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Surveillance Open Access
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Abstract

Background

Since 2008, Danish national surveillance of has focused on binary toxin-positive strains in order to monitor epidemic types such as PCR ribotype (RT) 027 and 078. Additional surveillance is needed to provide a more unbiased representation of all strains from the clinical reservoir.

Aim

Setting up a new sentinel surveillance scheme for an improved understanding of type distribution relative to time, geography and epidemiology, here presenting data from 2016 to 2019.

Methods

For 2─4 weeks in spring and autumn each year between 2016 and 2019, all 10 Danish Departments of Clinical Microbiology collected faecal samples containing toxigenic . Isolates were typed at the national reference laboratory at Statens Serum Institut. The typing method in 2016–17 used tandem-repeat-sequence typing, while the typing method in 2018–19 was whole genome sequencing.

Results

During the study period, the sentinel surveillance scheme included ca 14–15% of all Danish cases of infections. Binary toxin-negative strains accounted for 75% and 16 of the 20 most prevalent types. The most common sequence types (ST) were ST2/13 (RT014/020) (19.5%), ST1 (RT027) (10.8%), ST11 (RT078) (6.7%), ST8 (RT002) (6.6%) and ST6 (RT005/117) (5.1%). The data also highlighted geographical differences, mostly related to ST1 and temporal decline of ST1 (p = 0.0008) and the increase of ST103 (p = 0.002), ST17 (p = 0.004) and ST37 (p = 0.003), the latter three binary toxin-negative.

Conclusion

Sentinel surveillance allowed nationwide monitoring of geographical differences and temporal changes in infections in Denmark, including emerging types, regardless of binary toxin status.

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/content/10.2807/1560-7917.ES.2022.27.49.2200244
2022-12-08
2024-02-28
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2022.27.49.2200244
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References

  1. Czepiel J, Dróżdż M, Pituch H, Kuijper EJ, Perucki W, Mielimonka A, et al. Clostridium difficile infection: review. Eur J Clin Microbiol Infect Dis. 2019;38(7):1211-21.  https://doi.org/10.1007/s10096-019-03539-6  PMID: 30945014 
  2. Kuijper EJ, Coignard B, Tüll P, ESCMID Study Group for Clostridium difficile, EU Member States, European Centre for Disease Prevention and Control. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect. 2006;12(Suppl 6):2-18.  https://doi.org/10.1111/j.1469-0691.2006.01580.x  PMID: 16965399 
  3. Warny M, Pepin J, Fang A, Killgore G, Thompson A, Brazier J, et al. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet. 2005;366(9491):1079-84.  https://doi.org/10.1016/S0140-6736(05)67420-X  PMID: 16182895 
  4. He M, Miyajima F, Roberts P, Ellison L, Pickard DJ, Martin MJ, et al. Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nat Genet. 2013;45(1):109-13.  https://doi.org/10.1038/ng.2478  PMID: 23222960 
  5. Bauer MP, Notermans DW, van Benthem BH, Brazier JS, Wilcox MH, Rupnik M, et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet. 2011;377(9759):63-73.  https://doi.org/10.1016/S0140-6736(10)61266-4  PMID: 21084111 
  6. Ofori E, Ramai D, Dhawan M, Mustafa F, Gasperino J, Reddy M. Community-acquired Clostridium difficile: epidemiology, ribotype, risk factors, hospital and intensive care unit outcomes, and current and emerging therapies. J Hosp Infect. 2018;99(4):436-42.  https://doi.org/10.1016/j.jhin.2018.01.015  PMID: 29410012 
  7. Brown AWW, Wilson RB. Clostridium difficile colitis and zoonotic origins-a narrative review. Gastroenterol Rep (Oxf). 2018;6(3):157-66.  https://doi.org/10.1093/gastro/goy016  PMID: 30151199 
  8. Søes L, Mølbak K, Strøbaek S, Truberg Jensen K, Torpdahl M, Persson S, et al. The emergence of Clostridium difficile PCR ribotype 027 in Denmark--a possible link with the increased consumption of fluoroquinolones and cephalosporins? Euro Surveill. 2009;14(15):19176.  https://doi.org/10.2807/ese.14.15.19176-en  PMID: 19371514 
  9. Bacci S, St-Martin G, Olesen B, Bruun B, Olsen KE, Nielsen EM, et al. Outbreak of Clostridium difficile 027 in North Zealand, Denmark, 2008-2009. Euro Surveill. 2009;14(16):19183.  https://doi.org/10.2807/ese.14.16.19183-en  PMID: 19389341 
  10. Carlson TJ, Blasingame D, Gonzales-Luna AJ, Alnezary F, Garey KW. Clostridioides difficile ribotype 106: A systematic review of the antimicrobial susceptibility, genetics, and clinical outcomes of this common worldwide strain. Anaerobe. 2020;62:102142.  https://doi.org/10.1016/j.anaerobe.2019.102142  PMID: 32007682 
  11. Barbanti F, Spigaglia P. Microbiological characteristics of human and animal isolates of Clostridioides difficile in Italy: Results of the Istituto Superiore di Sanità in the years 2006-2016. Anaerobe. 2020;61:102136.  https://doi.org/10.1016/j.anaerobe.2019.102136  PMID: 31857201 
  12. Imwattana K, Knight DR, Kullin B, Collins DA, Putsathit P, Kiratisin P, et al. Clostridium difficile ribotype 017 - characterization, evolution and epidemiology of the dominant strain in Asia. Emerg Microbes Infect. 2019;8(1):796-807.  https://doi.org/10.1080/22221751.2019.1621670  PMID: 31138041 
  13. European Centre for Disease Prevention and Control (ECDC). European Surveillance of Clostridioides (Clostridium) difficile infections. Stockholm: ECDC; 2019. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/clostridium-difficile-infections-EU-surveillance-protocol-vers2.4.pdf
  14. Zaiss NH, Rupnik M, Kuijper EJ, Harmanus C, Michielsen D, Janssens K, et al. Typing Clostridium difficile strains based on tandem repeat sequences. BMC Microbiol. 2009;9(1):6.  https://doi.org/10.1186/1471-2180-9-6  PMID: 19133124 
  15. Persson S, Jensen JN, Olsen KE. Multiplex PCR method for detection of Clostridium difficile tcdA, tcdB, cdtA, and cdtB and internal in-frame deletion of tcdC. J Clin Microbiol. 2011;49(12):4299-300.  https://doi.org/10.1128/JCM.05161-11  PMID: 21976756 
  16. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124.  https://doi.org/10.12688/wellcomeopenres.14826.1  PMID: 30345391 
  17. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2022. Available from: https://www.R-project.org/
  18. Freeman J, Vernon J, Morris K, Nicholson S, Todhunter S, Longshaw C, et al. Pan-European longitudinal surveillance of antibiotic resistance among prevalent Clostridium difficile ribotypes. Clin Microbiol Infect. 2015 Mar;21(3):248 e9-16.
  19. van Dorp SM, Kinross P, Gastmeier P, Behnke M, Kola A, Delmée M, et al. Standardised surveillance of Clostridium difficile infection in European acute care hospitals: a pilot study, 2013. Euro Surveill. 2016;21(29).  https://doi.org/10.2807/1560-7917.ES.2016.21.29.30293  PMID: 27472820 
  20. Davies KA, Ashwin H, Longshaw CM, Burns DA, Davis GL, Wilcox MH, EUCLID study group. Diversity of Clostridium difficile PCR ribotypes in Europe: results from the European, multicentre, prospective, biannual, point-prevalence study of Clostridium difficile infection in hospitalised patients with diarrhoea (EUCLID), 2012 and 2013. Euro Surveill. 2016;21(29).  https://doi.org/10.2807/1560-7917.ES.2016.21.29.30294  PMID: 27470194 
  21. Eyre DW, Davies KA, Davis G, Fawley WN, Dingle KE, De Maio N, et al. Two Distinct Patterns of Clostridium difficile Diversity Across Europe Indicating Contrasting Routes of Spread. Clin Infect Dis. 2018;67(7):1035-44.  https://doi.org/10.1093/cid/ciy252  PMID: 29659747 
  22. Rizzardi K, Norén T, Aspevall O, Mäkitalo B, Toepfer M, Johansson Å, et al. National Surveillance for Clostridioides difficile Infection, Sweden, 2009-2016. Emerg Infect Dis. 2018;24(9):1617-25.  https://doi.org/10.3201/eid2409.171658  PMID: 30124193 
  23. Sandell S, Rashid MU, Jorup-Rönström C, Ellström K, Nord CE, Weintraub A. Clostridium difficile recurrences in Stockholm. Anaerobe. 2016;38:97-102.  https://doi.org/10.1016/j.anaerobe.2016.01.005  PMID: 26802875 
  24. Banks A, Brown DJ, Mather H, Coia JE, Wiuff C. Sentinel community Clostridium difficile infection (CDI) surveillance in Scotland, April 2013 to March 2014. Anaerobe. 2016;37:49-53.  https://doi.org/10.1016/j.anaerobe.2015.12.008  PMID: 26708405 
  25. Waslawski S, Lo ES, Ewing SA, Young VB, Aronoff DM, Sharp SE, et al. Clostridium difficile ribotype diversity at six health care institutions in the United States. J Clin Microbiol. 2013;51(6):1938-41.  https://doi.org/10.1128/JCM.00056-13  PMID: 23554188 
  26. Gonzales-Luna AJ, Carlson TJ, Dotson KM, Poblete K, Costa G, Miranda J, et al. PCR ribotypes of Clostridioides difficile across Texas from 2011 to 2018 including emergence of ribotype 255. Emerg Microbes Infect. 2020;9(1):341-7.  https://doi.org/10.1080/22221751.2020.1721335  PMID: 32037964 
  27. Cheknis A, Johnson S, Chesnel L, Petrella L, Sambol S, Dale SE, et al. Molecular epidemiology of Clostridioides (Clostridium) difficile strains recovered from clinical trials in the US, Canada and Europe from 2006-2009 to 2012-2015. Anaerobe. 2018;53:38-42.  https://doi.org/10.1016/j.anaerobe.2018.05.009  PMID: 29886050 
  28. Martin JS, Monaghan TM, Wilcox MH. Clostridium difficile infection: epidemiology, diagnosis and understanding transmission. Nat Rev Gastroenterol Hepatol. 2016;13(4):206-16.  https://doi.org/10.1038/nrgastro.2016.25  PMID: 26956066 
  29. Hong S, Putsathit P, George N, Hemphill C, Huntington PG, Korman TM, et al. Laboratory-Based Surveillance of Clostridium difficile Infection in Australian Health Care and Community Settings, 2013 to 2018. J Clin Microbiol. 2020;58(11):e01552-20.  https://doi.org/10.1128/JCM.01552-20  PMID: 32848038 
  30. Bjöersdorff OG, Lindberg S, Kiil K, Persson S, Guardabassi L, Damborg P. Dogs are carriers of Clostridioides difficile lineages associated with human community-acquired infections. Anaerobe. 2021;67:102317.  https://doi.org/10.1016/j.anaerobe.2020.102317  PMID: 33418077 
  31. Dingle KE, Didelot X, Quan TP, Eyre DW, Stoesser N, Marwick CA, et al. A Role for Tetracycline Selection in Recent Evolution of Agriculture-Associated Clostridium difficile PCR Ribotype 078. MBio. 2019;10(2):e02790-18.  https://doi.org/10.1128/mBio.02790-18  PMID: 30862754 
  32. Walker AS, Eyre DW, Wyllie DH, Dingle KE, Griffiths D, Shine B, et al. Relationship between bacterial strain type, host biomarkers, and mortality in Clostridium difficile infection. Clin Infect Dis. 2013;56(11):1589-600.  https://doi.org/10.1093/cid/cit127  PMID: 23463640 
  33. Riley TV, Collins DA, Karunakaran R, Kahar MA, Adnan A, Hassan SA, et al. High Prevalence of Toxigenic and Nontoxigenic Clostridium difficile Strains in Malaysia. J Clin Microbiol. 2018;56(6):e00170-18.  https://doi.org/10.1128/JCM.00170-18  PMID: 29563206 
  34. Senoh M, Kato H, Fukuda T, Niikawa A, Hori Y, Hagiya H, et al. Predominance of PCR-ribotypes, 018 (smz) and 369 (trf) of Clostridium difficile in Japan: a potential relationship with other global circulating strains? J Med Microbiol. 2015;64(10):1226-36.  https://doi.org/10.1099/jmm.0.000149  PMID: 26238868 
  35. Shaw HA, Preston MD, Vendrik KEW, Cairns MD, Browne HP, Stabler RA, et al. The recent emergence of a highly related virulent Clostridium difficile clade with unique characteristics. Clin Microbiol Infect. 2020;26(4):492-8.  https://doi.org/10.1016/j.cmi.2019.09.004  PMID: 31525517 
  36. Collins DA, Sohn KM, Wu Y, Ouchi K, Ishii Y, Elliott B, et al. Clostridioides difficile infection in the Asia-Pacific region. Emerg Microbes Infect. 2019;9(1):42-52.  https://doi.org/10.1080/22221751.2019.1702480  PMID: 31873046 
  37. Statens Serum Institut (SSI). Uge 24 – 2020. Stigning i Clostridioides (tidligere Clostridium) difficile ST37/PCR ribotype 017. [Increase of Clostridioides (former Clostridium) difficile ST37/PCR ribotype 017]. Copenhagen: SSI; 2020. Danish. Available from: https://www.ssi.dk/aktuelt/nyhedsbreve/epi-nyt/2020/uge-24---2020
  38. Borali E, De Giacomo C. Clostridium Difficile Infection in Children: A Review. J Pediatr Gastroenterol Nutr. 2016;63(6):e130-40.  https://doi.org/10.1097/MPG.0000000000001264  PMID: 27182626 
  39. van Dorp SM, Smajlović E, Knetsch CW, Notermans DW, de Greeff SC, Kuijper EJ. Clinical and Microbiological Characteristics of Clostridium difficile Infection Among Hospitalized Children in the Netherlands. Clin Infect Dis. 2017;64(2):192-8.  https://doi.org/10.1093/cid/ciw699  PMID: 27986664 
  40. Adlerberth I, Huang H, Lindberg E, Åberg N, Hesselmar B, Saalman R, et al. Toxin-producing Clostridium difficile strains as long-term gut colonizers in healthy infants. J Clin Microbiol. 2014;52(1):173-9.  https://doi.org/10.1128/JCM.01701-13  PMID: 24172156 
  41. Thomas E, Bémer P, Eckert C, Guillouzouic A, Orain J, Corvec S, et al. Clostridium difficile infections: analysis of recurrence in an area with low prevalence of 027 strain. J Hosp Infect. 2016;93(1):109-12.  https://doi.org/10.1016/j.jhin.2016.01.015  PMID: 26944905 
  42. Sachsenheimer FE, Yang I, Zimmermann O, Wrede C, Müller LV, Gunka K, et al. Genomic and phenotypic diversity of Clostridium difficile during long-term sequential recurrences of infection. Int J Med Microbiol. 2018;308(3):364-77.  https://doi.org/10.1016/j.ijmm.2018.02.002  PMID: 29490877 
  43. Crobach MJ, Planche T, Eckert C, Barbut F, Terveer EM, Dekkers OM, et al. European Society of Clinical Microbiology and Infectious Diseases: update of the diagnostic guidance document for Clostridium difficile infection. Clin Microbiol Infect. 2016;22(Suppl 4):S63-81.  https://doi.org/10.1016/j.cmi.2016.03.010  PMID: 27460910 
  44. Martínez-Meléndez A, Morfin-Otero R, Villarreal-Treviño L, Baines SD, Camacho-Ortíz A, Garza-González E. Molecular epidemiology of predominant and emerging Clostridioides difficile ribotypes. J Microbiol Methods. 2020;175:105974.  https://doi.org/10.1016/j.mimet.2020.105974  PMID: 32531232 
  45. Janezic S, Rupnik M. Genomic diversity of Clostridium difficile strains. Res Microbiol. 2015;166(4):353-60.  https://doi.org/10.1016/j.resmic.2015.02.002  PMID: 25700631 
  46. Krutova M, Nyc O, Matejkova J, Allerberger F, Wilcox MH, Kuijper EJ. Molecular characterisation of Czech Clostridium difficile isolates collected in 2013-2015. Int J Med Microbiol. 2016;306(7):479-85.  https://doi.org/10.1016/j.ijmm.2016.07.003  PMID: 27519407 
  47. Griffiths D, Fawley W, Kachrimanidou M, Bowden R, Crook DW, Fung R, et al. Multilocus sequence typing of Clostridium difficile. J Clin Microbiol. 2010;48(3):770-8.  https://doi.org/10.1128/JCM.01796-09  PMID: 20042623 
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