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Abstract

Introduction

Water supply and air-conditioner cooling towers (ACCT) are potential sources of infection in people. During outbreaks, traditional typing methods cannot sufficiently segregate strains to reliably trace back transmissions to these artificial water systems. Moreover, because multiple strains may be present within these systems, methods to adequately distinguish strains are needed. Whole genome sequencing (WGS) and core genome multilocus sequence typing (cgMLST), with their higher resolution are helpful in this respect. In summer 2017, the health administration of the city of Basel detected an increase of infections compared with previous months, signalling an outbreak.

Aim

We aimed to identify strains populating suspected environmental sources of the outbreak, and to assess the relations between these strains and clinical outbreak strains.

Methods

An epidemiological and WGS-based microbiological investigation was performed, involving isolates from the local water supply and two ACCTs (n = 60), clinical outbreak and non-outbreak related isolates from 2017 (n = 8) and historic isolates from 2003–2016 (n = 26).

Results

In both ACCTs, multiple strains were found. Phylogenetic analysis of the ACCT isolates showed a diversity of a few hundred allelic differences in cgMLST. Furthermore, two isolates from one ACCT showed no allelic differences to three clinical isolates from 2017. Five clinical isolates collected in the Basel area in the last decade were also identical in cgMLST to recent isolates from the two ACCTs.

Conclusion

Current outbreak-related and historic isolates were linked to ACCTs, which form a complex environmental habitat where strains are conserved over years.

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/content/10.2807/1560-7917.ES.2019.24.4.1800192
2019-01-24
2024-04-20
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.4.1800192
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References

  1. Winn WC Jr. Legionnaires disease: historical perspective. Clin Microbiol Rev. 1988;1(1):60-81.  https://doi.org/10.1128/CMR.1.1.60  PMID: 3060246 
  2. Beauté JThe European Legionnaires’ Disease Surveillance Network. Legionnaires’ disease in Europe, 2011 to 2015. Euro Surveill. 2017;22(27).  https://doi.org/10.2807/1560-7917.ES.2017.22.27.30566  PMID: 28703097 
  3. Federal Office of Public Health (FOPH). Liebefeld: FOPH. Available from: https://www.bag.admin.ch
  4. Cunha BA, Burillo A, Bouza E. Legionnaires’ disease. Lancet. 2016;387(10016):376-85.  https://doi.org/10.1016/S0140-6736(15)60078-2  PMID: 26231463 
  5. Schjørring S, Stegger M, Kjelsø C, Lilje B, Bangsborg JM, Petersen RF, et al. ESCMID Study Group for Legionella Infections (ESGLI). Genomic investigation of a suspected outbreak of Legionella pneumophila ST82 reveals undetected heterogeneity by the present gold-standard methods, Denmark, July to November 2014. Euro Surveill. 2017;22(25):30558.  https://doi.org/10.2807/1560-7917.ES.2017.22.25.30558  PMID: 28662761 
  6. Laganà P, Gambuzza ME, Delia S. Legionella risk assessment in cruise ships and ferries. Ann Agric Environ Med. 2017;24(2):276-82.  https://doi.org/10.26444/aaem/74717  PMID: 28664708 
  7. Yoshida M, Furuya N, Hosokawa N, Kanamori H, Kaku M, Koide M, et al. Legionella pneumophila contamination of hospital dishwashers. Am J Infect Control. 2018;46(8):943-5.  https://doi.org/10.1016/j.ajic.2018.01.024  PMID: 29502885 
  8. Rosendahl Madsen AM, Holm A, Jensen TG, Knudsen E, Lundgaard H, Skov MN, et al. Whole-genome sequencing for identification of the source in hospital-acquired Legionnaires’ disease. J Hosp Infect. 2017;96(4):392-5.  https://doi.org/10.1016/j.jhin.2017.04.020  PMID: 28622979 
  9. Lucas KD, Wheeler C, McLendon P, Leistikow BN, Mohle-Boetani JC. Outbreak of Legionnaires’ disease associated with cooling towers at a California state prison, 2015. Epidemiol Infect. 2018;146(3):297-302.  https://doi.org/10.1017/S0950268818000110  PMID: 29386076 
  10. Llewellyn AC, Lucas CE, Roberts SE, Brown EW, Nayak BS, Raphael BH, et al. Distribution of Legionella and bacterial community composition among regionally diverse US cooling towers. PLoS One. 2017;12(12):e0189937.  https://doi.org/10.1371/journal.pone.0189937  PMID: 29261791 
  11. Timms VJ, Rockett R, Bachmann NL, Martinez E, Wang Q, Chen SC, et al. Genome sequencing links persistent outbreak of legionellosis in Sydney (New South Wales, Australia) to an emerging clone of Legionella pneumophila sequence type 211. Appl Environ Microbiol. 2018;84(5):e02020-17.  https://doi.org/10.1128/AEM.02020-17  PMID: 29247056 
  12. Lapierre P, Nazarian E, Zhu Y, Wroblewski D, Saylors A, Passaretti T, et al. Legionnaires’ disease outbreak caused by endemic strain of Legionella pneumophila, New York, New York, USA, 2015. Emerg Infect Dis. 2017;23(11):1784-91.  https://doi.org/10.3201/eid2311.170308  PMID: 29047425 
  13. David S, Rusniok C, Mentasti M, Gomez-Valero L, Harris SR, Lechat P, et al. Multiple major disease-associated clones of Legionella pneumophila have emerged recently and independently. Genome Res. 2016;26(11):1555-64.  https://doi.org/10.1101/gr.209536.116  PMID: 27662900 
  14. Sabat AJ, Budimir A, Nashev D, Sá-Leão R, van Dijl J, Laurent F, et al. . Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill. 2013;18(4):20380.  https://doi.org/10.2807/ese.18.04.20380-en  PMID: 23369389 
  15. Moran-Gilad J, Prior K, Yakunin E, Harrison TG, Underwood A, Lazarovitch T, et al. Design and application of a core genome multilocus sequence typing scheme for investigation of Legionnaires’ disease incidents. Euro Surveill. 2015;20(28):1-9.  https://doi.org/10.2807/1560-7917.ES2015.20.28.21186  PMID: 26212142 
  16. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50(4):1355-61.  https://doi.org/10.1128/JCM.06094-11  PMID: 22238442 
  17. Shivaji T, Sousa Pinto C, San-Bento A, Oliveira Serra LA, Valente J, Machado J, et al. A large community outbreak of Legionnaires disease in Vila Franca de Xira, Portugal, October to November 2014. Euro Surveill. 2014;19(50):20991.  https://doi.org/10.2807/1560-7917.ES2014.19.50.20991  PMID: 25597540 
  18. David S, Afshar B, Mentasti M, Ginevra C, Podglajen I, Harris SR, et al. Seeding and establishment of legionella pneumophila in hospitals: Implications for genomic investigations of nosocomial legionnaires’ disease. Clin Infect Dis. 2017;64(9):1251-9.  https://doi.org/10.1093/cid/cix153  PMID: 28203790 
  19. Garbe PL, Davis BJ, Weisfeld JS, Markowitz L, Miner P, Garrity F, et al. Nosocomial Legionnaires’ disease. Epidemiologic demonstration of cooling towers as a source. JAMA. 1985;254(4):521-4.  https://doi.org/10.1001/jama.1985.03360040075028  PMID: 4009880 
  20. Bosch X. Legionnaire’s outbreak in Spanish town may be largest ever. Lancet. 2001;358(9277):220.  https://doi.org/10.1016/S0140-6736(01)05465-4  PMID: 11476856 
  21. McAdam PR, Vander Broek CW, Lindsay DS, Ward MJ, Hanson MF, Gillies M, et al. Gene flow in environmental Legionella pneumophila leads to genetic and pathogenic heterogeneity within a Legionnaires’ disease outbreak. Genome Biol. 2014;15(11):504. PMID: 25370747 
  22. Piso RJ, Käch R, Pop R, Zillig D, Schibli U, Bassetti S, et al. A cross-sectional study of colonization rates with Methicillin-Resistant Staphylococcus aureus (MRSA) and Extended-Spectrum Beta-Lactamase (ESBL) and carbapenemase-producing Enterobacteriaceae in four Swiss refugee centres. PLoS One. 2017;12(1):e0170251.  https://doi.org/10.1371/journal.pone.0170251  PMID: 28085966 
  23. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLOS Comput Biol. 2017;13(6):e1005595.  https://doi.org/10.1371/journal.pcbi.1005595  PMID: 28594827 
  24. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068-9.  https://doi.org/10.1093/bioinformatics/btu153  PMID: 24642063 
  25. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31(22):3691-3.  https://doi.org/10.1093/bioinformatics/btv421  PMID: 26198102 
  26. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5(3):e9490.  https://doi.org/10.1371/journal.pone.0009490  PMID: 20224823 
  27. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23(1):127-8.  https://doi.org/10.1093/bioinformatics/btl529  PMID: 17050570 
  28. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-60.  https://doi.org/10.1093/bioinformatics/btp324  PMID: 19451168 
  29. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9(11):e112963.  https://doi.org/10.1371/journal.pone.0112963  PMID: 25409509 
  30. Wéry N, Bru-Adan V, Minervini C, Delgénes JP, Garrelly L, Godon JJ. Dynamics of Legionella spp. and bacterial populations during the proliferation of L. pneumophila in a cooling tower facility. Appl Environ Microbiol. 2008;74(10):3030-7.  https://doi.org/10.1128/AEM.02760-07  PMID: 18390683 
  31. Scholz M, Ward DV, Pasolli E, Tolio T, Zolfo M, Asnicar F, et al. Strain-level microbial epidemiology and population genomics from shotgun metagenomics. Nat Methods. 2016;13(5):435-8.  https://doi.org/10.1038/nmeth.3802  PMID: 26999001 
  32. Truong DT, Tett A, Pasolli E, Huttenhower C, Segata N. Microbial strain-level population structure and genetic diversity from metagenomes. Genome Res. 2017;27(4):626-38.  https://doi.org/10.1101/gr.216242.116  PMID: 28167665 
  33. Türetgen I, Sungur EI, Cotuk A. Enumeration of Legionella pneumophila in cooling tower water systems. Environ Monit Assess. 2005;100(1-3):53-8.  https://doi.org/10.1007/s10661-005-7058-3  PMID: 15727299 
  34. Mouchtouri VA, Goutziana G, Kremastinou J, Hadjichristodoulou C. Legionella species colonization in cooling towers: risk factors and assessment of control measures. Am J Infect Control. 2010;38(1):50-5.  https://doi.org/10.1016/j.ajic.2009.04.285  PMID: 19699013 
  35. Yu VL. Cooling towers and legionellosis: a conundrum with proposed solutions. Int J Hyg Environ Health. 2008;211(3-4):229-34.  https://doi.org/10.1016/j.ijheh.2008.02.003  PMID: 18406666 
  36. Reller BL, Weinstein MP, Murdoch DR. Diagnosis of Legionella infection. Clin Infect Dis. 2003;36(1):64-9.  https://doi.org/10.1086/345529  PMID: 12491204 
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