Skip to main content
Top
Published in: Antimicrobial Resistance & Infection Control 1/2019

Open Access 01-12-2019 | Antibiotic | Research

Genomic analysis of multidrug-resistant clinical Enterococcus faecalis isolates for antimicrobial resistance genes and virulence factors from the western region of Saudi Arabia

Authors: Muhammad Farman, Muhammad Yasir, Rashad R. Al-Hindi, Suha A. Farraj, Asif A. Jiman-Fatani, Maha Alawi, Esam I. Azhar

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2019

Login to get access

Abstract

Background

Enterococcus faecalis is a ubiquitous member of the gut microbiota and has emerged as a life- threatening multidrug-resistant (MDR) nosocomial pathogen. The aim of this study was to survey the prevalence of multidrug-resistant and epidemiologically important strains of E. faecalis in the western region of Saudi Arabia using phenotypic and whole genome sequencing approaches.

Methods

In total, 155 patients positive for E. faecalis infection were included in this study. The isolates were identified by MALDI-TOF, and screen for antimicrobial resistance using VITEK-2 system. Genome sequencing was performed with paired-end strategy using MiSeq platform.

Results

Seventeen sequence types (STs) were identified through multilocus sequence typing (MLST) analysis of the E. faecalis genomes, including two novels STs (ST862 and ST863). The most common STs in the Saudi patients were ST179 and ST16 from clonal complex 16 (CC16). Around 96% (n = 149) isolates were MDR. The antibiotics quinupristin/dalfopristin, clindamycin, and erythromycin demonstrated almost no coverage, and high-level streptomycin, gentamycin, and ciprofloxacin demonstrated suboptimal coverage. Low resistance was observed against vancomycin, linezolid, and ampicillin. Moreover, 34 antimicrobial resistance genes and variants, and three families of insertion sequences were found in the E. faecalis genomes, which likely contributed to the observed antimicrobial resistance. Twenty-two virulence factors, which were mainly associated with biofilm formation, endocarditis, cell adherence, and colonization, were detected in the isolates.

Conclusions

Diverse STs of E. faecalis, including strains associated with common nosocomial infections are circulating in the healthcare facility of Saudi Arabia and carried multi-drug resistance, which has important implications for infection control.
Appendix
Available only for authorised users
Literature
1.
go back to reference Upadhyaya PG, Ravikumar K, Umapathy B. Review of virulence factors of enterococcus: an emerging nosocomial pathogen. Indian J Med Microbiol. 2009;27(4):301.CrossRef Upadhyaya PG, Ravikumar K, Umapathy B. Review of virulence factors of enterococcus: an emerging nosocomial pathogen. Indian J Med Microbiol. 2009;27(4):301.CrossRef
2.
go back to reference Gordon S, Swenson JM, Hill B, Pigott N, Facklam R, Cooksey R, Thornsberry C, Jarvis W, Tenover F. Antimicrobial susceptibility patterns of common and unusual species of enterococci causing infections in the United States. Enterococcal study group. J Clin Microbiol. 1992;30(9):2373–8.PubMedPubMedCentral Gordon S, Swenson JM, Hill B, Pigott N, Facklam R, Cooksey R, Thornsberry C, Jarvis W, Tenover F. Antimicrobial susceptibility patterns of common and unusual species of enterococci causing infections in the United States. Enterococcal study group. J Clin Microbiol. 1992;30(9):2373–8.PubMedPubMedCentral
3.
go back to reference Moellering RC Jr. Emergence of Enterococcus as a significant pathogen. Clin Infect Dis. 1992:1173–6. Moellering RC Jr. Emergence of Enterococcus as a significant pathogen. Clin Infect Dis. 1992:1173–6.
5.
go back to reference Arias CA, Contreras GA, Murray BE. Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect. 2010;16(6):555–62.CrossRef Arias CA, Contreras GA, Murray BE. Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect. 2010;16(6):555–62.CrossRef
6.
go back to reference Werner G, Coque T, Hammerum A, Hope R, Hryniewicz W, Johnson A, Klare I, Kristinsson K, Leclercq R, Lester C: Emergence and spread of vancomycin resistance among enterococci in Europe. 2008. Werner G, Coque T, Hammerum A, Hope R, Hryniewicz W, Johnson A, Klare I, Kristinsson K, Leclercq R, Lester C: Emergence and spread of vancomycin resistance among enterococci in Europe. 2008.
7.
go back to reference Ruoff KL, De La Maza L, Murtagh MJ, Spargo JD, Ferraro MJ. Species identities of enterococci isolated from clinical specimens. J Clin Microbiol. 1990;28(3):435–7.PubMedPubMedCentral Ruoff KL, De La Maza L, Murtagh MJ, Spargo JD, Ferraro MJ. Species identities of enterococci isolated from clinical specimens. J Clin Microbiol. 1990;28(3):435–7.PubMedPubMedCentral
8.
go back to reference Homan WL, Tribe D, Poznanski S, Li M, Hogg G, Spalburg E, van Embden JD, Willems RJ. Multilocus sequence typing scheme for Enterococcus faecium. J Clin Microbiol. 2002;40(6):1963–71.CrossRef Homan WL, Tribe D, Poznanski S, Li M, Hogg G, Spalburg E, van Embden JD, Willems RJ. Multilocus sequence typing scheme for Enterococcus faecium. J Clin Microbiol. 2002;40(6):1963–71.CrossRef
9.
go back to reference Ruiz-Garbajosa P, Bonten MJ, Robinson DA, Top J, Nallapareddy SR, Torres C, Coque TM, Cantón R, Baquero F, Murray BE. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J Clin Microbiol. 2006;44(6):2220–8.CrossRef Ruiz-Garbajosa P, Bonten MJ, Robinson DA, Top J, Nallapareddy SR, Torres C, Coque TM, Cantón R, Baquero F, Murray BE. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J Clin Microbiol. 2006;44(6):2220–8.CrossRef
10.
go back to reference Rice HE, Brown RL, Gollin G, Caty MG, Gilbert J, Skinner MA, Glick PL, Azizkhan RG. Results of a pilot trial comparing prolonged intravenous antibiotics with sequential intravenous/oral antibiotics for children with perforated appendicitis. Arch Surg. 2001;136(12):1391–5.CrossRef Rice HE, Brown RL, Gollin G, Caty MG, Gilbert J, Skinner MA, Glick PL, Azizkhan RG. Results of a pilot trial comparing prolonged intravenous antibiotics with sequential intravenous/oral antibiotics for children with perforated appendicitis. Arch Surg. 2001;136(12):1391–5.CrossRef
11.
go back to reference Courvalin P. Vancomycin resistance in gram-positive cocci. Clin Infect Dis. 2006;42(Supplement_1):S25–34.CrossRef Courvalin P. Vancomycin resistance in gram-positive cocci. Clin Infect Dis. 2006;42(Supplement_1):S25–34.CrossRef
12.
go back to reference Woodford N. Epidemiology of the genetic elements responsible for acquired glycopeptide resistance in enterococci. Microb Drug Resist. 2001;7(3):229–36.CrossRef Woodford N. Epidemiology of the genetic elements responsible for acquired glycopeptide resistance in enterococci. Microb Drug Resist. 2001;7(3):229–36.CrossRef
13.
go back to reference Chang S, Sievert DM, Hageman JC, Boulton ML, Tenover FC, Downes FP, Shah S, Rudrik JT, Pupp GR, Brown WJ. Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med. 2003;348(14):1342–7.CrossRef Chang S, Sievert DM, Hageman JC, Boulton ML, Tenover FC, Downes FP, Shah S, Rudrik JT, Pupp GR, Brown WJ. Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med. 2003;348(14):1342–7.CrossRef
14.
go back to reference Salem-Bekhit MM, Moussa IM, Muharram MM, Alanazy FK, Hefni HM. Prevalence and antimicrobial resistance pattern of multidrug-resistant enterococci isolated from clinical specimens. Indian J Med Microbiol. 2012;30(1):44–51.CrossRef Salem-Bekhit MM, Moussa IM, Muharram MM, Alanazy FK, Hefni HM. Prevalence and antimicrobial resistance pattern of multidrug-resistant enterococci isolated from clinical specimens. Indian J Med Microbiol. 2012;30(1):44–51.CrossRef
15.
go back to reference Wattal C, Oberoi J, Goel N, Raveendran R, Khanna S. Matrix-assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF MS) for rapid identification of micro-organisms in the routine clinical microbiology laboratory. Eur J Clin Microbiol Infect Dis. 2017;36(5):807–12.CrossRef Wattal C, Oberoi J, Goel N, Raveendran R, Khanna S. Matrix-assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF MS) for rapid identification of micro-organisms in the routine clinical microbiology laboratory. Eur J Clin Microbiol Infect Dis. 2017;36(5):807–12.CrossRef
16.
go back to reference CLSI. Performance standards for antimicrobial susceptibility testing; 26 ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2016. CLSI. Performance standards for antimicrobial susceptibility testing; 26 ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2016.
17.
go back to reference Magiorakos AP, Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, Harbarth S, Hindler J, Kahlmeter G, Olsson-Liljequist B. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.CrossRef Magiorakos AP, Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, Harbarth S, Hindler J, Kahlmeter G, Olsson-Liljequist B. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.CrossRef
18.
go back to reference Miele A, Bandera M, Goldstein BP. Use of primers selective for vancomycin resistance genes to determine van genotype in enterococci and to study gene organization in VanA isolates. Antimicrob Agents Chemother. 1995;39(8):1772–8.CrossRef Miele A, Bandera M, Goldstein BP. Use of primers selective for vancomycin resistance genes to determine van genotype in enterococci and to study gene organization in VanA isolates. Antimicrob Agents Chemother. 1995;39(8):1772–8.CrossRef
19.
go back to reference Nallapareddy SR, Duh R-W, Singh KV, Murray BE. Molecular typing of selected Enterococcus faecalis isolates: pilot study using multilocus sequence typing and pulsed-field gel electrophoresis. J Clin Microbiol. 2002;40(3):868–76.CrossRef Nallapareddy SR, Duh R-W, Singh KV, Murray BE. Molecular typing of selected Enterococcus faecalis isolates: pilot study using multilocus sequence typing and pulsed-field gel electrophoresis. J Clin Microbiol. 2002;40(3):868–76.CrossRef
20.
go back to reference Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS One. 2014;9(8):e104984.CrossRef Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS One. 2014;9(8):e104984.CrossRef
21.
go back to reference Letunic I, Bork P. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2006;23(1):127–8.CrossRef Letunic I, Bork P. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2006;23(1):127–8.CrossRef
22.
go back to reference Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC bioinformatics. 2009;10(1):421.CrossRef Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC bioinformatics. 2009;10(1):421.CrossRef
23.
go back to reference Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain J-M. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother. 2014;58(1):212–20.CrossRef Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain J-M. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother. 2014;58(1):212–20.CrossRef
24.
go back to reference Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, Lago BA, Dave BM, Pereira S, Sharma AN. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2016:gkw1004. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, Lago BA, Dave BM, Pereira S, Sharma AN. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2016:gkw1004.
25.
go back to reference Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, Aarestrup FM. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014;52(5):1501–10.CrossRef Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, Aarestrup FM. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014;52(5):1501–10.CrossRef
26.
go back to reference Carattoli A, Zankari E, García-Fernández A, Larsen MV, Lund O, Villa L, Aarestrup FM, Hasman H. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895–903.CrossRef Carattoli A, Zankari E, García-Fernández A, Larsen MV, Lund O, Villa L, Aarestrup FM, Hasman H. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895–903.CrossRef
27.
go back to reference Siguier P, Pérochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006;34(suppl_1):D32–6.CrossRef Siguier P, Pérochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006;34(suppl_1):D32–6.CrossRef
28.
go back to reference Kristich CJ, Rice LB, Arias CA: Enterococcal infection—treatment and antibiotic resistance. 2014. Kristich CJ, Rice LB, Arias CA: Enterococcal infection—treatment and antibiotic resistance. 2014.
29.
go back to reference El-Kersh TA, Marie MA, Al-Sheikh YA, Al-Agamy MH, Al-Bloushy AA. Prevalence and risk factors of early fecal carriage of Enterococcus faecalis and Staphylococcus spp and their antimicrobial resistant patterns among healthy neonates born in a hospital setting in Central Saudi Arabia. Saudi Med J. 2016;37(3):280.CrossRef El-Kersh TA, Marie MA, Al-Sheikh YA, Al-Agamy MH, Al-Bloushy AA. Prevalence and risk factors of early fecal carriage of Enterococcus faecalis and Staphylococcus spp and their antimicrobial resistant patterns among healthy neonates born in a hospital setting in Central Saudi Arabia. Saudi Med J. 2016;37(3):280.CrossRef
30.
go back to reference Salem-Bekhit MM, Moussa IMI, Elsherbini MMAM, AlRejaie S. Increasing prevalence of high-level gentamicin resistant enterococci: an emerging clinical problem. Afr J Microbiol Res. 2011;5(31):5713–20. Salem-Bekhit MM, Moussa IMI, Elsherbini MMAM, AlRejaie S. Increasing prevalence of high-level gentamicin resistant enterococci: an emerging clinical problem. Afr J Microbiol Res. 2011;5(31):5713–20.
31.
go back to reference Fernández-Hidalgo N, Almirante B, Gavaldà J, Gurgui M, Peña C, de Alarcón A, Ruiz J, Vilacosta I, Montejo M, Vallejo N. Ampicillin plus ceftriaxone is as effective as ampicillin plus gentamicin for treating Enterococcus faecalis infective endocarditis. Clin Infect Dis. 2013;56(9):1261–8.CrossRef Fernández-Hidalgo N, Almirante B, Gavaldà J, Gurgui M, Peña C, de Alarcón A, Ruiz J, Vilacosta I, Montejo M, Vallejo N. Ampicillin plus ceftriaxone is as effective as ampicillin plus gentamicin for treating Enterococcus faecalis infective endocarditis. Clin Infect Dis. 2013;56(9):1261–8.CrossRef
32.
go back to reference Richey E, Waters P, Jovic M, Rakhman C. Treatment of ampicillin-resistant enterococcus faecium urinary tract infections. Fed Pract. 2015;32:20–3.PubMedPubMedCentral Richey E, Waters P, Jovic M, Rakhman C. Treatment of ampicillin-resistant enterococcus faecium urinary tract infections. Fed Pract. 2015;32:20–3.PubMedPubMedCentral
33.
go back to reference Zeyaullah M, Kaul V. Prevalence of urinary tract infection and antibiotic resistance pattern in Saudi Arabia population. Glob J Biol, Agric Health Sci. 2015;4(1):206–14. Zeyaullah M, Kaul V. Prevalence of urinary tract infection and antibiotic resistance pattern in Saudi Arabia population. Glob J Biol, Agric Health Sci. 2015;4(1):206–14.
34.
go back to reference Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, Kallen A, Limbago B, Fridkin S. Antimicrobial-resistant pathogens associated with healthcare-associated infections summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010. Infect Control Hosp Epidemiol. 2013;34(1):1–14.CrossRef Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, Kallen A, Limbago B, Fridkin S. Antimicrobial-resistant pathogens associated with healthcare-associated infections summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010. Infect Control Hosp Epidemiol. 2013;34(1):1–14.CrossRef
35.
go back to reference Padmasini E, Padmaraj R, Ramesh SS. High level aminoglycoside resistance and distribution of aminoglycoside resistant genes among clinical isolates of Enterococcus species in Chennai, India. Sci World J. 2014;2014. Padmasini E, Padmaraj R, Ramesh SS. High level aminoglycoside resistance and distribution of aminoglycoside resistant genes among clinical isolates of Enterococcus species in Chennai, India. Sci World J. 2014;2014.
36.
go back to reference Singh KV, Weinstock GM, Murray BE. An Enterococcus faecalis ABC homologue (Lsa) is required for the resistance of this species to clindamycin and quinupristin-dalfopristin. Antimicrob Agents Chemother. 2002;46(6):1845–50.CrossRef Singh KV, Weinstock GM, Murray BE. An Enterococcus faecalis ABC homologue (Lsa) is required for the resistance of this species to clindamycin and quinupristin-dalfopristin. Antimicrob Agents Chemother. 2002;46(6):1845–50.CrossRef
37.
go back to reference Portillo A, Ruiz-Larrea F, Zarazaga M, Alonso A, Martinez JL, Torres C. Macrolide Resistance Genes inEnterococcus spp. Antimicrob Agents Chemother. 2000;44(4):967–71.CrossRef Portillo A, Ruiz-Larrea F, Zarazaga M, Alonso A, Martinez JL, Torres C. Macrolide Resistance Genes inEnterococcus spp. Antimicrob Agents Chemother. 2000;44(4):967–71.CrossRef
38.
go back to reference Jia W, Li G, Wang W. Prevalence and antimicrobial resistance of Enterococcus species: a hospital-based study in China. Int J Environ Res Public Health. 2014;11(3):3424–42.CrossRef Jia W, Li G, Wang W. Prevalence and antimicrobial resistance of Enterococcus species: a hospital-based study in China. Int J Environ Res Public Health. 2014;11(3):3424–42.CrossRef
39.
go back to reference Lee E-W, Huda MN, Kuroda T, Mizushima T, Tsuchiya T. EfrAB, an ABC multidrug efflux pump in Enterococcus faecalis. Antimicrob Agents Chemother. 2003;47(12):3733–8.CrossRef Lee E-W, Huda MN, Kuroda T, Mizushima T, Tsuchiya T. EfrAB, an ABC multidrug efflux pump in Enterococcus faecalis. Antimicrob Agents Chemother. 2003;47(12):3733–8.CrossRef
40.
go back to reference Sanchez Valenzuela A, Lavilla Lerma L, Benomar N, Gálvez A, Perez Pulido R, Abriouel H. Phenotypic and molecular antibiotic resistance profile of Enterococcus faecalis and Enterococcus faecium isolated from different traditional fermented foods. Foodborne Pathog Dis. 2013;10(2):143–9.CrossRef Sanchez Valenzuela A, Lavilla Lerma L, Benomar N, Gálvez A, Perez Pulido R, Abriouel H. Phenotypic and molecular antibiotic resistance profile of Enterococcus faecalis and Enterococcus faecium isolated from different traditional fermented foods. Foodborne Pathog Dis. 2013;10(2):143–9.CrossRef
41.
go back to reference Toledo-Arana A, Valle J, Solano C, MaJ A, Cucarella C, Lamata M, Amorena B, Leiva J, Penadés JR, Lasa I. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl Environ Microbiol. 2001;67(10):4538–45.CrossRef Toledo-Arana A, Valle J, Solano C, MaJ A, Cucarella C, Lamata M, Amorena B, Leiva J, Penadés JR, Lasa I. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl Environ Microbiol. 2001;67(10):4538–45.CrossRef
42.
go back to reference Guiton PS, Hung CS, Kline KA, Roth R, Kau AL, Hayes E, Heuser J, Dodson KW, Caparon MG, Hultgren SJ. Contribution of autolysin and sortase a during Enterococcus faecalis DNA-dependent biofilm development. Infect Immun. 2009;77(9):3626–38.CrossRef Guiton PS, Hung CS, Kline KA, Roth R, Kau AL, Hayes E, Heuser J, Dodson KW, Caparon MG, Hultgren SJ. Contribution of autolysin and sortase a during Enterococcus faecalis DNA-dependent biofilm development. Infect Immun. 2009;77(9):3626–38.CrossRef
43.
go back to reference Garg S, Mohan B, Taneja N. Biofilm formation capability of enterococcal strains causing urinary tract infection Vis-a-Vis colonisation and correlation with enterococcal surface protein gene. Indian J Med Microbiol. 2017;35(1):48.CrossRef Garg S, Mohan B, Taneja N. Biofilm formation capability of enterococcal strains causing urinary tract infection Vis-a-Vis colonisation and correlation with enterococcal surface protein gene. Indian J Med Microbiol. 2017;35(1):48.CrossRef
44.
go back to reference Seno Y, Kariyama R, Mitsuhata R, Monden K, Kumon H. Clinical implications of biofilm formation by Enterococcus faecalis in the urinary tract. Acta Med Okayama. 2005;59(3):79–87.PubMed Seno Y, Kariyama R, Mitsuhata R, Monden K, Kumon H. Clinical implications of biofilm formation by Enterococcus faecalis in the urinary tract. Acta Med Okayama. 2005;59(3):79–87.PubMed
45.
go back to reference Dunny G. Genetic functions and cell–cell interactions in the pheromone-inducible plasmid transfer system of Enterococcus faecalis. Mol Microbiol. 1990;4(5):689–96.CrossRef Dunny G. Genetic functions and cell–cell interactions in the pheromone-inducible plasmid transfer system of Enterococcus faecalis. Mol Microbiol. 1990;4(5):689–96.CrossRef
46.
go back to reference Ben HY, Chairat S, Hamdi N, Gharsa H, Ben RS, Ceballos S, Torres C, Ben KS. Antimicrobial resistance and genetic lineages of faecal enterococci of wild birds: emergence of vanA and vanB2 harbouring Enterococcus faecalis. Int J Antimicrob Agents. 2018. Ben HY, Chairat S, Hamdi N, Gharsa H, Ben RS, Ceballos S, Torres C, Ben KS. Antimicrobial resistance and genetic lineages of faecal enterococci of wild birds: emergence of vanA and vanB2 harbouring Enterococcus faecalis. Int J Antimicrob Agents. 2018.
47.
go back to reference Freitas AR, Novais C, Ruiz-Garbajosa P, Coque TM, Peixe L. Clonal expansion within clonal complex 2 and spread of vancomycin-resistant plasmids among different genetic lineages of Enterococcus faecalis from Portugal. J Antimicrob Chemother. 2009;63(6):1104–11.CrossRef Freitas AR, Novais C, Ruiz-Garbajosa P, Coque TM, Peixe L. Clonal expansion within clonal complex 2 and spread of vancomycin-resistant plasmids among different genetic lineages of Enterococcus faecalis from Portugal. J Antimicrob Chemother. 2009;63(6):1104–11.CrossRef
48.
go back to reference Oravcova V, Zurek L, Townsend A, Clark AB, Ellis JC, Cizek A, Literak I. A merican crows as carriers of vancomycin-resistant enterococci with vanA gene. Environ Microbiol. 2014;16(4):939–49.CrossRef Oravcova V, Zurek L, Townsend A, Clark AB, Ellis JC, Cizek A, Literak I. A merican crows as carriers of vancomycin-resistant enterococci with vanA gene. Environ Microbiol. 2014;16(4):939–49.CrossRef
49.
go back to reference Tedim AP, Ruiz-Garbajosa P, Corander J, Rodríguez CM, Cantón R, Willems RJ, Baquero F, Coque TM. Population biology of intestinal Enterococcus isolates from hospitalized and nonhospitalized individuals in different age groups. Appl Environ Microbiol. 2015;81(5):1820–31.CrossRef Tedim AP, Ruiz-Garbajosa P, Corander J, Rodríguez CM, Cantón R, Willems RJ, Baquero F, Coque TM. Population biology of intestinal Enterococcus isolates from hospitalized and nonhospitalized individuals in different age groups. Appl Environ Microbiol. 2015;81(5):1820–31.CrossRef
50.
go back to reference Quinones D, Kobayashi N, Nagashima S. Molecular epidemiologic analysis of Enterococcus faecalis isolates in Cuba by multilocus sequence typing. Microb Drug Resist. 2009;15(4):287–93.CrossRef Quinones D, Kobayashi N, Nagashima S. Molecular epidemiologic analysis of Enterococcus faecalis isolates in Cuba by multilocus sequence typing. Microb Drug Resist. 2009;15(4):287–93.CrossRef
51.
go back to reference Cai J, Wang Y, Schwarz S, Lv H, Li Y, Liao K, Yu S, Zhao K, Gu D, Wang X. Enterococcal isolates carrying the novel oxazolidinone resistance gene optrA from hospitals in Zhejiang, Guangdong, and Henan, China, 2010–2014. Clin Microbiol Infect. 2015;21(12):1095. e1091–4.CrossRef Cai J, Wang Y, Schwarz S, Lv H, Li Y, Liao K, Yu S, Zhao K, Gu D, Wang X. Enterococcal isolates carrying the novel oxazolidinone resistance gene optrA from hospitals in Zhejiang, Guangdong, and Henan, China, 2010–2014. Clin Microbiol Infect. 2015;21(12):1095. e1091–4.CrossRef
52.
go back to reference Zischka M, Künne CT, Blom J, Wobser D, Sakιnç T, Schmidt-Hohagen K, Dabrowski PW, Nitsche A, Hübner J, Hain T. Comprehensive molecular, genomic and phenotypic analysis of a major clone of Enterococcus faecalis MLST ST40. BMC Genomics. 2015;16(1):175.CrossRef Zischka M, Künne CT, Blom J, Wobser D, Sakιnç T, Schmidt-Hohagen K, Dabrowski PW, Nitsche A, Hübner J, Hain T. Comprehensive molecular, genomic and phenotypic analysis of a major clone of Enterococcus faecalis MLST ST40. BMC Genomics. 2015;16(1):175.CrossRef
Metadata
Title
Genomic analysis of multidrug-resistant clinical Enterococcus faecalis isolates for antimicrobial resistance genes and virulence factors from the western region of Saudi Arabia
Authors
Muhammad Farman
Muhammad Yasir
Rashad R. Al-Hindi
Suha A. Farraj
Asif A. Jiman-Fatani
Maha Alawi
Esam I. Azhar
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2019
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-019-0508-4

Other articles of this Issue 1/2019

Antimicrobial Resistance & Infection Control 1/2019 Go to the issue