Fosfomycin Resistant Enterobacterales IsolatedFrom Chicken Meat in Turkey

PDF (English)
Publicado: Apr 18, 2023
Actualizado: 2023-04-18
Versiones:
2023-04-18 (2)
DOI: https://doi.org/10.12681/jhvms.28245
S Al
Erciyes University
https://orcid.org/0000-0001-8255-3802
HB Dişli
Hatay Mustafa Kemal University
C Kurekci
Hatay Mustafa Kemal University
https://orcid.org/0000-0002-6442-2865
Resumen

This study was conducted to obtain the relative prevalence of fosfomycin resistant (FOSr) Enterobacterales in raw chicken meat samples in Turkey. Samples (n=85) were enriched in non-selective media and transferred to MacConkey agar plates containing FOS and glucose-6-phosphate. As a result, FOSr Enterobacterales isolates were detected by a selective method in 27% of raw chicken meat samples (n=23) and identified as Escherichia coli (21/26), Klebsiella oxytoca (2/26), Escherichia vulneris (1/26), Raoultella terrigena (1/26) and Kluyvera intermedia (1/26). PFGE analysis showed 16 different band patterns in Escherichia spp. isolates (n=22) based on the 85% similarity. The minimum inhibitory concentration for FOS against all isolates was determined to be ≥64 mg/L. In addition, the highest rate of resistance was determined for nalidixic acid (72.7%), ampicillin (68.2%), tetracycline (59.1%), trimethoprim-sulfamethoxazole (54.5%), and chloramphenicol (59.1%) among all Escherichia isolates. PCR screening and sequencing identified the presence of fosA4 and fosA3 genes in ten (47.6%) and seven (33.3%) E. coli isolates, respectively. The fosA3 gene has also appeared in K. intermedia, and R. terrigena isolates.  Only two E. coli isolates were positive for the blaCTX-M-55 gene, whereas the aac(6')-Ib-cr gene was identified in eight E. coli and one K. intermedia isolates. In addition, 19 different replicon types were determined by PCR-based plasmid replicon typing with IncFII (n=20) being the most common and followed by IncI1α (n=10), IncFIIS (n=8), and IncFIB (n=8). We report, to our knowledge, the first evidence on the presence of FOSr Enterobacterales isolates in raw chicken meat samples in Turkey that might be an important reservoir for FOSr organisms to humans.

Article Details
  • Sección
  • Research Articles
Creative Commons License

Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial 4.0.

Authors who publish with this journal agree to the following terms:

· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.

Descargas
Los datos de descargas todavía no están disponibles.
Citas
Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H, Fukumoto Y, Shimamoto T (2007) Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl Environ Microbiol 73(20):6686–6690. https://doi.org/10.1128/AEM.01054-07.
Benzerara Y, Gallah S, Hommeril B, Genel N, Decré D, Rottman M, Arlet G (2017) Emergence of Plasmid-Mediated Fosfomycin-Resistance Genes among Escherichia coli Isolates, France. Emerg Infect Dis 23(9):1564–1567. https://dx.doi.org/10.3201/eid2309.170560.
Biggel M, Zurfluh K, Treier A, Nüesch-Inderbinen M, Stephan R (2021) Characteristics of fosA-carrying plasmids in E. coli and Klebsiella spp. isolates originating from food and environmental samples. J Antimicrob Chemother 76(8):2004–2011. https://doi:10.1093/jac/dkab119.
Castañeda-García A, Blázquez J, Rodríguez-Rojas A (2013) Molecular mechanisms and clinical impact of acquired and intrinsic fosfomycin resistance. Antibiotics (Basel) 2(2):217–236. https://doi.org/10.3390/antibiotics2020217.
Cattoir V, Poirel L, Rotimi V, Soussy C-J, Nordmann P (2007) Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60(2):394–397. https://doi.org/10.1093/jac/dkm204.
Cavaco LM, Frimodt-Møller N, Hasman H, Guardabassi L, Nielsen L, Aarestrup FM (2008) Prevalence of quinolone resistance mechanisms and associations to minimum inhibitory concentrations in quinolone-Resistant Escherichia coli Isolated from humans and swine in Denmark. Microb Drug Resist 14(2):163–169. https://doi.org/10.1089/mdr.2008.0821.
Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) QnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and bovismorbificans strains of human origin. Antimicrob Agents Chemother 53(2):603–608. https://doi.org/10.1128/AAC.00997-08.
Chapman TA, Wu XY, Barchia I, Bettelheim KA, Driesen S, Trott D, Wilson M, Chin JJC (2006) Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarrheic swine. Appl Environ Microbiol 72(7):4782–4795. https://doi.org/10.1128/AEM.02885-05.
Chen J, Griffiths MW (1998) PCR differentiation of Escherichia coli from other gram-negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein. Lett Appl Microbiol 27(6):369–371. https://doi.org/10.1046/j.1472-765x.1998.00445.x
Chen J, Wang D, Ding Y, Zhang L, Li X (2019) Molecular Epidemiology of Plasmid-Mediated Fosfomycin Resistance Gene Determinants in Klebsiella pneumoniae Carbapenemase-Producing Klebsiella pneumoniae Isolates in China. Microb Drug Resist 25(2):251–257. https://doi.org/10.1089/mdr.2018.0137.
Chen L, Ou B, Zhang M, Chou C-H, Chang S-K, Zhu G (2021) Coexistence of fosfomycin resistance determinant fosA and fosA3 in Enterobacter cloacae isolated from pets with urinary tract infection in Taiwan. Microb Drug Resist 27(3):415–423. https://doi.org/10.1089/mdr.2020.0077.
Clermont O, Bonacorsi S, Bingen E (2000) Rapid and Simple Determination of the Escherichia coli Phylogenetic Group. Appl Environ Microbiol 66(10):4555–4558. https://doi.org/10.1128/aem.66.10.4555-4558.2000.
Clinical and Laboratory Standards Institute (CLSI) (2018a) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, M07. 11th Edition. CLSI, Wayne, PA.
Clinical and Laboratory Standards Institute (CLSI) (2018b) Performance standards for antimicrobial disk susceptibility tests, M02. 13th Edition. CLSI, Wayne, PA.
Clinical and Laboratory Standards Institute (CLSI) (2020) Performance standards for antimicrobial susceptibility testing, M100. 30th Edition. CLSI, Wayne, PA.
Cottell JL, Webber MA (2019) Experiences in fosfomycin susceptibility testing and resistance mechanism determination in Escherichia coli from urinary tract infections in the UK. J Med Microbiol 68(2):161–168. https://doi.org/10.1099/jmm.0.000901.
Demirci-Duarte S, Unalan-Altintop T, Eser OK, Cakar A, Altun B, Sancak B, Gur D (2020) Prevalence of O25b-ST131 clone and fosfomycin resistance in urinary Escherichia coli isolates and their relation to CTX-M determinant. Diagn Microbiol Infect Dis 98(1):115098. https://doi.org/10.1016/j.diagmicrobio.2020.115098.
Dijkmans AC, Zacarías NVO, Burggraaf J, Mouton JW, Wilms E, van Nieuwkoop C, Touw DJ, Stevens J, Kamerling IMC (2017) Fosfomycin: Pharmacological, clinical and future perspectives. Antibiotics (Basel) 6(4):24. https://doi.org/10.3390/antibiotics6040024.
Eschenburg S, Priestman M, Schönbrunn E (2005) Evidence that the fosfomycin target Cys115 in UDP-N-acetylglucosamine enolpyruvyl transferase (MurA) is essential for product release. J Biol Chem 280(5):3757–3763. https://doi.org/10.1074/jbc.M411325200.
Falagas ME, Athanasaki F, Voulgaris GL, Triarides NA, Vardakas KZ (2019) Resistance to fosfomycin: Mechanisms, Frequency and Clinical Consequences. Int J Antimicrob Agents 53(1):22–28. https://doi.org/10.1016/j.ijantimicag.2018.09.013.
Fillgrove KL, Pakhomova S, Schaab MR, Newcomer ME, Armstrong RN (2007) Structure and mechanism of the genomically encoded fosfomycin resistance protein, FosX, from Listeria monocytogenes. Biochemistry 46(27):8110–8120. https://doi.org/10.1021/bi700625p.
Flamm RK, Rhomberg PR, Lindley JM, Sweeney K, Ellis-Grosse EJ, Shortridge D (2019) Evaluation of the bactericidal activity of fosfomycin in combination with selected antimicrobial comparison agents tested against Gram-negative bacterial strains by using time-kill curves. Antimicrob Agents Chemother 63(5). https://doi.org/10.1128/AAC.02549-18.
Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM (2005) β-Lactamases among extended-spectrum β-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 56(1):115–121. https://doi.org/10.1093/jac/dki190.
Hendlin D, Stapley EO, Jackson M, Wallick H, Miller AK, Wolf FJ, Miller TW, Chaiet L, Kahan FM, Foltz EL, et al (1969) Phosphonomycin, a new antibiotic produced by strains of Streptomyces. Science 166(3901):122–123. https://doi.org/10.1126/science.166.3901.122.
Ho PL, Chan J, Lo WU, Law PY, Li Z, Lai EL, Chow KH (2013) Dissemination of plasmid-mediated fosfomycin resistance fosA3 among multidrug-resistant Escherichia coli from livestock and other animals. J Appl Microbiol 114(3):695–702. https://doi.org/10.1111/jam.12099.
Jiang W, Men S, Kong L, Ma S, Yang Y, Wang Y, Yuan Q, Cheng G, Zou W, Wang H (2017) Prevalence of Plasmid-mediated fosfomycin resistance gene fosA3 among CTX-M-producing Escherichia coli isolates from chickens in China. Foodborne Pathog Dis 14(4):210–218. https://doi.org/10.1089/fpd.2016.2230.
Kaase M, Szabados F, Anders A, Gatermann SG (2014) Fosfomycin susceptibility in carbapenem-resistant Enterobacteriaceae from Germany. J Clin Microbiol 52(6):1893–1897. https://doi.org/10.1128/JCM.03484-13.
Kürekci C, Osek J, Aydın M, Tekeli İO, Kurpas M, Wieczorek K, Sakin F (2019) Evaluation of bulk tank raw milk and raw chicken meat samples as source of ESBL producing Escherichia coli in Turkey: Recent insights. J Food Saf 39(2):e12605. https://doi.org/10.1111/jfs.12605.
Leinberger DM, Grimm V, Rubtsova M, Weile J, Schroppel K, Wichelhaus TA, Knabbe C, Schmid RD, Bachmann TT (2010) Integrated detection of extended-spectrum-beta-lactam resistance by DNA microarray-based genotyping of TEM, SHV, and CTX-M genes. J Clin Microbiol 48(2):460–471. https://doi.org/10.1128/JCM.00765-09.
Mendoza C, Garcia JM, Llaneza J, Mendez FJ, Hardisson C, Ortiz JM (1980) Plasmid-determined resistance to fosfomycin in Serratia marcescens. Antimicrob Agents Chemother 18(2):215–219. https://doi.org/10.1128/aac.18.2.215.
Mueller L, Cimen C, Poirel L, Descombes M-C, Nordmann P (2019) Prevalence of fosfomycin resistance among ESBL-producing Escherichia coli isolates in the community, Switzerland. Eur J Clin Microbiol Infect Dis 38(5):945–949. https://doi.org/10.1007/s10096-019-03531-0.
Nakamura G, Wachino J-I, Sato N, Kimura K, Yamada K, Jin W, Shibayama K, Yagi T, Kawamura K, Arakawa Y (2014) Practical agar-based disk potentiation test for detection of fosfomycin-nonsusceptible Escherichia coli clinical isolates producing GlutathioneS-transferases. J Clin Microbiol 52(9):3175–3179. https://doi.org/10.1128/JCM.01094-14.
Oteo J, Bautista V, Lara N, Cuevas O, Arroyo M, Fernandez S, Lazaro E, de Abajo FJ, Campos J, on behalf of the Spanish ESBL-EARS-Net Study Group (2010) Parallel increase in community use of fosfomycin and resistance to fosfomycin in extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli. J Antimicrob Chemother 65(11):2459–2463. https://doi.org/10.1093/jac/dkq346.
Pérez DS, Tapia MO, Soraci AL (2014) Fosfomycin: Uses and potentialities in veterinary medicine. Open Vet J 4(1):26–43.
Pontikis K, Karaiskos I, Bastani S, Dimopoulos G, Kalogirou M, Katsiari M, Oikonomou A, Poulakou G, Roilides E, Giamarellou H (2014) Outcomes of critically ill intensive care unit patients treated with fosfomycin for infections due to pandrug-resistant and extensively drug-resistant carbapenemase-producing Gram-negative bacteria. Int J Antimicrob Agents 43(1):52–59. https://doi.org/10.1016/j.ijantimicag.2013.09.010.
Sánchez-García JM, Sorlózano-Puerto A, Navarro-Marí JM, Gutiérrez Fernández J (2019) Evolución de la resistencia a antibióticos de microorganismos causantes de infecciones del tracto urinario: un estudio de vigilancia epidemiológica de 4 años en población hospitalaria. Rev Clin Esp 219(3):116–123. https://doi.org/10.1016/j.rce.2018.07.005
Sato N, Kawamura K, Nakane K, Wachino J-I, Arakawa Y (2013) First detection of fosfomycin resistance gene fosA3 in CTX-M-producing Escherichia coli isolates from healthy individuals in japan. Microb Drug Resist 19(6):477–482. https://doi.org/10.1089/mdr.2013.0061.
Van TTH, Chin J, Chapman T, Tran LT, Coloe PJ (2008) Safety of raw meat and shellfish in Vietnam: An analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol 124(3):217–223. https://doi.org/10.1016/j.ijfoodmicro.2008.03.029.
Wang XM, Dong Z, Schwarz S, Zhu Y, Hua X, Zhang Y, Liu S, Zhang WJ (2017) Plasmids of diverse inc groups disseminate the fosfomycin resistance gene fosA3 among Escherichia coli isolates from pigs, chickens, and dairy cows in northeast China. Antimicrob Agents Chemother 61(9). https://doi.org/10.1128/aac.00859-17.
World Organization for Animal Health (OIE) (2019) OIE list of antimicrobial agents of veterinary importance. https://www.oie.int/en/document/a_oie_list_antimicrobials_june2019/ Access date: August 2021.
Yang X, Liu W, Liu Y, Wang J, Lv L, Chen X, He D, Yang T, Hou J, Tan Y, Xing L, Zeng Z, Liu JH (2014) F33: A-: B-, IncHI2/ST3, and IncI1/ST71 plasmids drive the dissemination of fosA3 and bla CTX-M-55/-14/-65 in Escherichia coli from chickens in China. Front Microbiol 5. https://doi.org/10.3389/fmicb.2014.00688.
Zurfluh K, Treier A, Schmitt K, Stephan R (2020) Mobile fosfomycin resistance genes in Enterobacteriaceae-An increasing threat. Microbiologyopen 9(12). https://doi.org/10.1002/mbo3.1135.