Please wait a minute...
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2011, Vol. 6 Issue (5) : 357-366    https://doi.org/10.1007/s11515-011-1167-x
REVIEW
Enterococcus: review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology
John VU, John CARVALHO()
Biology Department, California State University Dominguez Hills (CSUDH), Carson, CA 90747, USA
 Download: PDF(186 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
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.

Keywords enterococci      Staphylococcus      antibiotic resistance      bacteriology      microbiology     
Corresponding Author(s): CARVALHO John,Email:jcarvalho@csudh.edu   
Issue Date: 01 October 2011
 Cite this article:   
John VU,John CARVALHO. Enterococcus: review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology[J]. Front Biol, 2011, 6(5): 357-366.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-011-1167-x
https://academic.hep.com.cn/fib/EN/Y2011/V6/I5/357
Virulence factorBiological effects
Surface adhesins Aggregation substanceHair-like protein embedded in cytoplasmic membrane; facilitates binding to host cells; enables cell-to-cell contact between donor and recipient strains for conjugation
Enterococcal surface protein (Esp)Discovered in E. faecalis for adherence in urinary bladder; associated with biofilm production in E. faecium (nosocomial infections related to medical devices)
Secreted factors CytolysinHemolytic protein associated with bacteremic strains; bacteriocin that inhibits growth of Gram-positive bacteria (facilitates colonization); can lyse macrophages and neutrophils (gain additional nutrients and escape immune clearance)
GelatinaseHydrolyzes gelatin, collagen, casein, hemoglobin; associated with enhanced virulence for endocarditis
Extracellular superoxidePurpose unknown but may have role in lysis of red blood cells
Antibiotic resistance Multiple plasmid and chromosome genesTransferred via conjugation, transposons or bacteriophages; resistant to aminoglycosides, β-lactams, vancomycin
Tab.1  Enterococcal virulence factors
DiseaseClinical summary
Urinary tract infectionsDysuria and pyuria; frequently nosocomial and derived from patients using urinary catheters
BacteremiaCaused by organism entering blood stream from sources such as UTI or intraabdominal abscess; can increase likelihood of endocarditis
EndocarditisInfection of heart endothelium or valves; can lead to significant morbidity and mortality; occurs from sources of infection involving genitourinary and gastrointestinal tracts, wounds, bacteremia
MeningitisRare; primarily diagnosed in neonates
Wound infectionsLargely attributed to surgery, decubitus ulcers, and burns
PeritonitisIntraabdominal or pelvic infections; abdominal swelling; polymicrobial; patients typically acutely ill
Tab.2  Clinical diseases caused by enterococci
1 Archibald L K, Reller L B (2001). Clinical microbiology in developing countries. Emerg Infect Dis , 7(2): 302–305
doi: 10.3201/eid0702.010232 pmid:11294729
2 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
doi: 10.1016/S0923-2508(01)01291-8 pmid:11900266
3 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
pmid:11249027
4 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
pmid:2275539
5 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
pmid:9472288
6 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
doi: 10.1086/318717 pmid:11181122
7 Cetinkaya Y, Falk P, Mayhall C G (2000). Vancomycin-resistant enterococci. Clin Microbiol Rev , 13(4): 686–707
doi: 10.1128/CMR.13.4.686-707.2000 pmid:11023964
8 Chan E D, Iseman M D (2008). Multidrug-resistant and extensively drug-resistant tuberculosis: a review. Curr Opin Infect Dis , 21(6): 587–595
doi: 10.1097/QCO.0b013e328319bce6 pmid:18978526
9 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
pmid:8285611
10 Clewell D B (1990). Movable genetic elements and antibiotic resistance in enterococci. Eur J Clin Microbiol Infect Dis , 9(2): 90–102
doi: 10.1007/BF01963632 pmid:2156704
11 Clewell D B (1993). Bacterial sex pheromone-induced plasmid transfer. Cell , 73(1): 9–12
doi: 10.1016/0092-8674(93)90153-H pmid:8462105
12 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
doi: 10.1016/j.plasmid.2007.05.001 pmid:17590438
13 Cohen M L (1997). Epidemiological factors influencing the emergence of antimicrobial resistance. Ciba Found Symp , 207: 223–231, discussion 231-237
pmid:9189644
14 Courvalin P (2006). Vancomycin resistance in gram-positive cocci. Clin Infect Dis , 42(Suppl 1): S25–S34
doi: 10.1086/491711 pmid:16323116
15 Daly J A, Clifton N L, Seskin K C, Gooch W M 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
pmid:1704385
16 Devriese L, Baele M, Butaye P (2006). The genus Enterococcus. The Procaryotes . New York: Springer, 163–174
17 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
pmid:8300442
18 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
doi: 10.1016/S0168-1605(03)00178-8 pmid:14596988
19 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
doi: 10.1111/j.1365-2958.1990.tb00639.x pmid:2117692
20 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
pmid:7699051
21 Elzinga G, Raviglione M C, Maher D (2004). Scale up: meeting targets in global tuberculosis control. Lancet , 363(9411): 814–819
doi: 10.1016/S0140-6736(04)15698-5 pmid:15016493
22 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
pmid:8269394
23 Facklam R (2002). What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin Microbiol Rev , 15(4): 613–630
doi: 10.1128/CMR.15.4.613-630.2002 pmid:12364372
24 Farber J M (1996). An introduction to the how’s and why’s of molecular biotyping. J Food Prot , 59: 1091–1101
25 Fisher K, Phillips C (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiology , 155(Pt 6): 1749–1757
doi: 10.1099/mic.0.026385-0 pmid:19383684
26 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
27 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
doi: 10.1016/j.ijfoodmicro.2005.06.026 pmid:16216368
28 Gilmore M S, Segarra R A, Booth M C (1990). An HlyB-type function is required for expression of the Enterococcus faecalis hemolysin/bacteriocin. Infect Immun , 58(12): 3914–3923
pmid:2123826
29 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
doi: 10.1007/s004300050091 pmid:10363674
30 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
doi: 10.1016/j.ijmm.2008.10.001 pmid:19042153
31 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
doi: 10.1128/JB.01205-07 pmid:17827282
32 Herman D J, Gerding D N (1991). Antimicrobial resistance among enterococci. Antimicrob Agents Chemother , 35(1): 1–4
pmid:1901693
33 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
pmid:9331768
34 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
doi: 10.1093/infdis/173.3.743 pmid:8627044
35 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
doi: 10.3201/eid0402.980211 pmid:9621194
36 Jett B D, Huycke M M, Gilmore M S (1994). Virulence of enterococci. Clin Microbiol Rev , 7(4): 462–478
pmid:7834601
37 Kayaoglu G, ?rstavik D (2004). Virulence factors of Enterococcus faecalis: relationship to endodontic disease. Crit Rev Oral Biol Med , 15(5): 308–320
doi: 10.1177/154411130401500506 pmid:15470268
38 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
pmid:10523541
39 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
doi: 10.1080/00365540701203501 pmid:17654341
40 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
pmid:1729187
41 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
42 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
doi: 10.1111/j.1472-765X.2011.03043.x pmid:21395627
43 Megran D W (1992). Enterococcal endocarditis. Clin Infect Dis , 15(1): 63–71
doi: 10.1093/clinids/15.1.63 pmid:1617074
44 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
pmid:8350769
45 Moellering R C Jr (1992). Emergence of Enterococcus as a significant pathogen. Clin Infect Dis , 14(6): 1173–1176
doi: 10.1093/clinids/14.6.1173 pmid:1623072
46 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
doi: 10.1034/j.1600-0463.2000.d01-7.x pmid:10698087
47 Morrison D, Woodford N, Cookson B (1997). Enterococci as emerging pathogens of humans. Soc Appl Bacteriol Symp Ser , 26: 89S–99S
pmid:9436321
48 Murray B E (1990). The life and times of the Enterococcus. Clin Microbiol Rev , 3(1): 46–65
pmid:2404568
49 Murray P R, Rosenthal K S, Pfaller M A (2009). Enterococcus and other Gram-positive cocci. Medical Microbiology (6th Ed) , 243–246
50 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
doi: 10.1111/j.1574-6968.1992.tb05089.x pmid:1505742
51 Palmer K L, Kos V N, Gilmore M S (2010). Horizontal gene transfer and the genomics of enterococcal antibiotic resistance. Curr Opin Microbiol , 13(5): 632–639
doi: 10.1016/j.mib.2010.08.004 pmid:20837397
52 Panesso D, Reyes J, Rincón S, Díaz L, Galloway-Pe?a 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
doi: 10.1128/JCM.02526-09 pmid:20220167
53 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
doi: 10.1016/j.trstmh.2007.04.014 pmid:17544047
54 Patel R, Piper K E, Rouse M S, Steckelberg J M, Uhl J R, Kohner P, Hopkins M K, 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
pmid:9774606
55 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
doi: 10.1086/377451 pmid:13130397
56 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
doi: 10.1086/320542 pmid:11340524
57 Rice L B (2006). Antimicrobial resistance in Gram-positive bacteria. Am J Med , 119(6 Suppl 1): S11–S19, discussion S62-S70
doi: 10.1016/j.amjmed.2006.03.012 pmid:16735146
58 Sava I G, Heikens E, Huebner J (2010). Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect , 16(6): 533–540
doi: 10.1111/j.1469-0691.2010.03213.x pmid:20569264
59 Scott J R (1992). Sex and the single circle: conjugative transposition. J Bacteriol , 174(19): 6005–6010
pmid:1328149
60 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
pmid:1900808
61 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
pmid:9864215
62 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
doi: 10.3855/jidc.467 pmid:19762967
63 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
doi: 10.1086/502196 pmid:12725353
64 Stephenson K, Hoch J A (2002). Virulence- and antibiotic resistance-associated two-component signal transduction systems of Gram-positive pathogenic bacteria as targets for antimicrobial therapy. Pharmacol Ther , 93(2-3): 293–305
doi: 10.1016/S0163-7258(02)00198-5 pmid:12191621
65 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
doi: 10.1097/00002030-199703110-00015 pmid:9147429
66 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
pmid:1846126
67 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
68 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
doi: 10.1128/AAC.01442-06 pmid:17371826
69 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
70 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
doi: 10.1128/AEM.67.10.4538-4545.2001 pmid:11571153
71 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
pmid:8576343
72 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
doi: 10.1086/650384 pmid:20225951
73 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
doi: 10.1086/341977 pmid:12173131
74 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
doi: 10.4103/0377-4929.77333 pmid:21393885
75 Wang X, Huycke M M (2007). Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology , 132(2): 551–561
doi: 10.1053/j.gastro.2006.11.040 pmid:17258726
76 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
doi: 10.1097/00002030-199703110-00016 pmid:9147430
77 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
doi: 10.1016/0923-2508(91)90098-U pmid:1712504
78 Woodford N, Johnson A P, Morrison D, Speller D C (1995). Current perspectives on glycopeptide resistance. Clin Microbiol Rev , 8(4): 585–615
pmid:8665471
79 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
doi: 10.1021/es062822n pmid:17695890
[1] Kapil Dev SHARMA,Rajendra Prasad SAINI,Loganathan KARTHIK. Current trends of antibiotic resistance in clinical isolates of Staphylococcus aureus[J]. Front. Biol., 2014, 9(4): 287-290.
[2] Jeremy GROSS, Ian J. PASSMORE, Jade C. S. CHUNG, Olena RZHEPISHEVSKA, Madeleine RAMSTEDT, Martin WELCH. Universal soldier: Pseudomonas aeruginosa – an opportunistic generalist[J]. Front Biol, 2013, 8(4): 387-394.
[3] Maria L. G. Quiloan, John Vu, John Carvalho. Enterococcus faecalis can be distinguished from Enterococcus faecium via differential susceptibility to antibiotics and growth and fermentation characteristics on mannitol salt agar[J]. Front Biol, 2012, 7(2): 167-177.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed