{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T22:37:57Z","timestamp":1790203077155,"version":"4.1.0"},"reference-count":41,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,4,28]],"date-time":"2023-04-28T00:00:00Z","timestamp":1682640000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Major Science and Technology special sub-projects in Henan Province","award":["221100110500"],"award-info":[{"award-number":["221100110500"]}]},{"name":"Major Science and Technology special sub-projects in Henan Province","award":["212300410008"],"award-info":[{"award-number":["212300410008"]}]},{"name":"Major Science and Technology special sub-projects in Henan Province","award":["22 IRTS THN021"],"award-info":[{"award-number":["22 IRTS THN021"]}]},{"name":"Major Science and Technology special sub-projects in Henan Province","award":["CARS-37"],"award-info":[{"award-number":["CARS-37"]}]},{"name":"Science Foundation for Outstanding Youth of Henan Province","award":["221100110500"],"award-info":[{"award-number":["221100110500"]}]},{"name":"Science Foundation for Outstanding Youth of Henan Province","award":["212300410008"],"award-info":[{"award-number":["212300410008"]}]},{"name":"Science Foundation for Outstanding Youth of Henan Province","award":["22 IRTS THN021"],"award-info":[{"award-number":["22 IRTS THN021"]}]},{"name":"Science Foundation for Outstanding Youth of Henan Province","award":["CARS-37"],"award-info":[{"award-number":["CARS-37"]}]},{"name":"Science and Technology Innovation Team of Henan Universities","award":["221100110500"],"award-info":[{"award-number":["221100110500"]}]},{"name":"Science and Technology Innovation Team of Henan Universities","award":["212300410008"],"award-info":[{"award-number":["212300410008"]}]},{"name":"Science and Technology Innovation Team of Henan Universities","award":["22 IRTS THN021"],"award-info":[{"award-number":["22 IRTS THN021"]}]},{"name":"Science and Technology Innovation Team of Henan Universities","award":["CARS-37"],"award-info":[{"award-number":["CARS-37"]}]},{"name":"National modern agriculture (beef yak) industrial technology system construction special","award":["221100110500"],"award-info":[{"award-number":["221100110500"]}]},{"name":"National modern agriculture (beef yak) industrial technology system construction special","award":["212300410008"],"award-info":[{"award-number":["212300410008"]}]},{"name":"National modern agriculture (beef yak) industrial technology system construction special","award":["22 IRTS THN021"],"award-info":[{"award-number":["22 IRTS THN021"]}]},{"name":"National modern agriculture (beef yak) industrial technology system construction special","award":["CARS-37"],"award-info":[{"award-number":["CARS-37"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Foods"],"abstract":"<jats:p>Bacteriostats, as chemical substances that inhibit bacterial growth, are widely used in the sterilization process; however, their effects on spindle spores are unclear. In this study, the effects of bacteriostats, including nine commonly used food additives and four detergents, on the growth of Clostridium perfringens spores were investigated. The results showed that 0.07\u2030 ethylenediaminetetraacetate had a good inhibitory effect on C. perfringens spore growth, and the spore turbidity decreased by 4.8% after incubation for 60 min. Furthermore, 0.3\u2030 tea polyphenols, 0.8\u2030 D-isoascorbic acid, and 0.75\u2030 potassium sorbate promoted leakage of contents during spore germination. Among the four detergents, 5\u2030 glutaraldehyde solution presented the best inhibitory effect on the growth of C. perfringens spores, and the spore turbidity decreased by 5.6% after incubation for 60 min. Further analysis of the inactivation mechanism of spores by the bacteriostats was performed by comparing the leakage of UV-absorbing substances during germination. The results revealed that bacteriostats could not directly kill the spores, but could inactivate them by inhibiting germination or damaging the spore structure during germination, thus preventing the formation of bacterial vegetative bodies. These findings provide important information and reference for the mechanism underlying the effects of different bacteriostatic agents on spore growth.<\/jats:p>","DOI":"10.3390\/foods12091834","type":"journal-article","created":{"date-parts":[[2023,4,28]],"date-time":"2023-04-28T06:12:55Z","timestamp":1682662375000},"page":"1834","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Effects of Different Bacteriostats on the Dynamic Germination of Clostridium perfringens Spores"],"prefix":"10.3390","volume":"12","author":[{"given":"Dong","family":"Liang","sequence":"first","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6647-2823","authenticated-orcid":false,"given":"Shengnan","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miaoyun","family":"Li","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaodi","family":"Zhu","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lijun","family":"Zhao","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lingxia","family":"Sun","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yangyang","family":"Ma","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gaiming","family":"Zhao","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China"},{"name":"International Joint Laboratory of Meat Processing and Safety in Henan Province, Henan Agricultural University, Zhengzhou 450002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,28]]},"reference":[{"key":"ref_1","first-page":"221","article-title":"Advance in spore germination","volume":"18","author":"Liang","year":"2018","journal-title":"J. China Food"},{"key":"ref_2","first-page":"352","article-title":"Advances in research on the hazards and control of Clostridium perfringens in food","volume":"42","author":"Ren","year":"2021","journal-title":"Food Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1484","DOI":"10.1111\/j.1365-2672.2005.02744.x","article-title":"Effect of mechanical abrasion on the viability, disruption and germination of spores of Bacillus subtilis","volume":"99","author":"Jones","year":"2005","journal-title":"J. Appl. Microbiol."},{"key":"ref_4","first-page":"29","article-title":"Research progress on harm and control of spores in vacuum-packed food","volume":"42","author":"Zhang","year":"2021","journal-title":"Packag. Eng."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1111\/j.1365-2672.2004.02236.x","article-title":"Mechanisms of Bacillus subtilis spore resistance to and killing by aqueous ozone","volume":"96","author":"Young","year":"2004","journal-title":"J. Appl. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.esas.2010.09.002","article-title":"Navigation-assisted fluoroscopy in minimally invasive direct lateral interbody fusion: A cadaveric study","volume":"4","author":"Webb","year":"2010","journal-title":"SAS J."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.cofs.2020.12.014","article-title":"Bacterial spore inactivation by non-thermal technologies: Resistance and inactivation mechanisms","volume":"42","author":"Lv","year":"2021","journal-title":"Curr. Opin. Food Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"103951","DOI":"10.1016\/j.fm.2021.103951","article-title":"Inactivation mechanism of slightly acidic electrolyzed water on Bacillus cereus spores","volume":"103","author":"Zhang","year":"2022","journal-title":"Food Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1099\/jmm.0.000515","article-title":"Carvacrol reduces Clostridium difficile sporulation and spore outgrowth in vitro","volume":"66","author":"Mooyottu","year":"2017","journal-title":"J. Med. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.fm.2013.02.008","article-title":"Effect of meat ingredients (sodium nitrite and erythorbate) and processing (vacuum storage and packaging atmosphere) on germination and outgrowth of Clostridium perfringens spores in ham during abusive cooling","volume":"35","author":"Cassada","year":"2013","journal-title":"Food Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/j.1365-2621.1966.tb01039.x","article-title":"The effect of sodium chloride, potassium nitrate and sodium nitrite on the recovery of heated bacterial spores","volume":"1","author":"Roberts","year":"2007","journal-title":"Int. J. Food Sci. Tech."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"4675","DOI":"10.1007\/s13197-018-3384-7","article-title":"Sporicidal activities and mechanism of surfactant components against Clostridium sporogenes spores","volume":"55","author":"Cho","year":"2018","journal-title":"J. Food Sci. Technol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"103832","DOI":"10.1016\/j.fm.2021.103832","article-title":"The synergic interaction between environmental factors (pH and NaCl) and the physiological state (vegetative cells and spores) provides new possibilities for optimizing processes to manage risk of C. sporogenes spoilage","volume":"100","author":"Boix","year":"2021","journal-title":"Food Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1038\/s41579-021-00540-9","article-title":"Bacillus subtilis biofilm formation and social interactions","volume":"19","author":"Arnaouteli","year":"2021","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"4944","DOI":"10.1038\/s41598-022-09147-3","article-title":"Organization and dynamics of the SpoVAEa protein and its surrounding inner membrane lipids, upon germination of Bacillus subtilis spores","volume":"12","author":"Wen","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.chemosphere.2014.05.038","article-title":"Rice, Disinfection of Bacillus spores with acidified nitrite","volume":"113","author":"Szabo","year":"2014","journal-title":"Chemosphere"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.fm.2022.104137","article-title":"Combined treatment of epsilon-polylysine and heat damages protective structures and spore inner membranes to inactivate Bacillus subtilis spores","volume":"109","author":"Bi","year":"2023","journal-title":"Food Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"110395","DOI":"10.1016\/j.lwt.2020.110395","article-title":"Control of Clostridium perfringens spore germination and outgrowth by potassium lactate and sodium diacetate in ham containing reduced sodium chloride","volume":"137","author":"Juneja","year":"2021","journal-title":"LWT"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Yang, Y., and Zhang, T. (2019). Antimicrobial Activities of Tea Polyphenol on Phytopathogens: A Review. Molecules, 24.","DOI":"10.3390\/molecules24040816"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1007\/s42770-022-00695-4","article-title":"Sporicidal mechanism of the combination of ortho-phthalaldehyde and benzyldimethyldodecylammonium chloride as a disinfectant against the Bacillus subtilis spores","volume":"53","author":"Sun","year":"2022","journal-title":"Braz. J. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1111\/j.1365-2672.2012.05336.x","article-title":"Bacterial spore structures and their protective role in biocide resistance","volume":"113","author":"Leggett","year":"2012","journal-title":"J. Appl. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.ijfoodmicro.2020.108915","article-title":"Effects of temperature, pH and water activity on the growth and the sporulation abilities of Bacillus subtilis BSB1","volume":"337","author":"Gauvry","year":"2021","journal-title":"Int. J. Food Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Ojha, S.C., Phanchana, M., Harnvoravongchai, P., Chankhamhaengdecha, S., Singhakaew, S., Ounjai, P., and Janvilisri, T. (2021). Teicoplanin Suppresses Vegetative Clostridioides difficile and Spore Outgrowth. Antibiotics, 10.","DOI":"10.3390\/antibiotics10080984"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"5287","DOI":"10.1128\/AEM.01363-16","article-title":"Effects of High-Pressure Treatment on Spores of Clostridium Species","volume":"82","author":"Doona","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.fm.2017.11.012","article-title":"Effects of lowering water activity by various humectants on germination of spores of Bacillus species with different germinants","volume":"72","author":"Rao","year":"2018","journal-title":"Food Microbiol."},{"key":"ref_26","first-page":"178","article-title":"Induction of spore germination of Clostridium perfringens by peptidoglycan of different bacteria","volume":"36","author":"Ren","year":"2020","journal-title":"Mod. Food Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.mib.2021.11.001","article-title":"Clostridioides difficile spore germination: Initiation to DPA release","volume":"65","author":"Baloh","year":"2022","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1046\/j.1365-2672.2003.02015.x","article-title":"Germination of spores of Bacillus subtilis with dodecylamine","volume":"95","author":"Setlow","year":"2003","journal-title":"J. Appl. Microbiol."},{"key":"ref_29","first-page":"22","article-title":"Study on bacteriostasis of edible composite film of cinnamon essential oil","volume":"47","author":"Huang","year":"2022","journal-title":"China Condiment"},{"key":"ref_30","first-page":"313","article-title":"Ultra-high pressure causes sublethal damage to spores and further increases the thermal sensitivity of spores","volume":"42","author":"Sun","year":"2017","journal-title":"Food Sci."},{"key":"ref_31","unstructured":"Rao, L. (2017). Efficacy and Mechanisms of High Pressure Carbon Dioxide Combined with Temperature in Killing Bacillus Subtilis Spores, China Agricultural University."},{"key":"ref_32","unstructured":"Li, F.J. (2013). Inactivation Efficiency and Mechanism of High Pressure CO2 on Bacillus Subtilis Spores, Hefei University of Technology."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1146\/annurev-micro-090816-093558","article-title":"Germination of Spores of the Orders Bacillales and Clostridiales","volume":"71","author":"Setlow","year":"2017","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e02731-16","DOI":"10.1128\/AEM.02731-16","article-title":"Inactivation Strategies for Clostridium perfringens Spores and Vegetative Cells","volume":"83","author":"Talukdar","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1111\/jfpp.12669","article-title":"Inhibitory Activity of Tea Polyphenols on Biofilm Development of Shewanella putrefaciens","volume":"40","author":"Zhang","year":"2016","journal-title":"J. Food Process. Preserv."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1111\/lam.12615","article-title":"Bacillus spore wet heat resistance and evidence for the role of an expanded osmoregulatory spore cortex","volume":"63","author":"Rao","year":"2016","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.1016\/j.isci.2022.105242","article-title":"Glutamate catabolism during sporulation determines the success of the future spore germination","volume":"25","author":"Rao","year":"2022","journal-title":"iScience"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"592","DOI":"10.3389\/fmicb.2020.596092","article-title":"Bacterial Spore mRNA\u2014What\u2019s Up With That?","volume":"11","author":"Setlow","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.anaerobe.2019.102085","article-title":"Phosphorothioation of foreign DNA influences the transformation efficiency in Clostridium perfringens NCTC 8239","volume":"61","author":"Yasugi","year":"2020","journal-title":"Anaerobe"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1111\/j.1365-2672.1974.tb00437.x","article-title":"Smart Inhib. Spores Clostridium spp. by Sodium Nitrite","volume":"37","author":"Roberts","year":"1974","journal-title":"J. Appl. Bacteriol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e00424-20","DOI":"10.1128\/mSphere.00424-20","article-title":"Architecture and Self-Assembly of Clostridium sporogenes and Clostridium botulinum Spore Surfaces Illustrate a General Protective Strategy across Spore Formers","volume":"5","author":"Janganan","year":"2020","journal-title":"mSphere"}],"container-title":["Foods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-8158\/12\/9\/1834\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:25:39Z","timestamp":1760124339000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-8158\/12\/9\/1834"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,28]]},"references-count":41,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["foods12091834"],"URL":"https:\/\/doi.org\/10.3390\/foods12091834","relation":{},"ISSN":["2304-8158"],"issn-type":[{"value":"2304-8158","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,28]]}}}