Multiple-locus variable number of tandem repeat analysis as a tool for molecular epidemiology of botulism: The Italian experience

Infection, Genetics and Evolution

Volumn 46, Issue , 2016, Pages 28-32

  Anniballi, Fabrizio ^a   Fillo, Silvia ^b   Giordani, Francesco ^b   Auricchio, Bruna ^a   Tehran, Domenico Azarnia ^b   di Stefano, Enrica ^b   Mandarino, Giuseppina ^a   De Medici, Dario ^a   Lista, Florigio ^b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Army Medical and Veterinary Research Center   (Italy)

Author keywords

Botulism; Control; Epidemiology; Molecular tools; Sub typing; Surveillance

Indexed keywords

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BOTULISM; CLOSTRIDIUM BOTULINUM; DNA ISOLATION; ITALY; MOLECULAR EPIDEMIOLOGY; MOLECULAR PHYLOGENY; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; TANDEM REPEAT; CLUSTER ANALYSIS; GENETICS; HUMAN; MICROBIOLOGY; MULTILOCUS SEQUENCE TYPING; PROCEDURES;

BOTULISM; CLOSTRIDIUM BOTULINUM; CLUSTER ANALYSIS; HUMANS; ITALY; MOLECULAR EPIDEMIOLOGY; MULTILOCUS SEQUENCE TYPING; TANDEM REPEAT SEQUENCES;

EID: 84993960818     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2016.10.014     Document Type: Article

References (41)

1. Anniballi, F., Auricchio, B., Fiore, A., Fillo, S., Giordani, F., Azarnia Tehran, D., Di Stefano, E., Lonati, D., Locatelli, C.A., De Medici, D., Lista, F., Molecular Epidemiology of Botulism, 1986–2015. 2016, Eurosurveillance (submitted for publication).
2. Auricchio, B., Anniballi, F., Fiore, A., Skiby, J.E., De Medici, D., Evaluation of DNA extraction methods suitable for PCR-based detection and genotyping of Clostridium botulinum. Biosecur. Bioterror. Suppl. 1 (2013), S200–S206.
3. Centers for Disease Control and Prevention, Botulism in the United States, 1899–1996. Handbook for Epidemiologists, Clinicians, and Laboratory Workers. 1998, Centers for Disease Control and Prevention, Atlanta, GA.
4. Dabritz, H.A., Hill, K.K., Barash, J.R., Ticknor, L.O., Helma, C.H., Dover, N., Payne, J.R., Arnon, S.S., Molecular epidemiology of infant botulism in California and elsewhere, 1976-2010. J. Infect. Dis. 210 (2014), 1711–1722.
5. De Valk, H.A., Meis, J.F.G.M., Bretagne, S., Costa, J.M., Lasker, B.A., Balajee, S.A., Pasqualotto, A.C., Anderson, M.J., Alcàzar-Fuoli, L., Mellado, E., Klaassen, C.H.W., Interlaboratory reproducibility of a microsatellite-based typing assay for Aspergillus fumigatus through the use of allelic ladders: proof of concept. Clin. Microbiol. Infect. 15 (2008), 180–187.
6. Döpfer, D., Buist, W., Soyer, Y., Munoz, M.A., Zadoks, R.N., Leue, L., Engel, B., Assessing genetic heterogeneity within bacterial species isolated from gastrointestinal and environmental samples: how many isolates does it take?. Appl. Environ. Microbiol. 74 (2008), 3490–3496.
7. Dover, N., Barash, J.R., Hill, K.K., Davenport, K.W., Teshima, H., Xie, G., Arnon, S.S., Clostridium botulinum strain Af84 contains three neurotoxin gene clusters: bont/A2, bont/F4 and bont/F5. PLoS One, 8, 2013, e61205.
8. ECDC (European Centre for Disease Prevention and Control), Surveillance of Communicable Diseases in the European Union. A Long-term Strategy, 2008-2013. Available at: http://www.ecdc.europa.eu/en/aboutus/key%20documents/08-13_kd_surveillance:of_cd.pdf, 2007 (Accessed 08 August 2016).
9. Eklund, M.W., Poysky, F.T., Peterson, M.E., Paranjpye, R.N., Pelroy, G.A., Competitive inhibition between different Clostridium botulinum types and strains. J. Food Prot. 67 (2004), 2682–2687.
10. Fillo, S., Giordani, F., Anniballi, F., Gorgè, O., Ramisse, V., Vergnaud, G., Reihm, J.M., Scholz, H.C., Splettstoesser, W.D., Kieboom, J., Olsen, J.S., Fenicia, L., Lista, F., Clostridium botulinum group I strain genotyping by 15-locus multilocus variable-number tandem-repeat analysis. J. Clin. Microbiol. 49 (2011), 4252–4263.
11. Foley, S.T., Lynne, A.M., Nayak, R., Molecular typing for microbial source tracking and epidemiological investigations of gram-negative bacterial foodborne pathogens. Infect. Genet. Evol. 9 (2009), 430–440.
12. Giordani, F., Fillo, S., Anselmo, A., Palozzi, A.M., Fortunato, A., Gentile, B., Azarnia, T.D., Ciammaruconi, A., Spagnolo, F., Pittiglio, V., Anniballi, F., Auricchio, B., De Medici, D., Lista, F., Genomic characterization of Italian Clostridium botulinum group I strains. Infect. Genet. Evol. 36 (2015), 62–71.
13. Gonzales-Escalona, N., Timme, R., Raphael, B.H., Zink, D., Sharma, S.K., Whole-genome single-nucleotide-polymorphism analysis for discrimination of Clostridium botulinum group I strains. Appl. Environ. Microbiol. 80 (2014), 2125–2132.
14. Hatheway, C.L., Toxigenic clostridia. Clin. Microbiol. Rev. 3 (1990), 66–98.
15. Hill, K.K., Xie, G., Foley, B.T., Smith, T.J., Genetic diversity within botulinum neurotoxin-producing bacteria and their toxins. Toxicon 107:Pt A (2015), 2–8.
16. Hopkins, K.L., Peters, T.M., de Pinna, E., Wain, J., Standardisation of multilocus variable-number tandem-repeat analysis (MLVA) for subtyping of Salmonella enterica serovar Enteritidis. Euro Surveill., 16, 2011 (pii = 19942).
17. Kenri, T., Sekizuka, T., Yamamoto, A., Iwaki, M., Komiya, T., Hatakeyama, T., Nakajima, H., Takahashi, M., Kuroda, M., Shibayama, K., Genetic characterization and comparison of Clostridium botulinum isolates from botulism cases in Japan between 2006 and 2011. Appl. Environ. Microbiol. 80 (2014), 6954–6964.
18. Lindström, M., Hielm, S., Nevas, M., Tuisku, S., Korkeala, H., Proteolytic Clostridium botulinum type B in the gastric content of a patient with type E botulism due to Whitefish eggs. Foodborne Pathog. Dis. 1 (2004), 53–57.
19. Lúquez, C., Joseph, L.A., Maslanka, S.E., Molecular subtyping of Clostridium botulinum by pulsed-field gel electrophoresis. Methods Mol. Biol. 1301 (2015), 103–113.
20. McCallum, N., Gray, T.J., Wang, Q., NG, J., Hicks, L., Nguyen, T., Yuen, M., Hill-Cawthorne, G.A., Sintchenko, V., Genomic epidemiology of Clostridium botulinum isolates from temporally related cases of infant botulism in New South Wales, Australia. J. Clin. Microbiol. 53 (2015), 2846–2853.
21. McDonald, T.E., Helamm, C.H., Ticknorm, L.O., Jackson, P.J., Okinaka, R.T., Smith, L.A., Smith, T.J., Hill, K.K., Differentiation of Clostridium botulinum serotype A strains by multiple-locus variable-number tandem-repeat analysis. Appl. Environ. Microbiol. 74 (2008), 875–882.
22. Ministry of Health, Circular of the Ministry of Health No. 9 of 1 July 1996. Botulism: Prevention and Control, 1996.
23. Nadon, C.A., Trees, E., Ng, L.K., Moller Nielsen, E., Reimer, A., Maxwell, N., Kubota, K.A., Gerner-Smidt, P., the MLVA Harmonization Working Group, Development and application of MLVA method as a tool for inter-laboratory surveillance. Euro Surveill., 18, 2013 (pii = 20565).
24. Nevas, M., Lindström, M., Hörman, A., Keto-Timonen, R.K., Korkeala, H., Contamination routes of Clostridium botulinum in the honey production environment. Environ. Microbiol. 8 (2006), 1085–1094.
25. Olsen, J.S., Scholz, H., Fillo, S., Ramisse, V., Lista, F., Trømborg, A.K., Aarskaug, T., Thrane, I., Blatny, J.M., Analysis of the genetic distribution among members of Clostridium botulinum group I using a novel multilocus sequence typing (MLST) assay. J. Microbiol. Methods 96 (2014), 84–91.
26. Peck, M.W., Biology and genomic analysis of Clostridium botulinum. Adv. Microb. Physiol., 55(183–265), 2009, 320.
27. Peck, M.W., Stringer, S.C., Carter, A.T., Clostridium botulinum in the post-genomic era. Food Microbiol. 28 (2011), 183–191.
28. Popoff, M.R., Ecology of neurotoxigenic strains of clostridia. Curr. Top. Microbiol. Immunol. 195 (1995), 1–29.
29. Popoff, M.R., Bouvet, P., Genetic characterization of toxigenic clostridia and toxin gene evolution. Toxicon 75 (2013), 63–89.
30. Pruvost, O., Magne, M., Boyer, K., Leduc, A., Tourterel, C., Drevet, C., Ravigné, V., Gagnevin, L., Guérin, F., Chiroleu, F., Koebnik, R., Verdier, V., Vernière, C., A MLVA genotyping scheme for global surveillance of citrus pathogen Xanthomonas citri pv. citri suggests a worldwide geographical expansion of a single genetic lineage. PLoS One, 9, 2014, e98129.
31. Raphael, B.H., Shirey, T.B., Lúquez, C., Maslanka, S.E., Distinguishing highly-related outbreak-associated Clostridium botulinum type A(B) strains. BMC Microbiol., 14, 2014, 192.
32. Skarin, H., Segerman, B., Horizontal gene transfer of toxin genes in Clostridium botulinum: involvement of mobile elements and plasmids. Mob. Genet. Elem. 1 (2011), 213–215.
33. Smith, T.J., Hill, K.K., Xie, G., Foley, B.T., Williamson, C.H., Foster, J.T., Johnson, S.L., Chertkow, O., Teshima, H., Gibbons, H.S., Johnsky, L.A., Karavis, M.A., Smith, L.A., Genomic sequences of six botulinum neurotoxin-producing strains representing three clostridial species illustrate the mobility and diversity of botulinum neurotoxin genes. Infect. Genet. Evol. 30 (2015), 102–113.
34. Stringer, S.C., Carter, A.T., Webb, M.D., Wachnicka, E., Crossman, L.C., Sebaihia, M., Peck, M.W., Genomic and physiological variability within group II (non-proteolytic) Clostridium botulinum. BMC Genomics, 14, 2013, 333.
35. Thierry, S., Tourterel, C., Le Flèche, P., Derzelle, S., Dekhil, N., Mendy, C., Colaneri, C., Vergnaud, G., Madani, N., Genotyping of French Bacillus anthracis strains based on 31-loci multi locus VNTR analysis: epidemiology, marker evaluation, and update of the internet genotype database. PLos One, 9, 2014, e95131.
36. Umeda, K., Wada, T., Kohda, T., Kozaki, S., Multi-locus variable tandem repeat analysis for Clostridium botulinum type B isolates in Japan: comparison with other isolates and genotyping methods. Infect. Genet. Evol. 16 (2013), 298–304.
37. Vanhomwegen, J., Berthet, N., Mazuet, C., Guigon, G., Vallaeys, T., Stamboliyska, R., Dubois, P., Kennedy, G.C., Cole, S.T., Caro, V., Manuguerra, J.C., Popoff, M.R., Application of high-density DNA resequencing microarray for detection and characterization of botulinum neurotoxin-producing clostridia. PLoS One, 8, 2013, e67510.
38. Wangroongsarb, P., Kohda, T., Jittaprasartisin, C., Suthivarakom, K., Kamthalang, T., Umeda, K., Sawanpanyalert, P., Kozaki, S., Ikuta, K., Molecular characterization of Clostridium botulinum isolates from foodborne outbreaks in Thailand, 2010. PLoS One, 9, 2014, e77792.
39. Weedmark, K.A., Mabon, P., Hayden, K.L., Lambert, D., Van Domselaar, G., Austin, J.W., Corbett, C.R., Phylogenomic profiling of Clostridium botulinum group II isolates using whole genome sequence data. Appl. Environ. Microbiol. 81 (2015), 5938–5948.
40. Woudstra, C., Lambert, D., Anniballi, F., De Medici, D., Austin, J.W., Fach, P., Genetic diversity of the flagellin genes of Clostridium botulinum groups I and II. Appl. Environ. Microbiol. 79 (2013), 3926–3932.
41. Woudstra, C., Le Maréchal, C., Souillard, R., Bayo-Auboyer, M.H., Anniballi, F., Auricchio, B., De Medici, D., Bano, L., Koene, M., Sansonetti, M.H., Desoutter, D., Hansbauder, E.M., Dorner, M.B., Dorner, B.G., Fach, P., Molecular gene profiling of Clostridium botulinum group III and its detection in naturally contaminated samples originating from various European countries. Appl. Environ. Microbiol. 81 (2015), 2495–2505.