Genomic identification of streptococcal strains and relation to clinical characteristics. A substudy to The Partial Oral Treatment of Endocarditis (POET) Trial.

Main Article Content

Jens J. Christensen Christian S. Jensen Rimtas Dargis Xiaohui C. Nielsen Mia M. Pries- Heje Christoffer Wiingaard Nikolaj Ihlemann Sabine Gill Niels E. Bruun Hanne Elming Jonas A. Povlsen Trine Madsen Kaare T. Jensen Kurt Fuursted Lauge Østergaard Ulrik Christiansen Flemming S. Rosenvinge Jannik Helweg-Larsen Emil L. Fosbøl Lars Køber Christian Torp-Pedersen Niels Tønder Claus Moser Kasper Iversen Henning Bundgaard

Abstract

The Danish National Partial Oral Treatment of Endocarditis Trial (POET) demonstrated non-inferiority of partly peroral compared to intravenous antibiotic therapy for infective endocarditis (IE) caused by Streptococcus spp, Enterococcus faecalis, Staphylococcus aureus, or coagulase-negative staphylococci. Identifications by whole genome sequencing (WGS) of available streptococcal strains were related to clinical data. Sequences were obtained using Illumina technology (MiseqÒ) followed by core genome analysis and single-nucleotide polymorphism phylogeny examinations. Average nucleotide identification (ANI) calculated using the tool fastANI. Informations on +/- preexisting valve prosthesis, valve surgery and outcome related to obtained identifications. Streptococcal strains (n=123) from 117 patients were WGS examined. Twelve percent were pyogenic group strains and 88% belonged to viridans groups, mainly mitis and bovis groups. Phylogenetic trees were in accordance regarding species and subspecies identifications. High ANI percentages to type strains were found. Respectively 39, 60 and 16 IE cases involved mitral, aortic or both valves. IE caused by pyogenic group or mitis plus bovis group streptococci most frequent affected, respectively, mitral and aortic valves.  Thirty-one patients (26%) had a preexisting prosthesis; notably, in 50% of bovis group IE cases. Fifty-six patients had valve surgery done during the current disease; 8% and 93% of patients having, respectively, pyogenic group and mitis group strains as causative agents. Of patients allocated to intravenous or intravenous followed by peroral antibiotic treatment, respectively 26 and 30 had valve surgery done during the current disease. Composite outcome (all-cause mortality, unplanned cardiac surgery, embolic events, or relapse of bacteremia with the primary pathogen) at five-year follow-up comprised in total 39 events. In conclusion, molecular examinations adds on substantially by detailing species and subspecies affiliations.  A broad spectrum of streptococcal species and subspecies causing IE were identified with mitis- and bovis group strains dominating. Relating strain identifications to clinical data can assist in planning and treating confirmed/suspected IE patients. Adding WGS identification of streptococci in selected patients groups (e.g. IE) in order to expand number of cases characterized in detail seems ideal and advocates for centralized registration of results to reveal important clinical relations. 

Keywords: whole-genome sequencing, infective endocarditis, streptococci, partial oral antibiotic treatment, clinical outcome

Article Details

How to Cite
CHRISTENSEN, Jens J. et al. Genomic identification of streptococcal strains and relation to clinical characteristics. A substudy to The Partial Oral Treatment of Endocarditis (POET) Trial.. Medical Research Archives, [S.l.], v. 10, n. 9, sep. 2022. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/3037>. Date accessed: 20 apr. 2024. doi: https://doi.org/10.18103/mra.v10i9.3037.
Section
Research Articles

References

1. Allen CJ, Klein JL, Prendergast BD. Streptococcal Infective Endocarditis: ‘On the Origin of Species’. Circulation. 2020;142(8):731-733. doi:10.1161/CIRCULATIONAHA.120.049055
2. Pant S, Patel NJ, Deshmukh A, et al. Trends in infective endocarditis incidence, microbiology, and valve replacement in the United States from 2000 to 2011. J Am Coll Cardiol. 2015;65(19):2070-2076. doi:10.1016/j.jacc.2015.03.518
3. Cresti A, Chiavarelli M, Scalese M, et al. Epidemiological and mortality trends in infective endocarditis, a 17-year population-based prospective study. Cardiovasc Diagn Ther. 2017;7(1):27-35. doi:10.21037/cdt.2016.08.09
4. Iversen K, Ihlemann N, Gill SU, et al. Partial oral versus intravenous antibiotic treatment of endocarditis. N Engl J Med. 2019;380(5). doi:10.1056/NEJMoa1808312
5. Bundgaard H, Ihlemann N, Gill SU, et al. Long-term outcomes of partial oral treatment of endocarditis. N Engl J Med. 2019;380(14). doi:10.1056/NEJMc1902096
6. Pries-Heje MM, Wiingaard C, Ihlemann N, et al. Five-Year Outcomes of the Partial Oral Treatment of Endocarditis (POET) Trial. N Engl J Med. 2022;386(6):601-602. doi:10.1056/NEJMc2114046
7. Tsuchida S, Umemura H, Nakayama T. Current Status of Matrix-Assisted Laser Desorption/Ionization–Time-of-Flight Mass Spectrometry (MALDI-TOF MS) in Clinical Diagnostic Microbiology. Molecules. 2020;25(20). doi:10.3390/molecules25204775
8. Chamat-Hedemand S, Dahl A, Østergaard L, et al. Prevalence of Infective Endocarditis in Streptococcal Bloodstream Infections Is Dependent on Streptococcal Species. Circulation. 2020;142(8):720-730. doi:10.1161/CIRCULATIONAHA.120.046723
9. Nilson B, Olaison L, Rasmussen M. Clinical presentation of infective endocarditis caused by different groups of non-beta haemolytic streptococci. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2016;35(2):215-218. doi:10.1007/s10096-015-2532-5
10. Jensen A, Scholz CFP, Kilian M. Re-evaluation of the taxonomy of the Mitis group of the genus Streptococcus based on whole genome phylogenetic analyses, and proposed reclassification of Streptococcus dentisani as Streptococcus oralis subsp. dentisani comb. nov., Streptococcus tigurinus. Int J Syst Evol Microbiol. 2016;66(11):4803-4820. doi:10.1099/ijsem.0.001433
11. Facklam R. What Happened to the Streptococci : Overview of Taxonomic and Nomenclature Changes. Clin Microbiol Rev. 2002;15(4):616-630. doi:10.1128/CMR.15.4.613
12. Harju I, Lange C, Kostrzewa M, Maier T, Rantakokko-Jalava K, Haanperä M. Improved Differentiation of Streptococcus pneumoniae and Other S. mitis Group Streptococci by MALDI Biotyper Using an Improved MALDI Biotyper Database Content and a Novel Result Interpretation Algorithm. J Clin Microbiol. 2017;55(3):914-922. doi:10.1128/JCM.01990-16
13. Isaksson J, Rasmussen M, Nilson B, et al. Comparison of species identification of endocarditis associated viridans streptococci using rnpB genotyping and 2 MALDI-TOF systems. Diagn Microbiol Infect Dis. 2015;81(4):240-245. doi:10.1016/j.diagmicrobio.2014.12.007
14. Kilian M, Riley DR, Jensen A, Brüggemann H, Tettelin H. Parallel evolution of Streptococcus pneumoniae and Streptococcus mitis to pathogenic and mutualistic lifestyles. MBio. 2014;5(4):e01490-14. doi:10.1128/mBio.01490-14
15. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072-1075. doi:10.1093/bioinformatics/btt086
16. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307-321. doi:10.1093/sysbio/syq010
17. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47(W1):W256-W259. doi:10.1093/nar/gkz239
18. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9(1):5114. doi:10.1038/s41467-018-07641-9
19. Su T-Y, Lee M-H, Huang C-T, Liu T-P, Lu J-J. The clinical impact of patients with bloodstream infection with different groups of Viridans group streptococci by using matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS). Medicine (Baltimore). 2018;97(50):e13607. doi:10.1097/MD.0000000000013607
20. Jensen CS, Dargis R, Shewmaker P, Nielsen XC, Christensen JJ. Identification of Streptococcus pseudopneumoniae and other mitis group streptococci using matrix assisted laser desorption/ionization - time of flight mass spectrometry. Diagn Microbiol Infect Dis. 2021;101(3):115487. doi:10.1016/j.diagmicrobio.2021.115487
21. Rasmussen LH, Højholt K, Dargis R, et al. In silico assessment of virulence factors in strains of streptococcus oralis and Streptococcus mitis isolated from patients with infective endocarditis. J Med Microbiol. 2017;66(9). doi:10.1099/jmm.0.000573
22. Rasmussen LH, Dargis R, H?jholt K, et al. Whole genome sequencing as a tool for phylogenetic analysis of clinical strains of Mitis group streptococci. Eur J Clin Microbiol Infect Dis. 2016;35(10). doi:10.1007/s10096-016-2700-2
23. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 2009;106(45):19126-19131. doi:10.1073/pnas.0906412106
24. Ben-Chetrit E, Wiener-Well Y, Kashat L, Yinnon AM, Assous M V. Streptococcus bovis new taxonomy: does subspecies distinction matter? Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2017;36(2):387-393. doi:10.1007/s10096-016-2814-6
25. Schlegel L, Grimont F, Ageron E, Grimont PAD, Bouvet A. Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. Int J Syst Evol Microbiol. 2003;53(Pt 3):631-645. doi:10.1099/ijs.0.02361-0
26. Poyart C, Quesne G, Trieu-Cuot P. Taxonomic dissection of the Streptococcus bovis group by analysis of manganese-dependent superoxide dismutase gene (sodA) sequences: reclassification of ‘Streptococcus infantarius subsp. coli’ as Streptococcus lutetiensis sp. nov. and of Streptococcus bo. Int J Syst Evol Microbiol. 2002;52(Pt 4):1247-1255. doi:10.1099/00207713-52-4-1247
27. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol. 2020;70(11):5607-5612. doi:10.1099/ijsem.0.004332
28. Habib G, Lancellotti P, Erba P-A, et al. The ESC-EORP EURO-ENDO (European Infective Endocarditis) registry. Eur Hear journal Qual care Clin outcomes. 2019;5(3):202-207. doi:10.1093/ehjqcco/qcz018
29. Muñoz P, Kestler M, De Alarcon A, et al. Current Epidemiology and Outcome of Infective Endocarditis: A Multicenter, Prospective, Cohort Study. Medicine (Baltimore). 2015;94(43):e1816. doi:10.1097/MD.0000000000001816
30. Habib G, Erba PA, Iung B, et al. Clinical presentation, aetiology and outcome of infective endocarditis. Results of the ESC-EORP EURO-ENDO (European infective endocarditis) registry: a prospective cohort study. Eur Heart J. 2019;40(39):3222-3232. doi:10.1093/eurheartj/ehz620
31. Bläckberg A, Nilson B, Özenci V, Olaison L, Rasmussen M. Infective endocarditis due to Streptococcus dysgalactiae: clinical presentation and microbiological features. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2018;37(12):2261-2272. doi:10.1007/s10096-018-3367-7
32. de Egea V, Muñoz P, Valerio M, et al. Characteristics and Outcome of Streptococcus pneumoniae Endocarditis in the XXI Century: A Systematic Review of 111 Cases (2000-2013). Medicine (Baltimore). 2015;94(39):e1562. doi:10.1097/MD.0000000000001562