A global genomic analysis of Salmonella Concord reveals lineages with high antimicrobial resistance in Ethiopia
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, přehledy, práce podpořená grantem
Grantová podpora
BBS/E/F/000PR10349
Biotechnology and Biological Sciences Research Council - United Kingdom
BB/R012504/1
Biotechnology and Biological Sciences Research Council - United Kingdom
MC_PC_16093
Medical Research Council - United Kingdom
BB/CCG1720/1
Biotechnology and Biological Sciences Research Council - United Kingdom
Wellcome Trust - United Kingdom
206194
Wellcome Trust - United Kingdom
PubMed
37316492
PubMed Central
PMC10267216
DOI
10.1038/s41467-023-38902-x
PII: 10.1038/s41467-023-38902-x
Knihovny.cz E-zdroje
- MeSH
- antibakteriální látky * farmakologie MeSH
- bakteriální léková rezistence * genetika MeSH
- genomika MeSH
- lidé MeSH
- Salmonella genetika MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Geografické názvy
- Etiopie epidemiologie MeSH
- Názvy látek
- antibakteriální látky * MeSH
Antimicrobial resistant Salmonella enterica serovar Concord (S. Concord) is known to cause severe gastrointestinal and bloodstream infections in patients from Ethiopia and Ethiopian adoptees, and occasional records exist of S. Concord linked to other countries. The evolution and geographical distribution of S. Concord remained unclear. Here, we provide a genomic overview of the population structure and antimicrobial resistance (AMR) of S. Concord by analysing genomes from 284 historical and contemporary isolates obtained between 1944 and 2022 across the globe. We demonstrate that S. Concord is a polyphyletic serovar distributed among three Salmonella super-lineages. Super-lineage A is composed of eight S. Concord lineages, of which four are associated with multiple countries and low levels of AMR. Other lineages are restricted to Ethiopia and horizontally acquired resistance to most antimicrobials used for treating invasive Salmonella infections in low- and middle-income countries. By reconstructing complete genomes for 10 representative strains, we demonstrate the presence of AMR markers integrated in structurally diverse IncHI2 and IncA/C2 plasmids, and/or the chromosome. Molecular surveillance of pathogens such as S. Concord supports the understanding of AMR and the multi-sector response to the global AMR threat. This study provides a comprehensive baseline data set essential for future molecular surveillance.
Adrem Data Lab Department of Computer Science University of Antwerp Antwerp Belgium
Department of Biomedical Sciences Institute of Tropical Medicine Antwerp Belgium
Department of Medical Laboratory Sciences Faculty of Health Sciences Jimma University Jimma Ethiopia
Department of Microbiology Immunology and Transplantation KU Leuven Leuven Belgium
Division of Human Bacterial Diseases Sciensano Brussels Belgium
Gastrointestinal Bacterial Reference Unit United Kingdom Health Security Agency Colindale London UK
Institute of Infection Veterinary and Ecological Sciences University of Liverpool Liverpool UK
London School of Hygiene and Tropical Medicine Bloomsbury London UK
MRC Centre for Molecular Bacteriology and Infection Imperial College London London UK
National Reference Laboratory for salmonella State Veterinary Institute Prague Prague Czech Republic
Norwich Medical School University of East Anglia Norwich UK
Quadram Institute Bioscience Norwich Research Park Norwich UK
Wellcome Trust Sanger Institute Genome Campus Hinxton Cambridge United Kingdom
Zobrazit více v PubMed
Grimont PAD, W. F. X. Antigenic formulae of the Salmonella serovars, 9th ed. (World health organization collaborating center for reference and research on Salmonella, Insitut Pasteur, 2007).
Gal-Mor O, Boyle EC, Grassl GA. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol. 2014;5:391. doi: 10.3389/fmicb.2014.00391. PubMed DOI PMC
Silva C, Calva E, Maloy S. One Health and food-borne disease: Salmonella transmission between humans, animals, and plants. Microbiol. Spectr. 2014;2:OH-0020–OH-2013. doi: 10.1128/microbiolspec.OH-0020-2013. PubMed DOI
Liu, H., Whitehouse, C. A. & Li, B. Presence and persistence of salmonella in water: the impact on microbial quality of water and food safety. Front. Public Health6, 159 (2018). PubMed PMC
Hohmann EL. Nontyphoidal salmonellosis. Clin. Infect. Dis. 2001;32:263–269. doi: 10.1086/318457. PubMed DOI
Gordon MA. Salmonella infections in immunocompromised adults. J. Infect. 2008;56:413–422. doi: 10.1016/j.jinf.2008.03.012. PubMed DOI
Van Puyvelde S, et al. An African Salmonella Typhimurium ST313 sublineage with extensive drug-resistance and signatures of host adaptation. Nat. Commun. 2019;10:1–12. PubMed PMC
Tanner JR, Kingsley RA. Evolution of Salmonella within Hosts. Trends Microbiol. 2018;26:986. doi: 10.1016/j.tim.2018.06.001. PubMed DOI PMC
Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 2012;379:2489–2499. doi: 10.1016/S0140-6736(11)61752-2. PubMed DOI PMC
GBD 2017 Non-Typhoidal Salmonella Invasive Disease Collaborators. The global burden of non-typhoidal salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect. Dis. 2019;19:1312–1324. doi: 10.1016/S1473-3099(19)30418-9. PubMed DOI PMC
Marchello CS, Birkhold M, Crump JA, Vacc-iNTS consortium collaborators. Complications and mortality of non-typhoidal salmonella invasive disease: a global systematic review and meta-analysis. Lancet Infect. Dis. 2022;22:692–705. doi: 10.1016/S1473-3099(21)00615-0. PubMed DOI PMC
Edwards PR, Hughes H. A new salmonella type isolated from man and fowls. J. Bacteriol. 1944;47:574–575. doi: 10.1128/jb.47.6.574-575.1944. PubMed DOI PMC
Gebre-Yohannes A. Salmonella from Ethiopia: prevalent species and their susceptibility to drugs. Ethiop. Med. J. 1985;23:97–102. PubMed
Pegram RG, Roeder PL, Hall ML, Rowe B. Salmonella in livestock and animal by-products in Ethiopia. Trop. Anim. Health Prod. 1981;13:203–207. doi: 10.1007/BF02237926. PubMed DOI
Nabbut NH, Barbour EK, Al-Nakhli HM. Salmonella species and serotypes isolated from farm animals, animal feed, sewage, and sludge in Saudi Arabia. Bull. World Health Organ. 1982;60:803–807. PubMed PMC
Barbour EK, Nabbut NH. Isolation of salmonella and some other potential pathogens from two chicken breeding farms in Saudi Arabia. Avian Dis. 1982;26:234. doi: 10.2307/1590092. PubMed DOI
Erdem B, Ercis S, Hascelik G, Gur D, Aysev AD. Antimicrobial resistance of Salmonella enterica group C strains isolated from humans in Turkey, 2000-2002. Int. J. Antimicrob. Agents. 2005;26:33–37. doi: 10.1016/j.ijantimicag.2005.03.007. PubMed DOI
Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup F. M. beta-Lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J. Antimicrob. Chemother. 2005;56:115–121. doi: 10.1093/jac/dki190. PubMed DOI
Veldman K, Dierikx C, van Essen-Zandbergen A, van Pelt W, Mevius D. Characterization of multidrug-resistant, qnrB2-positive and extended-spectrum-lactamase-producing Salmonella Concord and Salmonella Senftenberg isolates. J. Antimicrob. Chemother. 2010;65:872–875. doi: 10.1093/jac/dkq049. PubMed DOI
Fabre L, et al. Chromosomal integration of the extended-spectrum beta-lactamase gene blaCTX-M-15 in Salmonella enterica serotype Concord isolates from internationally adopted children. Antimicrob. Agents Chemother. 2009;53:1808–1816. doi: 10.1128/AAC.00451-08. PubMed DOI PMC
Hendriksen, R. S. et al. Upsurge of infections caused by Salmonella Concord among Ethiopian adoptees in Denmark, 2009. Euro Surveill. 15, 19587 (2010). PubMed
Morris D, et al. First report of extended-spectrum-ß-lactamase-producing salmonella enterica isolates in ireland. Antimicrobial Agents Chemother. 2006;50:1608–1609. doi: 10.1128/AAC.50.4.1608-1609.2006. PubMed DOI PMC
Sjölund-Karlsson M, et al. CTX-M-producing non-Typhi Salmonella spp. isolated from humans, United States. Emerg. Infect. Dis. 2011;17:97–99. doi: 10.3201/eid1701.100511. PubMed DOI PMC
Hendriksen RS, et al. Emergence of multidrug-resistant salmonella concord infections in europe and the united states in children adopted from ethiopia, 2003–2007. Pediatr. Infect. Dis. J. 2009;28:814–818. doi: 10.1097/INF.0b013e3181a3aeac. PubMed DOI
Vanhoof R, et al. Transmission of multiple resistant Salmonella Concord from internationally adopted children to their adoptive families and social environment: proposition of guidelines. Eur. J. Clin. Microbiol. Infect. Dis. 2012;31:491–497. doi: 10.1007/s10096-011-1336-5. PubMed DOI PMC
Beyene G, et al. Multidrug resistant Salmonella Concord is a major cause of salmonellosis in children in Ethiopia. J. Infect. Dev. Ctries. 2011;5:23–33. doi: 10.3855/jidc.906. PubMed DOI
Popa GL, Papa MI. Salmonella spp. infection—a continuous threat worldwide. Germs. 2021;11:88–96. doi: 10.18683/germs.2021.1244. PubMed DOI PMC
Outbreak investigation of Salmonella Concord: Tahini (November 2018). U.S. Food and Drug Administrationhttps://www.fda.gov/food/outbreaks-foodborne-illness/outbreak-investigation-salmonella-concord-tahini-november-2018.
Kariuki S, Gordon MA, Feasey N, Parry CM. Antimicrobial resistance and management of invasive Salmonella disease. Vaccine. 2015;33:C21–C29. doi: 10.1016/j.vaccine.2015.03.102. PubMed DOI PMC
Tack B, Vanaenrode J, Verbakel JY, Toelen J, Jacobs J. Invasive non-typhoidal Salmonella infections in sub-Saharan Africa: a systematic review on antimicrobial resistance and treatment. BMC Med. 2020;18:212. doi: 10.1186/s12916-020-01652-4. PubMed DOI PMC
Tack B, et al. Non-typhoidal Salmonella bloodstream infections in Kisantu, DR Congo: Emergence of O5-negative Salmonella Typhimurium and extensive drug resistance. PLoS Negl. Trop. Dis. 2020;14:e0008121. doi: 10.1371/journal.pntd.0008121. PubMed DOI PMC
Zhou Z, et al. The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res. 2020;30:138–152. doi: 10.1101/gr.251678.119. PubMed DOI PMC
Outbreak of Salmonella Infections Linked to karawan brand tahini. https://www.cdc.gov/salmonella/concord-05-19/index.html (2019).
Outbreak investigation of Salmonella Concord: Tahini (May 2019). U.S. Food and Drug Administrationhttps://www.fda.gov/food/outbreaks-foodborne-illness/outbreak-investigation-salmonella-concord-tahini-may-2019.
Tyson, G. H. et al. The mcr-9 gene of Salmonella and Escherichia coli is not associated with colistin resistance in the United States. Antimicrob. Agents Chemother. 64, e00573-20 (2020). PubMed PMC
Macesic N, et al. Silent spread of mobile colistin resistance gene mcr-9.1 on IncHI2 ‘superplasmids’ in clinical carbapenem-resistant Enterobacterales. Clin. Microbiol. Infect. 2021;27:12. doi: 10.1016/j.cmi.2021.04.020. PubMed DOI
Poirel L, et al. The mgrB gene as a key target for acquired resistance to colistin in Klebsiella pneumoniae. J. Antimicrob. Chemother. 2015;70:75–80. doi: 10.1093/jac/dku323. PubMed DOI
Cannatelli A, et al. MgrB inactivation is a common mechanism of colistin resistance in KPC-producing Klebsiella pneumoniae of clinical origin. Antimicrob. Agents Chemother. 2014;58:5696–5703. doi: 10.1128/AAC.03110-14. PubMed DOI PMC
Livermore DM, et al. Activity of temocillin against prevalent ESBL- and AmpC-producing Enterobacteriaceae from south-east England. J. Antimicrob. Chemother. 2006;57:1012–1014. doi: 10.1093/jac/dkl043. PubMed DOI
Feasey NA, et al. Drug resistance in Salmonella enterica ser. Typhimurium bloodstream infection, Malawi. Emerg. Infect. Dis. 2014;20:1957–1959. doi: 10.3201/eid2011.141175. PubMed DOI PMC
Kariuki S, et al. Ceftriaxone-resistant Salmonella enterica serotype typhimurium sequence type 313 from Kenyan patients is associated with the blaCTX-M-15 gene on a novel IncHI2 plasmid. Antimicrob. Agents Chemother. 2015;59:3133–3139. doi: 10.1128/AAC.00078-15. PubMed DOI PMC
Hendrickx, A. P. A. et al. BlaOXA-48-like genome architecture among carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in the Netherlands. Microb. Genom.7, 000512 (2021). PubMed PMC
Beyrouthy R, et al. IS1R-mediated plasticity of IncL/M plasmids leads to the insertion of bla OXA-48 into the Escherichia coli Chromosome. Antimicrob. Agents Chemother. 2014;58:3785–3790. doi: 10.1128/AAC.02669-14. PubMed DOI PMC
Hawkey, J. et al. Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. Microb. Genom.5, e000269 (2019). PubMed PMC
Levings RS, Lightfoot D, Partridge SR, Hall RM, Djordjevic SP. The genomic island SGI1, containing the multiple antibiotic resistance region of Salmonella enterica serovar Typhimurium DT104 or variants of it, is widely distributed in other S. enterica serovars. J. Bacteriol. 2005;187:4401–4409. doi: 10.1128/JB.187.13.4401-4409.2005. PubMed DOI PMC
Nair, S. et al. ESBL-producing strains isolated from imported cases of enteric fever in England and Wales reveal multiple chromosomal integrations of blaCTX-M-15 in XDR Salmonella Typhi. J. Antimicrob. Chemother. 76, 1459–1466 (2021). PubMed
Shawa, M. et al. Novel chromosomal insertions of ISEcp1-blaCTX-M-15 and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli. Antimicrob. Resist. Infect. Control.10, 79 (2021). PubMed PMC
Goswami, C. et al. Origin, maintenance and spread of antibiotic resistance genes within plasmids and chromosomes of bloodstream isolates of Escherichia coli. Microb. Genom.6, e000353 (2020). PubMed PMC
Teklu, D. S. et al. Extended-spectrum beta-lactamase production and multi-drug resistance among Enterobacteriaceae isolated in Addis Ababa, Ethiopia. Antimicrob. Resist. Infect. Control.8, 39 (2019). PubMed PMC
Bitew A, Tsige E. High prevalence of multidrug-resistant and extended-spectrum -lactamase-producing enterobacteriaceae: a cross-sectional study at arsho advanced medical laboratory, addis ababa, ethiopia. J. Trop. Med. 2020;2020:6167234. doi: 10.1155/2020/6167234. PubMed DOI PMC
Abdeta A, et al. Phenotypic characterization of carbapenem non-susceptible gram-negative bacilli isolated from clinical specimens. PLoS One. 2021;16:e0256556. doi: 10.1371/journal.pone.0256556. PubMed DOI PMC
Carattoli A. Plasmids in Gram negatives: molecular typing of resistance plasmids. Int. J. Med. Microbiol. 2011;301:654–658. doi: 10.1016/j.ijmm.2011.09.003. PubMed DOI
Kariuki S, et al. High relatedness of invasive multi-drug resistant non-typhoidal Salmonella genotypes among patients and asymptomatic carriers in endemic informal settlements in Kenya. PLOS Negl. Trop. Dis. 2020;14:e0008440. doi: 10.1371/journal.pntd.0008440. PubMed DOI PMC
Gelalcha, S. D. Sesame trade arrangements, costs and risks in Ethiopia: A baseline survey. (Netherlands’ Ministry of Foreign Affairs Government and Wageningen UR, 2009).
Hendriksen RS, et al. Emergence of multidrug-resistant salmonella concord infections in Europe and the United States in children adopted from Ethiopia, 2003-2007. Pediatr. Infect. Dis. J. 2009;28:814–818. doi: 10.1097/INF.0b013e3181a3aeac. PubMed DOI
Chin C-S, et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods. 2013;10:563–569. doi: 10.1038/nmeth.2474. PubMed DOI
Hunt M, et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol. 2015;16:294. doi: 10.1186/s13059-015-0849-0. PubMed DOI PMC
Chattaway MA, et al. The Transformation of Reference Microbiology Methods and Surveillance for With the Use of Whole Genome Sequencing in England and Wales. Front Public Health. 2019;7:317. doi: 10.3389/fpubh.2019.00317. PubMed DOI PMC
Perez-Sepulveda BM, et al. An accessible, efficient and global approach for the large-scale sequencing of bacterial genomes. Genome Biol. 2021;22:349. doi: 10.1186/s13059-021-02536-3. PubMed DOI PMC
Jones, G. et al. Outbreak of Salmonella enterica serotype Poona in infants linked to persistent Salmonella contamination in an infant formula manufacturing facility, France, August 2018 to February 2019. Euro Surveill. 24, 1900161 (2019). PubMed PMC
No, D. & Pnl38, V. Laboratory standard operating procedure for whole genome sequencing on miseq. https://www.cdc.gov/pulsenet/pdf/PNL38-WGS-on-MiSeq-508.pdf.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32:3047–3048. doi: 10.1093/bioinformatics/btw354. PubMed DOI PMC
Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–3100. doi: 10.1093/bioinformatics/bty191. PubMed DOI PMC
Li H, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC
Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:257. doi: 10.1186/s13059-019-1891-0. PubMed DOI PMC
Bankevich A, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC
Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–1075. doi: 10.1093/bioinformatics/btt086. PubMed DOI PMC
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–2069. doi: 10.1093/bioinformatics/btu153. PubMed DOI
Zhang, S. et al. SeqSero2: Rapid and improved Salmonella serotype determination using whole-genome sequencing data. Appl. Environ. Microbiol. 85, e01746-19 (2019). PubMed PMC
Carattoli, A. et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903 (2014). PubMed PMC
Feldgarden, M. et al. Validating the AMRFinder tool and resistance gene database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob. Agents Chemother. 63, e00483-19 (2019). PubMed PMC
Zhou Z, et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res. 2018;28:1395–1404. doi: 10.1101/gr.232397.117. PubMed DOI PMC
Croucher NJ, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43:e15. doi: 10.1093/nar/gku1196. PubMed DOI PMC
Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35:4453–4455. doi: 10.1093/bioinformatics/btz305. PubMed DOI PMC
Page AJ, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:3691–3693. doi: 10.1093/bioinformatics/btv421. PubMed DOI PMC
Löytynoja A. Phylogeny-aware alignment with PRANK. Methods Mol. Biol. 2014;1079:155–170. doi: 10.1007/978-1-62703-646-7_10. PubMed DOI
Yu G, Smith DK, Zhu H, Guan Y, Lam TT. ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 2017;8:28–36. doi: 10.1111/2041-210X.12628. DOI
Gu Z, Eils R, Schlesner M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 2016;32:2847–2849. doi: 10.1093/bioinformatics/btw313. PubMed DOI
Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic Acids Res. 2019;47:5539–5549. doi: 10.1093/nar/gkz361. PubMed DOI PMC
Leger, A. & Leonardi, T. pycoQC, interactive quality control for Oxford Nanopore Sequencing. Journal of Open Source Software4, 1236 (2019) https://github.com/a-slide/pycoQC.
Koren S, et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome res. 2017;27:722–736. doi: 10.1101/gr.215087.116. PubMed DOI PMC
Ruan J, Li H. Fast and accurate long-read assembly with wtdbg2. Nat. Methods. 2020;17:155–158. doi: 10.1038/s41592-019-0669-3. PubMed DOI PMC
Vaser R, Šikić M. Time- and memory-efficient genome assembly with Raven. Nat. Comput Sci. 2021;1:332–336. doi: 10.1038/s43588-021-00073-4. PubMed DOI
Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 2019;37:540–546. doi: 10.1038/s41587-019-0072-8. PubMed DOI
Wick RR, et al. Trycycler: consensus long-read assemblies for bacterial genomes. Genome Biol. 2021;22:266. doi: 10.1186/s13059-021-02483-z. PubMed DOI PMC
Walker BJ, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9:e112963. doi: 10.1371/journal.pone.0112963. PubMed DOI PMC
Pedersen BS, Quinlan AR. Mosdepth: quick coverage calculation for genomes and exomes. Bioinformatics. 2018;34:867–868. doi: 10.1093/bioinformatics/btx699. PubMed DOI PMC
Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394–1403. doi: 10.1101/gr.2289704. PubMed DOI PMC
Guy, L., Roat Kultima, J. & Andersson, S. G. E. genoPlotR: comparative gene and genome visualization in R. Bioinformatics26, 2334–2335 (2010). PubMed PMC
Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing supplement M100. 31st ed. Wayne: Clinical and Laboratory Standards Institute, (2021). PubMed PMC
European Food Safety Authority (EFSA) et al. Manual for reporting 2021 antimicrobial resistance data within the framework of Directive 2003/99/EC and Decision 2020/1729/EU. EFSA support. publ. 18, 10.2903/sp.efsa.2021.EN-6652 (2021).