Analysis of biofilm production in Enterococcus faecium strains depending on clinical source.
Purpose: Enterococcus faecium strains have been reported worldwide as etiologic factors of many nosocomial infections, which are difficult to manage because of the constantly increasing resistance of these microorganisms to antibiotics and the ability to form biofilm. The aim of this study was to analyze the ability to produce a biofilm in E. faecium strains, depending on the patient's clinical material.
Materials and methods: Sixty-six E. faecium strains were investigated. Identification and susceptibility testing were conducted by the VITEK2 system. The ability to form biofilm was assessed by phenotypic methods. The presence of selected virulence genes was established by PCR followed by gel electrophoresis and sequencing.
Results: Among the tested E. faecium isolates, 72.7% were biofilm-positive (BIO+) and 27.3% biofilm-negative (BIO-). Strains were collected mostly from rectal swabs (30.4%) and blood (18.3%). BIO+ strains from infections constituted 31.8% (52.4% isolated from blood) and from colonization 40.9% (48.2% from rectal swabs). 91.7% of the Blood Group strains and 68.5% of the Other Group strains produced biofilm. Strains from the Colonization Group produced biofilm in a proportion similar to the Infection Group (about 75%). There were no statistically significant differences in virulence and resistance, except for vancomycin (more resistant BIO+ Other than the BIO+ Blood Group, and more resistant BIO+ Colonization than BIO+ Infection Group) and teicoplanin (more resistant BIO+ Colonization than the BIO+ Infection Group).
Conclusion: The majority of E. faecium isolates carries high levels of resistance to many antimicrobials, is well equipped with virulence genes, and possesses the ability to form biofilm.
Key words: Enterococcus faecium, biofilm, antibiotic, resistance, virulence
Enterococcus faecium strains have been reported worldwide as etiologic factors of many nosocomial infections, which are difficult to manage because of the constantly increasing resistance of these microorganisms to antibiotics and their ability to form strong biofilms [1,2]. The largest threat is infections caused by vancomycin-resistant E. faecium (VRE), particularly for critically ill or immunocompromised patients [3,4]. Moreover, VRE strains are often simultaneously resistant to [beta]-lactams and aminoglycosides, and are considered multidrug resistant (MDR) [2,4]. Alarmingly, antimicrobial resistance genes from MDR strains can be transferred by transposons or pheromone-mediated conjugative plasmids not only to susceptible enterococcal isolates, but also to other more virulent nosocomial pathogens, like Staphylococcus aureus . Furthermore, E. faecium isolates are characterized by a high frequency of genes encoding putative virulence factors, such as collagen adhesin (acm gene), enterococcal surface protein (esp gene), hyaluronidase (hyl gene), gelatinase (gelE gene), endocarditis antigen (efa gene), and cytolysin (cyl operon) .
The ability to form biofilm among E. faecium strains is considered to be an important virulence property, and these bacteria are often responsible for conditions in which they may be associated with biofilm, such as endocarditis or catheter-associated urinary tract infections [1, 7]. Unfortunately, due to the rapidly increasing number of conflicting literature reports about biofilm formation among enterococci, we still do not know the true impact of biofilm growth on the expression and transfer of resistance and virulence traits, especially among the E. faecium species [8-10].
Moreover, very limited data about biofilm formation, virulence, and antibiotic resistance among E. faecium strains are available in Poland . This prompted us to determine the prevalence of the biofilm-forming ability among E. faecium clinical strains, depending on the patient's clinical material. In the next step, we searched for differences in resistance and virulence determinants between BIO+ and BIO- E. faecium isolates. This study also aimed to investigate the differences among E. faecium strains isolated from infections and colonization, and to determine differences between strains isolated from blood and other clinical sources.
MATERIALS AND METHODS
Tests were performed on sixty-six randomly selected E. faecium strains, isolated from clinical specimens from patients hospitalized at the University Hospital in Bialystok (Poland) from December 2013 to January 2015. The majority of strains were collected from intensive care units (42.8%) and a hematology clinic (31.8%).
Identification and susceptibility testing
The identification and susceptibility testing of study isolates were conducted on the automated VITEK 2 system (bioMerieux, France) according to the manufacturer's guidelines using VITEK 2 GP and AST-P516 cards, respectively.
Susceptibility to ampicillin, imipenem, gentamicin, streptomycin, vancomycin, teicoplanin, linezolid, and tigecycline was interpreted according to the European Committee on Antimicrobial Susceptibility Testing (EUCAST) recommend-dations (breakpoint tables for interpretation of minimum inhibitory concentrations, MIC, and zone diameters; version 5.0. 2015; http://www.eucast.org).
The Congo red agar (CRA) method [12, 13] and the tube method [14, 15] were used to assess biofilm-forming ability. Each experiment was repeated three times for each strain. Isolates that demonstrated the ability to form biofilm by both methods were considered biofilm positive (BIO+) strains.
Hemolysin production was established on Columbia blood agar with 5% sheep blood (OXOID, United Kingdom), as previously described .
Genomic DNA was extracted from overnight E. faecium cultures using a Genomic Mini Kit (A&A Biotechnology, Poland) according to the manufacturer's instructions.
PCR detection of virulence genes
PCR assays were performed to detect the following virulence genes: gelE, acm, hyl, esp, efaA, and cyl. The primers used in this survey were selected from the literature and their sequences are listed in Table 1. PCR amplification was performed in 25 [micro]l mixtures using 2 [micro]l of DNA solution, 1 [micro]l of each primer, 8.5 [micro]l of nuclease-free water, and 12.5 [micro]l of PCR master mix (DNA Gdansk, Poland). Samples were subjected to an initial denaturation at 94[degrees]C for 5 min, followed by 30 cycles of denaturation at 94[degrees]C for 1 min, annealing at an appropriate temperature for 1 min, and elongation at 72[degrees]C for 1 min using a DNA thermocycler (SensoQuest GmbH, Germany).
PCR products were separated electrophoretically on the Sub-Cell GT apparatus (Bio-Rad, USA) at 5 V/cm for 100 min on a 1.5% agarose gel (Sigma-Aldrich, USA) containing 0.5% ethidium bromide (MP Biomedicals, USA) in Tris-borate-EDTA (ethylenediaminetetraacetic acid) buffer. Then, amplicons were visualized and photographed using the ChemiDoc XRS imaging system and Quantity One 1-D analysis software (Bio-Rad). To confirm the presence of the above-mentioned virulence genes, DNA sequencing was carried out on selected PCR products by the GENOMED S.A. company in Poland. The sequences were aligned and compared with reference sequences achieved using GenBank with the Basic Local Alignment Search Tool (BLAST) algorithm.
STATA 13.1 (StataCorp LP, USA) was used for statistical analysis. Differences between various groups of E. faecium strains were assessed using the Chi-square and Fisher's exact tests. Results with p<0.05 were considered significant.
Sixty-six E. faecalis strains were divided into various groups based on their source of isolation: Infection Group, strains isolated from blood (18.2%), urine (13.7%), pus (3%), and bronchoalveolar lavage (BAL) (3%); Colonization Group, isolates from rectal swabs (30.3%), feces (12.1%), pharyngeal swabs (7.6%), and groin swabs (3%); Blood Group, isolates only from blood (18.2%); and Other Group, isolates from all other clinical materials (71.8%). Moreover, after determining the biofilm-forming ability of all tested E. faecium strains, we created BIO+ (72.7%) and BIO- (27.3%) groups. We also divided the previous groups into BIO+ subgroups: BIO+ Infection/BIO+ Colonization, and BIO+ Blood/BIO+ Other.
The exact characteristics of differences in virulence and antibiotic resistance between the tested E. faecium groups are presented in Table 2. A significant difference (p=0.001) was reported only in the case of the phenotypic ability to hemolyze (97.9% BIO+ and 72.2% BIO-). The most frequent virulence genes among the tested isolates were acm (>95.5%) and efa (>81.8%). There were no statistically significant differences in the prevalence of all tested virulence genes (P>0.05).
All tested E. faecium groups showed high resistance to ampicillin (>96.3% resistant isolates) and imipenem (>94.4% resistant isolates). Resistance to gentamicin was detected in more than 41.7% of the tested isolates, whereas more than 81.5% were resistant to streptomycin. Differences between the various groups of E. faecium were not statistically significant (P>0.05), except for glycopeptides (Table 2). In the case of vancomycin, 71.1% of E. faecium from the Colonization group and 17.9% of E. faecium from the Infection group (p<0.001), 70.4% of the BIO+ Colonization group and 19% of the BIO+ Infection Group (p<0.001), 55.6% of other, 16.7% of blood isolates (p=0.015), 56.8% of BIO+ other, and 18.2% of BIO+ blood isolates (p=0.026) were resistant. Resistance to teicoplanin was detected in 63.2% of strains from the Colonization group and 14.3% of strains from the Infection group (p<0.001), in 59.3% of the BIO+ Colonization group and 14.3% of the BIO+ Infection group (p<0.001), and in 48.1% of other and 16.7% of blood isolates (p=0.046). Linezolid and tigecycline had the highest activity against all studied isolates (100% susceptibility).
Our results revealed that 72.7% of the tested E. faecium strains had the ability to form biofilm. Studies by other authors showed different results; in India, Italy, and Turkey, the percentages of BIO+ E. faecium strains were much lower (25.2%, 28.8%, and 48%, respectively) [8, 19, 20]. When comparing strains from the Infection Group with strains from the Colonization Group, we found that this ability was on a similar level (75% and 72.7%, respectively). Di Rosa et al.  described only 35.7% of biofilm-producing E. faecium isolated from infections. In our survey, the highest difference in biofilm formation was observed when comparing the Blood Group with the Other Group (91.1% and 68.5%, respectively), but it was statistically insignificant (p=0.103). Researchers from Greece  detected 55.9% of BIO+ E. faecium strains in blood isolates, while our study revealed that all strains from the analogous group had this ability. Thus, worryingly, we can consider that the percentages of BIO+ E. faecium strains in our hospital are very high, and the appropriate surveillance methods should be implemented.
According to the European Committee on Antimicrobial Susceptibility Testing (EUCAST) interpretation tables for clinical breakpoints, almost all (>95%) E. faecium isolates were resistant to tested B-lactams, and more than 60% showed high levels of resistance to aminoglycosides. Moreover, in this research we observed very high rates of resistance to glycopeptides: 48.5% strains were VRE, and 42.4% were also resistant to teicoplanin. Likewise, the latest research conducted in our hospital revealed similar levels of resistance among E. faecium strains . Therefore, we can conclude that the problem with MDR E. faecium isolates in our hospital environment is large and the infections caused by these strains should not be underestimated. The only antimicrobial agents that showed 100% activity against these strains were tigecycline and linezolid. These findings are consistent with previous surveys that describe these drugs as valuable therapeutic options in infections caused by MDR Enterococcus strains, although their clinical use is limited [21-23].
Taking into account the levels of resistance among the tested groups and subgroups, we found no statistically significant differences, except for vancomycin and teicoplanin (Table 2). In the case of our isolates from the Blood Group, we found very high levels of resistance to all tested antibiotics (except linezolid and tigecycline). Previous American research revealed significantly smaller percentages of resistance toward ampicillin (75.6%) and aminoglycosides (about 30%) among E. faecium isolated from blood. However, the same study showed higher levels of resistance to vancomycin (22.2%) . Different results were presented by Saeedi et al. , who reported resistance to gentamicin in all E. faecium blood isolates. Interestingly, we revealed no significant differences in antibiotic resistance between BIO+ and BIO- isolates; therefore, the hypothesis that bacteria in biofilms are more resistant to antibiotics than planktonically grown microorganisms [3,9,26,27] is not confirmed in our study.
Unfortunately, we did not find any statistically significant differences in the prevalence of all tested virulence genes among the tested E. faecium groups (P>0.05). The only significant disparity (p=0.001) was reported in the case of the phenotypic ability to hemolyze: more BIO+ (97.9%) than BIO- (72.2%) strains had this feature, indicating that BIO+ isolates are slightly more virulent than the BIO- group.
The results obtained in this study agree with previous statements that there is no relationship between the occurrence of the esp gene and biofilm formation among Enterococcus strains [3,6,8]. Nevertheless, esp seems to be an important virulence trait among E. faecium strains. Hallgren et al.  noticed that it was the only virulence factor found among these species; it occurred in 75% of blood isolates and 70% of rectal isolates. On the other hand, Diani et al.  found that 46% of blood and 22% of fecal isolates contained this gene. An American survey conducted concurrently revealed that esp was present in 33% of BIO+ and 53.8% of BIO- isolates .
Interestingly, the hyl gene was detected much less frequently, in only 22% of BIO+ and 38.5% of BIO- strains . In our BIO+ Infection Group, 85.7% of strains had the esp gene, while Di Rosa et al.  detected it in only 50% of analogous strains. Unfortunately, in our research we observed much higher rates of these genes among corresponding groups. Astonishingly, Tsikrikonis et al.  revealed that 83.8% of BIO+ and 26.7% of BIO- E. faecium clinical strains had esp, and 61.9% of BIO+ and 0% of BIO- fecal isolates carried this gene. The authors concluded that the presence of esp has a strong connection with biofilm-forming ability, which is not in concordance with our findings. All of these varied results indicate that esp may require certain interactions with other virulence traits to result in biofilm enhancement; more studies are definitely needed in this area.
A noteworthy fact is that the presence of cyl and gelE genes among E. faecium strains is very rare [20,28]. Vankerckhoven et al.  did not detect any cyl and gelE genes with PCR in 271 E. faecium isolates. In our study, the majority of E. faecium isolates were shown to be cytolysin/hemolysin producers (>89%) on blood agar plates, but only two (3%) strains carried the genes of the cyl operon. This may be due to the expression of other hemolysin genes that are not yet known or not so well studied. Interestingly, we found that these cyl-positive strains also had the gelE gene. A small percentage of strains with the gelE gene have also been reported , but without the coexistence of the cyl gene.
In summary, this study demonstrated a lack of significant differences in virulence and resistance among various tested E. faecium groups. Nevertheless, we revealed that all E. faecium isolates in our hospital carry high levels of resistance to many antimicrobials and are extremely well equipped with virulence genes. Furthermore, the majority of these strains were able to form biofilm structures; therefore, they can persist in a hospital environment for a long time. This creates the need for more effective surveillance and an appropriate antibiotic policy. Only a complete understanding of the exact role of resistance and virulence factors in the development of biofilm can lead to improved strategies for the control of infections caused by MDR E. faecium isolates. There is an urgent need for larger multicenter studies to assess reports about levels of resistance and virulence among E. faecium strains in Poland.
We would like to thank Steven J. Snodgrass for his editorial assistance.
The results of this work were presented in part at the Biofilms 7 Conference 2016 in Porto, Portugal (06/26-26/2016).
Conflicts of interest
The authors have no conflicts of interest to declare.
This work was supported by funds from the Leading National Research Center (137/KNOW/2015) in Bialystok, Poland.
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Sienko A. (*#A-E), Wieczorek P. (#A-E), Majewski P. (B,C), Sacha P. (B), Wieczorek A. (B), Ojdana D. (B), Tryniszewska E. (E,F)
Department of Microbiological Diagnostics and Infectious Immunology, Faculty of Pharmacy, Medical University of Bialystok, Poland (#) Both authors contributed equally to this work
(A) - Conception and study design; (B) - Collection of data; (C) - Data analysis; (D) - Writing the paper; (E) - Review article; (F) - Approval of the final version of the article; (G) - Other (please specify)
(*) Corresponding author: Sienko Anna Department of Microbiological Diagnostics and Infectious Immunology Medical University of Bialystok, 15a Waszyngtona Street, 15-269 Bialystok, Poland Tel.: + 48 85 746 85 71; e-mail: firstname.lastname@example.org
Table 1. PCR primers, annealing temperatures, and product sizes for the detection of virulence genes virulence primers product size gene (bp) gelE AAT TGC TTT ACA CGG AAC GG 548 GAG CCA TGG TTT CTG GTT GT acm GGC CAG AAA CGT AAC CGA TA 353 CGC TGG GGA AAT CTT GTA AA hyl ACA GAA GAG CTG CAG GAA ATG 276 GAC TGA CGT CCA AGT TTC CAA esp AGA TTT CAT CTT TGA TTC TTG G 510 AAT TGA TTC TTT AGC ATC TGG efaA CACGCTATTACGAACTATGA 375 TAAGAAAGAACATCACCACGA cyl TGG ATG ATA GTG ATA GGA AGT 517 TCT TTC ATC ATC TGA TAG TA virulence annealing gene temperature reference ([degrees]C) gelE 52  acm hyl esp 55 efaA  cyl Table 2. Characteristics and statistical analysis (Chi square test, significance level a=0.05) of differences in virulence and antibiotic resistance between the tested E. faecium groups; BIO+, biofilm-positive; BIO-, biofilm-negative; n, number of strains; acm, collagen adhesin; gelE, gelatinase; esp, enterococcal surface protein; hyl, hyaluronidase; efa, endocarditis antigen; cyl, cytolysin; AMP, ampicillin; IMP, imipenem; GN, gentamicin; S, streptomycin; VA, vancomycin; TEI, teicoplanin; TG, tigecycline; LZD, linezolid; *lack of differences between groups. virulence strains n hemolysis p acm p BIO+ 48 97.9% 0.001 97.9% 0.117 BIO- 18 72.2% 88.9% Infection 28 92.9% 0.636 100% 0.128 Colonization 38 90.9% 95.5% BIO+ Infection 21 100% 0.373 100% 0.373 BIO+ Colonization 27 96.3% 96.3% Blood 12 100% 0.226 100% 0.403 Other 54 88.9% 94.4% BIO+ blood 11 100% 0.582 100% 0.582 BIO+ other 37 97.3% 97.3% antibiotic resistance AMP p IMP p BIO+ 48 97.9% 0.464 100% 0.273 BIO- 18 94.4% 94.4% Infection 28 96.4% 0.826 96.4% 0.240 Colonization 38 97.4% 100% BIO+ Infection 21 100% 0.372 100% * BIO+ Colonization 27 96.3% 100% Blood 12 100% 0.498 100% 0.635 Other 54 96.3% 98.1% BIO+ blood 11 100% 0.5 82 100% * BIO+ other 37 97.3% 100% virulence strains gelE p esp p hyl BIO+ 4.2% 0.809 87.5% 0.138 83.3% BIO- 5.6% 72.2% 83.3% Infection 0% 0.128 85.7% 0.656 85.7% Colonization 4.5% 83.3% 83.3% BIO+ Infection 0% 0.203 85.7% 0.741 90.5% BIO+ Colonization 7.4% 88.9% 77.8% Blood 0% 0.403 91.7% 0.392 83.3% Other 5.6% 81.5% 83.3% BIO+ blood 0% 0.430 90.9% 0.697 81.8% BIO+ other 5.4% 86.5% 83.8% antibiotic resistance GN p S p VA BIO+ 62.5% 0.917 83.3% 0.575 47.9% BIO- 61.1% 88.9% 50% Infection 60.7% 0.840 85.7% 0.866 17.9% Colonization 63.2% 84.2% 71.1% BIO+ Infection 61.9% 0.940 85.7% 0.696 19% BIO+ Colonization 63% 81.5% 70.4% Blood 41.7% 0.129 91.7% 0.466 16.7% Other 63% 83.3% 55.6% BIO+ blood 45.5% 0.183 90.9% 0.443 18.2% BIO+ other 67.6% 81.1% 56.8% virulence strains p efa p cyl p BIO+ * 89.6% 0.154 2.1% 0.463 BIO- 100% 5.6% Infection 0.656 89.3% 0.408 0% 0.218 Colonization 92.4% 3% BIO+ Infection 0.214 85.7% 0.439 0% 0.373 BIO+ Colonization 92.6% 3.7% Blood * 83.3% 0.188 0% 0.498 Other 94.4% 3.7% BIO+ blood 0.878 81.8% 0.337 0% 0.582 BIO+ other 91.9% 2.7% antibiotic resistance p TEI p TG/LZD p BIO+ 0.880 39.6% 0.446 0% * BIO- 50% 0% Infection <0.001 14.3% <0.001 0% * Colonization 63.2% 0% BIO+ Infection <0.001 14.3% <0.001 0% * BIO+ Colonization 59.3% 0% Blood 0.015 16.7% 0.046 0% * Other 48.1% 0% BIO+ blood 0.026% 18.2% 0.098 0% * BIO+ other 45.9% 0%
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|Author:||Sienko, A.; Wieczorek, P.; Majewski, P.; Sacha, P.; Wieczorek, A.; Ojdana, D.; Tryniszewska, E.|
|Publication:||Progress in Health Sciences|
|Date:||Jun 1, 2017|
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