Presence of genes encoding aminoglycoside-modifying enzyme (AME) and virulence factors in high-level aminoglycoside-resistant (HLAR) Enterococcus strains isolated from retail chicken meat in Turkey


Veröffentlicht: Jan 18, 2024
Aktualisiert: 2024-01-18
M Yalçın
B Özden Tuncer
D Akpınar Kankaya
Y Tuncer
https://orcid.org/0000-0002-2075-5027
Abstract

In this study, the presence of aminoglycoside-modifying enzyme (AME) and virulence factor genes were investigated in previously isolated 32 high-level aminoglycoside-resistant (HLAR) Enterococcus strains isolated from retail chicken meat in Turkey. At least one AME-encoding gene was detected in HLAR enterococci by polymerase chain reaction (PCR). The ant(6ʹ)-Ia was identified as the most prevalent (87.5%, 28/32) AME gene. The aph(3ʹ)-IIIa (78.13%, 25/32), ant(4ʹ)-Ia (68.75%, 22/32), aph(2ʹʹ)-Ib (62.5%, 20/32), aac(6ʹ)-Ie-aph(2ʹʹ)-Ia (21.88%, 7/32) and aph(2ʹʹ)-Ic (9.38%, 3/32) are the other detected AME-encoding genes in strains. The aph(2ʹʹ)-Id was found in none of the HLAR strains. The aph(2ʹʹ)-Ib and ant(6ʹ)-Ia were identified as the most frequently AME-encoding genes in high-level gentamicin-resistant (HLGR) and high-level streptomycin-resistant (HLSR) strains, respectively. Among the 32 HLAR strains, only E. faecalis MSE61.1 and E. avium MSE63.1 were found capable of hydrolyzing gelatine. All HLAR strains showed α-hemolytic activity except E. durans MG13.4 and E. casseliflavus MGM111.1, which were exhibited β- and γ-hemolytic activity, respectively.  It was determined that all HLAR strains, except E. durans MGE13.1 and MGE63.1, contain at least one virulence factor gene. The efaAfm (87.5%, 28/32), acm (65.63%, 21/32) and gelE (37.5%, 12/32) were found to be the most prevalent virulence factor genes. HLAR enterococci strains that have the virulence factor genes may pose a risk to consumer health.

Article Details
  • Rubrik
  • Research Articles
Downloads
Keine Nutzungsdaten vorhanden.
Literaturhinweise
Abauelnaga M, Lamas A, Quintela-Baluja M, Osman M, Miranda JM,
Cepeda A, Franco CM (2016) Evaluation of the extent of virulence
factors and antibiotic resistance in enterococci isolated from fermented and unfermented foods. Ann Microbiol 66:577-585.
Adifon E, Tuncer Y (2019) Investigation of virulence factors using phenotypic and genotypic methods in high-level aminoglycoside resistant
enterococci isolated from cheese. Gıda, 44(4):719-732.
Akpınar Kankaya D and Tuncer Y (2022) Detection of virulence factors,
biofilm formation and biogenic amine production in vancomycin‐resistant lactic acid bacteria (VRLAB) isolated from foods of animal
origin. J Food Process Preserv 46:e16423.
Amini F, Krimpour HA, Ghaderi M, Vaziri S, Ferdowsi S, Azizi M, Amini
S (2018) Prevalence of aminoglycoside resistance genes in Enterococcus strains in Kermanshah, Iran. Iran J Med Sci 43(5):487-493.
Arias CA and Murray BE (2012) The rise of the Enterococcus: beyond
vancomycin resistance. Nat Rev Microbiol 10:266-278.
Ben Belgacem Z, Abriouel H, Omar NB, Lucas R, Martinez-Canamero
M, Galvez A, Manai M (2010) Antimicrobial activity, safety aspects,
and some technological properties of bacteriocinegenic Enterococcus faecium from artisanal Tunusian fermented meat. Food Control
(4):462-470.
Bortolaia V, Espinosa-Gongora C, Guardabassi L (2016) Human health
risks associated with antimicrobial-resistant enterococci and Staphylococcus aureus on poultry meat. Clin Microbiol Infect 22(2):130-
Camargo ILBC, Gilmore MS, Darini ALC (2006) Multilocus sequence
typing and analysis of putative virulence factors in vancomycin-resistant and vancomycin-sensitive Enterococcus faecium isolates from
Brazil. Clin Microbiol Infect 12(11):1123-1130.
Cancilla MR, Powell LB, Hillier AJ, Davidson BE (1992) Rapid genomic
fingerprinting of Lactococcus lastis strains by arbitrarily primed polymerase chain reaction with 32P and fluorescent labels. Appl Environ
Microbiol 58(5):1772-1775.
Cariolato D, Andrighetto C, Lombardi A (2008) Occurrence of virulence
factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North
Italy. Food Control 19(9):886-892.
Chajęcka-Wierzchowska W, Zadernowska A, Łaniewska-Trokenheim
Ł (2016) Diversity of antibiotic resistance genes in Enterococcus strains isolated from ready-to-eat meat products. J Food Sci
(11):M2799-M2807.
Chajęcka-Wierzchowska W, Zadernowska A, Łaniewska-Trokenheim
Ł (2017) Virulence factors of Enterococcus spp. presented in food.
LWT-Food Sci Technol 75:670-676.
Chajęcka-Wierzchowska W, Zadernowska A, Mónica García-Solache M
(2020) Ready-to-eat dairy products as a source of multidrug-resistant Enterococcus strains: phenotypic and genotypic characteristics. J
Dairy Sci 103(5):4068-4077.
Choi J-M and Woo G-J (2013) Molecular characterization of high-level
gentamicin-resistant Enterococcus faecalis from chicken meat in Korea. Int J Food Microbiol 165(1):1-6.
Donabedian SM, Thal LA, Hershberger E, Perri MB, Chow JW, Bartlett
P, Jones R, Joyce K, Rossiter S, Gay K, Johnson J, Mackinson C,
Debess E, Madden J, Angulo F, Zervos MJ (2003) Molecular characterization of gentamicin-resistant Enterococci in the United States:
evidence of spread from animals to humans through food. J Clin Microbiol 41(3):1109-1113.
Eaton TJ and Gasson MJ (2001) Molecular screening of Enterococcus
virulence determinants and potential for genetic exchange between
food and medical isolates. Appl Environ Microbiol 67(4):1628-1635.
Guzman Prieto AM, van Schaik W, Rogers MRC, Coque TM, Baquero
F, Corander J, Willems RJL (2016) Global emergence and dissemination of enterococci as nosocomial pathogens: attack of the clones?
Front Microbiol 7:788.
Han D, Unno T, Jang J, Lim K, Lee SN, Ko G, Sadowsky MJ, Hur HG
(2011) The occurrence of virulence traits among high-level aminoglycosides resistant Enterococcus isolates obtained from feces of
humans, animals, and birds in South Korea. Int J Food Microbiol
(3):387-392.
Harada T, Mito Y, Otsuki K, Murase T (2004) Resistance to gentamicin
and vancomycin in enterococcal strains isolated from retail broiler
chickens in Japan. J Food Prot 67(10):2292-2295.
Hollenbeck BL and Rice LB (2012) Intrinsic and acquired resistance
mechanisms in enterococcus. Virulence 3(5):421-433.
Hugas M, Garriga M, Aymerich MT (2003) Functionalty of enterococci in
meat products. Int J Food Microbiol 88:223-233.
Inoğlu Z and Tuncer Y (2013) Safety assessment of Enterococcus faecium
and Enterococcus faecalis strains isolated from Turkish tulum cheese.
J Food Saf 33:369-377.
Jackson CR, Fedorka-Cray PJ, Barrett JB, Ladely SR (2004) Genetic relatedness of high-level aminoglycoside-resistant enterococci isolated
from poultry carcasses. Avian Dis 48(1):100-107.
Jaimee G and Halami PM (2016) High level aminoglycoside resistance
in Enterococcus, Pediococcus and Lactobacillus species from farm
animals and commercial meat products. Ann Microbiol 66:101-110.
Kang HJ, Yoon S, Kim K, Lee YJ (2021) Characteristics of high-level
aminoglycoside resistant Enterococcus faecalis isolated from bulk
tank milk in Korea. Animals 11(6):1724.
Kim YB, Seo KH, Son SH, Noh EB, Lee YJ (2019) Genetic characterization of high-level aminoglycoside-resistant Enterococcus faecalis
and Enterococcus faecium isolated from retail chicken meat. Poult
Sci 98:5981-5988.
Kim Y-J, Park J-H, Seo KH (2018) Comparison of the loads and antibiotic-resistance profiles of Enterococcus species from conventional and
organic chicken carcasses in South Korea. Poult Sci 97:271-278.
Li W, Li J, Wei Q, Hu Q, Lin X, Chen M, Ye R, Lv H (2015) Characterization of aminoglycoside resistance and virulence genes among
Enterococcus spp. isolated from a hospital in China. Int J Environ Res
Public Health 12(3):3014-3025.
Niu H, Yu H, Hu T, Tian G, Zhang L, Guo X, Hu H, Wang Z (2016)
The prevalence of aminoglycoside-modifying enzyme and virulence
genes among enterococci with high-level aminoglycoside resistance
in Inner Mongolia, China. Braz J Microbiol 47(3):691-696.
M’hir S, Minervini F, Di Cagno R, Chammem N, Hamdi M (2012) Technological, functional and safety aspects of enterococci in fermented
vegetable products: a mini-review. Ann Microbiol 62:469-481.
Nowakiewicz A, Ziόlkowska G, Trościańczyk A, Zieba P, Gnat S (2017)
Determination of resistance and virulence genes in Enterococcus faecalis and E. faecium strains isolated from poultry and their genotypic
characterization by ADSRRS-fingerprinting. Poult Sci 96(4):986-
Onaran B, Göncüoğlu M, Bilir Ormancı FS (2019) Antibiotic resistance
profiles of vancomycin resistant enterococci in chicken meat samples.
Ankara Üniv Vet Fak Derg 66(4):331-336.
Özdemir R and Tuncer Y (2020) Detection of antibiotic resistance profiles
and aminoglycoside-modifying enzyme (AME) genes in high-level
aminoglycoside-resistant (HLAR) enterococci isolated from raw milk
and traditional cheeses in Turkey. Mol Biol Rep 47(3):1703-1712.
Padmasini E, Padmaraj R, Ramesh SS (2014) High level aminoglycoside
resistance and distribution of aminoglycoside resistant genes among
clinical isolates of Enterococcus species in Chennai, India. Sci World
J Article ID:329157.
Peyvasti VS, Mobarez AM, Shahcheraghi F, Khoramabadi N, Rahmati
NR, Doust RH (2020) High-level aminoglycoside resistance genes among Enterococcus spp. clinical isolates in Tehran, Iran. J Glob Antimicrob Resist
:318-323.
Ramin B, Asadpour L, Tehrani HF, Amirmozafari N (2018) Detection and
distribution of various HLAR gene in Enterococcus faecalis and Enterococcus faecium by multiplex-PCR. Mod Med Lab J 1(2):68-76.
Ramirez MS and Tolmasky ME (2010) Aminoglycoside modifiying enzymes. Drug Resist Updates 13(6):151-171.
J HELLENIC VET MED SOC 2023, 74 (4
Am häufigsten gelesenen Artikel dieser/dieses Autor/in