Potential risk of botulinum neurotoxin -producing clostridia occurrence in canned fish

1Al-Baali A.A.G., Farid M.M.: Chapter 5, Thermal Sterilization of Food in Cans. In: Sterilization of Food in Retort Pouches, Food Engineering Series, Springer Science+Business Media, New York, NY, 2006, pp. 45–62, doi: 10.1007/0-387-311297_5. Al-Baali A.A.G. Farid M.M. Chapter 5, Thermal Sterilization of Food in Cans In Sterilization of Food in Retort Pouches, Food Engineering Series Springer Science+Business Media New York, NY 2006 pp 45 62 10.1007/0-387-311297_5Open DOISearch in Google Scholar

2Banga J.R., Balsa-Canto E., Moles C.G., Alonso A.A.: Improving food processing using modern optimization methods. Trends Food Sci Technol 2003, 14, 131–144, doi: 10.1016/S0924-2244(03)00048-7. Banga J.R. Balsa-Canto E. Moles C.G. Alonso A.A. Improving food processing using modern optimization methods Trends Food Sci Technol 2003 14 131 144 10.1016/S0924-2244(03)00048-7Open DOISearch in Google Scholar

3Barra–Carrasco J., Olguín–Araneda V., Plaza–Garrido A., Miranda–Cárdenas C., Cofré–Araneda G., Pizarro–Guajardo M., Sarker M.R., Paredes–Sabja D.: The Clostridium difficile exosporium cysteine (CdeC)-rich protein is required for exosporium morphogenesis and coat assembly. J Bacteriol 2013, 195, 3863–3875, doi: 10.1128/JB.00369-13. Barra–Carrasco J. Olguín–Araneda V. Plaza–Garrido A. Miranda–Cárdenas C. Cofré–Araneda G. Pizarro–Guajardo M. Sarker M.R. Paredes–Sabja D. The Clostridium difficile exosporium cysteine (CdeC)-rich protein is required for exosporium morphogenesis and coat assembly J Bacteriol 2013 195 3863 3875 10.1128/JB.00369-13375458723794627Open DOISearch in Google Scholar

4Benoit R.M.: Botulinum neurotoxin diversity from a genecentered view. Toxins 2018, 10, 310, doi: 10.3390/toxins10080310. Benoit R.M. Botulinum neurotoxin diversity from a genecentered view Toxins 2018 10 310 10.3390/toxins10080310611579130071587Open DOISearch in Google Scholar

5Brown J.L., Tran-Dinh N., Chapman B.: Clostridium sporogenes PA 3679 and its uses in the derivation of thermal processing schedules for low-acid shelf-stable foods and as a research model for proteolytic Clostridium botulinum. J Food Prot 2012, 75, 779–792, doi: 10.4315/0362-028X.JFP-11-391. Brown J.L. Tran-Dinh N. Chapman B. Clostridium sporogenes PA 3679 and its uses in the derivation of thermal processing schedules for low-acid shelf-stable foods and as a research model for proteolytic Clostridium botulinum J Food Prot 2012 75 779 792 10.4315/0362-028X.JFP-11-39122488072Open DOISearch in Google Scholar

6Brunt J., Van Vliet A.H.M., Carter A.T., Stringer S.C., Amar C., Grant K.A., Godbole G., Peck M.W.: Diversity of the genomes and neurotoxins of strains of Clostridium botulinum group I and Clostridium sporogenes associated with foodborne, infant and wound botulism. Toxins 2020, 12, 586, doi: 10.3390/toxins12090586. Brunt J. Van Vliet A.H.M. Carter A.T. Stringer S.C. Amar C. Grant K.A. Godbole G. Peck M.W. Diversity of the genomes and neurotoxins of strains of Clostridium botulinum group I and Clostridium sporogenes associated with foodborne, infant and wound botulism Toxins 2020 12 586 10.3390/toxins12090586755195432932818Open DOISearch in Google Scholar

7Brunt J., Plowman J., Gaskin D.J.H., Itchner M., Carter A.T., Peck M.W.: Functional characterisation of germinant receptors in Clostridium botulinum and Clostridium sporogenes presents novel insights into spore germination systems.PLOS Pathog 2014, 10, doi: 10.1371/journal.ppat.1004382. Brunt J. Plowman J. Gaskin D.J.H. Itchner M. Carter A.T. Peck M.W. Functional characterisation of germinant receptors in Clostridium botulinum and Clostridium sporogenes presents novel insights into spore germination systems PLOS Pathog 2014 10 10.1371/journal.ppat.1004382416148125210747Open DOISearch in Google Scholar

8Cortés-Sánchez A.: About Clostridium botulinum, Fish and Tilapa, Mod Appl Sci 2021, 15, doi: 10.5539/mas.v15n3p1 Cortés-Sánchez A. About Clostridium botulinum, Fish and Tilapa, Mod Appl Sci 2021 15 10.5539/mas.v15n3p1Open DOISearch in Google Scholar

9Doornmalen J.P.C.M., Kopinga K.: Temperature dependence of F-, D- and z-values used in steam sterilization processes. J Appl Microbiol 2009, 107, 1054–1060, doi: 10.1111/j.1365-2672.2009.04290.x. Doornmalen J.P.C.M. Kopinga K. Temperature dependence of F-, D- and z-values used in steam sterilization processes J Appl Microbiol 2009 107 1054 1060 10.1111/j.1365-2672.2009.04290.x19486408Open DOISearch in Google Scholar

10Grenda T., Kwiatek K., Goldsztejn M., Sapała M., Kozieł N., Domaradzki P.: Clostridia in insect processed animal proteins–is an epidemiological problem possible? Agriculture 2021, 11, 270, doi:10.2290/agriculture11030270. Grenda T. Kwiatek K. Goldsztejn M. Sapała M. Kozieł N. Domaradzki P. Clostridia in insect processed animal proteins–is an epidemiological problem possible? Agriculture 2021 11 270 10.2290/agriculture11030270Open DOISearch in Google Scholar

11Hill K.K., Xie G., Foley B.T., Smith T.J., Munk A.C., Bruce D., Smith L.A., Brettin T.S., Detter J.C.: Recombination and insertion events involving the botulinum neurotoxin complex genes in Clostridium botulinum types A, B, E and F and Clostridium butyricum type E strains. BMC Biol 2009, 7, doi: 10.1186/1741-7007-7-66. Hill K.K. Xie G. Foley B.T. Smith T.J. Munk A.C. Bruce D. Smith L.A. Brettin T.S. Detter J.C. Recombination and insertion events involving the botulinum neurotoxin complex genes in Clostridium botulinum types A, B, E and F and Clostridium butyricum type E strains BMC Biol 2009 7 10.1186/1741-7007-7-66276457019804621Open DOISearch in Google Scholar

12Ismail I.M., Fahmy A., Azab A., Abadir M., Fateen S.E.,: Optimizing the sterilization process of canned food using temperature distribution studiem. IOSR-JAVS 2013, 6, 26–33, doi: 10.9790/2380-0642633. Ismail I.M. Fahmy A. Azab A. Abadir M. Fateen S.E. Optimizing the sterilization process of canned food using temperature distribution studiem IOSR-JAVS 2013 6 26 33 10.9790/2380-0642633Open DOISearch in Google Scholar

13Johnson E.A., Bradshaw M.: Clostridium botulinum and its neurotoxins; a metabolic and cellular perspective. Toxicon 2001, 39, 1703–1722, doi: 10.1016/s0041-0101(01)00157-x. Johnson E.A. Bradshaw M. Clostridium botulinum and its neurotoxins; a metabolic and cellular perspective Toxicon 2001 39 1703 1722 10.1016/s0041-0101(01)00157-x11595633Open DOISearch in Google Scholar

14Lalitha K.V., Gopakumar K.: Growth and toxin production by Clostridium botulinum in fish (Mugil cephalus) and shrimp (Penaeus indicus) tissue homogenates stored under vacuum. Food Microbiol 2001, 18, 651–657, doi: 10.1006/fmic.2001.0433. Lalitha K.V. Gopakumar K. Growth and toxin production by Clostridium botulinum in fish (Mugil cephalus) and shrimp (Penaeus indicus) tissue homogenates stored under vacuum Food Microbiol 2001 18 651 657 10.1006/fmic.2001.0433Open DOISearch in Google Scholar

15Lonati D., Schicchi A., Crevani M., Buscaglia E., Scaravaggi G., Maida F., Cirronis M., Petrolini V.M., Locatelli C.A.: Foodborne botulism: clinical diagnosis and medical treatment. Toxins 2020, 12, 509, doi: 10.3390/toxins12080509. Lonati D. Schicchi A. Crevani M. Buscaglia E. Scaravaggi G. Maida F. Cirronis M. Petrolini V.M. Locatelli C.A. Foodborne botulism: clinical diagnosis and medical treatment Toxins 2020 12 509 10.3390/toxins12080509747213332784744Open DOISearch in Google Scholar

16Mah J.H., Kang D.H., Tang J.: Comparison of viability and heat resistance of Clostridium sporogenes stored at different temperatures. J Food Sci 2009, 74, 23–27, doi: 10.1111/j.1750-3841.2008.00984.x. Mah J.H. Kang D.H. Tang J. Comparison of viability and heat resistance of Clostridium sporogenes stored at different temperatures J Food Sci 2009 74 23 27 10.1111/j.1750-3841.2008.00984.x19200102Open DOISearch in Google Scholar

17Maikanov B., Mustafina R., Auteleyeva L., Wiśniewski J., Anusz K., Grenda T., Kwiatek K., Goldsztejn M., Grabczak M.: Clostridium botulinum and Clostridium perfringens occurrence in Kazakh honey samples. Toxins 2019, 11, 472, doi: 10.3390/toxins11080472. Maikanov B. Mustafina R. Auteleyeva L. Wiśniewski J. Anusz K. Grenda T. Kwiatek K. Goldsztejn M. Grabczak M. Clostridium botulinum and Clostridium perfringens occurrence in Kazakh honey samples Toxins 2019 11 472 10.3390/toxins11080472672306731412583Open DOISearch in Google Scholar

18Nawrocki E.M., Bradshaw M., Johnson E.A.: Botulinum neurotoxin–encoding plasmids can be conjugatively transferred to diverse clostridial strains. Sci Rep 2018, 8, doi: 10.1038/s41598-018-21342-9. Nawrocki E.M. Bradshaw M. Johnson E.A. Botulinum neurotoxin–encoding plasmids can be conjugatively transferred to diverse clostridial strains Sci Rep 2018 8 10.1038/s41598-018-21342-9581455829449580Open DOISearch in Google Scholar

19Num S.M., Useh N.M.: Clostridium: pathogenic roles, industrial uses and medicinal prospects of natural products as ameliorative agents against pathogenic species. JJBS 2014, 7, 81–94, doi: 10.12816/0008220. Num S.M. Useh N.M. Clostridium: pathogenic roles, industrial uses and medicinal prospects of natural products as ameliorative agents against pathogenic species JJBS 2014 7 81 94 10.12816/0008220Open DOISearch in Google Scholar

20Peck M., Smith T.J., Anniballi F., Austin J.W., Bano L., Bradshaw M., Cuervo P., Cheng L.W., Derman Y., Dorner B.G., Fisher A., Hill K.K., Kalb S.R., Korkeala H., Lindström M., Lista F., Lúquez C., Mazuet C., Pirazzini M., Popoff M.R., Rossetto O., Rummel A., Sesardic D., Singh B.R., Stringer S.C.: Historical perspectives and guidelines for botulinum neurotoxin subtype nomenclature. Toxins 2017, 18, doi: 10.3390/toxins9010038. Peck M. Smith T.J. Anniballi F. Austin J.W. Bano L. Bradshaw M. Cuervo P. Cheng L.W. Derman Y. Dorner B.G. Fisher A. Hill K.K. Kalb S.R. Korkeala H. Lindström M. Lista F. Lúquez C. Mazuet C. Pirazzini M. Popoff M.R. Rossetto O. Rummel A. Sesardic D. Singh B.R. Stringer S.C. Historical perspectives and guidelines for botulinum neurotoxin subtype nomenclature Toxins 2017 18 10.3390/toxins9010038530827028106761Open DOISearch in Google Scholar

21Peck M.W., Van Vliet A.H.M.: Impact of Clostridium botulinum genomic diversity on food safety. Curr Opin Food Sci 2016, 10, 52–59, doi: 10.1016/j.cofs.2016.09.006. Peck M.W. Van Vliet A.H.M. Impact of Clostridium botulinum genomic diversity on food safety Curr Opin Food Sci 2016 10 52 59 10.1016/j.cofs.2016.09.006518178428058209Open DOISearch in Google Scholar

22Poortmans M., Vanoirbeek K., Dorner M.B., Michiels C.W.: Selection and development of nontoxic nonproteolytic Clostridium botulinum surrogate strains for food challenge testing. Foods 2022, 11, doi: 10.3390/foods11111577. Poortmans M. Vanoirbeek K. Dorner M.B. Michiels C.W. Selection and development of nontoxic nonproteolytic Clostridium botulinum surrogate strains for food challenge testing Foods 2022 11 10.3390/foods11111577918061235681327Open DOISearch in Google Scholar

23Poulain B., Popoff M.R.: Why are botulinum neurotoxin-producing bacteria so diverse and botulinum neurotoxins so toxic? Toxins 2019, 11, 34, doi: 10.3390/toxins11010034. Poulain B. Popoff M.R. Why are botulinum neurotoxin-producing bacteria so diverse and botulinum neurotoxins so toxic? Toxins 2019 11 34 10.3390/toxins11010034635719430641949Open DOISearch in Google Scholar

24Rahman M.S.: Canning and Sterilization of Foods. In: Handbook of Food Preservation. CRC Press Taylor&Francis Group, Danvers, 2007, pp. 585-625. Rahman M.S. Canning and Sterilization of Foods. In: Handbook of Food Preservation CRC Press Taylor&Francis Group, Danvers 2007 pp 585 62510.1201/9781420017373Search in Google Scholar

25Raphael B.H., Andreadis J.D.: Real-time PCR detection of the nontoxic nonhemagglutinin gene as a rapid screening method for bacterial isolates harboring the botulinum neurotoxin (A–G) gene complex. J. Microbiol Methods 2007, 71, 343–346, doi: 10.1016/j.mimet.2007.09.016. Raphael B.H. Andreadis J.D. Real-time PCR detection of the nontoxic nonhemagglutinin gene as a rapid screening method for bacterial isolates harboring the botulinum neurotoxin (A–G) gene complex J. Microbiol Methods 2007 71 343 346 10.1016/j.mimet.2007.09.01617961766Open DOISearch in Google Scholar

26Raseta M., Brankovic-Lazic I., Mrdovic B., Baltic B., Zsolt B., Djordjevic V.: Optimization of liver pate sterilization from the aspect of preserving nutritional value and ensuring food safety. Meat Technology 2019, 60, 97–105, doi: 10.18485/meattech.2019.60.2.4. Raseta M. Brankovic-Lazic I. Mrdovic B. Baltic B. Zsolt B. Djordjevic V. Optimization of liver pate sterilization from the aspect of preserving nutritional value and ensuring food safety Meat Technology 2019 60 97 105 10.18485/meattech.2019.60.2.4Open DOISearch in Google Scholar

27Reddy N.R., Skinner G.E., Oh S.: Clostridium botulinum and its control in low-acid canned foods. Food Sci Biotechnol 2006, 15, 499–505. Reddy N.R. Skinner G.E. Oh S. Clostridium botulinum and its control in low-acid canned foods Food Sci Biotechnol 2006 15 499 505Search in Google Scholar

28Saeed E.M.A.: Studies on Isolation and Identification of Clostridium botulinum Investigating Field Samples Specially from Equine Grass Sickness Cases, Doctoral dissertation, Faculty of Agriculture, Georg-August-University Göttingen, Göttingen, 2004 Saeed E.M.A. Studies on Isolation and Identification of Clostridium botulinum Investigating Field Samples Specially from Equine Grass Sickness Cases, Doctoral dissertation, Faculty of Agriculture Georg-August-University Göttingen Göttingen 2004Search in Google Scholar

29Simpson L.: The life history of a botulinum toxin molecule. Toxicon 2013, 68, 40–59, doi: 10.1016/j.toxicon.2013.02.014. Simpson L. The life history of a botulinum toxin molecule Toxicon 2013 68 40 59 10.1016/j.toxicon.2013.02.01423518040Open DOISearch in Google Scholar

30Smith T.J., Hill K.K., Raphael B.H.: Historical and current perspectives on Clostridium botulinum diversity. Res Microbiol 2015, 166, 290–302, doi: 10.1016/j.resmic.2014.09.007. Smith T.J. Hill K.K. Raphael B.H. Historical and current perspectives on Clostridium botulinum diversity Res Microbiol 2015 166 290 302 10.1016/j.resmic.2014.09.00725312020Open DOISearch in Google Scholar

31Smith T.J., Tian R., Imanian B., Williamson Ch.H.D., Johnson S.L., Daligault H.E., Schill K.M.: Integration of complete plasmids containing bont genes into chromosomes of Clostridium parabotulinum, Clostridium sporogenes, and Clostridium argentinense. Toxins 2021, 13, 473, doi: 10.3390/toxins13070473. Smith T.J. Tian R. Imanian B. Williamson Ch.H.D. Johnson S.L. Daligault H.E. Schill K.M. Integration of complete plasmids containing bont genes into chromosomes of Clostridium parabotulinum, Clostridium sporogenes, and Clostridium argentinense Toxins 2021 13 473 10.3390/toxins13070473831015434357945Open DOISearch in Google Scholar

32Stersky A., Todd E., Pivnick H.: Food poisoning associated with post-process leakage (PPL) in canned foods. J Food Prot 1980, 43, 465–476, doi: 10.4315/0362-028X-43.6.465. Stersky A. Todd E. Pivnick H. Food poisoning associated with post-process leakage (PPL) in canned foods J Food Prot 1980 43 465 476 10.4315/0362-028X-43.6.46530822946Open DOISearch in Google Scholar

33Sumner J., Ross T.: A semi-quantitative seafood safety risk assessment. Int J Food Microbiol 2002, 25, 55–59, doi: 10.1016/s0168-1605(02)00062-4. Sumner J. Ross T. A semi-quantitative seafood safety risk assessment Int J Food Microbiol 2002 25 55 59 10.1016/s0168-1605(02)00062-412076038Open DOISearch in Google Scholar

34Taylor R.H., Dunn M.L., Ogden L.V., Jefferies L.K., Eggett D.L., Steele F.M.: Conditions associated with Clostridium sporogenes growth as a surrogate for Clostridium botulinum in nonthermally processed canned butter. J Dairy Sci 2013, 96, 2754–2764, doi: 10.3168/jds.2012-6209. Taylor R.H. Dunn M.L. Ogden L.V. Jefferies L.K. Eggett D.L. Steele F.M. Conditions associated with Clostridium sporogenes growth as a surrogate for Clostridium botulinum in nonthermally processed canned butter J Dairy Sci 2013 96 2754 2764 10.3168/jds.2012-620923453518Open DOISearch in Google Scholar

35Valentas K.J., Rotstein E., Singh R.P (red).: Chapter 2, Sterilization Process Engineering. In: Handbook of Food Engineering Practice. CRC Press LLC, Salem, 1997, pp. 46–78, doi: 10.1201/9780367802110. Valentas K.J. Rotstein E. Singh R P (red) Chapter 2, Sterilization Process Engineering In Handbook of Food Engineering Practice CRC Press LLC Salem 1997 pp 46 78 10.1201/9780367802110Open DOISearch in Google Scholar

36Vaneechoutte M., Cartwright C.P., Williams E.C., Jäger B., Tichy H.V., de Baere T., de Rouck A., Verschraegen G.: Evaluation of 16S rRNA gene restriction analysis for the identification of cultured organisms of clinically important Clostridium species. Anaerobe 1996, 4, 249–256, doi: 0.1128/JCM.42.5.2197–2202.2004. Vaneechoutte M. Cartwright C.P. Williams E.C. Jäger B. Tichy H.V. de Baere T. de Rouck A. Verschraegen G. Evaluation of 16S rRNA gene restriction analysis for the identification of cultured organisms of clinically important Clostridium species Anaerobe 1996 4 249 256 0.1128/JCM.42.5.2197–2202.200410.1006/anae.1996.0034Search in Google Scholar

37Weigand MR., Pena-Gonzales A., Shirey T.B., Broeker R.G., Ishaq M.K., Konstantinidis K.T., Raphael B.H.: Implications of genome-based discrimination between Clostridium botulinum group I and Clostridium sporogenes strains for bacterial taxonomy. Appl Environ Microbiol 2015, 81, 5420–5429, doi: 10.1128/AEM.01159-15. Weigand MR. Pena-Gonzales A. Shirey T.B. Broeker R.G. Ishaq M.K. Konstantinidis K.T. Raphael B.H. Implications of genome-based discrimination between Clostridium botulinum group I and Clostridium sporogenes strains for bacterial taxonomy Appl Environ Microbiol 2015 81 5420 5429 10.1128/AEM.01159-15451019426048939Open DOISearch in Google Scholar

38Wentz T.G., Tremblay B.J.M., Bradshaw M., Doxey A.C., Sharma S.K., Sauer J.D., Pellett S.: Endogenous CRISPR-Cas systems in group I Clostridium botulinum and Clostridium sporogenes do not directly target the botulinum neurotoxin gene cluster. Front Microbiol 2022, 12, doi: 10.3389/fmicb.2021.787726. Wentz T.G. Tremblay B.J.M. Bradshaw M. Doxey A.C. Sharma S.K. Sauer J.D. Pellett S. Endogenous CRISPR-Cas systems in group I Clostridium botulinum and Clostridium sporogenes do not directly target the botulinum neurotoxin gene cluster Front Microbiol 2022 12 10.3389/fmicb.2021.787726886542035222299Open DOISearch in Google Scholar

39Williamson Ch.H.D.,Vazquez A.J., Hill K., Smith T.J., Nottingham R., Stone N.E., Sobek C.J., Cocking J.H., Fernández R.A., Caballero P.A., Leiser O.P., Kelm P., Sahl J.W: Differentiating botulinum neurotoxin- producing clostridia with a simple, multiplex PCR Assay. Appl Environ Microbiol 2017, 83, doi: 10.1128/AEM.00806-17. Williamson Ch.H.D. Vazquez A.J. Hill K. Smith T.J. Nottingham R. Stone N.E. Sobek C.J. Cocking J.H. Fernández R.A. Caballero P.A. Leiser O.P. Kelm P. Sahl J.W Differentiating botulinum neurotoxin- producing clostridia with a simple, multiplex PCR Assay Appl Environ Microbiol 2017 83 10.1128/AEM.00806-17558349028733282Open DOISearch in Google Scholar

40Wrzosek A.: Weitere Untersuchungen uiber die Zuchtung von obli-gatorischen Anaeroben in a&rober Weise. Cent. f. Bakt. Abt. I. Orig. 1907, xliv, 607–616. Wrzosek A. Weitere Untersuchungen uiber die Zuchtung von obli-gatorischen Anaeroben in a&rober Weise Cent. f. Bakt. Abt. I. Orig 1907 xliv 607–616Search in Google Scholar