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Volume 26, Number 7—July 2020
Research

Large Nationwide Outbreak of Invasive Listeriosis Associated with Blood Sausage, Germany, 2018–2019

Sven Halbedel1Comments to Author , Hendrik Wilking1, Alexandra Holzer, Sylvia Kleta, Martin A. Fischer, Stefanie Lüth, Ariane Pietzka, Steliana Huhulescu, Raskit Lachmann, Amrei Krings, Werner Ruppitsch, Alexandre Leclercq, Rolf Kamphausen, Maylin Meincke, Christiane Wagner-Wiening, Matthias Contzen, Iris Barbara Kraemer, Sascha Al Dahouk, Franz Allerberger, Klaus Stark2, and Antje Flieger2Comments to Author 
Author affiliations: Robert Koch Institute, Wernigerode, Germany (S. Halbedel, M.A. Fischer, A. Flieger); Robert Koch Institute, Berlin, Germany (H. Wilking, A. Holzer, R. Lachmann, A. Krings, M. Meincke, K. Stark); German Federal Institute for Risk Assessment, Berlin (S. Kleta, S. Lüth, S.A. Dahouk); Freie Universität Berlin, Berlin (S. Lüth); Austrian Agency for Health and Food Safety, Vienna, Austria (A. Pietzka, S. Huhulescu, W. Ruppitsch, F. Allerberger); European Centre for Disease Prevention and Control, Stockholm, Sweden (A. Krings, M. Meincke); Institut Pasteur, Paris, France (A. Leclercq); Ministry for Environment, Agriculture, Conservation and Consumer Protection of the State of North Rhine-Westphalia, Düsseldorf, Germany (R. Kamphausen); State Health Office Baden-Wuerttemberg, Stuttgart, Germany (M. Meincke, C. Wagner-Wiening); Chemical and Veterinary Investigations Office, Fellbach, Germany (M. Contzen); Bavarian Health and Food Safety Authority, Oberschleißheim, Germany (I.B. Kraemer); Rheinisch-Westfälische Technische Hochschule, Aachen, Germany (S.A. Dahouk)

Main Article

Figure 1

Phylogenic tree constructed by using unweighted pair group method with arithmetic mean and core genome multilocus sequence typing data of Listeria monocytogenes isolates from a large listeriosis outbreak, Germany. Green indicates clinical isolates of Epsilon1a subcluster; blue indicates food isolates of Epsilon1a subcluster; pink indicates isolates from the Epsilon1 cluster; violet indicates 2 complex type 4465 isolates not belonging to Epsilon1a from earlier listeriosis cases in July 2017 and J

Figure 1. Phylogenic tree constructed by using unweighted pair group method with arithmetic mean and core genome multilocus sequence typing data of Listeria monocytogenes isolates from a large listeriosis outbreak, Germany. Green indicates clinical isolates of Epsilon1a subcluster; blue indicates food isolates of Epsilon1a subcluster; pink indicates isolates from the Epsilon1 cluster; violet indicates 2 complex type 4465 isolates not belonging to Epsilon1a from earlier listeriosis cases in July 2017 and June 2018; yellow indicates isolates from a listeriosis outbreak in South Africa (11); black indicates reference strain 10-092876-0769 LM12 used for SNP calling (Appendix Figure 2). Scale bar indicates allelic substitutions per site. SNP, single-nucleotide polymorphism.

Main Article

References
  1. Werber  D, Hille  K, Frank  C, Dehnert  M, Altmann  D, Müller-Nordhorn  J, et al. Years of potential life lost for six major enteric pathogens, Germany, 2004-2008. Epidemiol Infect. 2013;141:9618. DOIPubMedGoogle Scholar
  2. Ooi  ST, Lorber  B. Gastroenteritis due to Listeria monocytogenes. Clin Infect Dis. 2005;40:132732. DOIPubMedGoogle Scholar
  3. Halbedel  S, Prager  R, Banerji  S, Kleta  S, Trost  E, Nishanth  G, et al. A Listeria monocytogenes ST2 clone lacking chitinase ChiB from an outbreak of non-invasive gastroenteritis. Emerg Microbes Infect. 2019;8:1728. DOIPubMedGoogle Scholar
  4. Allerberger  F, Wagner  M. Listeriosis: a resurgent foodborne infection. Clin Microbiol Infect. 2010;16:1623. DOIPubMedGoogle Scholar
  5. Charlier  C, Perrodeau  É, Leclercq  A, Cazenave  B, Pilmis  B, Henry  B, et al.; MONALISA study group. Clinical features and prognostic factors of listeriosis: the MONALISA national prospective cohort study. Lancet Infect Dis. 2017;17:5109. DOIPubMedGoogle Scholar
  6. de Noordhout  CM, Devleesschauwer  B, Angulo  FJ, Verbeke  G, Haagsma  J, Kirk  M, et al. The global burden of listeriosis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14:107382. DOIPubMedGoogle Scholar
  7. European Centre for Disease Prevention and Control. Surveillance atlas of infectious diseases. 2018 [cited 2020 Mar 16]. https://atlas.ecdc.europa.eu/public/index.aspx
  8. Ferreira  V, Wiedmann  M, Teixeira  P, Stasiewicz  MJ. Listeria monocytogenes persistence in food-associated environments: epidemiology, strain characteristics, and implications for public health. J Food Prot. 2014;77:15070. DOIPubMedGoogle Scholar
  9. Swaminathan  B, Gerner-Smidt  P. The epidemiology of human listeriosis. Microbes Infect. 2007;9:123643. DOIPubMedGoogle Scholar
  10. McCollum  JT, Cronquist  AB, Silk  BJ, Jackson  KA, O’Connor  KA, Cosgrove  S, et al. Multistate outbreak of listeriosis associated with cantaloupe. N Engl J Med. 2013;369:94453. DOIPubMedGoogle Scholar
  11. Smith  AM, Tau  NP, Smouse  SL, Allam  M, Ismail  A, Ramalwa  NR, et al. Outbreak of Listeria monocytogenes in South Africa, 2017–2018: laboratory activities and experiences associated with whole-genome sequencing analysis of isolates. Foodborne Pathog Dis. 2019;16:52430. DOIPubMedGoogle Scholar
  12. Stephan  R, Althaus  D, Kiefer  S, Lehner  A, Hatz  C, Schmutz  C, et al. Foodborne transmission of Listeria monocytogenes via ready-to-eat salad: A nationwide outbreak in Switzerland, 2013–2014. Food Control. 2015;57:147. DOIGoogle Scholar
  13. Goulet  V, King  LA, Vaillant  V, de Valk  H. What is the incubation period for listeriosis? BMC Infect Dis. 2013;13:11. DOIPubMedGoogle Scholar
  14. Heiman  KE, Garalde  VB, Gronostaj  M, Jackson  KA, Beam  S, Joseph  L, et al. Multistate outbreak of listeriosis caused by imported cheese and evidence of cross-contamination of other cheeses, USA, 2012. Epidemiol Infect. 2016;144:2698708. DOIPubMedGoogle Scholar
  15. European Centre for Disease Prevention and Control and European Food Safety Authority. Multi-country outbreak of Listeria monocytogenes sequence type 8 infections linked to consumption of salmon products—25 October 2018. Stockholm and Parma: ECDC/EFSA; 2018 [cited 2019 Dec 17]. https://www.ecdc.europa.eu/sites/default/files/documents/listeria-multi-country-outbreak-october-2018.pdf
  16. Ruppitsch  W, Prager  R, Halbedel  S, Hyden  P, Pietzka  A, Huhulescu  S, et al. Ongoing outbreak of invasive listeriosis, Germany, 2012 to 2015. Euro Surveill. 2015;20:30094. DOIPubMedGoogle Scholar
  17. Halbedel  S, Prager  R, Fuchs  S, Trost  E, Werner  G, Flieger  A. Whole-genome sequencing of recent Listeria monocytogenes isolates from Germany reveals population structure and disease clusters. J Clin Microbiol. 2018;56:e0011918. DOIPubMedGoogle Scholar
  18. Kleta  S, Hammerl  JA, Dieckmann  R, Malorny  B, Borowiak  M, Halbedel  S, et al. Molecular tracing to find source of protracted invasive listeriosis outbreak, southern Germany, 2012–2016. Emerg Infect Dis. 2017;23:16803. DOIPubMedGoogle Scholar
  19. Jackson  BR, Tarr  C, Strain  E, Jackson  KA, Conrad  A, Carleton  H, et al. Implementation of nationwide real-time whole-genome sequencing to enhance listeriosis outbreak detection and investigation. Clin Infect Dis. 2016;63:3806. DOIPubMedGoogle Scholar
  20. Moura  A, Tourdjman  M, Leclercq  A, Hamelin  E, Laurent  E, Fredriksen  N, et al. Real-time whole-genome sequencing for surveillance of Listeria monocytogenes, France. Emerg Infect Dis. 2017;23:146270. DOIPubMedGoogle Scholar
  21. Kwong  JC, Mercoulia  K, Tomita  T, Easton  M, Li  HY, Bulach  DM, et al. Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol. 2016;54:33342. DOIPubMedGoogle Scholar
  22. Chen  Y, Gonzalez-Escalona  N, Hammack  TS, Allard  MW, Strain  EA, Brown  EW. Core genome multilocus sequence typing for identification of globally distributed clonal groups and differentiation of outbreak strains of Listeria monocytogenes. Appl Environ Microbiol. 2016;82:625872. DOIPubMedGoogle Scholar
  23. World Health Organization. Listeriosis–Spain, disease outbreak news. Geneva: the Organization; updated 2019 Sep 16 [cited 2019 Oct 1]. https://www.who.int/csr/don/16-september-2019-listeriosis-spain
  24. International Organization for Standardization. ISO 11290-1:2017. Microbiology of the food chain—Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp.—part 1: detection method. Geneva: The Organization; 2017 [cited 2019 Dec 17]. https://www.iso.org/standard/60313.html
  25. International Organization for Standardization. ISO 11290-2:2017. Microbiology of the food chain—horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp.—part 2: enumeration method. Geneva: The Organization; 2017 [cited 2019 Dec 17]. https://www.iso.org/standard/60314.html
  26. Bubert  A, Hein  I, Rauch  M, Lehner  A, Yoon  B, Goebel  W, et al. Detection and differentiation of Listeria spp. by a single reaction based on multiplex PCR. Appl Environ Microbiol. 1999;65:468892. DOIPubMedGoogle Scholar
  27. Kérouanton  A, Marault  M, Petit  L, Grout  J, Dao  TT, Brisabois  A. Evaluation of a multiplex PCR assay as an alternative method for Listeria monocytogenes serotyping. J Microbiol Methods. 2010;80:1347. DOIPubMedGoogle Scholar
  28. Ruppitsch  W, Pietzka  A, Prior  K, Bletz  S, Fernandez  HL, Allerberger  F, et al. Defining and evaluating a core genome multilocus sequence typing scheme for whole-genome sequence-based typing of Listeria monocytogenes. J Clin Microbiol. 2015;53:286976. DOIPubMedGoogle Scholar
  29. Moura  A, Criscuolo  A, Pouseele  H, Maury  MM, Leclercq  A, Tarr  C, et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol. 2016;2:16185. DOIPubMedGoogle Scholar
  30. Noll  M, Kleta  S, Al Dahouk  S. Antibiotic susceptibility of 259 Listeria monocytogenes strains isolated from food, food-processing plants and human samples in Germany. J Infect Public Health. 2018;11:5727. DOIPubMedGoogle Scholar
  31. European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 9.0, 2019. Basal (Switzerland): EUCAST; 2019 Jan 1 [cited 2019 Dec 5]. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_9.0_Breakpoint_Tables.pdf
  32. Maury  MM, Tsai  YH, Charlier  C, Touchon  M, Chenal-Francisque  V, Leclercq  A, et al. Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet. 2016;48:30813. DOIPubMedGoogle Scholar
  33. Jacquet  C, Catimel  B, Brosch  R, Buchrieser  C, Dehaumont  P, Goulet  V, et al. Investigations related to the epidemic strain involved in the French listeriosis outbreak in 1992. Appl Environ Microbiol. 1995;61:22426. DOIPubMedGoogle Scholar
  34. Pereira  JA, Silva  P, Matos  TJ, Patarata  L. Shelf life determination of sliced Portuguese traditional blood sausage—Morcela de Arroz de Monchique through microbiological challenge and consumer test. J Food Sci. 2015;80:M6428. DOIPubMedGoogle Scholar
  35. Allerberger  F, Huhulescu  S. Pregnancy related listeriosis: treatment and control. Expert Rev Anti Infect Ther. 2015;13:395403. DOIPubMedGoogle Scholar
  36. Groeneveld  M, Wichmann-Schauer  H, Oehlenschläger  J, Werber  D, Maschkowski  G; Federal Institute of Agriculture and Food. Listeriosis and toxoplasmosis-safe eating during pregnancy, 2nd edition; B. Klein editor [in German]. Bonn, Germany: Bundesanstalt für Landwirtschaft und Ernährung; 2017 [cited 2019 Dec 17]. https://www.ble-medienservice.de/frontend/esddownload/index/id/513/on/0346_DL/act/dl
  37. Cantinelli  T, Chenal-Francisque  V, Diancourt  L, Frezal  L, Leclercq  A, Wirth  T, et al. “Epidemic clones” of Listeria monocytogenes are widespread and ancient clonal groups. J Clin Microbiol. 2013;51:37709. DOIPubMedGoogle Scholar
  38. Koopmans  MM, Brouwer  MC, Bijlsma  MW, Bovenkerk  S, Keijzers  W, van der Ende  A, et al. Listeria monocytogenes sequence type 6 and increased rate of unfavorable outcome in meningitis: epidemiologic cohort study. Clin Infect Dis. 2013;57:24753. DOIPubMedGoogle Scholar
  39. Kremer  PH, Lees  JA, Koopmans  MM, Ferwerda  B, Arends  AW, Feller  MM, et al. Benzalkonium tolerance genes and outcome in Listeria monocytogenes meningitis. Clin Microbiol Infect. 2017;23:265.e17. DOIPubMedGoogle Scholar
  40. European Union. Commission implementing decision (EU) 2016/1950 of 4 November 2016 on the non-approval of certain biocidal active substances pursuant to Regulation (EU) No. 528/2012 of the European Parliament and of the Council. Official Journal of the European Union 2016. p. 16–20 [cited 2019 Dec 17]. https://www.helpdesk-biocides.fr/files/PDF/reglementation_europe/en_non_inscription_sa/20161104_decision_2016_1950_eu_non_approval_susbtances_bpr.pdf

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1These authors contributed equally to this article.

2These authors contributed equally to this article.

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