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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 9  |  Issue : 1  |  Page : 27-32

Virulence determinants and biofilm formation in clinical isolates of Enterococcus: A cross-sectional study


1 Student Research Committee; Department of Microbiology, Faculty of Medicine; Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
2 Department of Microbiology, Faculty of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
3 Student Research Committee, School of Medicine, Bam University of Medical Sciences, Bam, Iran
4 Department of Microbiology, Faculty of Medicine; Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

Date of Submission23-Sep-2019
Date of Decision03-Jan-2020
Date of Acceptance06-Jan-2020
Date of Web Publication24-Jan-2020

Correspondence Address:
Ahmad Farajzadeh Sheikh
Department of Microbiology, Faculty of Medicine; Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2221-6189.276079

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  Abstract 


Objective: To evaluate the relationship between biofilm formation and incidence of virulence determinants in clinical isolates of Enterococcus.
Methods: In this cross-sectional study, the clinical isolates of Enterococcus strains were collected from the university teaching hospitals in Ahvaz, Iran from June 2017 to June 2018. Then, the prevalence of Enterococcus species, antibiotic resistance, virulence factors, and biofilm-producing ability were determined.
Results: Of the 119 tested isolates, 17 (14.3%) were Enterococcus faecalis, 72 (60.5%) were Enterococcus faecium and 30 (25.2%) were other Enterococcus spp. Gelatinase was detected in 97 (81.5%) isolates, enterococcal surface protein in 41 (34.5%) isolates, serine protease in 39 (32.8%) cases, accessory colonization factor in 111 (93.3%) cases and pathogenicity islands in 17 (14.3%) cases. The biofilm formation ability was observed in 75 (63.0%) of all isolates and the association between the presence of enterococcal surface protein gene and biofilm formation was statistically significant. Higher resistance to vancomycin, gentamycin, and teicoplanin was indicated in Enterococcus faecium with 81.8%, 58.4%, and 85.7% resistance rate, respectively. All Enterococcus faecalis isolates were sensitive to teicoplanin and vancomycin.
Conclusions: The presence of antibiotic-resistance with several virulence factors in Enterococcus spp has become a concern. High prevalence of enterococcal surface protein gene among biofilm- producing isolates suggests a potential relation between biofilm formation and the enterococcal surface protein gene, and further studies are needed to identify the mechanism of biofilm inhibition.

Keywords: Enterococcus spp; Biofilm formation; Antibiotic resistance; Virulence genes


How to cite this article:
Shahi F, Hamidi H, Khoshnood S, Mehdipour G, Dezfouli AA, Sheikh AF. Virulence determinants and biofilm formation in clinical isolates of Enterococcus: A cross-sectional study. J Acute Dis 2020;9:27-32

How to cite this URL:
Shahi F, Hamidi H, Khoshnood S, Mehdipour G, Dezfouli AA, Sheikh AF. Virulence determinants and biofilm formation in clinical isolates of Enterococcus: A cross-sectional study. J Acute Dis [serial online] 2020 [cited 2021 Feb 27];9:27-32. Available from: http://www.jadweb.org/text.asp?2020/9/1/27/276079




  1. Introduction Top


Enterococci are commensal bacteria in the gastrointestinal flora of animals and humans. In recent years, enterococci have evolved into the main causes of nosocomial infections, and they are one of the most frequent opportunistic pathogens isolated from urinary tract infections, infected surgical sites, and septicemia[1],[2].

Enterococcus has two common species Enterococcus faecalis (E. faecalis) and Enterococcus faecium (E. faecium) which are involved in nosocomial infections with the prevalence of about 90% and 10%, respectively. The most infections caused by these bacteria are endogenous but cross-infection usually happens in hospitalized patients[3]. Also, the treatment of these infections has been clinically challenging because of the increasing resistance to different types of antibiotics, including β lactams, glycopeptides, aminoglycosides, macrolides and fluroquinolones[4],[5]. The capability of Enterococcus to acquire antibiotic resistance through the chromosomal exchange, transfer of transposons and plasmids, or mutation makes it difficult to implement appropriate therapeutic measures[6].

Virulence factors involve in the pathogenesis through the mediation of adherence and colonization, invasion into the host tissues, modulation of the host immunity, secretion of toxins and enzymes, which can enhance the infection intensity. Several virulence factors including the capsule formation and gelatinase [encoded by the chromosomal gelatinase (gelE)], aggregation substance, enterococcal surface protein [encoded by the chromosomal enterococcal surface protein (esp)] are involved in bacterial adherence and/or in biofilm production in the environment of hospitals[7].

Several enterococcal virulence factors have been identified to date, of which pathogenicity islands (pai), accessory colonization factor (ace), esp, serine protease (sprE) and gelE have been studied most intensively. Gelatinase, an extracellular zinc-containing metalloprotease, hydrolyzed collagen, and gelatin, has been recognized in dairy strains of E. faecium and has been shown to aggravate endocarditis in an animal model. Pathogenicity islands represent genetic elements that encode virulence factors related to bacterial pathogenesis[8],[9].

In addition, one of the virulence factors that play a significant role in the pathogenesis of enterococcal infections is biofilm formation, which also helps the survival of the disease by preventing the penetration of antimicrobial agents[7]. The clinical impact of E. faecium may be increased by biofilm production, and these bacteria are frequently found in conditions where biofilm is necessary, including periodontitis, catheter-associated urinary tract infections, endocarditis, and other device-related infections, thereby making treatment of E. faecium with antibiotics more difficult. According to the study of Almohamad et al., biofilm formation occurs less commonly in E. faecium compared with E. faecalis[10].

The aim of our study is to identify virulence genes, evaluate biofilm production and the antibiotic resistance in clinical isolates of Enterococcus obtained from the teaching hospital of Ahvaz and find the relationship between virulence genes and biofilm formation ability.


  2. Materials and methods Top


2.1. Ethics statement

This study was approved by the ethics committee of Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran (IR. AJUMS.REC.1396.1047).

2.2. Strains collection

In this cross-sectional study, clinical isolates that were suspected to be Enterococcus strains were collected from teaching hospitals in Ahvaz, Iran, from June 2017 to June 2018. All isolates were cultured on MacConkey agar, blood agar, and bile esculin agar (Himedia, India). Culture characteristics and colony morphology were observed macroscopically. The genus Enterococcus was identified using gram staining, cultural characteristics, and biochemical tests, including L-pyrrolidinyl-β-naphthalyamide hydrolysis, bile esculin hydrolysis, and growth on 6.5% NaCl media at pH 9.6[11].

2.3. Identification of Enterococcus spp. strains by PCR assay

The DNA was extracted by the boiling method. Specific primers for E. faecalis and E. faecium were used [Table 1]. Species were identified by PCR assay as follows: 1.5 mM MgCl2, 1.5 pmol of each primer, 0.2 mM of each dNTP, and 0.625 U of Taq DNA polymerase[12]. The PCR conditions were as follows: 94°C for 4 min, followed by 30 cycles of 94°C for 40 s, 55°C or 56°C for 40 s, and 72°C for 40 s and an extension at 72°C for 5 min. The PCR amplicons were electrophoresed on 1% agarose gel. E. faecium ATCC 19434 and E. faecalis ATCC 29212 were used as control strains.
Table 1: The primers used in PCR.

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2.4. Susceptibility testing

Susceptibility of enterococcal isolates against teicoplanin (30 μg), vancomycin (30 μg), linezolid (30 μg), gentamycin (10 μg), fosfomycin (200 μg), nitrofurantoin (200 μg), ampicillin (10 μg), ciprofloxacin (5 μg), erythromycin (15 μg), tetracycline (30 μg), chloramphenicol (30 μg) disks (Mast, United Kingdom) was determined using the Kirby-Bauer disk diffusion method on muller-Hinton agar, according to CLSI (2017) guidelines[13]. E. faecalis ATCC 29212 and Staphylococcus aureus ATCC 25923 were used as quality control organisms.

2.5. Detection of virulence genes

The DNA was extracted by the boiling method. Genes including ace, gelE, sprE , esp, and pai were detected by PCR using primers listed in [Table 1][8]. The PCR conditions were as follows: initial denaturation at 94 °C for 4 min; 30 cycles at 94°C for 30 s, annealing for 30 s at the TA of the primer pairs, and extension at 72°C for 30 s; followed by an extension at 72°C for 5 min. PCR products were analyzed in 1.5% agarose gel (Invitrogen, Carlsbad, CA, USA) prepared in TBE buffer at 95 V for 60 min. After staining with ethidium bromide, it was observed under ultraviolet light.

2.6. Detection of biofilm production

For the detection of biofilm production, a 1: 10 dilution of overnight cultures in tryptone soy broth was inoculated in a microtitre polystyrene plate. After growth for 18 h at 37°C, the plates were washed thrice with phosphate-buffered saline. The adherent bacterial film was fixed by air drying at 60°C for 1 h and stained with crystal violet; excess stain was washed with tap water. Then, the biofilm optical density was measured at 570 nm by a spectrophotometer. Biofilm formation ability was recorded as follows: OD<0.120, nonproducers, 0.120<OD<0.240, weak producers, OD>0.240, strong producers. Biofilm measurements were repeated at least thrice for each isolate[14].

2.7. Statistical analysis

SPSS v.22.0 statistics software (IBM Corporation, Armonk, NY, USA) was used for statistical analysis. Data were expressed as percentages, and analyzed by Chi-square test. The significance level was set as α=0.05.


  3. Results Top


3.1. Bacterial isolates

A total of 119 clinical strains of Enterococcus spp. were obtained from different wards of Ahvaz teaching hospitals. A total of 43 (36.1%) isolates were from female patients and 76 (63.9%) were from male patients. A total of 92.5% of Enterococcus spp. were isolated from urine, 3.4%, 3.4% and 0.8% from blood wound secretion and ascites fluid, respectively. In addition, 72 (60.5%) isolates were identified as E. faecium, 17 (14.3%) as E. faecalis and 30 (25.2%) as other Enterococcus spp.

3.2. Antibiotic resistance pattern

The antibiotic-resistance of Enterococcus spp in different samples is shown in [Table 2]. More Enterococcus isolates were resistant to erythromycin (80.7%), followed by gentamicin (74.8%) and ampicillin (69.7%), tetracycline (59.7%). Resistance to these antibiotics was higher in E. faecium than other species. In this study, high sensitivity was observed to linezolid, fosfomycin, and nitrofurantoin.
Table 2: Prevalence of antibiotic resistance among Enterococcus spp. isolates.

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3.3. Virulence factors

According to PCR results, 41 (34.5%) had esp gene, 97 (81.5%) had gelE gene, 39 (32.8%) had sprE gene, 111 (93.3%) had ace gene and 17 (14.3%) had pai gene [Table 3]. One hundred twelve (94.1%) of the enterococci isolates carried 2-5 tested virulence genes. Three of E. faecium, 2 of E. faecalis and 1 of other Enterococcus spp harbored all tested virulence genes. In contrast, only one of the other Enterococcus spp was negative for all virulence genes.

3.4. Biofilm formation
Table 3: Prevalence of virulence genes and biofilm among Enterococcus spp.

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The biofilm formation ability was observed in 75 (63.0%) of all isolates; 24 (20.2%), 33 (27.7%) and 18 (15.1%) were classified as weekly, moderately and strongly adherent, respectively. The relationship between virulence genes and biofilm formation is shown in [Table 4]. Association between esp positive and biofilm positive strains was statistically significant (P=0.030). No significant differences were found when comparing gelE, sprE, ace, pai positive and biofilm positive isolates (P>0.05) [Table 4].
Table 4: Relation between the presence of virulence gene and biofilm formation.

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Among the biofilm formers isolates, the highest resistance rate was 73% to gentamicin. Although, the resistance was higher in biofilm positive isolates there were no statistically significant differences between biofilm formation and antimicrobial resistance (P>0.05).


  4. Discussion Top


Over the past decades, enterococci have emerged as important nosocomial pathogens[15]. Because of its intrinsic resistance to harsh environments and antibacterial drugs, it can survive and spread in hospitals.

Biofilm plays a critical role in enterococcal infections and produces a context to increase bacterial survival in the host[16]. Due to the controversial status of enterococci, this research assessed biofilm formation, virulence genes and antibiotic resistance in 119 clinical enterococci isolates. Based on the results, the incidence of E. faecium was higher than E. faecalis isolates; however, E. faecalis is the main cause of enterococcal infections. This is in accordance with Arshadi et al.[17] and Moosavian et al.[18] who isolated enterococci from clinical samples in Ahvaz in the southwest of Iran. But it was different from the results of Shokoohizadeh et al.[19] and Emaneini et al.[11] in Tehran and Hashem et al.[20] in Egypt. They showed that the prevalence of E. faecalis (62.5%, 64.4%, and 72.2%) was higher than E. faecium isolates (37.5%, 35.6%, and 24.4%). In current years, an increase in E. faecium nosocomial infections can be seen in hospitals due to the emergence of vancomycin-resistant enterococci strains[17]. On the other hand, 92.5% of Enterococcus spp. were isolated from urine which is similar to previous studies[17],[21],[22].

Antibiotic resistance is a factor contributing to the pathogenesis of enterococci that can be acquired or found internally[23]. The highest resistance among all isolates was to erythromycin, gentamycin, and ampicillin. A similar study by Khani et al.[24] in Kermanshah indicated that most isolates of enterococci were resistant to ampicillin and erythromycin.

Also, the high prevalence of resistance to gentamycin has been previously reported[25],[26]. In this study, according to drug susceptibility testing, 7.6% of our isolates showed resistance to linezolid and 3.4% of them had intermediate resistance. Previous studies conducted by Arabestani et al.[27] in 2017 and Feizabadi et al.[28] in 2008 in the west of Iran and Tehran shows that no resistance was reported for linezolid. In the Yasliani et al., a study in 2009, 17 (8.5%), 6 (3%) and 4 (2%) of the isolates were resistant to vancomycin, teicoplanin, and linezolid, respectively[29]. Also, Labibzadeh in 2018 reported the same resistance to these antibiotics. Our study showed a higher resistance of linezolid, teicoplanin, and vancomycin among clinical enterococcal isolates in Ahvaz. In this study, antibiotic resistance rate in E. faecalis isolates was higher than E. faecium, and all the linezolid-resistant isolates were vancomycin- resistant enterococci and teicoplanin-resistant, which is a major therapeutic concern.

In this study, the gelE gene was the most important virulence factor. The gelE gene is responsible for gelatinase production which can hydrolyze fibrinogen, insulin, casein, collagen, gelatin, and hemoglobulin[30].

Biofilm formation in enterococci is a multifactorial property and the role of various virulence genes in this process is controversial[12]. Several studies were performed to report the main virulence genes of enterococci that are related to biofilm formation in these bacteria[12],[20],[31],[32],[33]. Previous studies investigated the relation of virulence genes and biofilm formation, especially the presence of esp and gelE. Esp has been implicated as a contributing factor in the colonization and persistence of the infection[31]. In this study, the prevalence of all 5 virulence factors was significantly high in E. faecium than E. faecalis. Our study demonstrates a high frequency (63%) of biofilm formation, which is consistent with other studies[34],[35],[36]. In our study, 41.33% of biofilm positive isolates carried esp gene, which is in agreement with the incidence reported by other researchers[16],[34].

Also, the prevalence of the esp gene in biofilm positive isolated from different sources showed a significant trend (P=0.03), which was similar to the Soares et al.[12] and Zheng et al.[37] studies (P<0.001) while others found no significant correlation between biofilm formation and the presence of esp.

The esp gene encodes an extracellular surface protein that helps adhesion, colonization, and evasion of the immune system. Also, this protein contributes to biofilm formation and persistence of E. faecalis in the urinary tract[16].[38]. Our results showed that there was no significant correlation between the presence of gelE, sprE, and ace and the ability of isolates to biofilm formation.

According to our findings, the presence of antibiotic-resistant Enterococcus with several virulence factors can be a concern. Also, the high prevalence of the esp gene among biofilm-producing clinical isolates suggests a potential link between biofilm formation and the esp gene but further studies should be needed to identify the mechanism of biofilm inhibition.

Conflict of interest statement

The authors report no conflict of interest.

Acknowledgments

Our study was a part of a research project (No.96s35) which was approved and financially supported by Deputy of Vice-Chancellor for Research Affairs and Student Research Committee of Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran, and the authors thank all of them.

Authors’ contribution

F.S. and H.H. conceived and designed the experiments; performed the experiments, contributed reagents, materials, analysis tools or data and interpreted. S.K., G.M. and A.A.D. performed the experiments, analyzed and interpreted the data. A.F.S. contributed reagents, materials and wrote the paper.



 
  References Top

1.
Jett BD, Huycke MM, Gilmore MS. Virulence of enterococci. Clin Microbiol Rev 1994; 7(4): 462-478.  Back to cited text no. 1
    
2.
Willems RJ, Homan W, Top J, van Santen-Verheuvel M, Tribe D, Manzioros X, et al. Variant esp gene as a marker of a distinct genetic lineage of vancomycin resistant Enterococcus faecium spreading in hospitals. Lancet 2001; 357(9259): 853-855.  Back to cited text no. 2
    
3.
Arbabi L, Boustanshenas M, Rahbar M, Majidpour A, Shayanfar N, Afshar M, et al. The correlation between resistance to antimicrobial agents and harboring virulence factors among Enterococcus strains isolated from clinical samples. J Mol Biol Res 2016; 6(1): 35-43.  Back to cited text no. 3
    
4.
Heidari H, Emaneini M, Dabiri H, Jabalameli F. Virulence factors, antimicrobial resistance pattern and molecular analysis of Enterococcal strains isolated from burn patients. Microb Pathog 2016; 90: 93-97.  Back to cited text no. 4
    
5.
Barbosa-Ribeiro M, De-Jesus-Soares A, Zaia AA, Ferraz CC, Almeida JF, Gomes BP. Antimicrobial susceptibility and characterization of virulence genes of Enterococcus faecalis isolates from teeth with failure of the endodontic treatment. J Endod 2016; 42(7): 1022-1028.  Back to cited text no. 5
    
6.
Diarra MS, Rempel H, Champagne J, Masson L, Pritchard J, Topp E. Distribution of antimicrobial resistance and virulence genes in Enterococcus spp. and characterization of isolates from broiler chickens. Appl Environ Microbiol 2010; 76(24): 8033-8043.  Back to cited text no. 6
    
7.
Strateva T, Atanasova D, Savov E, Petrova G, Mitov I. Incidence of virulence determinants in clinical Enterococcus faecalis and Enterococcus faecium isolates collected in Bulgaria. Braz J Infect Dis 2016; 20(2): 127133.  Back to cited text no. 7
    
8.
Yean CY. Genotypic variations of virulent genes in Enterococcus faecium and Enterococcus faecalis isolated from three hospitals in Malaysia. Adv Clin Exp Med 2015; 24(1): 121-127.  Back to cited text no. 8
    
9.
Lopes MdFS, Simões AP, Tenreiro R, Marques JJF, Crespo MTB. Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int J Food Microbiol 2006; 112(3): 208-214.  Back to cited text no. 9
    
10.
Almohamad S, Somarajan SR, Singh KV, Nallapareddy SR, Murray BE. Influence of isolate origin and presence of various genes on biofilm formation by Enterococcus faecium. FEMS Microbiol Lett 2014; 353(2): 151-156.  Back to cited text no. 10
    
11.
Emaneini M, Aligholi M, Aminshahi M. Characterization of glycopeptides, aminoglycosides and macrolide resistance among Enterococcus faecalis and Enterococcus faecium isolates from hospitals in Tehran. Pol J Microbiol 2008; 57(2): 173-178.  Back to cited text no. 11
    
12.
Soares RO, Fedi AC, Reiter KC, Caierão J, d’Azevedo PA. Correlation between biofilm formation and gelE, esp, and agg genes in Enterococcus spp. clinical isolates. Virulence 2014; 5(5): 634-637.  Back to cited text no. 12
    
13.
Clinical Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Standard. CLSI document. M7-A4. PA: CLSI; 2018.  Back to cited text no. 13
    
14.
Rosa R, Creti R, Venditti M, D’Amelio R, Arciola CR, Montanaro L, et al. Relationship between biofilm formation, the enterococcal surface protein (Esp) and gelatinase in clinical isolates of Enterococcus faecalis and Enterococcus faecium. FEMS Microbiol Lett 2006; 256(1): 145-150.  Back to cited text no. 14
    
15.
Higuita NIA, Huycke MM. Enterococcal disease, epidemiology, and implications for treatment. In: Gilmore MS, Clewell DB, Ike Y, et al. (eds) Enterococci: From commensals to leading causes of drug resistant infection [Internet]. Boston: Massachusetts Eye and Ear Infirmary; 2014.  Back to cited text no. 15
    
16.
Kashef M, Alvandi A, Hasanvand B, Azizi M, Abiri R. Virulence factor and biofilm formation in clinical Enterococcal isolates of the west of Iran. Jundishapur J Microbiol 2017; 10(7): e14379.  Back to cited text no. 16
    
17.
Arshadi M, Douraghi M, Shokoohizadeh L, Moosavian SM, Pourmand MR. High prevalence of diverse vancomycin resistance Enterococcus faecium isolates in clinical and environmental sources in ICU wards in southwest of Iran. Microb Pathog 2017; 111: 212-217.  Back to cited text no. 17
    
18.
Moosavian M, Ghadri H, Samli Z. Molecular detection of vanA and vanB genes among vancomycin-resistant enterococci in ICU-hospitalized patients in Ahvaz in southwest of Iran. Infect Drug Resist 2018; 11: 2269.  Back to cited text no. 18
    
19.
Shokoohizadeh L, Ekrami A, Labibzadeh M, Ali L, Alavi SM. Antimicrobial resistance patterns and virulence factors of enterococci isolates in hospitalized burn patients. BMC Res Notes 2018; 11(1): 1.  Back to cited text no. 19
    
20.
Hashem YA, Amin HM, Essam TM, Yassin AS, Aziz RK. Biofilm formation in enterococci: genotype-phenotype correlations and inhibition by vancomycin. Sci Rep 2017; 7(1): 5733.  Back to cited text no. 20
    
21.
Atray D, Sharma A, Atray M. Prevalence of enterococci and its antibiotic resistance in various clinical samples at tertiary care hospital in Southern Rajasthan, India. J Res Med Sci 2017; 4(8): 3413-3416.  Back to cited text no. 21
    
22.
Ran S, Jiang W, Zhu C, Liang J. Exploration of the mechanisms of biofilm formation by Enterococcus faecalis in glucose starvation environments. Aust Dent J 2015; 60(2): 143-153.  Back to cited text no. 22
    
23.
Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 2001; 65(2): 232-260.  Back to cited text no. 23
    
24.
Khani M, Fatollahzade M, Pajavand H, Bakhtiari S, Abiri R. Increasing prevalence of aminoglycoside-resistant Enterococcus faecalis isolates due to the aac (6’)-aph (2”) gene: A therapeutic problem in Kermanshah, Iran. Jundishapur J Microbiol 2016; 9(3) : e28923.  Back to cited text no. 24
    
25.
Labibzadeh M, Kaydani GA, Savari M, Ekrami A. Emergence of highlevel gentamicin resistance among enterococci clinical isolates from burn patients in south-west of Iran: vancomycin still working. Pol J Microbiol 2018; 67(4): 401-406.  Back to cited text no. 25
    
26.
Choukhachian M, Nahaei MR, Rezaee MA, Sadeghi J. High-level gentamicin resistance and detection of aac (6’) le-aph (2”) la gene in enterococci isolated from pediatric hospital in northwest of Iran. Arch Clin Infect Dis 2018; 13(5): e62921..  Back to cited text no. 26
    
27.
Arabestani MR, Nasaj M, Mousavi SM. Correlation between infective factors and antibiotic resistance in enterococci clinical isolates in West of Iran. Chonnam Med J 2017; 53(1): 56-63.  Back to cited text no. 27
    
28.
Feizabadi MM, Sayadi S, Shokrzadeh L, Parvin M, Yadegarynia D. Increase in prevalence of vancomycin resistant isolates of Enterococcous faecium at Labbafinejad hospital. Iran J Clin Infect Dis 2008; 3(2): 73-77.  Back to cited text no. 28
    
29.
Yasliani S, Mohabati Mobarez A, Doust RH, Satari M, Teymornejad O. Linezolid vancomycin resistant Enterococcus isolated from clinical samples in Tehran hospitals. Indian J Med Sci 2009; 63(7): 297-302.  Back to cited text no. 29
    
30.
Upadhyaya PG, Umapathy B, Ravikumar K. Comparative study for the presence of enterococcal virulence factors gelatinase, hemolysin and biofilm among clinical and commensal isolates of Enterococcus faecalis. J Lab Physicians 2010; 2(2):100-104.  Back to cited text no. 30
    
31.
Kafil HS, Mobarez AM. Assessment of biofilm formation by enterococci isolates from urinary tract infections with different virulence profiles. JKSUS 2015; 27(4): 312-317.  Back to cited text no. 31
    
32.
Chaj cka-Wierzchowska W, Zadernowska A, Laniewska-Trokenheim L. Virulence factors, antimicrobial resistance and biofilm formation in Enterococcus spp. isolated from retail shrimps. LWT-J Food Sci Technol 2016; 69: 117-122.  Back to cited text no. 32
    
33.
Frank KL, Vergidis P, Brinkman CL, Quaintance KEG, Barnes AM, Mandrekar JN, et al. Evaluation of the Enterococcus faecalis biofilm- associated virulence factors AhrC and Eep in rat foreign body osteomyelitis and in vitro biofilm-associated antimicrobial resistance. PloS One 2015; 10(6): e0130187.  Back to cited text no. 33
    
34.
Soltani S, Arshadi M, Getso MI, Aminharati F, Mahmoudi M, Pourmand MR. Prevalence of virulence genes and their association with biofilm formation in VRE faecium isolates from Ahvaz, Iran. J Infect Dev Ctries 2018; 12(11): 970-977.  Back to cited text no. 34
    
35.
Talebi M, Moghadam NA, Mamooii Z, Enayati M, Saifi M, Pourshafie MR. Antibiotic resistance and biofilm formation of Enterococcus faecalis in patient and environmental samples. Jundishapur J Microbiol 2015; 8(10): e23349.  Back to cited text no. 35
    
36.
Tendolkar PM, Baghdayan AS, Gilmore MS, Shankar N. Enterococcal surface protein, Esp, enhances biofilm formation by Enterococcus faecalis. Infect Immun 2004; 72(10): 6032-6039.  Back to cited text no. 36
    
37.
Zheng JX, Wu Y, Lin ZW, Pu ZY, Yao WM, Chen Z, et al. Characteristics of and virulence factors associated with biofilm formation in clinical Enterococcus faecalis isolates in China. Front Microbiol 2017; 8: 2338.  Back to cited text no. 37
    
38.
Popovi N, Dini M, Tolina ki M, Mihajlovi S, Terzi -Vidojevi A, Boji S, et al. New insight into biofilm formation ability, the presence of virulence genes and probiotic potential of Enterococcus sp. dairy isolates. Front Microbiol 2018; 9: 78.  Back to cited text no. 38
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]


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