https://doi.org/10.4081/ijfs.2022.9983
Investigation on the microbiological hazards in an artisanal soft cheese produced in northern Italy and its production environment in different seasonal periods
Submitted: 15 July 2021
Accepted: 10 January 2022
Published: 22 June 2022
Accepted: 10 January 2022
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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The present study aimed at assessing the occurrence of microbiological hazards (Listeria monocytogenes, Staphylococcus aureus, Salmonella spp. and Escherichia coli O157) in an artisanal soft cheese produced in northern Italy. In the same product total bacterial count, lactic acid bacteria and Enterobacteriaceae were enumerated, and pH and water activity measured in two batches sampled in summer and winter. Samples of raw materials, environmental swabs from the production processes and cheese during 15 days of storage at 2 and 8°C as well as dynamic temperature of 2°C for 5 days and 8°C for 10 days were collected and tested. The load of total bacterial count was significantly higher in the winter batch in comparison to the summer one, with a significant increase at the end of the storage period also noticed for lactic acid bacteria. Statistical higher values of pH were registered in raw materials and end of storage in winter batch. S. aureus was confirmed only in the winter batch within samples (n=4) of stored cheese. On plates used for E. coli O157 detection, colonies of Klebsiella pneumoniae and Klebsiella oxytoca were isolated. The results suggest that the highest bacterial population in the winter batch was associated to a higher pH in stored cheese and a higher number of biological hazards identified. Their isolation started in the maturation room suggesting this step as relevant for possible cheese contamination.
Ajayasree TS, Borkar SG, 2018. Survival of Klebsiella pneumoniae strain borkar in pomegranate orchard soil and its tolerance to temperature and pH. J Appl Biotechnol Bioeng 5:299-301.
DOI: https://doi.org/10.15406/jabb.2018.05.00153
Brakstad OG, Aasbakk K, Maeland JA, 1992. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 30:1654-60.
DOI: https://doi.org/10.1128/jcm.30.7.1654-1660.1992
Centers for Disease Control and Prevention (CDC), 2021. CDC Investigation Notice: CDC investigating outbreak of Salmonella infections linked to cashew brie cheese. https://www.cdc.gov/media/releases/2021/s0423-cashew-brie-cheese-salmonella.html. Accessed: July 11th, 2021.
Chander Y, Ramakrishnan MA, Jindal N, Hanson K, Goyal SM, 2011. Differentiation of Klebsiella pneumoniae and K. oxytoca by Multiplex Polymerase Chain Reaction. Intern J Appl Res Vet Med 9:138.
Choi KH, Lee H, Lee S, Kim S, Yoon Y, 2016. Cheese Microbial Risk Assessments - A Review. Asian-Australas J Anim Sci 29:307-314.
DOI: https://doi.org/10.5713/ajas.15.0332
Dos Santos Rosario AIL, da Silva Mutz Y, Castro VS, da Silva MCA, Conte-Junior CA, da Costa MP, 2021. Everybody loves cheese: crosslink between persistence and virulence of Shiga-toxin Escherichia coli. Crit Rev Food Sci Nutr 61:1877-99.
DOI: https://doi.org/10.1080/10408398.2020.1767033
European Union, 2012. Regulation (EU) No. 1151/2012 of the European Parliament and of the Council of 21 November 2012 on quality schemes for agricultural products and foodstuffs. Official Journal of the European Union 343:1-29.
Fusco V, Chieffi D, Fanelli F, 2020. Microbial quality and safety of milk and milk products in the 21st century. Compr Rev Food Sci Food Saf 19:2013–49.
DOI: https://doi.org/10.1111/1541-4337.12568
ISO, 1998. Microbiology of food and animal feeding stuffs. Horizontal method for the numeration of mesophilic lactic acid bacteria - Colony-count technique at 30 degrees C. ISO Norm 15214:1998. International Standardization Organization ed., Geneva, Switzerland.
ISO, 1999. International Standards Meat and Meat Products. Measurement of the pH (Reference Method). ISO Norm 2917:1999. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2001. Microbiology of food and animal feeding stuffs. Horizontal method for the detection of Escherichia coli O157. ISO Norm 16654:2001. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2004. 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. ISO Norm ISO 6888-1/A1:2004. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2004. Microbiology of food and animal feeding stuffs. Determination of water activity. ISO Norm 21807:2004. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2013. Microbiology of the food chain. Horizontal method for the enumeration of microorganisms - Part 2: Colony count at 30 °C by the surface plating technique. ISO Norm 4833-2:2013. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2017. Microbiology of the food chain. Horizontal method for the detection, enumeration and serotyping of Salmonella - Part 1: Detection of Salmonella spp. ISO Norm 6579-1:2017. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2017. Microbiology of the food chain. Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. - Part 1: Detection method. ISO Norm 11290-1:2017. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2017. Microbiology of the food chain. Horizontal method for the detection and enumeration of Enterobacteriaceae - Part 2: Colony‐count technique. ISO Norm 21528‐2:2017. International Standardization Organization ed., Geneva, Switzerland.
Jackson KA, Gould LH, Hunter JC, Kucerova Z, Jackson B, 2018. Listeriosis outbreaks associated with soft cheeses, United States, 1998–2014. Emerg Infect Dis 24:1116-8.
DOI: https://doi.org/10.3201/eid2406.171051
Johler S, Weder D, Bridy C, Huguenin MC, Robert L, Hummerjohann J, Stephan R, 2015a. Outbreak of staphylococcal food poisoning among children and staff at a Swiss boarding school due to soft cheese made from raw milk. J Dairy Sci 98:2944-8.
DOI: https://doi.org/10.3168/jds.2014-9123
Johler S, Giannini P, Jermini M, Hummerjohann J, Baumgartner A, Stephan R, 2015b. Further evidence for staphylococcal food poisoning outbreaks caused by egc-encoded enterotoxins. Toxins 7:997-1004.
DOI: https://doi.org/10.3390/toxins7030997
Johler S, Macori G, Bellio A, Acutis PL, Gallina S, Decastelli L, 2018. Characterization of Staphylococcus aureus isolated along the raw milk cheese production process in artisan dairies in Italy. J Dairy Sci 101:2915-20.
DOI: https://doi.org/10.3168/jds.2017-13815
Kongo JM, Gomes AP, Malcata FX, 2008. Monitoring and identification of bacteria associated with safety concerns in the manufacture of São Jorge, a Portuguese traditional cheese from raw cow's milk. J Food Protect 71:986-992.
DOI: https://doi.org/10.4315/0362-028X-71.5.986
Martinez-Rios V, Dalgaard P, 2018. Prevalence of Listeria monocytogenes in European cheeses: A systematic review and meta-analysis. Food Control 84:205-14.
DOI: https://doi.org/10.1016/j.foodcont.2017.07.020
Massa S, Gardini F, Sinigaglia M, Guerzoni ME, 1992. Klebsiella pneumoniae as a spoilage organism in mozzarella cheese. J Dairy Sci 75:1411-4.
DOI: https://doi.org/10.3168/jds.S0022-0302(92)77894-1
Perelle S, Dilasser F, Grout J, Fach P, 2004. Detection by 5'-nuclease PCR of Shiga-toxin producing Escherichia coli O26, O55, O91, O103, O111, O113, O145 and O157:H7, associated with the world's most frequent clinical cases. Mol Cell Probes 18:185-92.
DOI: https://doi.org/10.1016/j.mcp.2003.12.004
Rabello RF, Moreira BM, Lopes RM, Teixeira LM, Riley LW, Castro AC, 2007. Multilocus sequence typing of Staphylococcus aureus isolates recovered from cows with mastitis in Brazilian dairy herds. J Med Microbiol 56:1505-11.
DOI: https://doi.org/10.1099/jmm.0.47357-0
Singh L, Cariappa MP, Kaur M, 2016. Klebsiella oxytoca: An emerging?. Med J Armed Forces India 72:59-61.
DOI: https://doi.org/10.1016/j.mjafi.2016.05.002
Tornadijo E, Fresno JM, Carballo J, Martín-Sarmiento R, 1993. Study of Enterobacteriaceae throughout the manufacturing and ripening of hard goats' cheese. J Appl Bacteriol 75:240-6.
DOI: https://doi.org/10.1111/j.1365-2672.1993.tb02772.x
Vaishnavi C, Singh S, Grover R, Singh K, 2001. Bacteriological study of Indian cheese (paneer) sold in Chandigarh. Indian J Med Microbiol 19:224-6.
Wesley IV, Harmon KM, Dickson JS, Schwartz AR, 2002. Application of a multiplex polymerase chain reaction assay for the simultaneous confirmation of Listeria monocytogenes and other Listeria species in turkey sample surveillance. J Food Prot 65:780-5.
DOI: https://doi.org/10.4315/0362-028X-65.5.780
How to Cite
1.
Crippa C, Pasquali F, Lucchi A, Gambi L, De Cesare A. Investigation on the microbiological hazards in an artisanal soft cheese produced in northern Italy and its production environment in different seasonal periods. Ital J Food Safety [Internet]. 2022 Jun. 22 [cited 2024 Nov. 21];11(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/9983
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