwin, A. T. T., & Juliana, F. M. S. (2017). Staphylococcus aureus em alimentos. Revista Desafios. 4, 15-31. https://doi.org/10.20873/uft.2359-3652.2017v4n4p15

FDA-Food and Drug Administration. Recalls, Market Withdrawals & Safety Alerts. (2018). Available in : https://www.fda.gov/safety/archive-recalls-market-withdrawals-safety-alerts/2018-recalls-market-withdrawals-safety-alerts. Accessed in: January, 2019.

Gleeson, D., O’Connell, A., & Jordan, K. (2013). Review of potential sources and control of thermoduric bacteria in bulk-tank milk. Journal of Agricultural and Food Research,52, 217 – 227.

Hamadi, F., Asserne, F., Elabed, S., Bensouda,S., Mabrouki, M., & Latrache, H (2014). Adhesion of Staphylococcus aureus on stainless steel treated with three types of milk. Food Control, 38,104- 108. https://doi.org/10.1016/j.foodcont.2013.10.006

Herrera, J. J. R., Cabo, M. L., Gonza’lez, A., & Pastoriza, L. (2007). Adhesion and detachment kinetics of several strains of Staphylococcus aureus subsp. aureus under three different experimental conditions. Food Microbiology, 24, 585 – 591. https://doi.org/10.1016/j.fm.2007.01.001

Holy, A. V., & Geornaras, I. (2001). Antimicrobial susceptibilities of isolates of Staphylococcus aureus, Listeria species and Salmonella serotypes associated with poultry processing. International Journal Food Microbiology, 70, p.29-35. https://doi.org/10.1016/S0168-1605(01)00517-7

Huck, J. R., Sonnen, M, & Boor, K. J. (2008). Tracking Heat-Resistant, Cold-Thriving Fluid Milk Spoilage Bacteria from Farm to Packaged Product. Journal of Dairy Science, 91,1218 – 1228. https://doi.org/10.3168/jds.2007-0697

International Organization of Standardization “ISO” (1999) No. 6888- Microbiology of food and animal feeding stuffs — Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species) — Part 1: Technique using Baird-Parker agar medium.

Jakobsen, R. A., Heggebo,R., Sunde, E. B., & Skjervheim, M. (2011). Staphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production. Journal Food Microbiology, 28, 492-496. https://doi.org/10.1016/j.fm.2010.10.017

Malheiros, P.; Casarin, L. S.; Serraglio, L.; & Tondo, E. C. (2010). Evaluation of growth and transfer of Staphylococcus aureus from poultry meat to surfaces of stainless steel and poly hylene and their disinfection, Food Control, 298–301. https://doi.org/10.1016/j.foodcont.2009.06.008

Masters, K. (2002). Spray Drying in Practices. Denmark: SprayDryConsult International ApS, 464.

Mendes, F. S., & Souza, C. F. V. (2012). Avaliação da qualidade microbiológica do soro de queijo coalho artesanal no Município Nossa Senhora. Revista Brasileira de Tecnologia Agroindustrial, 34, 13-18.

Morton, R. D. (2001). Compendium of Methods for the Microbiological Examination of Foods. American Public Health Association. 66 – 67.

Necidová, L., Janštová, B., & Karpíšková, R. (2012). Dynamics of staphylococcal enterotoxin production in model experiments simulating the fresh cheese environment. Journal of the University of Veterinary and Pharmaceutical Sciences in Brno, 81, 391–396. https://doi.org/10.2754/avb201281040391

Oliveira, M. M. M.; Brugnera, D. F.; & Piccoli, R. H. (2010). Microbial biofilms in the food industry: a review. Revista do Instituto Adolfo Lutz, 277–284.

Peresi, J. T. M et al., (2004). Foodborne disease outbreaks caused by Staphylococcus aureus, in region of São José do Rio Preto - SP , during the period from December 2001 to April 2003. Revista Instituto Adolfo Lutz, 63,232-237.

Perin, L. M., Moraes, P. M., Almeida, M. V., & Nero, L. A. (2017). Interference of storage temperatures in the development of mesophilic, psychrotrophic, lipolytic and proteolytic microbiota of raw milk. Revista Ciências Agrárias, 333-342.

Rodrigues, J.B.S., Carvalho, R.J., Souza, N.T., Oliveira, K.S., Franco, O.L., Schaffner, D., Souza, E.L., & Magnan, M. (2017). Effects of oregano essential oil and carvacrol on biofilms of Staphylococcus aureus from food-contact surfaces. Food Control, 1237-1246. https://doi.org/10.1016/j.foodcont.2016.10.043

Ronner, A. B.; & Wong, A. C. L. (1993). Biofilm development and sanitizer inactivation of Listeria monocytogenes and Salmonella Typhimuriumon stainless steel and buna-n rubber. Journal of food Protection, 56,750-758. https://doi.org/10.4315/0362-028X-56.9.750

Rosmaninho, R., Santos, O., Nylander, T., Paulsson, M., Beuf, M., Benezech, T., Yiantsios, S., Andritos, N., Karabelas, G.E., Steinhagen, H.M., & Melo, L.F. (2007). Modified stainless steel surfaces targeted to reduce fouling – Evaluation of fouling by milk components. Journal of Food Engineering, 80 ,1176 – 1187. https://doi.org/10.1016/j.jfoodeng.2006.09.008

Rossoni, E. M. M.; & Gaylarde, C. C. (2000). Comparison of sodium hypochlorite and perac ic acid as sanitising agents for stainless steel food processing surfaces using epifluorescence microscopy .International Journal of Food Microbiology. 81–85. https://doi.org/10.1016/S0168-1605(00)00369-X

Rozand, C. V., Mazuy, C., Prevost, G., Lapeyre, C., Bes, M., Brun, Y., & Fleurette, J. (1996). Enterotoxin production by coagulase-negative staphylococci isolated from goats’ milk and cheese. International Journal of Food Microbiology, 30, 271-280. https://doi.org/10.1016/0168-1605(96)00952-X

Schuck. P. (2002). Spray Drying of dairy products: state of the art. Lait. 82, 375–382. https://doi.org/ 10.1051/lait:2002017

Schuck, P. (2009). Understanding the factors affecting spray-dried dairy powder properties and behaviour. Dairy derived ingredients: food and nutraceutical uses, 24-50.

Simeao, M., Stephani, R., Silva, C. R., & Oliveira, L. F. C. (2017). Lactose crystallisation in concentrated whey: the influence of vat type. International journal of dairy technology, 1-6. https://doi.org/10.1111/1471-0307.12455

SVS. (2019). Surtos de Doenças Transmitidas por Alimentos no Brasil. Brasil: Ministério Da Saúde: Secretaria de Vigilância Em Saúde.

Verraes, C., Vlaemynck, G., Weyenberg, S.V., Zutter, L.D., Daube, G., Sindic, M., Uyttendaele, M., & Herman, L. (2015). A review of the microbiological hazards of dairy products made from raw milk. International Dairy Journal, 50, 32-44. https://doi.org/ 10.1016/j.idairyj.2015.05.011

Wang, X., Meng, J., Zhang, J., Zhou, T., Zhang, Y., Yang, B., Xi, M., & Xia, X. (2012). Characterization of Staphylococcus aureus isolated from powdered infant formula milk and infant rice cereal in China. International Journal of Food Microbiology, 153, 142–147. https://doi.org/

1016/j.ijfoodmicro.2011.10.030

Wirtanen, G., Husmark, U., & Sandholm, T.M. (1996). Microbial evaluation of the bio transfer potencial from surfaces with Bacillus biofilms after rinsing and cleaning procedures in closed food-processing systems. Journal of Food Protection, 59, 727-733. https://doi.org/10.4315/0362-028X-59.7.727

Wolf C., Hochgrafe, F., Kusch, H., Albrecht, D., Hecker, M., & Engelmann, S. (2008). Proteomic analysis of antioxidant strategies of Staphylococcus aureus: Diverse responses of diferente oxidants. Journal of Proteomics. 8, 3139-3159. https://doi.org/10.1002/pmic.200701062

Xing, X., Zhang, Y., Wu, Q., Ge, W., & Wu, C. (2016). Prevalence and characterization of Staphylococcus aureus isolated from goat milk powder processing, Food Control, 59, 644 – 650. https://doi.org/10.1016/j.foodcont.2015.06.042

Yu, H., Liu, Y., Yang, F., Cie, Y., Guo, T., Cheng, Y., & Yaho, Weirong. (2021). Combined an acoustic pressure simulation of ultrasonic radiation and experimental studies to evaluate control efficacy of high-intensity ultrasound against Staphylococcus aureus biofilm. Ultrasonics Sonochemistry, 79, 105764. https://doi.org/10.1016/j.ultsonch.2021.105764

Zouaghi, S., Bellayer, S., Thomy, V., Dargent, T., Coffinier, Y., Andre, C., Delaplace G., & Jimenez, M. (2019). Biomimetic surface modifications of stainlesssteel targeting dairy fouling mitigation and bacterial adhesion. Food and Bioproducts Processing,113,32-38. https://doi.org/10.1016/j.fbp.2018.10.012

Zurita, J., Mejia, C., & Guzman, B. M. (2010). Diagnosis and susceptibility testing of methicillin-resistant Staphylococcus aureus in Latin America. Journal of Infectious Diases, 14, 1-7. https://doi.org/10.1590/S1413-86702010000800005

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Published

29/07/2022

How to Cite

EMILIANO, J. V. dos S.; MARTINS, E. .; FREITAS, R. de .; CARVALHO, A. F. de; PERRONE, Ítalo T. Assessment of the development of Staphylococcus aureus during the production of soro on a laboratory scale. Research, Society and Development, [S. l.], v. 11, n. 10, p. e254111022450, 2022. DOI: 10.33448/rsd-v11i10.22450. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/22450. Acesso em: 30 nov. 2022.

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Agrarian and Biological Sciences