1887
Surveillance and outbreak report Open Access
Like 0

Abstract

A case of food-borne botulism occurred in Slovakia in 2015. type A was isolated from three nearly empty commercial hummus tubes. The product, which was sold in Slovakia and the Czech Republic, was withdrawn from the market and a warning was issued immediately through the European Commission’s Rapid Alert System for Food and Feed (RASFF). Further investigation revealed the presence of botulinum neurotoxin (BoNT) subtype BoNT/A3, a very rare subtype implicated in only one previous outbreak (Loch Maree in Scotland, 1922). It is the most divergent subtype of BoNT/A with 15.4% difference at the amino acid level compared with the prototype BoNT/A1. This makes it more prone to evading immunological and PCR-based detection. It is recommended that testing laboratories are advised that this subtype has been associated with food-borne botulism for the second time since the first outbreak almost 100 years ago, and to validate their immunological or PCR-based methods against this divergent subtype.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2017.22.32.30591
2017-08-10
2017-10-17
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2017.22.32.30591
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/22/32/eurosurv-22-32-2.html?itemId=/content/10.2807/1560-7917.ES.2017.22.32.30591&mimeType=html&fmt=ahah

References

  1. Johnson EA, Montecucco C. Botulism. Handb Clin Neurol. 2008;91:333-68.  https://doi.org/10.1016/S0072-9752(07)01511-4  PMID: 18631849 
  2. Peck MW. Biology and genomic analysis of Clostridium botulinum. Adv Microb Physiol. 2009;55:183-265, 320.  https://doi.org/10.1016/S0065-2911(09)05503-9  PMID: 19573697 
  3. Williamson CH, Sahl JW, Smith TJ, Xie G, Foley BT, Smith LA, et al. Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia. BMC Genomics. 2016;17(1):180.  https://doi.org/10.1186/s12864-016-2502-z  PMID: 26939550 
  4. Kull S, Schulz KM, Weisemann J, Kirchner S, Schreiber T, Bollenbach A, et al. Isolation and functional characterization of the novel Clostridium botulinum neurotoxin A8 subtype. PLoS One. 2015;10(2):e0116381.  https://doi.org/10.1371/journal.pone.0116381  PMID: 25658638 
  5. Peck MW, Smith TJ, Anniballi F, Austin JW, Bano L, Bradshaw M, et al. Historical perspectives and guidelines for botulinum neurotoxin subtype nomenclature. Toxins (Basel). 2017;9(1):38.  https://doi.org/10.3390/toxins9010038  PMID: 28106761 
  6. Montecucco C, Rasotto MB. On botulinum neurotoxin variability. MBio. 2015;6(1):e02131-14.  https://doi.org/10.1128/mBio.02131-14  PMID: 25564463 
  7. Rummel A. The long journey of botulinum neurotoxins into the synapse. Toxicon. 2015;107(Pt A):9-24.  https://doi.org/doi: 10.1016/j.toxicon.2015.09.009  PMID: 26363288 
  8. Dorner MB, Schulz KM, Kull S, Dorner BG. Complexity of botulinum neurotoxins: challenges for detection technology. Curr Top Microbiol Immunol. 2013;364:219-55. https://doi.org/10.1007/978-3-662-45790-0_11  PMID: 23239356 
  9. Siegel L. Destruction of Botulinum Toxins in Food and Water. In: Hauschild A, Dodds K, editors. Clostridium botulinum: Ecology and Control in Foods. New York: Marcel Dekker Inc; 1992. p. 323-41.
  10. Weingart OG, Schreiber T, Mascher C, Pauly D, Dorner MB, Berger TFH, et al. The case of botulinum toxin in milk: experimental data. Appl Environ Microbiol. 2010;76(10):3293-300.  https://doi.org/10.1128/AEM.02937-09  PMID: 20363798 
  11. Cowden J. Food-borne Clostridium botulinum intoxication from mass produced foodstuffs in Europe. Euro Surveill. 2011;16(49):20033. PMID: 22172328 
  12. Peck MW, Stringer SC, Carter AT. Clostridium botulinum in the post-genomic era. Food Microbiol. 2011;28(2):183-91.  https://doi.org/10.1016/j.fm.2010.03.005  PMID: 21315972 
  13. Lindström M, Vuorela M, Hinderink K, Korkeala H, Dahlsten E, Raahenmaa M, et al. Botulism associated with vacuum-packed smoked whitefish in Finland, June-July 2006. Euro Surveill. 2006;11(7):E060720.3. PMID: 16966764 
  14. European Centre for Disease Prevention and Control (ECDC). Table 1. Reported confirmed botulism cases: number and rate per 100 000 population, EU/EEA, 2010–2014. Stockholm: ECDC. [Accessed 13 Jul 2017]. Available from: https://ecdc.europa.eu/en/publications-data/table-1-reported-confirmed-botulism-cases-number-and-rate-100-000-population
  15. Public Health Authority of the Slovak Republic (UVZSR). Analýza epidemiologickej situácie a činnosti odborov epidemiológie v Slovenskej republike za rok 2012. Z poverenia hlavného hygienika SR vypracovali pracovníci RÚVZ so sídlom v Banskej Bystrici. [Analysis of epidemiological situation and the activities of the departments of epidemiology in Slovak Republic in 2012. Drafted by the epidemiologists on behalf of Chief Public Health Officer of Slovak Republic]. Bratislava: UVZSR. [Accessed 20 Jul 2017]. Slovak. Available from: www.epis.sk/InformacnaCast/Publikacie/VyrocneSpravy/Files/VS_SR_2012.aspx
  16. De Medici D, Anniballi F, Wyatt GM, Lindström M, Messelhäußer U, Aldus CF, et al. Multiplex PCR for detection of botulinum neurotoxin-producing clostridia in clinical, food, and environmental samples. Appl Environ Microbiol. 2009;75(20):6457-61.  https://doi.org/10.1128/AEM.00805-09  PMID: 19684163 
  17. Kirchner S, Krämer KM, Schulze M, Pauly D, Jacob D, Gessler F, et al. Pentaplexed quantitative real-time PCR assay for the simultaneous detection and quantification of botulinum neurotoxin-producing clostridia in food and clinical samples. Appl Environ Microbiol. 2010;76(13):4387-95.  https://doi.org/10.1128/AEM.02490-09  PMID: 20435756 
  18. Raphael BH, Andreadis JD. 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(3):343-6.  https://doi.org/10.1016/j.mimet.2007.09.016  PMID: 17961766 
  19. Jacobson MJ, Lin G, Raphael B, Andreadis J, Johnson EA. Analysis of neurotoxin cluster genes in Clostridium botulinum strains producing botulinum neurotoxin serotype A subtypes. Appl Environ Microbiol. 2008;74(9):2778-86.  https://doi.org/10.1128/AEM.02828-07  PMID: 18326685 
  20. Pauly D, Kirchner S, Stoermann B, Schreiber T, Kaulfuss S, Schade R, et al. Simultaneous quantification of five bacterial and plant toxins from complex matrices using a multiplexed fluorescent magnetic suspension assay. Analyst (Lond). 2009;134(10):2028-39.  https://doi.org/10.1039/b911525k  PMID: 19768210 
  21. Simon S, Fiebig U, Liu Y, Tierney R, Dano J, Worbs S, et al. Recommended immunological strategies to screen for botulinum neurotoxin-containing samples. Toxins (Basel). 2015;7(12):5011-34.  https://doi.org/10.3390/toxins7124860  PMID: 26703727 
  22. Hill KK, Smith TJ, Helma CH, Ticknor LO, Foley BT, Svensson RT, et al. Genetic diversity among botulinum neurotoxin-producing clostridial strains. J Bacteriol. 2007;189(3):818-32.  https://doi.org/10.1128/JB.01180-06  PMID: 17114256 
  23. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-10.  https://doi.org/10.1016/S0022-2836(05)80360-2  PMID: 2231712 
  24. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-80.  https://doi.org/10.1093/molbev/mst010  PMID: 23329690 
  25. Weigand MR, Pena-Gonzalez A, Shirey TB, Broeker RG, Ishaq MK, Konstantinidis KT, et al. Implications of genome-based discrimination between Clostridium botulinum Group I and Clostridium sporogenes strains for bacterial taxonomy. Appl Environ Microbiol. 2015;81(16):5420-9.  https://doi.org/10.1128/AEM.01159-15  PMID: 26048939 
  26. Scottish Board of Health. Botulism at Loch Maree. Analyst (Lond). 1923;48(564):118-20.  https://doi.org/10.1039/an9234800118 
  27. Lúquez C, Raphael BH, Joseph LA, Meno SR, Fernández RA, Maslanka SE. Genetic diversity among Clostridium botulinum strains harboring bont/A2 and bont/A3 genes. Appl Environ Microbiol. 2012;78(24):8712-8.  https://doi.org/10.1128/AEM.02428-12  PMID: 23042179 
  28. Dowell VR Jr, McCroskey LM, Hatheway CL, Lombard GL, Hughes JM, Merson MH. Coproexamination for botulinal toxin and Clostridium botulinum. A new procedure for laboratory diagnosis of botulism. JAMA. 1977;238(17):1829-32.  https://doi.org/10.1001/jama.1977.03280180033021  PMID: 333132 
  29. Caya JG, Agni R, Miller JE. Clostridium botulinum and the clinical laboratorian: a detailed review of botulism, including biological warfare ramifications of botulinum toxin. Arch Pathol Lab Med. 2004;128(6):653-62. PMID: 15163234 
  30. Lindström M, Korkeala H. Laboratory diagnostics of botulism. Clin Microbiol Rev. 2006;19(2):298-314.  https://doi.org/10.1128/CMR.19.2.298-314.2006  PMID: 16614251 
  31. European Commission. Commission Decision 2002/253/EC of 19 March 2002 laying down case definitions for reporting communicable diseases to the Community network under Decision No 2119/98/EC of the European Parliament and of the Council. Official Journal of the European Union. Luxembourg: Publications Office of the European Union.03.04.2002: L 086. Available from: http://data.europa.eu/eli/dec/2002/253/oj
  32. Browning LM, Prempeh H, Little C, Houston C, Grant K, Cowden JMUnited Kingdom Botulism Incident Management Team. An outbreak of food-borne botulism in Scotland, United Kingdom, November 2011. Euro Surveill. 2011;16(49):20036. PMID: 22172331 
  33. Jalava K, Selby K, Pihlajasaari A, Kolho E, Dahlsten E, Forss N, et al. Two cases of food-borne botulism in Finland caused by conserved olives, October 2011. Euro Surveill. 2011;16(49):20034. PMID: 22172330 
  34. Pingeon JM, Vanbockstael C, Popoff MR, King LA, Deschamps B, Pradel G, et al. Two outbreaks of botulism associated with consumption of green olive paste, France, September 2011. Euro Surveill. 2011;16(49):20035. PMID: 22172329 
  35. Peck MW, Goodburn KE, Betts RP, Stringer SC. Assessment of the potential for growth and neurotoxin formation by non-proteolytic Clostridium botulinum in short shelf-life commercial foods designed to be stored chilled. Trends Food Sci Technol. 2008;19(4):207-16.  https://doi.org/10.1016/j.tifs.2007.12.006 
  36. Lindström M, Korkeala H. Food-borne Pathogenic Clostridia. In: Tham W, Danielsson-Tham ML, editors. Food Associated Pathogens. Boca Raton, Florida: CRC Press; 2013. p. 67-87
  37. Tepp WH, Lin G, Johnson EA. Purification and characterization of a novel subtype A3 botulinum neurotoxin. Appl Environ Microbiol. 2012;78(9):3108-13.  https://doi.org/10.1128/AEM.07967-11  PMID: 22367089 
  38. Gibson AM, Modi NK, Roberts TA, Shone CC, Hambleton P, Melling J. Evaluation of a monoclonal antibody-based immunoassay for detecting type A Clostridium botulinum toxin produced in pure culture and an inoculated model cured meat system. J Appl Bacteriol. 1987;63(3):217-26.  https://doi.org/10.1111/j.1365-2672.1987.tb04939.x  PMID: 3323154 
  39. Fach P, Gibert M, Griffais R, Guillou JP, Popoff MR. PCR and gene probe identification of botulinum neurotoxin A-, B-, E-, F-, and G-producing Clostridium spp. and evaluation in food samples. Appl Environ Microbiol. 1995;61(1):389-92. PMID: 7887623 
  40. Boyle B, Dallaire N, MacKay J. Evaluation of the impact of single nucleotide polymorphisms and primer mismatches on quantitative PCR. BMC Biotechnol. 2009;9(1):75.  https://doi.org/10.1186/1472-6750-9-75  PMID: 19715565 
  41. Bru D, Martin-Laurent F, Philippot L. Quantification of the detrimental effect of a single primer-template mismatch by real-time PCR using the 16S rRNA gene as an example. Appl Environ Microbiol. 2008;74(5):1660-3.  https://doi.org/10.1128/AEM.02403-07  PMID: 18192413 
  42. Bhattacharjee Y. Biosecurity. Panel selects most dangerous select agents. Science. 2011;332(6037):1491-2.  https://doi.org/10.1126/science.332.6037.1491  PMID: 21700845 
  43. Hooper DC, Hirsch MS. Novel Clostridium botulinum toxin and dual use research of concern issues. J Infect Dis. 2014;209(2):167. . Available from: https://doi.org/10.1093/infdis/jit528 https://doi.org/10.1093/infdis/jit528  PMID: 24106293 
/content/10.2807/1560-7917.ES.2017.22.32.30591
Loading

Data & Media loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error