Abstract
Enterococci form a complex, diverse, and very important group of bacteria from the technological and food safety aspect, or from the health-improving aspect as probiotics. Generally, enterococci are considered to be of low pathogenic potential, which is associated mostly with clinical strains. In these strains, production of virulence factors as well as resistance to many antimicrobial drugs could complicate treatment of nosocomial infections. Because there is a lack of information on incidence of these attributes in animal commensal enterococci, we screened 160 strains originating from feces of clinically healthy dogs in Eastern Slovakia (n = 105). The predominant species were Enterococcus faecium (57.5%) followed by Enterococcus faecalis (21.9%), and Enterococcus hirae (17.5%), while Enterococcus casseliflavus (1.9%) and Enterococcus mundtii (1.2%) rarely occurred. Among the tested antibiotics, gentamicin (high level) was the most effective drug against canine enterococci (95% of isolates were sensitive). In contrast, the highest resistance recorded (71.9%) was to teicoplanin. PCR screening showed the highest incidence of virulence genes in E. faecalis species. The most frequently detected were genes encoding adhesins efa Afm and efa Afs and sex pheromone cpd. IS16 gene, a marker specific for hospital strains, appeared in nine E. faecium strains. No strain was positive for DNase activity, 8.8% of the isolated strains showed gelatinase activity, and almost 100% strains produced tyramine. It seems commensal-derived enterococci from dogs could also to some extent be potential reservoir of risk factors for other microbiota or organisms.
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References
Agudelo Higuita NI, Huycke MM (2014) Enterococcal disease, epidemiology, and implications for treatment. In: Gilmore MS, Clewell DB, Ike Y, Shankar N (eds) Enterococci: from commensals to leading causes of drug-resistant infection. Massachusetts Eye and Ear Infirmary, Boston, pp 1–27
Arias CA, Murray BE (2012) The rise of the Enterococcus beyond vancomycin resistance. Nat Rev Microbiol 10:266–278
Baele M, Chiers K, Davriese LA, Smith HE, Wisselink HJ, Vaneechoutte M, Haesebrouck F (2001) The gram-positive tonsillar and nasal flora of piglets before and after weaning. J Appl Microbiol 91:997–1003
Bessède E, Angla-gre M, Delagarde Y, Sep Hieng S, Ménard A, Mégraud F (2011) Matrix-assisted laser-desorption/ionization BIOTYPER: experience in the routine of a university hospital. Clin Microbiol Infect 17:533–538
Bover-Cid S, Holzapfel WH (1999) Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53:33–41
Bybee SN, Scorza AV, Lappin MR (2011) Effect of the probiotic Enterococcus faaecium SF68 on presence of diarrhea in cats and dogs housed in a animal shelter. J Vet Intern Med 25:856–860
Cattoir V, Leclercq R (2013) Twenty-five years of shared life with vancomycin-resistant enterococci: is it time to divorce? J Antimicrob Chemother 68:731–742
Cox CR, Coburn PS, Gilmore MS (2005) Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Curr Prot Pept Sci 6:77–84
Damborg P, Top J, Hendrickx APA, Dawson S, Willems RJ, Guardabassi L (2009) Dogs are a reservoir of ampicillin-resistant Enterococcus faecium lineages associated with human infections. Appl Environ Microbiol 75:2360–2365
Drahovská H, Slobodníková L, Kocínová D, Seman M, Končeková R (2004) Antibiotic resistance and virulence factors among clinical and food enterococci isolated in Slovakia. Folia Microbiol 49:763–768
Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67:1628–1635
EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) (2012) Guidance on the safety assessment of Enterococcus faecium in animal nutrition. The EFSA J 10:2682 (10 pages)
EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) (2014) Scientific opinion on the safety and efficacy of Oralin® (Enterococcus faecium) as a feed additive for calves for rearing, piglets, chickens for fattening, turkeys for fattening and dogs. The EFSA J 12:3727
Euzéby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the Internet (URL: http://www.bacterio.net/enterococcus.html, last update 2016). Int J Syst Bacteriol 64:590–592
Fisher K, Phillips P (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiol 155:1749–1757
Guardabassi L, Schwarz S, Lloyd DH (2004) Pet animals as reservoirs of antimicrobial-resistant bacteria. J Antimicrob Chemother 54:321–332
Iseppi R, Messi P, Anacarso I, Bondi M, Sabia C, Condò C, de Niederhausern S (2015) Antimicrobial resistance and virulence traits in Enterococcus strains isolated from dogs and cats. New Microbiol 38:369–378
Jackson CR, Fedorka-Cray PJ, Davis JA, Barrett JB, Frye JG (2009) Prevalence, species distribution and antimicrobial resistance of enterococci isolates from dogs and cats in the United States. J Appl Microbiol 107:1269–1278
Jiménez E, Ladero V, Chico E, Maldonado-Barragán A, López M, Martín V, Fernández L, Fernández M, Álvarez MA, Torres C, Rodríguez JM (2013) Antibiotic resistance, virulence determinants and production of biogenic amines among enterococci from ovine, feline, canine, porcine and human milk. BMC Microbiol 13:288
Kajihara T, Nakamura S, Iwanaga N, Oshima K, Takazono T, Miyazaki T, Izumikawa K, Yanagihara K, Kohno N, Kohno S (2015) Clinical characteristics and risk factors of enterococcal infections in Nagasaki, Japan: a retrospective study. BMC Infect Dis 15:426
Kataoka Y, Umino Y, Ochi H, Harada K, Sawada T (2014) Antimicrobial susceptibility of enterococcal species isolated from antibiotic-treated dogs and cats. J Vet Med Svi 76:1399–1402
Klare I, Konstabel C, Mueller-Bertling S, Werner G, Strommenger B, Kettlitz C, Borgmann S, Schulte B, Jonas D, Serr A, Fahr AM, Eigner U, Witte W (2005) Spread of ampicillin/vancomycin-resistant Enterococcus faecium of the epidemic-virulent clonal complex-17 carrying the genes esp and hyl in German hospitals. Eur J Clin Microbiol Infect Dis 24:815–825
Kwon KH, Moon BY, Hwang SY, Park YH (2012) Detection of CC17 Enterococcus faecium in dogs and a comparison with human isolates. Zoonoses Public Health 59:375–378
Ladero V, Fernández M, Alvarez MA (2009) Isolation and identification of tyramine-producing enterococci from human faecal samples. Can J Microbiol 55:215–218
Ladero V, Fernández M, Calles-Enriquez M, Sánches-Llana E, Canedo E, Martin MC, Alvarez MA (2012) Is the production of the biogenic amines tyramine and putrescine a species-level trait in enterococci? Food Microbiol 30:132–138
Lebreton F, Willems RJL, Gilmore MS (2014) Enterococcus diversity, origins in nature and gut colonization. In: Gilmore MS, Clewell DB, Ike Y, Shankar N (eds) Enterococci: from commensals to leading causes of drug resistant infection (internet). Massachusetts Eye and Ear Infirmary, Boston, pp 1–46
Lindenstrau AG, Pavlovic M, Bringmann A, Behr J, Ehrmann MA, Vogel RF (2011) Comparison of genotypic and phenotypic cluster analyses of virulence determinants and possible role of CRISPR elements towards their incidence in Enterococcus faecalis and Enterococcus faecium. Syst Appl Microbiol 34:553–560
Lopes MF, Simões AP, Tenreiro R, Marques JJ, Crespo MT (2006) Activity and expression of a virulence factor, gelatinase, in dairy enterococci. J Food Microbiol 112:208–214
MPSR (2016) Stav mikrobiálne rezistencie v Slovenskej republike. 53 strán. ISBN 978–80–89738-07-6
Performance standards for antimicrobial susceptibility testing: 25th Informational supplement (2015) CLSI M100-S25. Clinical and Laboratory Standards Institute. Wayne, PA, USA
Rubinstein E, Keynan Y (2013) Vancomycin-resistant enterococci. Crit Care Clin 29:841–852
Semedo T, Santos MA, Lopes MF, Marques JJF, Crespo MT, Tenreiro R (2003) Virulence factors in food, clinical and reference enterococci: a common trait in the genus? Syst Appl Microbiol 26:13–22
Sung JML, Lindsay JA (2007) Staphylococcus aureus strains that are hypersusceptible to resistance gene transfer from enterococci. Antimicrob Agents Chemother 51:2189–2191
Vu J, Carvalho J (2011) Enterococcus: review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology. Front Biol 6:357–366
Werner G, Fleige C, Geringer U, van Schaik W, Klare I, Witte W (2011) IS element IS16 as a molecular screening tool to identify hospital-associated strains of Enterococcus faecium. BMC Infect Dis 11:80
Wong C, Epstein SE, Westropp JL (2015) Antimicrobial susceptibility patterns in urinary tract infections in dogs (2010–2013). J Vet Inter Med 29:1045–1052
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The study was funded by the Slovak Scientific Agency VEGA (no. 2/0012/16).
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Kubašová, I., Strompfová, V. & Lauková, A. Safety assessment of commensal enterococci from dogs. Folia Microbiol 62, 491–498 (2017). https://doi.org/10.1007/s12223-017-0521-z
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DOI: https://doi.org/10.1007/s12223-017-0521-z