{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T07:15:45Z","timestamp":1788419745582,"version":"build-2803163510"},"reference-count":141,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T00:00:00Z","timestamp":1788393600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    Preventing toxin formation by proteolytic\n                    <jats:italic>Clostridium botulinum<\/jats:italic>\n                    is critical for food safety but remains a challenge for example when developing or reformulating various products including sodium-reduced or nitrite-free foods. Validated predictive food microbiology models can support this process by identifying combinations of product characteristics and storage conditions that prevent growth and toxin formation. An existing cardinal parameter growth and growth boundary model (\n                    <jats:xref>Koukou et al., 2022b<\/jats:xref>\n                    ), including the effect of 11 environmental factors and their interactions, was extended to predict time-to-toxicity (TTT) for proteolytic\n                    <jats:italic>C. botulinum<\/jats:italic>\n                    . Data from 962 published TTT experiments were compiled to evaluate performance for different versions of this model. Product characteristics, storage conditions and TTT were collected for meat, poultry, vegetables, seafood, dough, processed cheese, other cheeses and uncategorized foods. These data, with 648 TTT positive and 314 TTT negative, covered a wide range of environmental factors and included responses for 138 proteolytic\n                    <jats:italic>C. botulinum<\/jats:italic>\n                    strains. Model performance was evaluated using percentages of fail-dangerous, fail-safe and correct predictions along with bias and accuracy factors for predicted and observed TTT. Model performance was markedly different for non-dairy and dairy foods. For non-dairy foods and within a wide range of applicability, including 494 TTT-responses, the new and extensive Koukou-TTT-model had 0.2% fail-dangerous TTT predictions and bias\/accuracy factors of 0.53\/2.5. For dairy products (\n                    <jats:italic>n<\/jats:italic>\n                    \u202f=\u202f312), including processed and other cheeses, the Koukou-TTT-model provided 26.0% fail-dangerous TTT predictions. This unacceptable model performance was primarily due to calcium complexation with citric and lactic acids which reduced the inhibiting effect of these organic acids in the studied dairy foods. The Koukou-TTT-model was modified to predict the effect of total, rather than undissociated, concentrations of citric and lactic acids in dairy foods. This modified model predicted 144 TTT-responses with 0.0% fail-dangerous TTT predictions and bias\/accuracy factors of 0.37\/4.42. The original and the modified growth and growth boundary Koukou-models can be used, within defined and wide ranges of applicability, to determine combinations of product characteristics and storage conditions where growth and TTT for proteolytic\n                    <jats:italic>C. botulinum<\/jats:italic>\n                    are prevented in meat, poultry, vegetables, seafood, dough and dairy products.\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2026.1898380","type":"journal-article","created":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T06:43:27Z","timestamp":1788417807000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Proteolytic Clostridium botulinum (group I) \u2013 evaluation of predictive models for time-to-toxicity and identification of product characteristics that prevent growth and toxin formation in different types of foods"],"prefix":"10.3389","volume":"17","author":[{"given":"Edgar Remmet","family":"Snoeck","sequence":"first","affiliation":[{"name":"Food Microbiology and Hygiene, DTU National Food Institute, Technical University of Denmark (DTU)","place":["Kgs. Lyngby, Denmark"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ioulia","family":"Koukou","sequence":"additional","affiliation":[{"name":"Food Microbiology and Hygiene, DTU National Food Institute, Technical University of Denmark (DTU)","place":["Kgs. Lyngby, Denmark"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paw","family":"Dalgaard","sequence":"additional","affiliation":[{"name":"Food Microbiology and Hygiene, DTU National Food Institute, Technical University of Denmark (DTU)","place":["Kgs. Lyngby, Denmark"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,9,3]]},"reference":[{"key":"ref1","volume-title":"Report on Botulinum Neurotoxin-Producing Clostridia Working Group on Botulinum Neurotoxin-Producing Clostridia","year":"2023"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1956","DOI":"10.4315\/0362-028X.JFP-11-082","article-title":"Food safety objective approach for controlling Clostridium botulinum growth and toxin production in commercially sterile foods","volume":"74","author":"Anderson","year":"2011","journal-title":"J. Food Prot."},{"key":"ref3","year":"2022"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"324","DOI":"10.4315\/0362-028x-61.3.324","article-title":"Growth and toxin production by Clostridium botulinum on inoculated fresh-cut packaged vegetables","volume":"61","author":"Austin","year":"1998","journal-title":"J. Food Prot."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"1136","DOI":"10.1111\/j.1365-2621.1986.tb13066.x","article-title":"Effects of sodium chloride reduction and polyphosphate addition on Clostridium botulinum toxin production in Turkey frankfurters","volume":"51","author":"Barbut","year":"1986","journal-title":"J. Food Sci."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1128\/jb.79.1.18-23.1960","article-title":"Physiology of toxin production by Clostridium botulinum types A and B","volume":"79","author":"Bonventre","year":"1960","journal-title":"J. Bacteriol."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1150","DOI":"10.1128\/aem.45.3.1150-1152.1983","article-title":"Clostridium botulinum type A growth and toxin production in media and process cheese spread","volume":"45","author":"Briozzo","year":"1983","journal-title":"Appl. Environ. Microbiol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"66","DOI":"10.3989\/gya.2000.v51.i1-2.408","article-title":"The role of lipids in controlling microbial growth","volume":"51","author":"Brocklehurst","year":"2000","journal-title":"Grasas Aceites"},{"key":"ref9","volume-title":"The Merck Index: An Encyclopedia of Chemicals, Drugs and Biologicals","author":"Budavari","year":"1989"},{"key":"ref10","author":"Buege","year":"1980"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1016\/j.resmic.2014.10.010","article-title":"Genomes, neurotoxins and biology of Clostridium botulinum group I and group II","volume":"166","author":"Carter","year":"2014","journal-title":"Res. Microbiol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"41","DOI":"10.3892\/br.2022.1524","article-title":"Foodborne botulism: a brief review of cases transmitted by cheese products (review)","volume":"16","author":"Chaidoutis","year":"2022","journal-title":"Biomed. Rep."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1106","DOI":"10.1093\/ije\/dyac046","article-title":"Nitrites and nitrates from food additives and natural sources and cancer risk: results from the NutriNet-Sant\u00e9 cohort","volume":"51","author":"Chazelas","year":"2022","journal-title":"Int. J. Epidemiol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"733","DOI":"10.1128\/am.27.4.733-737.1974","article-title":"Effect of sodium nitrite on toxin production by Clostridium botulinum in bacon","volume":"27","author":"Christiansen","year":"1974","journal-title":"Appl. Microbiol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.toxicon.2013.06.001","article-title":"Regulation of toxin synthesis in Clostridium botulinum and Clostridium tetani","volume":"75","author":"Connan","year":"2013","journal-title":"Toxicon"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"1157","DOI":"10.4315\/0362-028x-62.10.1157","article-title":"Effect of pH and CO2 on growth and toxin production by Clostridium botulinum in English-style crumpets packaged under modified atmospheres","volume":"62","author":"Daifas","year":"","journal-title":"J. Food Prot."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"349","DOI":"10.4315\/0362-028x-62.4.349","article-title":"Growth and toxin production by Clostridium botulinum in English-style crumpets packaged under modified atmospheres","volume":"62","author":"Daifas","year":"","journal-title":"J. Food Prot."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1046\/j.1365-2621.2000.00402.x","article-title":"Cooked and brined shrimps packed in modified atmosphere have a shelf-life of >7 months at 0 \u00b0C, but spoil in 4-6 days at 25 \u00b0C","volume":"35","author":"Dalgaard","year":"2000","journal-title":"Int. J. Food Sci. Technol."},{"key":"ref19","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1007\/978-1-4939-9000-9_20","volume-title":"Foodborne Bacterial Pathogens: Methods and Protocols, Methods in Molecular Biology","author":"Dalgaard","year":"2019"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1017\/S002531540004652X","article-title":"Lactate metabolism in fish","volume":"49","author":"Dando","year":"1969","journal-title":"J. Mar. Biol. Assoc. U. K."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1629","DOI":"10.3390\/encyclopedia4040107","article-title":"Distribution of salts in milk and cheese: critical methodological aspects","volume":"4","author":"Deshwal","year":"2024","journal-title":"Encyclopedia"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1128\/aem.55.3.656-660.1989","article-title":"Combined effect of water activity and pH on inhibition of toxin production by Clostridium botulinum in cooked, vacuum-packed potatoes","volume":"55","author":"Dodds","year":"1989","journal-title":"Appl. Environ. Microbiol."},{"key":"ref23","first-page":"97","volume-title":"Foodborne Disease Handbook. Vol 1. Diseases Caused by Bacteria","author":"Dodds","year":"1994"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/j.ijfoodmicro.2014.12.022","article-title":"Anaerobic sporeformers and their significance with respect to milk and dairy products","volume":"197","author":"Doyle","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref25","volume-title":"Commission Regulation (EU) 2023\/2108 of 6 October 2023 Amending annex II to Regulation (EC) No 1333\/2008 of the European Parliament and of the Council and the annex to Commission Regulation (EU) No 231\/2012 as Regards Food Additives Nitrites (E 249\u2013250) and Nitrates (E 251\u2013252)","year":"2023"},{"key":"ref26","volume-title":"Technical Guidance Document on challenge Tests and Durability Studies for Assessing shelf-life of Ready-to-eat Foods Related to","year":"2026"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"S73","DOI":"10.1093\/cid\/cix846","article-title":"The epidemiology of foodborne botulism outbreaks: a systematic review","volume":"66","author":"Fleck-Derderian","year":"2018","journal-title":"Clin. Infect. Dis."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"1792","DOI":"10.1093\/cid\/ciz700","article-title":"What links the mascarpone and nacho cheese sauce outbreaks of botulism","volume":"70","author":"Franciosa","year":"2020","journal-title":"Clin. Infect. Dis."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1111\/j.1365-2672.1987.tb02680.x","article-title":"The effect of sodium chloride and temperature on the rate and extent of growth of Clostridium botulinum type a in pasteurized pork slurry","volume":"62","author":"Gibson","year":"1987","journal-title":"J. Appl. Bacteriol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"162","DOI":"10.4315\/0362-028X-54.3.162","article-title":"Relationship between water activity of fresh pasta and toxin production by proteolytic Clostridium botulinum","volume":"54","author":"Glass","year":"1991","journal-title":"J. Food Prot."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"100271","DOI":"10.1016\/j.jfp.2024.100271","article-title":"Inhibition of Listeria monocytogenes and Clostridium botulinum in uncured shredded pork and Turkey packaged under reduced oxygen conditions","volume":"87","author":"Glass","year":"2024","journal-title":"J. Food Prot."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"1687","DOI":"10.4315\/0362-028x-67.8.1687","article-title":"Factors that contribute to the botulinal safety of reduced-fat and fat-free process cheese products","volume":"67","author":"Glass","year":"","journal-title":"J. Food Prot."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1016\/j.fm.2004.03.002","article-title":"Antagonistic effect of fat on the antibotulinal activity of food preservatives and fatty acids","volume":"21","author":"Glass","year":"","journal-title":"Food Microbiol."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"1478","DOI":"10.4315\/0362-028X.JFP-17-027","article-title":"Inhibition of Clostridium botulinum in model reduced-sodium pasteurized prepared cheese products","volume":"80","author":"Glass","year":"2017","journal-title":"J. Food Prot."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"1259","DOI":"10.4315\/0362-028X.JFP-17-011","article-title":"Effect of cultured celery juice, temperature, and product composition on the inhibition of proteolytic Clostridium botulinum toxin production","volume":"80","author":"Golden","year":"2017","journal-title":"J. Food Prot."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1111\/j.1365-2672.1986.tb03756.x","article-title":"The effect of citric acid on growth of proteolytic strains of Clostridium botulinum","volume":"61","author":"Graham","year":"1986","journal-title":"J. Appl. Bacteriol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1038\/s41538-023-00228-9","article-title":"Effects of sodium nitrite reduction, removal or replacement on cured and cooked meat for microbiological growth, food safety, colon ecosystem, and colorectal carcinogenesis in Fischer 344 rats","volume":"7","author":"Gu\u00e9raud","year":"2023","journal-title":"NPJ Sci. Food."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1655","DOI":"10.3168\/jds.S0022-0302(02)74238-0","article-title":"Effect of pH and calcium concentration on some textural and functional properties of mozzarella cheese","volume":"85","author":"Guinee","year":"2002","journal-title":"J. Dairy Sci."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1051\/dst\/2009009","article-title":"The effect of calcium content of Cheddar-style cheese on the biochemical and rheological properties of processed cheese","volume":"89","author":"Guinee","year":"2009","journal-title":"Dairy Sci. Technol."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1007\/s10953-007-9233-3","article-title":"Complex formation of acetic acid with ca(II) and Mg(II) under physiological conditions","volume":"37","author":"Hacht","year":"2007","journal-title":"J. Solut. Chem."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"245","DOI":"10.4315\/0362-028X-42.3.245","article-title":"Effect of salt content and pH on toxigenesis by Clostridium botulinum in caviar","volume":"42","author":"Hauschild","year":"1979","journal-title":"J. Food Prot."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"500","DOI":"10.4315\/0362-028X-45.6.500","article-title":"Contribution of nitrite to the control of Clostridium botulinum in liver sausage","volume":"45","author":"Hauschild","year":"1982","journal-title":"J. Food Prot."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/0168-1605(86)90013-9","article-title":"Primary multiplication of Clostridium botulinum type A in mustard-miso stuffing of 'karashi-renkon' (deep-fried mustard-stuffed lotus root)","volume":"3","author":"Hayashi","year":"1986","journal-title":"Int. J. Food Microbiol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"807","DOI":"10.4315\/0362-028X-46.9.807","article-title":"Acid enhancement of Clostridium botulinum inhibition in ham and bacon prepared with potassium sorbate and sorbic acid","volume":"46","author":"Huhtanen","year":"1983","journal-title":"J. Food Prot."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1109\/MCSE.2007.55","article-title":"Matplotlib: a 2D graphics environment","volume":"9","author":"Hunter","year":"2007","journal-title":"Comput. Sci. Eng."},{"key":"ref46","volume-title":"Microorganisms in Foods 5: Characteristics of Microbial Pathogens","year":"1996"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1128\/aem.32.1.121-124.1976","article-title":"Effect of acid and salt concentration in fresh-pack pickles on the growth of Clostridium botulinum spores","volume":"32","author":"Ito","year":"1976","journal-title":"Appl. Environ. Microbiol."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"1634","DOI":"10.1111\/j.1365-2621.1978.tb02564.x","article-title":"Effect of pH on the growth of Clostridium botulinum in canned figs","volume":"43","author":"Ito","year":"1978","journal-title":"J. Food Sci."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"1782","DOI":"10.1111\/j.1365-2621.1978.tb07413.x","article-title":"Effect of sorbic acid and sodium nitrite on Clostridium botulinum outgrowth and toxin production in canned comminuted pork","volume":"43","author":"Ivey","year":"1978","journal-title":"J. Food Sci."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"621","DOI":"10.4315\/0362-028X-41.8.621","article-title":"Effect of potassium sorbate on toxinogenesis by Clostridium botulinum in bacon","volume":"41","author":"Ivey","year":"1978","journal-title":"J. Food Prot."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"105518","DOI":"10.1016\/j.idairyj.2022.105518","article-title":"Temperature effects on calcium partition kinetics in pasteurised skim milk during storage","volume":"137","author":"Jiang","year":"2023","journal-title":"Int. Dairy J."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/s41240-017-0057-9","article-title":"Postmortem changes in physiochemical and sensory properties of red snow crab (Chionoecetes japonicus) leg muscle during freeze storage","volume":"20","author":"Jun","year":"2017","journal-title":"Fish. Aquat. Sci."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1006\/fmic.1999.0270","article-title":"Proteolytic Clostridium botulinum growth at 12\u201348\u00b0C simulating the cooling of cooked meat: development of a predictive model","volume":"16","author":"Juneja","year":"1999","journal-title":"Food Microbiol."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"103618","DOI":"10.1016\/j.fm.2020.103618","article-title":"A predictive growth model for Clostridium botulinum during cooling of cooked uncured ground beef","volume":"93","author":"Juneja","year":"","journal-title":"Food Microbiol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"102960","DOI":"10.1016\/j.ifset.2022.102960","article-title":"Predictive model for growth of Clostridium botulinum from spores at temperatures applicable to cooling of cooked ground pork","volume":"77","author":"Juneja","year":"2022","journal-title":"Innov. Food Sci. Emerg. Technol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"110695","DOI":"10.1016\/j.foodres.2021.110695","article-title":"Predictive model for growth of Clostridium botulinum from spores during cooling of cooked ground chicken","volume":"149","author":"Juneja","year":"","journal-title":"Food Res. Int."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"909","DOI":"10.3168\/jds.S0022-0302(87)80094-2","article-title":"Integrated roles of lactate, ammonia, and calcium in texture development of mold surface-ripened cheese","volume":"70","author":"Karahadian","year":"1987","journal-title":"J. Dairy Sci."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.4315\/0362-028X-68.5.1005","article-title":"Growth and toxin production by Clostridium botulinum in steamed rice aseptically packed under modified atmosphere","volume":"68","author":"Kasai","year":"2005","journal-title":"J. Food Prot."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1128\/am.13.4.521-526.1965","article-title":"Factors affecting the development of Clostridium botulinum in whole milk","volume":"13","author":"Kaufmann","year":"1965","journal-title":"Appl. Microbiol."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"1338","DOI":"10.5851\/kosfa.2016.36.1.29","article-title":"Pork quality traits according to postmortem pH and temperature in Berkshire","volume":"29","author":"Kim","year":"2016","journal-title":"Asian Australas. J. Anim. Sci."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"468","DOI":"10.4315\/0362-028X-71.3.468","article-title":"Growth and toxin production of proteolytic Clostridium botulinum in aseptically steamed rice products at pH 4.6 to 6.8, packed under modified atmosphere, using a deoxidant pack","volume":"71","author":"Kimura","year":"2008","journal-title":"J. Food Prot."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"103931","DOI":"10.1016\/j.fm.2021.103931","article-title":"Extensive growth and growth boundary model for non-proteolytic Clostridium botulinum \u2013 evaluation and validation with MAP and smoked foods","volume":"102","author":"Koukou","year":"","journal-title":"Food Microbiol."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"109162","DOI":"10.1016\/j.ijfoodmicro.2021.109162","article-title":"Cardinal parameter growth and growth boundary model for non-proteolytic Clostridium botulinum \u2013 effect of eight environmental factors","volume":"346","author":"Koukou","year":"2021","journal-title":"Int. J. Food Microbiol."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"104060","DOI":"10.1016\/j.fm.2022.104060","article-title":"Clostridium sporogenes as surrogate for proteolytic C. botulinum - development and validation of extensive growth and growth-boundary model","volume":"107","author":"Koukou","year":"","journal-title":"Food Microbiol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1006\/fmic.2001.0433","article-title":"Growth and toxin production by Clostridium botulinum in fish (Mugil cephalus) and shrimp (Penaeus indicus) tissue homogenates stored under vacuum","volume":"18","author":"Lalitha","year":"2001","journal-title":"Food Microbiol."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"588","DOI":"10.4315\/0362-028X-54.8.588","article-title":"Effect of headspace C02 concentration on toxin production by Clostridium botulinum in MAP, irradiated fresh pork","volume":"54","author":"Lambert","year":"1991","journal-title":"J. Food Prot."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.4315\/0362-028X-60.10.1208","article-title":"Evaluation of the botulism hazard from vegetables in modified atmosphere packaging","volume":"60","author":"Larson","year":"1997","journal-title":"J. Food Prot."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/S0168-1605(01)00640-7","article-title":"Modelling the growth kinetics of Listeria as a function of temperature, pH and organic acid concentration","volume":"73","author":"Le Marc","year":"2002","journal-title":"Int. J. Food Microbiol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"788","DOI":"10.46234\/ccdcw2022.114","article-title":"Epidemiological analysis of foodborne botulism outbreaks \u2014 China, 2004\u20132020","volume":"4","author":"Li","year":"2022","journal-title":"China CDC Wkly"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1080\/10408390802544405","article-title":"Clostridium botulinum in cattle and dairy products","volume":"50","author":"Lindstr\u00f6m","year":"2010","journal-title":"Crit. Rev. Food Sci. Nutr."},{"key":"ref71","doi-asserted-by":"publisher","first-page":"105023","DOI":"10.1016\/j.idairyj.2021.105023","article-title":"Temperature effects on spontaneous supersaturation of calcium citrate in presence of lactate","volume":"118","author":"Liu","year":"2021","journal-title":"Int. Dairy J."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"2919","DOI":"10.1128\/aem.70.5.2919-2927.2004","article-title":"Relative neurotoxin gene expression in Clostridium botulinum type B, determined using quantitative reverse transcription-PCR","volume":"70","author":"L\u00f6venklev","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"2934","DOI":"10.1111\/j.1365-2621.2002.tb08841.x","article-title":"Effects of fruit size on fresh cucumber composition and the chemical and physical consequences of fermentation","volume":"67","author":"Lu","year":"2002","journal-title":"J. Food Sci."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"969","DOI":"10.1111\/j.1365-2621.1985.tb12991.x","article-title":"Toxin production in hard-cooked eggs experimentally inoculated with Clostridium botulinum","volume":"50","author":"Lubin","year":"1985","journal-title":"J. Food Sci."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1111\/j.1365-2672.1988.tb03381.x","article-title":"Growth and formation of toxin by Clostridium botulinum in peeled, inoculated, vacuum-packed potatoes after a double pasteurization and storage at 25 \u00b0C","volume":"64","author":"Lund","year":"1988","journal-title":"J. Appl. Bacteriol."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"713101","DOI":"10.3389\/fmicb.2021.713101","article-title":"Foodborne botulism outbreaks in the United States, 2001\u20132017","volume":"12","author":"L\u00faquez","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"2226","DOI":"10.1128\/aem.55.9.2226-2229.1989","article-title":"Sodium lactate delays toxin production by Clostridium botulinum in cook-in-bag Turkey products","volume":"55","author":"Maas","year":"1989","journal-title":"Appl. Environ. 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J. Food Sci. Technol."},{"key":"ref100","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1111\/j.1365-2621.1982.tb00187.x","article-title":"Factors controlling the growth of Clostridium botulinum types a and B in pasteurized, cured meats. III. The effect of potassium sorbate","volume":"17","author":"Roberts","year":"1982","journal-title":"Int. J. Food Sci. Technol."},{"key":"ref101","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1111\/j.1365-2621.1982.tb00233.x","article-title":"Factors controlling the growth of Clostridium botulinum types a and B in pasteurized, cured meats. V. Prediction of toxin production. Non-linear effects of storage temperature and salt concentration","volume":"17","author":"Robinson","year":"1982","journal-title":"Int. J. Food Sci. 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Microbiol."},{"key":"ref108","doi-asserted-by":"publisher","DOI":"10.2903\/fr.efsa.2025.fr-0059","article-title":"Opinion of the French Agency for Food, environmental and Occupational Health & Safety (ANSES) on the risks associated with the consumption of nitrites and nitrates","volume":"3","author":"Scippo","year":"2025","journal-title":"Food Risk Assess Europe"},{"key":"ref109","doi-asserted-by":"publisher","first-page":"3355","DOI":"10.3390\/foods11213355","article-title":"Nitrites in cured meats, health risk issues, alternatives to nitrites: a review","volume":"11","author":"Shakil","year":"2022","journal-title":"Foods"},{"key":"ref110","doi-asserted-by":"publisher","DOI":"10.3390\/nu14010180","article-title":"Calcium absorption from food products: food matrix effects","volume":"14","author":"Shkembi","year":"2022","journal-title":"Nutrients"},{"key":"ref111","doi-asserted-by":"publisher","first-page":"100002","DOI":"10.1016\/j.afres.2021.100002","article-title":"Physico-mechanical characterization of different grades of Lotus rhizome (Nelumbo nucifera Gaertn) for valorisation and smart post-harvest management","volume":"1","author":"Showkat","year":"2021","journal-title":"Appl. Food Res."},{"key":"ref112","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.foodchem.2015.03.037","article-title":"NMR approach for monitoring post-mortem changes in Atlantic salmon fillets stored at 0 and 4\u00b0C","volume":"184","author":"Shumilina","year":"2015","journal-title":"Food Chem."},{"key":"ref113","doi-asserted-by":"publisher","first-page":"229","DOI":"10.4315\/0362-028X-58.3.229","article-title":"Challenge studies with Clostridium botulinum in a sous-vide spaghetti and meat-sauce product","volume":"58","author":"Simpson","year":"1995","journal-title":"J. Food Prot."},{"key":"ref114","doi-asserted-by":"publisher","first-page":"724","DOI":"10.1111\/j.1365-2621.1999.tb15119.x","article-title":"Prevention of Clostridium botulinum type a proteolytic B and E toxin formation in refrigerated pea soup by Lactobacillus plantarum ATCC 8014","volume":"64","author":"Skinner","year":"1999","journal-title":"J. Food Sci."},{"key":"ref115","doi-asserted-by":"publisher","first-page":"1768","DOI":"10.3382\/ps.0711768","article-title":"Post-mortem biochemistry of Pekin duckling and broiler chicken pectoralis muscle","volume":"71","author":"Smith","year":"1992","journal-title":"Poultry Sci."},{"key":"ref116","doi-asserted-by":"publisher","first-page":"618","DOI":"10.4315\/0362-028X-49.8.618","article-title":"Growth and toxin production by Clostridium botulinum in sauteed onions","volume":"49","author":"Solomon","year":"1986","journal-title":"J. Food Prot."},{"key":"ref117","doi-asserted-by":"publisher","first-page":"5","DOI":"10.4315\/0362-028X-40.1.5","article-title":"Effect of low temperatures on growth of Clostridium botulinum spores in neat of the blue crab","volume":"40","author":"Solomon","year":"1977","journal-title":"J. Food Prot."},{"key":"ref118","doi-asserted-by":"publisher","first-page":"878","DOI":"10.4315\/0362-028X-57.10.878","article-title":"Growth and toxin production by Clostridium botulinum in sliced raw potatoes under vacuum with and without sulfite","volume":"57","author":"Solomon","year":"1994","journal-title":"J. Food Prot."},{"key":"ref119","doi-asserted-by":"publisher","first-page":"1639","DOI":"10.1111\/j.1365-2621.1981.tb04450.x","article-title":"Effect of modified atmosphere storage on C. botulinum toxigenesis and the spoilage microflora of salmon fillets","volume":"46","author":"Stier","year":"1981","journal-title":"J. Food Sci."},{"key":"ref120","doi-asserted-by":"publisher","first-page":"896","DOI":"10.4315\/0362-028x-44.12.896","article-title":"Production of botulinum toxin in inoculated pack studies of foil-wrapped baked potatoes","volume":"44","author":"Sugiyama","year":"1981","journal-title":"J. Food Prot."},{"key":"ref121","doi-asserted-by":"publisher","first-page":"1044","DOI":"10.4315\/0362-028X-45.11.1044","article-title":"Challenge of pasteurized process cheese spreads with Clostridium botulinum using in-process and post-process inoculation","volume":"45","author":"Tanaka","year":"1982","journal-title":"J. Food Prot."},{"key":"ref122","doi-asserted-by":"publisher","first-page":"787","DOI":"10.4315\/0362-028X-42.10.787","article-title":"A challenge of pasteurized process cheese spread with Clostridium botulinum spores","volume":"42","author":"Tanaka","year":"1979","journal-title":"J. Food Prot."},{"key":"ref123","doi-asserted-by":"publisher","first-page":"526","DOI":"10.4315\/0362-028X-49.7.526","article-title":"Evaluation of factors involved in antibotulinal properties of pasteurized process cheese spreads","volume":"49","author":"Tanaka","year":"1986","journal-title":"J. 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Agents Chemother."},{"key":"ref140","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/s0168-1605(02)00111-3","article-title":"Time-to-detection, percent-growth positive and maximum growth rate models for Clostridium botulinum 56A at multiple temperatures","volume":"77","author":"Zhao","year":"2002","journal-title":"Int. J. Food Microbiol."},{"key":"ref141","doi-asserted-by":"publisher","first-page":"26","DOI":"10.4314\/sajas.v50i1.4","article-title":"Relationship of glycogen and lactate concentrations as a pork quality indicator","volume":"50","author":"Zybert","year":"2020","journal-title":"S. Afr. J. Anim. 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