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Enterococcus: review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology

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Frontiers in Biology

Abstract

The genus Enterococcus is composed of 38 species, the most important of which are Enterococcus faecalis and Enterococcus faecium—both human intestinal colonizers. Hospitals within the United States and around the world commonly isolate these bacteria because they are a cause of bacteremia, urinary tract infections (UTIs), endocarditis, wound infections, meningitis, intraabdominal and pelvic infections, and nosocomial and iatrogenic infections. Given the ubiquity of enterococci within the human population, it is important for laboratories to be able to distinguish these agents within hospitalized patients from other bacterial genera and also differentiate different species within the Enterococcus genus as well as different strains within each species. Unfortunately, the enterococci are emerging as serious pathogens in both the developed world, where surveillance needs to be improved and speciation procedures are inadequate or cumbersome, and in developing nations, which lack the trained hospital personnel or funding to sufficiently identify enterococci to the genus or species level. This review explores the Enterococcus genus and highlights some of the concerns for national and international clinical microbiology laboratories.

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References

  • Archibald L K, Reller L B (2001). Clinical microbiology in developing countries. Emerg Infect Dis, 7(2): 302–305

    Article  PubMed  CAS  Google Scholar 

  • Archimbaud C, Shankar N, Forestier C, Baghdayan A, Gilmore M S, Charbonné F, Joly B (2002). In vitro adhesive properties and virulence factors of Enterococcus faecalis strains. Res Microbiol, 153(2): 75–80

    Article  PubMed  CAS  Google Scholar 

  • Behr T, Koob C, Schedl M, Mehlen A, Meier H, Knopp D, Frahm E, Obst U, Schleifer K, Niessner R, Ludwig W (2000). A nested array of rRNA targeted probes for the detection and identification of enterococci by reverse hybridization. Syst Appl Microbiol, 23(4): 563–572

    PubMed  CAS  Google Scholar 

  • Betzl D, Ludwig W, Schleifer K H (1990). Identification of lactococci and enterococci by colony hybridization with 23S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol, 56(9): 2927–2929

    PubMed  CAS  Google Scholar 

  • Budavari S M, Saunders G L, Liebowitz L D, Khoosal M, Crewe-Brown H H (1997). Emergence of vancomycin-resistant enterococci in South Africa. S Afr Med J, 87(11): 1557

    PubMed  CAS  Google Scholar 

  • Caballero-Granado F J, Becerril B, Cuberos L, Bernabeu M, Cisneros J M, Pachón J (2001). Attributable mortality rate and duration of hospital stay associated with enterococcal bacteremia. Clin Infect Dis, 32(4): 587–594

    Article  PubMed  CAS  Google Scholar 

  • Cetinkaya Y, Falk P, Mayhall C G (2000). Vancomycin-resistant enterococci. Clin Microbiol Rev, 13(4): 686–707

    Article  PubMed  CAS  Google Scholar 

  • Chan E D, Iseman M D (2008). Multidrug-resistant and extensively drug-resistant tuberculosis: a review. Curr Opin Infect Dis, 21(6): 587–595

    Article  PubMed  CAS  Google Scholar 

  • Clark N C, Cooksey R C, Hill B C, Swenson J M, Tenover F C (1993). Characterization of glycopeptide-resistant enterococci from U.S. hospitals. Antimicrob Agents Chemother, 37(11): 2311–2317

    PubMed  CAS  Google Scholar 

  • Clewell D B (1990). Movable genetic elements and antibiotic resistance in enterococci. Eur J Clin Microbiol Infect Dis, 9(2): 90–102

    Article  PubMed  CAS  Google Scholar 

  • Clewell D B (1993). Bacterial sex pheromone-induced plasmid transfer. Cell, 73(1): 9–12

    Article  PubMed  CAS  Google Scholar 

  • Clewell D B (2007). Properties of Enterococcus faecalis plasmid pAD1, a member of a widely disseminated family of pheromone-responding, conjugative, virulence elements encoding cytolysin. Plasmid, 58(3): 205–227

    Article  PubMed  CAS  Google Scholar 

  • Cohen M L (1997). Epidemiological factors influencing the emergence of antimicrobial resistance. Ciba Found Symp, 207: 223–231, discussion 231–237

    PubMed  CAS  Google Scholar 

  • Courvalin P (2006). Vancomycin resistance in gram-positive cocci. Clin Infect Dis, 42(Suppl 1): S25–S34

    Article  PubMed  CAS  Google Scholar 

  • Daly J A, Clifton N L, Seskin K C, Gooch WM 3rd (1991). Use of rapid, nonradioactive DNA probes in culture confirmation tests to detect Streptococcus agalactiae, Haemophilus influenzae, and Enterococcus spp. from pediatric patients with significant infections. J Clin Microbiol, 29(1): 80–82

    PubMed  CAS  Google Scholar 

  • Devriese L, Baele M, Butaye P (2006). The genus Enterococcus. The Procaryotes. New York: Springer, 163–174

    Chapter  Google Scholar 

  • Devriese L A, Pot B, Collins M D (1993). Phenotypic identification of the genus Enterococcus and differentiation of phylogenetically distinct enterococcal species and species groups. J Appl Bacteriol, 75(5): 399–408

    Article  PubMed  CAS  Google Scholar 

  • Domig K J, Mayer H K, Kneifel W (2003). Methods used for the isolation, enumeration, characterisation and identification of Enterococcus spp. 2. Pheno- and genotypic criteria. Int J Food Microbiol, 88(2–3): 165–188

    Article  PubMed  Google Scholar 

  • Dunny G M (1990). Genetic functions and cell-cell interactions in the pheromone-inducible plasmid transfer system of Enterococcus faecalis. Mol Microbiol, 4(5): 689–696

    Article  PubMed  CAS  Google Scholar 

  • Dutka-Malen S, Evers S, Courvalin P (1995). Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol, 33(1): 24–27

    PubMed  CAS  Google Scholar 

  • Elzinga G, Raviglione M C, Maher D (2004). Scale up: meeting targets in global tuberculosis control. Lancet, 363(9411): 814–819

    Article  PubMed  Google Scholar 

  • Emori T G, Gaynes R P (1993). An overview of nosocomial infections, including the role of the microbiology laboratory. Clin Microbiol Rev, 6(4): 428–442

    PubMed  CAS  Google Scholar 

  • Facklam R (2002). What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin Microbiol Rev, 15(4): 613–630

    Article  PubMed  Google Scholar 

  • Farber J M (1996). An introduction to the how’s and why’s of molecular biotyping. J Food Prot, 59: 1091–1101

    CAS  Google Scholar 

  • Fisher K, Phillips C (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiology, 155(Pt 6): 1749–1757

    Article  PubMed  CAS  Google Scholar 

  • Forbes B A, Sahm D F, Weissfeld A S (2007). Infections of the urinary tract. In: Forbes B A, Sahm D F, Weissfeld A S. Bailey and Scott’s Diagnostic Microbiology. 12th ed. St. Louis: Mosby-Elsevier, 842–854

    Google Scholar 

  • Foulquié Moreno M R, Sarantinopoulos P, Tsakalidou E, De Vuyst L (2006). The role and application of enterococci in food and health. Int J Food Microbiol, 106(1): 1–24

    Article  PubMed  Google Scholar 

  • Gilmore MS, Segarra R A, Booth MC (1990). An HlyB-type function is required for expression of the Enterococcus faecalis hemolysin/bacteriocin. Infect Immun, 58(12): 3914–3923

    PubMed  CAS  Google Scholar 

  • Haas W, Gilmore M S (1999). Molecular nature of a novel bacterial toxin: the cytolysin of Enterococcus faecalis. Med Microbiol Immunol (Berl), 187(4): 183–190

    Article  CAS  Google Scholar 

  • Hallgren A, Claesson C, Saeedi B, Monstein H J, Hanberger H, Nilsson L E (2009). Molecular detection of aggregation substance, enterococcal surface protein, and cytolysin genes and in vitro adhesion to urinary catheters of Enterococcus faecalis and E. faecium of clinical origin. Int J Med Microbiol, 299(5): 323–332

    Article  PubMed  Google Scholar 

  • Heikens E, Bonten M J, Willems R J (2007). Enterococcal surface protein Esp is important for biofilm formation of Enterococcus faecium E1162. J Bacteriol, 189(22): 8233–8240

    Article  PubMed  CAS  Google Scholar 

  • Herman D J, Gerding D N (1991). Antimicrobial resistance among enterococci. Antimicrob Agents Chemother, 35(1): 1–4

    PubMed  CAS  Google Scholar 

  • Huycke M M, Gilmore M S (1997). In vivo survival of Enterococcus faecalis is enhanced by extracellular superoxide production. Adv Exp Med Biol, 418: 781–784

    PubMed  CAS  Google Scholar 

  • Huycke M M, Joyce W, Wack M F (1996). Augmented production of extracellular superoxide by blood isolates of Enterococcus faecalis. J Infect Dis, 173(3): 743–746

    Article  PubMed  CAS  Google Scholar 

  • Huycke M M, Sahm D F, Gilmore M S (1998). Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis, 4(2): 239–249

    Article  PubMed  CAS  Google Scholar 

  • Jett B D, Huycke M M, Gilmore M S (1994). Virulence of enterococci. Clin Microbiol Rev, 7(4): 462–478

    PubMed  CAS  Google Scholar 

  • Kayaoglu G, Ørstavik D (2004). Virulence factors of Enterococcus faecalis: relationship to endodontic disease. Crit Rev Oral Biol Med, 15(5): 308–320

    Article  PubMed  Google Scholar 

  • Ke D, Picard F J, Martineau F, Ménard C, Roy P H, Ouellette M, Bergeron M G (1999). Development of a PCR assay for rapid detection of enterococci. J Clin Microbiol, 37(11): 3497–3503

    PubMed  CAS  Google Scholar 

  • Khudaier B Y, Tewari R, Shafiani S, Sharma M, Emmanuel R, Sharma M, Taneja N (2007). Epidemiology and molecular characterization of vancomycin resistant enterococci isolates in India. Scand J Infect Dis, 39(8): 662–670

    Article  PubMed  CAS  Google Scholar 

  • Kreft B, Marre R, Schramm U, Wirth R (1992). Aggregation substance of Enterococcus faecalis mediates adhesion to cultured renal tubular cells. Infect Immun, 60(1): 25–30

    PubMed  CAS  Google Scholar 

  • Lehman D C, Mahon C R, Swarna K (2007). Streptococcus, enterococcus, and other catalase-negative Gram-positive cocci. Textbook of Diagnostic Microbiology (3rd Ed). St. Louis: Saunders-Elsevier, 382–409

    Google Scholar 

  • Mazaheri Nezhad Fard R, Barton M D, Heuzenroeder M W (2011). Bacteriophage-mediated transduction of antibiotic resistance in enterococci. Lett Appl Microbiol, 52(6): 559–564

    Article  PubMed  CAS  Google Scholar 

  • Megran D W (1992). Enterococcal endocarditis. Clin Infect Dis, 15(1): 63–71

    Article  PubMed  CAS  Google Scholar 

  • Miyazaki S, Ohno A, Kobayashi I, Uji T, Yamaguchi K, Goto S (1993). Cytotoxic effect of hemolytic culture supernatant from Enterococcus faecalis on mouse polymorphonuclear neutrophils and macrophages. Microbiol Immunol, 37(4): 265–270

    PubMed  CAS  Google Scholar 

  • Moellering R C Jr (1992). Emergence of Enterococcus as a significant pathogen. Clin Infect Dis, 14(6): 1173–1176

    Article  PubMed  Google Scholar 

  • Monstein H J, Johansson Y, Jonasson J (2000). Detection of vancomycin resistance genes combined with typing of Enterococci by means of multiplex PCR amplification and multiple primer DNA sequencing. APMIS, 108(1): 67–73

    Article  PubMed  CAS  Google Scholar 

  • Morrison D, Woodford N, Cookson B (1997). Enterococci as emerging pathogens of humans. Soc Appl Bacteriol Symp Ser, 26: 89S–99S

    PubMed  CAS  Google Scholar 

  • Murray B E (1990). The life and times of the Enterococcus. Clin Microbiol Rev, 3(1): 46–65

    PubMed  CAS  Google Scholar 

  • Murray P R, Rosenthal K S, Pfaller M A (2009). Enterococcus and other Gram-positive cocci. Medical Microbiology (6th Ed), 243–246

    Google Scholar 

  • Noble W C, Virani Z, Cree R G (1992). Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureus. FEMS Microbiol Lett, 72(2): 195–198

    Article  PubMed  CAS  Google Scholar 

  • Palmer K L, Kos V N, Gilmore MS (2010). Horizontal gene transfer and the genomics of enterococcal antibiotic resistance. Curr Opin Microbiol, 13(5): 632–639

    Article  PubMed  CAS  Google Scholar 

  • Panesso D, Reyes J, Rincón S, Díaz L, Galloway-Peña J, Zurita J, Carrillo C, Merentes A, Guzmán M, Adachi J A, Murray B E, Arias C A, Arias C A (2010). Molecular epidemiology of vancomycin-resistant Enterococcus faecium: a prospective, multicenter study in South American hospitals. J Clin Microbiol, 48(5): 1562–1569

    Article  PubMed  CAS  Google Scholar 

  • Pang T, Peeling R W (2007). Diagnostic tests for infectious diseases in the developing world: two sides of the coin. Trans R Soc Trop Med Hyg, 101(9): 856–857

    Article  PubMed  Google Scholar 

  • Patel R, Piper K E, Rouse M S, Steckelberg J M, Uhl J R, Kohner P, Hopkins MK, Cockerill F R 3rd, Kline B C (1998). Determination of 16S rRNA sequences of enterococci and application to species identification of nonmotile Enterococcus gallinarum isolates. J Clin Microbiol, 36(11): 3399–3407

    PubMed  CAS  Google Scholar 

  • Ray A J, Pultz N J, Bhalla A, Aron D C, Donskey C J (2003). Coexistence of vancomycin-resistant enterococci and Staphylococcus aureus in the intestinal tracts of hospitalized patients. Clin Infect Dis, 37(7): 875–881

    Article  PubMed  Google Scholar 

  • Reid K C, Cockerill F R III, Patel R (2001). Clinical and epidemiological features of Enterococcus casseliflavus/flavescens and Enterococcus gallinarum bacteremia: a report of 20 cases. Clin Infect Dis, 32(11): 1540–1546

    Article  PubMed  CAS  Google Scholar 

  • Rice L B (2006). Antimicrobial resistance in Gram-positive bacteria. Am J Med, 119(6 Suppl 1): S11–S19, discussion S62–S70

    Article  PubMed  CAS  Google Scholar 

  • Sava I G, Heikens E, Huebner J (2010). Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect, 16(6): 533–540

    Article  PubMed  CAS  Google Scholar 

  • Scott J R (1992). Sex and the single circle: conjugative transposition. J Bacteriol, 174(19): 6005–6010

    PubMed  CAS  Google Scholar 

  • Segarra R A, Booth M C, Morales D A, Huycke M M, Gilmore M S (1991). Molecular characterization of the Enterococcus faecalis cytolysin activator. Infect Immun, 59(4): 1239–1246

    PubMed  CAS  Google Scholar 

  • Shankar V, Baghdayan A S, Huycke M M, Lindahl G, Gilmore M S (1999). Infection-derived Enterococcus faecalis strains are enriched in esp, a gene encoding a novel surface protein. Infect Immun, 67(1): 193–200

    PubMed  CAS  Google Scholar 

  • Singh B R (2009). Prevalence of vancomycin resistance and multiple drug resistance in enterococci in equids in North India. J Infect Dev Ctries, 3(7): 498–503

    Article  PubMed  CAS  Google Scholar 

  • Song X, Srinivasan A, Plaut D, Perl T M (2003). Effect of nosocomial vancomycin-resistant enterococcal bacteremia on mortality, length of stay, and costs. Infect Control Hosp Epidemiol, 24(4): 251–256

    Article  PubMed  Google Scholar 

  • Stephenson K, Hoch J A (2002). Virulence- and antibiotic resistance-associated two-component signal transduction systems of Grampositive pathogenic bacteria as targets for antimicrobial therapy. Pharmacol Ther, 93(2–3): 293–305

    Article  PubMed  CAS  Google Scholar 

  • Stetler H C, Granade T C, Nunez C A, Meza R, Terrell S, Amador L, George J R (1997). Field evaluation of rapid HIV serologic tests for screening and confirming HIV-1 infection in Honduras. AIDS, 11(3): 369–375

    Article  PubMed  CAS  Google Scholar 

  • Su Y A, Sulavik M C, He P, Makinen K K, Makinen P L, Fiedler S, Wirth R, Clewell D B (1991). Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. Liquefaciens. Infect Immun, 59(1): 415–420

    PubMed  CAS  Google Scholar 

  • Sundqvist G, Figdor D, Persson S, Sjorgren U (1998). Microbiologic analysis of teeth with failed endodontic treatment and the outcome of conservative retreatment. Oral Surg Oral Med Oral Pathol, 85: 86–93

    CAS  Google Scholar 

  • Sung J M L, Lindsay J A (2007). Staphylococcus aureus strains that are hypersusceptible to resistance gene transfer from enterococci. Antimicrob Agents Chemother, 51(6): 2189–2191

    Article  PubMed  CAS  Google Scholar 

  • Teixeira L M, Carvalho M G S, Shewmaker P L, Facklam R R (2011). Manual of Clinical Microbiology. Washington, D.C.: ASM Press, 350–364

    Google Scholar 

  • Toledo-Arana A, Valle J, Solano C, Arrizubieta M J, Cucarella C, Lamata M, Amorena B, Leiva J, Penadés J R, Lasa I (2001). The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl Environ Microbiol, 67(10): 4538–4545

    Article  PubMed  CAS  Google Scholar 

  • Tomayko J F, Murray B E (1995). Analysis of Enterococcus faecalis isolates from intercontinental sources by multilocus enzyme electrophoresis and pulsed-field gel electrophoresis. J Clin Microbiol, 33(11): 2903–2907

    PubMed  CAS  Google Scholar 

  • Usdin M, Guillerm M, Calmy A (2010). Patient needs and point-of-care requirements for HIV load testing in resource-limited settings. J Infect Dis, 201(Suppl 1): S73–S77

    Article  PubMed  Google Scholar 

  • Vergis E N, Shankar N, Chow J W, Hayden M K, Snydman D R, Zervos M J, Linden P K, Wagener M M, Muder R R (2002). Association between the presence of enterococcal virulence factors gelatinase, hemolysin, and enterococcal surface protein and mortality among patients with bacteremia due to Enterococcus faecalis. Clin Infect Dis, 35(5): 570–575

    Article  PubMed  CAS  Google Scholar 

  • Vinodkumar C S, Srinivasa H, Basavarajappa K G, Geethalakshmi S, Bandekar N (2011). Isolation of bacteriophages to multi-drug resistant enterococci obtained from diabetic foot: a novel antimicrobial agent waiting in the shelf? Indian J Pathol Microbiol, 54(1): 90–95

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Huycke M M (2007). Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology, 132(2): 551–561

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson D, Wilkinson N, Lombard C, Martin D, Smith A, Floyd K, Ballard R (1997). On-site HIV testing in resource-poor settings: is one rapid test enough? AIDS, 11(3): 377–381

    Article  PubMed  CAS  Google Scholar 

  • Williams A M, Rodrigues U M, Collins M D (1991). Intrageneric relationships of enterococci as determined by reverse transcriptase sequencing of small-subunit rRNA. Res Microbiol, 142(1): 67–74

    Article  PubMed  CAS  Google Scholar 

  • Woodford N, Johnson A P, Morrison D, Speller D C (1995). Current perspectives on glycopeptide resistance. Clin Microbiol Rev, 8(4): 585–615

    PubMed  CAS  Google Scholar 

  • Yamahara K M, Layton B A, Santoro A E, Boehm A B (2007). Beach sands along the California coast are diffuse sources of fecal bacteria to coastal waters. Environ Sci Technol, 41(13): 4515–4521

    Article  PubMed  CAS  Google Scholar 

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Vu, J., Carvalho, J. Enterococcus: review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology. Front. Biol. 6, 357–366 (2011). https://doi.org/10.1007/s11515-011-1167-x

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