{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,20]],"date-time":"2026-06-20T18:02:29Z","timestamp":1781978549115,"version":"3.54.5"},"reference-count":24,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2019,5,23]],"date-time":"2019-05-23T00:00:00Z","timestamp":1558569600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>Possible contamination by Staphylococcus aureus of the production environment and of the meat of a canned meat production factory was analysed. A total of 108 samples were taken from nine critical control points, 13 of them were positive for S. aureus. None of the isolates produced enterotoxins. To determine how much time can elapse between can seaming and sterilisation in the autoclave without any risk of enterotoxin production by S. aureus, the growth and enterotoxin production of three enterotoxin A producing strains of S. aureus (one ATCC strain and two field strains) in canned meat before sterilisation was investigated at three different temperatures (37, 20 and 10 \u00b0C). Two types of meat were used, one with and one without sodium nitrite. In the canned products, the spiked bacteria spread throughout the meat and reached high levels. Enterotoxin production was shown to start 10 hours after incubation at 37 \u00b0C and after 48 h after incubation at 20 \u00b0C; the production of enterotoxin was always detected in the transition between the exponential and the stationary growth phase. At 10 \u00b0C, the enterotoxin was never detected. The statistical analysis of the data showed that the difference between the two different types of meat was not statistically significant (p value &gt; 0.05). Since it is well known that following heat treatment, staphylococcal enterotoxins, although still active (in in vivo assays), can be undetectable (loss of serological recognition) depending on the food matrix and pH, it is quite difficult to foresee the impact of heat treatment on enterotoxin activity. Therefore, although the bacteria are eliminated, the toxins may remain and cause food poisoning. The significance of the results of this study towards implementing good manufacturing practices and hazard analysis critical control points in a canned meat factory are discussed with reference to the management of pre-retorting steps after seaming.<\/jats:p>","DOI":"10.3390\/toxins11050291","type":"journal-article","created":{"date-parts":[[2019,5,24]],"date-time":"2019-05-24T02:22:00Z","timestamp":1558664520000},"page":"291","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Study on the Growth and Enterotoxin Production by Staphylococcus aureus in Canned Meat before Retorting"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6887-3383","authenticated-orcid":false,"given":"Luca","family":"Grispoldi","sequence":"first","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul Alexanderu","family":"Popescu","sequence":"additional","affiliation":[{"name":"Faculty of Biotechnology, University of Agronomical Science and Veterinary Medicine, 011464 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6197-5309","authenticated-orcid":false,"given":"Musafiri","family":"Karama","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Science, Department of Paraclinical Sciences, University of Pretoria, Onderstepoort 0110, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vito","family":"Gullo","sequence":"additional","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giusi","family":"Poerio","sequence":"additional","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"Borgogni","sequence":"additional","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paolo","family":"Torlai","sequence":"additional","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppina","family":"Chianese","sequence":"additional","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna Giovanna","family":"Fermani","sequence":"additional","affiliation":[{"name":"Department of prevention, Azienda Unit\u00e0 Sanitaria Locale Latina, 04012 Lazio, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4606-3261","authenticated-orcid":false,"given":"Paola","family":"Sechi","sequence":"additional","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3993-6258","authenticated-orcid":false,"given":"Beniamino","family":"Cenci-Goga","sequence":"additional","affiliation":[{"name":"Medicina Veterinaria, Laboratorio di Ispezione degli Alimenti di Origine Animale, Universit\u00e0 degli Studi di Perugia, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,5,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"S69","DOI":"10.1016\/j.ijfoodmicro.2010.03.028","article-title":"Prolonged expression and production of Staphylococcus aureus enterotoxin A in processed pork meat","volume":"141","author":"Borch","year":"2010","journal-title":"Int. J. Food Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/j.sjbs.2014.08.003","article-title":"Molecular identification of isolated fungi, microbial and heavy metal contamination of canned meat products sold in Riyadh, Saudi Arabia","volume":"22","author":"Nasser","year":"2015","journal-title":"Saudi J. Biol. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1097\/00007611-197701000-00004","article-title":"Type A botulism from commercially canned beef stew","volume":"70","author":"Blake","year":"1977","journal-title":"South. Med. J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1017\/S0022172400022865","article-title":"Observations on the microbiological flora of canned Parma ham","volume":"71","author":"Cragg","year":"1973","journal-title":"J. Hyg."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1007\/BF01353406","article-title":"The amylase-producing microflora of semi-preserved canned sausages: Identification of the bacteria and characterization of their amylases","volume":"169","author":"Mitrica","year":"1979","journal-title":"Z. Fur Lebensm.-Unters. Forsch."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1080\/09603123.2014.958135","article-title":"Tracing Staphylococcus aureus in small and medium-sized food-processing factories on the basis of molecular sub-species typing","volume":"25","author":"Kuchta","year":"2015","journal-title":"Int. J. Environ. Health Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.4315\/0362-028X-66.9.1693","article-title":"Enterotoxin Production by Staphylococcus aureus Isolated from Mastitic Cows","volume":"66","author":"Karama","year":"2003","journal-title":"J. Food Prot."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.3168\/jds.2018-15373","article-title":"Characterization of enterotoxin producing Staphylococcus aureus isolated from mastitic cows","volume":"102","author":"Grispoldi","year":"2019","journal-title":"J. Dairy Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1111\/j.1574-6976.2011.00311.x","article-title":"Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation","volume":"36","author":"Hennekinne","year":"2012","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1017\/S0950268802007951","article-title":"An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: Estimation of enterotoxin A in the incriminated milk and powdered skim milk","volume":"130","author":"Asao","year":"2003","journal-title":"Epidemiol. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1080\/08927019109378226","article-title":"Contribution of surface attachment to the establishment of micro-organisms in food processing plants: A review","volume":"5","author":"Notermans","year":"1991","journal-title":"Biofouling"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Denayer, S., Delbrassinne, L., Nia, Y., and Botteldoorn, N. (2017). Food-Borne Outbreak Investigation and Molecular Typing: High Diversity of Staphylococcus aureus Strains and Importance of Toxin Detection. Toxins, 9.","DOI":"10.3390\/toxins9120407"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1111\/j.1365-2672.2006.02957.x","article-title":"Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea","volume":"101","author":"Cha","year":"2006","journal-title":"J. Appl. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/j.ijfoodmicro.2006.10.050","article-title":"Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France","volume":"115","author":"Kerouanton","year":"2007","journal-title":"Int. J. Food Microbiol."},{"key":"ref_15","first-page":"41","article-title":"Canned foods - the problems of food poisoning and spoilage","volume":"4","author":"Gilbert","year":"1982","journal-title":"Health Hyg."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1017\/S0022172400060514","article-title":"Studies on the growth and survival of Staphylococcus aureus in corned beef","volume":"91","author":"Mansfield","year":"1983","journal-title":"J. Hyg."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"465","DOI":"10.4315\/0362-028X-43.6.465","article-title":"Food Poisoning Associated with Post-Process Leakage (PPL) in Canned Foods","volume":"43","author":"Stersky","year":"1980","journal-title":"J. Food Protect."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4665","DOI":"10.1128\/JB.186.14.4665-4684.2004","article-title":"Global Gene Expression in Staphylococcus aureus biofilms","volume":"186","author":"Beenken","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2663","DOI":"10.1128\/AEM.71.5.2663-2676.2005","article-title":"Differential Gene Expression Profiling of Staphylococcus aureus Cultivated under Biofilm and Planktonic Conditions","volume":"71","author":"Resch","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1271\/bbb.120391","article-title":"Temperature dependence of the production of staphylococcal enterotoxin a by Staphylococcus aureus","volume":"77","author":"Tsutsuura","year":"2013","journal-title":"Biosci. Biotech. Biochem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.ijfoodmicro.2009.05.023","article-title":"Modelling the growth boundaries of Staphylococcus aureus: Effect of temperature, pH and water activity","volume":"133","author":"Valero","year":"2009","journal-title":"Int. J. Food Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1126\/science.3160112","article-title":"Staphylococcal enterotoxin A is encoded by phage","volume":"229","author":"Betley","year":"1985","journal-title":"Science"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Schelin, J., Susilo, Y.B., and Johler, S. (2017). Expression of staphylococcal enterotoxins under stress encountered during food production and preservation. Toxins, 9.","DOI":"10.3390\/toxins9120401"},{"key":"ref_24","first-page":"68","article-title":"Factors in canned ham controlling Cl. botulinum and Staph. aureus","volume":"7","author":"Scott","year":"1955","journal-title":"Annales de l\u2019Institut Pasteur de Lille"}],"container-title":["Toxins"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6651\/11\/5\/291\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:54:28Z","timestamp":1760187268000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6651\/11\/5\/291"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,5,23]]},"references-count":24,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2019,5]]}},"alternative-id":["toxins11050291"],"URL":"https:\/\/doi.org\/10.3390\/toxins11050291","relation":{},"ISSN":["2072-6651"],"issn-type":[{"value":"2072-6651","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,5,23]]}}}