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Published in: European Journal of Clinical Microbiology & Infectious Diseases 11/2017

Open Access 01-11-2017 | Review

Bacterial genome sequencing in clinical microbiology: a pathogen-oriented review

Authors: F. Tagini, G. Greub

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 11/2017

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Abstract

In recent years, whole-genome sequencing (WGS) has been perceived as a technology with the potential to revolutionise clinical microbiology. Herein, we reviewed the literature on the use of WGS for the most commonly encountered pathogens in clinical microbiology laboratories: Escherichia coli and other Enterobacteriaceae, Staphylococcus aureus and coagulase-negative staphylococci, streptococci and enterococci, mycobacteria and Chlamydia trachomatis. For each pathogen group, we focused on five different aspects: the genome characteristics, the most common genomic approaches and the clinical uses of WGS for (i) typing and outbreak analysis, (ii) virulence investigation and (iii) in silico antimicrobial susceptibility testing. Of all the clinical usages, the most frequent and straightforward usage was to type bacteria and to trace outbreaks back. A next step toward standardisation was made thanks to the development of several new genome-wide multi-locus sequence typing systems based on WGS data. Although virulence characterisation could help in various particular clinical settings, it was done mainly to describe outbreak strains. An increasing number of studies compared genotypic to phenotypic antibiotic susceptibility testing, with mostly promising results. However, routine implementation will preferentially be done in the workflow of particular pathogens, such as mycobacteria, rather than as a broadly applicable generic tool. Overall, concrete uses of WGS in routine clinical microbiology or infection control laboratories were done, but the next big challenges will be the standardisation and validation of the procedures and bioinformatics pipelines in order to reach clinical standards.
Literature
4.
go back to reference Fleischmann RD, Adams MD, White O et al (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512PubMedCrossRef Fleischmann RD, Adams MD, White O et al (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512PubMedCrossRef
6.
15.
go back to reference Blagden T, Schneider W, Melcher U et al (2016) Adaptation and validation of E-probe diagnostic nucleic acid analysis for detection of Escherichia coli O157:H7 in metagenomic data from complex food matrices. J Food Prot 79:574–581. doi:10.4315/0362-028X.JFP-15-440 PubMedCrossRef Blagden T, Schneider W, Melcher U et al (2016) Adaptation and validation of E-probe diagnostic nucleic acid analysis for detection of Escherichia coli O157:H7 in metagenomic data from complex food matrices. J Food Prot 79:574–581. doi:10.​4315/​0362-028X.​JFP-15-440 PubMedCrossRef
17.
go back to reference Loman NJ, Constantinidou C, Christner M et al (2013) A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of Shiga-toxigenic Escherichia coli O104:H4. JAMA 309:1502–1510. doi:10.1001/jama.2013.3231 PubMedCrossRef Loman NJ, Constantinidou C, Christner M et al (2013) A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of Shiga-toxigenic Escherichia coli O104:H4. JAMA 309:1502–1510. doi:10.​1001/​jama.​2013.​3231 PubMedCrossRef
19.
go back to reference Ingle DJ, Valcanis M, Kuzevski A et al (2016) In silico serotyping of E. coli from short read data identifies limited novel O-loci but extensive diversity of O:H serotype combinations within and between pathogenic lineages. Microb Genom 2:e000064. doi:10.1099/mgen.0.000064 PubMedPubMedCentral Ingle DJ, Valcanis M, Kuzevski A et al (2016) In silico serotyping of E. coli from short read data identifies limited novel O-loci but extensive diversity of O:H serotype combinations within and between pathogenic lineages. Microb Genom 2:e000064. doi:10.​1099/​mgen.​0.​000064 PubMedPubMedCentral
27.
go back to reference Byrne L, Fisher I, Peters T et al (2014) A multi-country outbreak of Salmonella Newport gastroenteritis in Europe associated with watermelon from Brazil, confirmed by whole genome sequencing: October 2011 to January 2012. Euro Surveill 19:6–13PubMedPubMedCentralCrossRef Byrne L, Fisher I, Peters T et al (2014) A multi-country outbreak of Salmonella Newport gastroenteritis in Europe associated with watermelon from Brazil, confirmed by whole genome sequencing: October 2011 to January 2012. Euro Surveill 19:6–13PubMedPubMedCentralCrossRef
28.
29.
go back to reference Inns T, Lane C, Peters T et al (2015) A multi-country Salmonella enteritidis phage type 14b outbreak associated with eggs from a German producer: ‘near real-time’ application of whole genome sequencing and food chain investigations, United Kingdom, May to September 2014. Euro Surveill 20(16). pii: 21098 Inns T, Lane C, Peters T et al (2015) A multi-country Salmonella enteritidis phage type 14b outbreak associated with eggs from a German producer: ‘near real-time’ application of whole genome sequencing and food chain investigations, United Kingdom, May to September 2014. Euro Surveill 20(16). pii: 21098
30.
33.
go back to reference Kanamori H, Parobek CM, Juliano JJ et al (2017) A prolonged outbreak of KPC-3-producing Enterobacter cloacae and Klebsiella pneumoniae driven by multiple mechanisms of resistance transmission at a large academic burn center. Antimicrob Agents Chemother 61(2). pii: e01516-16. doi:10.1128/AAC.01516-16 Kanamori H, Parobek CM, Juliano JJ et al (2017) A prolonged outbreak of KPC-3-producing Enterobacter cloacae and Klebsiella pneumoniae driven by multiple mechanisms of resistance transmission at a large academic burn center. Antimicrob Agents Chemother 61(2). pii: e01516-16. doi:10.​1128/​AAC.​01516-16
34.
go back to reference Zhou K, Lokate M, Deurenberg RH et al (2016) Use of whole-genome sequencing to trace, control and characterize the regional expansion of extended-spectrum β-lactamase producing ST15 Klebsiella pneumoniae. Sci Rep 6:20840. doi:10.1038/srep20840 Zhou K, Lokate M, Deurenberg RH et al (2016) Use of whole-genome sequencing to trace, control and characterize the regional expansion of extended-spectrum β-lactamase producing ST15 Klebsiella pneumoniae. Sci Rep 6:20840. doi:10.​1038/​srep20840
41.
go back to reference Pettengill EA, Pettengill JB, Binet R (2016) Phylogenetic analyses of Shigella and enteroinvasive Escherichia coli for the identification of molecular epidemiological markers: whole-genome comparative analysis does not support distinct genera designation. Front Microbiol 6:1573. doi:10.3389/fmicb.2015.01573 PubMedPubMedCentralCrossRef Pettengill EA, Pettengill JB, Binet R (2016) Phylogenetic analyses of Shigella and enteroinvasive Escherichia coli for the identification of molecular epidemiological markers: whole-genome comparative analysis does not support distinct genera designation. Front Microbiol 6:1573. doi:10.​3389/​fmicb.​2015.​01573 PubMedPubMedCentralCrossRef
49.
go back to reference Zankari E, Hasman H, Kaas RS et al (2013) Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemother 68:771–777. doi:10.1093/jac/dks496 PubMedCrossRef Zankari E, Hasman H, Kaas RS et al (2013) Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemother 68:771–777. doi:10.​1093/​jac/​dks496 PubMedCrossRef
61.
62.
go back to reference International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53:4961–4967. doi:10.1128/AAC.00579-09 CrossRef International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53:4961–4967. doi:10.​1128/​AAC.​00579-09 CrossRef
65.
go back to reference Azarian T, Cook RL, Johnson JA et al (2015) Whole-genome sequencing for outbreak investigations of methicillin-resistant Staphylococcus aureus in the neonatal intensive care unit: time for routine practice? Infect Control Hosp Epidemiol 36:777–785. doi:10.1017/ice.2015.73 PubMedPubMedCentralCrossRef Azarian T, Cook RL, Johnson JA et al (2015) Whole-genome sequencing for outbreak investigations of methicillin-resistant Staphylococcus aureus in the neonatal intensive care unit: time for routine practice? Infect Control Hosp Epidemiol 36:777–785. doi:10.​1017/​ice.​2015.​73 PubMedPubMedCentralCrossRef
66.
go back to reference Layer F, Sanchini A, Strommenger B et al (2015) Molecular typing of toxic shock syndrome toxin-1- and enterotoxin A-producing methicillin-sensitive Staphylococcus aureus isolates from an outbreak in a neonatal intensive care unit. Int J Med Microbiol 305:790–798. doi:10.1016/j.ijmm.2015.08.033 PubMedCrossRef Layer F, Sanchini A, Strommenger B et al (2015) Molecular typing of toxic shock syndrome toxin-1- and enterotoxin A-producing methicillin-sensitive Staphylococcus aureus isolates from an outbreak in a neonatal intensive care unit. Int J Med Microbiol 305:790–798. doi:10.​1016/​j.​ijmm.​2015.​08.​033 PubMedCrossRef
67.
go back to reference Jaton L, Pillonel T, Jaton K et al (2016) Common skin infection due to Panton–Valentine leucocidin-producing Staphylococcus aureus strains in asylum seekers from Eritrea: a genome-based investigation of a suspected outbreak. Clin Microbiol Infect 22:739.e5–739.e8. doi:10.1016/j.cmi.2016.05.026 CrossRef Jaton L, Pillonel T, Jaton K et al (2016) Common skin infection due to Panton–Valentine leucocidin-producing Staphylococcus aureus strains in asylum seekers from Eritrea: a genome-based investigation of a suspected outbreak. Clin Microbiol Infect 22:739.e5–739.e8. doi:10.​1016/​j.​cmi.​2016.​05.​026 CrossRef
68.
69.
go back to reference Roisin S, Gaudin C, De Mendonça R et al (2016) Pan-genome multilocus sequence typing and outbreak-specific reference-based single nucleotide polymorphism analysis to resolve two concurrent Staphylococcus aureus outbreaks in neonatal services. Clin Microbiol Infect 22:520–526. doi:10.1016/j.cmi.2016.01.024 PubMedCrossRef Roisin S, Gaudin C, De Mendonça R et al (2016) Pan-genome multilocus sequence typing and outbreak-specific reference-based single nucleotide polymorphism analysis to resolve two concurrent Staphylococcus aureus outbreaks in neonatal services. Clin Microbiol Infect 22:520–526. doi:10.​1016/​j.​cmi.​2016.​01.​024 PubMedCrossRef
78.
go back to reference Lee GC, Long SW, Musser JM et al (2015) Comparative whole genome sequencing of community-associated methicillin-resistant Staphylococcus aureus sequence type 8 from primary care clinics in a Texas community. Pharmacotherapy 35:220–228. doi:10.1002/phar.1536 PubMedCrossRef Lee GC, Long SW, Musser JM et al (2015) Comparative whole genome sequencing of community-associated methicillin-resistant Staphylococcus aureus sequence type 8 from primary care clinics in a Texas community. Pharmacotherapy 35:220–228. doi:10.​1002/​phar.​1536 PubMedCrossRef
80.
86.
go back to reference Sanderson-Smith M, De Oliveira DM, Guglielmini J et al (2014) A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J Infect Dis 210:1325–1338. doi:10.1093/infdis/jiu260 PubMedCrossRef Sanderson-Smith M, De Oliveira DM, Guglielmini J et al (2014) A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J Infect Dis 210:1325–1338. doi:10.​1093/​infdis/​jiu260 PubMedCrossRef
91.
go back to reference Tagini F, Aubert B, Troillet N et al (2017) Importance of whole genome sequencing for the assessment of outbreaks in diagnostic laboratories: analysis of a case series of invasive Streptococcus pyogenes infections. Eur J Clin Microbiol Infect Dis. doi:10.1007/s10096-017-2905-z Tagini F, Aubert B, Troillet N et al (2017) Importance of whole genome sequencing for the assessment of outbreaks in diagnostic laboratories: analysis of a case series of invasive Streptococcus pyogenes infections. Eur J Clin Microbiol Infect Dis. doi:10.​1007/​s10096-017-2905-z
93.
go back to reference Harrison OB, Brueggemann AB, Caugant DA et al (2011) Molecular typing methods for outbreak detection and surveillance of invasive disease caused by Neisseria meningitidis, Haemophilus influenzae and Streptococcus pneumoniae, a review. Microbiology 157:2181–2195. doi:10.1099/mic.0.050518-0 PubMedPubMedCentralCrossRef Harrison OB, Brueggemann AB, Caugant DA et al (2011) Molecular typing methods for outbreak detection and surveillance of invasive disease caused by Neisseria meningitidis, Haemophilus influenzae and Streptococcus pneumoniae, a review. Microbiology 157:2181–2195. doi:10.​1099/​mic.​0.​050518-0 PubMedPubMedCentralCrossRef
94.
go back to reference Kapatai G, Sheppard CL, Al-Shahib A et al (2016) Whole genome sequencing of Streptococcus pneumoniae: development, evaluation and verification of targets for serogroup and serotype prediction using an automated pipeline. PeerJ 4:e2477. doi:10.7717/peerj.2477 PubMedPubMedCentralCrossRef Kapatai G, Sheppard CL, Al-Shahib A et al (2016) Whole genome sequencing of Streptococcus pneumoniae: development, evaluation and verification of targets for serogroup and serotype prediction using an automated pipeline. PeerJ 4:e2477. doi:10.​7717/​peerj.​2477 PubMedPubMedCentralCrossRef
100.
101.
go back to reference Santona A, Taviani E, Deligios M et al (2016) Vancomycin-resistant Enterococcus faecium high-resolution typing by core genome multilocus sequence typing. J Infect Dev Ctries 10:1159–1161. doi:10.3855/jidc.9223 PubMedCrossRef Santona A, Taviani E, Deligios M et al (2016) Vancomycin-resistant Enterococcus faecium high-resolution typing by core genome multilocus sequence typing. J Infect Dev Ctries 10:1159–1161. doi:10.​3855/​jidc.​9223 PubMedCrossRef
104.
go back to reference Reglinski M, Sriskandan S (2014) The contribution of group A streptococcal virulence determinants to the pathogenesis of sepsis. Virulence 5:127–136. doi:10.4161/viru.26400 Reglinski M, Sriskandan S (2014) The contribution of group A streptococcal virulence determinants to the pathogenesis of sepsis. Virulence 5:127–136. doi:10.​4161/​viru.​26400
106.
go back to reference Cattoir V (2016) Mechanisms of antibiotic resistance: Streptococcus pyogenes. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: basic biology to clinical manifestations. University of Oklahoma Health Sciences Center, Oklahoma City, pp 947–991 Cattoir V (2016) Mechanisms of antibiotic resistance: Streptococcus pyogenes. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: basic biology to clinical manifestations. University of Oklahoma Health Sciences Center, Oklahoma City, pp 947–991
116.
go back to reference Snyder LA, Loman NJ, Faraj LA et al (2013) Epidemiological investigation of Pseudomonas aeruginosa isolates from a six-year-long hospital outbreak using high-throughput whole genome sequencing. Euro Surveill 18:20611PubMedCrossRef Snyder LA, Loman NJ, Faraj LA et al (2013) Epidemiological investigation of Pseudomonas aeruginosa isolates from a six-year-long hospital outbreak using high-throughput whole genome sequencing. Euro Surveill 18:20611PubMedCrossRef
117.
go back to reference Witney AA, Gould KA, Pope CF et al (2014) Genome sequencing and characterization of an extensively drug-resistant sequence type 111 serotype O12 hospital outbreak strain of Pseudomonas aeruginosa. Clin Microbiol Infect 20:O609–O618. doi:10.1111/1469-0691.12528 PubMedCrossRef Witney AA, Gould KA, Pope CF et al (2014) Genome sequencing and characterization of an extensively drug-resistant sequence type 111 serotype O12 hospital outbreak strain of Pseudomonas aeruginosa. Clin Microbiol Infect 20:O609–O618. doi:10.​1111/​1469-0691.​12528 PubMedCrossRef
118.
go back to reference Turton JF, Wright L, Underwood A et al (2015) High-resolution analysis by whole-genome sequencing of an international lineage (sequence type 111) of Pseudomonas aeruginosa associated with metallo-carbapenemases in the United Kingdom. J Clin Microbiol 53:2622–2631. doi:10.1128/JCM.00505-15 PubMedPubMedCentralCrossRef Turton JF, Wright L, Underwood A et al (2015) High-resolution analysis by whole-genome sequencing of an international lineage (sequence type 111) of Pseudomonas aeruginosa associated with metallo-carbapenemases in the United Kingdom. J Clin Microbiol 53:2622–2631. doi:10.​1128/​JCM.​00505-15 PubMedPubMedCentralCrossRef
119.
125.
go back to reference Hammerum AM, Hansen F, Skov MN et al (2015) Investigation of a possible outbreak of carbapenem-resistant Acinetobacter baumannii in Odense, Denmark using PFGE, MLST and whole-genome-based SNPs. J Antimicrob Chemother 70:1965–1968. doi:10.1093/jac/dkv072 PubMed Hammerum AM, Hansen F, Skov MN et al (2015) Investigation of a possible outbreak of carbapenem-resistant Acinetobacter baumannii in Odense, Denmark using PFGE, MLST and whole-genome-based SNPs. J Antimicrob Chemother 70:1965–1968. doi:10.​1093/​jac/​dkv072 PubMed
127.
go back to reference Davis RJ, Jensen SO, Van Hal S et al (2015) Whole genome sequencing in real-time investigation and management of a Pseudomonas aeruginosa outbreak on a neonatal intensive care unit. Infect Control Hosp Epidemiol 36:1058–1064. doi:10.1017/ice.2015.133 PubMedCrossRef Davis RJ, Jensen SO, Van Hal S et al (2015) Whole genome sequencing in real-time investigation and management of a Pseudomonas aeruginosa outbreak on a neonatal intensive care unit. Infect Control Hosp Epidemiol 36:1058–1064. doi:10.​1017/​ice.​2015.​133 PubMedCrossRef
138.
140.
go back to reference Jamieson FB, Teatero S, Guthrie JL et al (2014) Whole-genome sequencing of the Mycobacterium tuberculosis Manila sublineage results in less clustering and better resolution than mycobacterial interspersed repetitive-unit–variable-number tandem-repeat (MIRU-VNTR) typing and spoligotyping. J Clin Microbiol 52:3795–3798. doi:10.1128/JCM.01726-14 PubMedPubMedCentralCrossRef Jamieson FB, Teatero S, Guthrie JL et al (2014) Whole-genome sequencing of the Mycobacterium tuberculosis Manila sublineage results in less clustering and better resolution than mycobacterial interspersed repetitive-unit–variable-number tandem-repeat (MIRU-VNTR) typing and spoligotyping. J Clin Microbiol 52:3795–3798. doi:10.​1128/​JCM.​01726-14 PubMedPubMedCentralCrossRef
141.
144.
go back to reference Otal I, Martín C, Vincent-Lévy-Frebault V et al (1991) Restriction fragment length polymorphism analysis using IS6110 as an epidemiological marker in tuberculosis. J Clin Microbiol 29:1252–1254PubMedPubMedCentral Otal I, Martín C, Vincent-Lévy-Frebault V et al (1991) Restriction fragment length polymorphism analysis using IS6110 as an epidemiological marker in tuberculosis. J Clin Microbiol 29:1252–1254PubMedPubMedCentral
145.
go back to reference Kamerbeek J, Schouls L, Kolk A et al (1997) Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35:907–914PubMedPubMedCentral Kamerbeek J, Schouls L, Kolk A et al (1997) Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35:907–914PubMedPubMedCentral
150.
go back to reference Stucki D, Ballif M, Bodmer T et al (2015) Tracking a tuberculosis outbreak over 21 years: strain-specific single-nucleotide polymorphism typing combined with targeted whole-genome sequencing. J Infect Dis 211:1306–1316. doi:10.1093/infdis/jiu601 PubMedCrossRef Stucki D, Ballif M, Bodmer T et al (2015) Tracking a tuberculosis outbreak over 21 years: strain-specific single-nucleotide polymorphism typing combined with targeted whole-genome sequencing. J Infect Dis 211:1306–1316. doi:10.​1093/​infdis/​jiu601 PubMedCrossRef
152.
154.
155.
go back to reference Ribeiro SCM, Gomes LL, Amaral EP et al (2014) Mycobacterium tuberculosis strains of the modern sublineage of the Beijing family are more likely to display increased virulence than strains of the ancient sublineage. J Clin Microbiol 52:2615–2624. doi:10.1128/JCM.00498-14 PubMedPubMedCentralCrossRef Ribeiro SCM, Gomes LL, Amaral EP et al (2014) Mycobacterium tuberculosis strains of the modern sublineage of the Beijing family are more likely to display increased virulence than strains of the ancient sublineage. J Clin Microbiol 52:2615–2624. doi:10.​1128/​JCM.​00498-14 PubMedPubMedCentralCrossRef
159.
go back to reference Iwai H, Kato-Miyazawa M, Kirikae T et al (2015) CASTB (the comprehensive analysis server for the Mycobacterium tuberculosis complex): a publicly accessible web server for epidemiological analyses, drug-resistance prediction and phylogenetic comparison of clinical isolates. Tuberculosis (Edinb) 95:843–844. doi:10.1016/j.tube.2015.09.002 CrossRef Iwai H, Kato-Miyazawa M, Kirikae T et al (2015) CASTB (the comprehensive analysis server for the Mycobacterium tuberculosis complex): a publicly accessible web server for epidemiological analyses, drug-resistance prediction and phylogenetic comparison of clinical isolates. Tuberculosis (Edinb) 95:843–844. doi:10.​1016/​j.​tube.​2015.​09.​002 CrossRef
160.
go back to reference Zhang H, Li D, Zhao L et al (2013) Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat Genet 45:1255–1260. doi:10.1038/ng.2735 PubMedCrossRef Zhang H, Li D, Zhao L et al (2013) Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat Genet 45:1255–1260. doi:10.​1038/​ng.​2735 PubMedCrossRef
166.
go back to reference Loman NJ, Pallen MJ (2015) Twenty years of bacterial genome sequencing. Nat Rev Microbiol 13:787–794PubMedCrossRef Loman NJ, Pallen MJ (2015) Twenty years of bacterial genome sequencing. Nat Rev Microbiol 13:787–794PubMedCrossRef
171.
go back to reference Andersson P, Klein M, Lilliebridge RA et al (2013) Sequences of multiple bacterial genomes and a Chlamydia trachomatis genotype from direct sequencing of DNA derived from a vaginal swab diagnostic specimen. Clin Microbiol Infect 19:E405–E408. doi:10.1111/1469-0691.12237 PubMedCrossRef Andersson P, Klein M, Lilliebridge RA et al (2013) Sequences of multiple bacterial genomes and a Chlamydia trachomatis genotype from direct sequencing of DNA derived from a vaginal swab diagnostic specimen. Clin Microbiol Infect 19:E405–E408. doi:10.​1111/​1469-0691.​12237 PubMedCrossRef
178.
Metadata
Title
Bacterial genome sequencing in clinical microbiology: a pathogen-oriented review
Authors
F. Tagini
G. Greub
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 11/2017
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-017-3024-6

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