Investigation of genetic relatedness, antimicrobial resistance, biofilm formation, biofilm-related virulence genes and integron-related genes of Stenotrophomonas maltophilia isolates obtained from bovine milk samples with mastitis Characteristics of Stenotrophomonas maltophilia isolates.


Δημοσιευμένα: Oct 18, 2023
Εκδόσεις:
2023-10-18 (1)
F Ocak
S Turkyilmaz
https://orcid.org/0000-0002-1363-4534
Περίληψη

Treatment of infections caused by opportunistic pathogenic Stenotrophomonas maltophilia is complicated by the bacterium's ability to produce biofilms and high antibiotic resistance. This study aimed to investigate the prevalence of genetic relatedness, antimicrobial resistance, biofilm formation, biofilm genes associated with virulence and integron genes among isolates of S. maltophilia recovered from bovine milk with subclinical mastitis. In this study, bacterial identification was performed using conventional methods. While using the smeT gene-based Polymerase Chain Reaction (PCR) to confirm the species-level identification of isolates; PCR was also used to detect virulence and integron genes, too. The quantitative Microplate Test (MP) method was used to determine the phenotypic biofilm production capacity of the isolates. The resistance patterns of the isolates against 9 antibiotics belonging to 9 antimicrobial families were examined using the disk diffusion method. Isolates resistant to at least three drug classes from various antimicrobial drug classes were defined as multi-drug resistant (MDR). The genetic linkage of S. maltophilia isolates was investigated by Enterobacterial Repetitive Intragenic Consensus (ERIC) PCR. The Chi-Square (χ2) test was used to compare the relationship between the biofilm-forming capacity of the isolates with the prevalence of biofilm-associated virulence genes and integron genes with MDR. In the study, a total of 312 milk samples with subclinical mastitis were taken from 27 farms. Ten isolates from five farms were phenotypically and genotypically identified as S. maltophilia. All isolates were resistant to cefepime and imipenem. While 70% of the isolates were MDR; 80% carried one of the integron genes. By the MP test, the phenotypically biofilm-forming capacity identified in isolates was detected at 80%. The prevalence of the studied virulence genes was rpfF 60%, rmlA 70%, spgM and smf1 80%. There was no significant relationship between the biofilm-forming capacity of the isolates with the prevalence of biofilm-associated virulence genes and MDR with integron genes. S. maltophilia isolates were detected simply and quickly, using PCR based on the smeT gene, from bovine milk samples for the first time in Turkey. In the UPGMA analysis performed in the PyElph 1.4 program, a total of 5 genotypes were found, 2 single and 3 multiple according to 18% similarity coefficient. ERIC-PCR can be useful in identifying S. maltophilia isolates with epidemic potential.

Λεπτομέρειες άρθρου
  • Ενότητα
  • Άρθρα
Λήψεις
Τα δεδομένα λήψης δεν είναι ακόμη διαθέσιμα.
Αναφορές
Abbassi MS, Touati A, Achour W, Cherif A, Jabnoun S., Khrouf N. and
Ben Hassen A (2009) Stenotrophomonas maltophilia responsible for
respiratory infections in neonatal intensive care unit: Antibiotic sus
ceptibility and molecular typing. Pathol. Biol. 57:363-36.
Aggarwal S (2008) Techniques in Molecular Biology. Lucknow: Interna
tional Book Distributing CO. Short tandem repeat genotyping. pp:
-134.
Akrami F, Rajabnia M and Pournajaf A (2019) Resistance integrons; A
mini review. Caspian J. Intern. Med. 1: 370-376.
Alonso A and Martínez JL (2000) Cloning and characterization of
SmeDEF, a novel multidrug efflux pump from Stenotrophomonas
maltophilia. Antimicrob Agents. Chemother. 44:3079-3086.
Amoli RI, Nowroozi J, Sabokbar A and Rajabniya R (2017) Isolation of
Stenotrophomonas maltophilia from clinical samples: An investiga
tion of patterns motility and production of melanin pigment. Asian
Pac. J. Trop. Biomed. 7:826-830.
Azimi A, Aslanimehr M, Yaseri M, Shadkam M and Douraghi M (2020).
Distribution of smf-1, rmlA, spgM and rpfF genes among Stenotro
phomonas maltophilia isolates in relation to biofilm-forming capaci
ty. J Glob. Antimicrob. Resist. 23:321-326.
Bass L, Liebert CA, Lee MD, Summers AO, White DG, Thayer SG and
Maurer JJ (1999) Incidence and characterization of integrons, genet
ic elements mediating multiple-drug resistance, in avian Escherichia
coli. Antimicrob. Agents Chemother. 43:2925-2929.
Bostanghadiri N, Ghalavand Z, Fallah F, Yadegar A, Ardebili A, Tarashi
S, Pournajaf, A, Mardaneh J, Shams S and Hashemi A (2019) Charac
terization of phenotypic and genotypic diversity of Stenotrophomon
as maltophilia strains isolated from selected hospitals in Iran. Front.
Microbiol. 10:1-12.
Brooke JS (2014) New strategies against Stenotrophomonas maltophilia:
a serious worldwide intrinsically drug-resistant opportunistic patho
gen. Expert Rev. Anti. Infect. Ther. 12:1-4.
Carmody LA, Spilker T and LiPuma J (2011) Reassessment of Stenotro
phomonas maltophilia phenotype. J. Clin. Microbiol. 49:1101-1103.
Celikel IU (2012) Isolation and characterization of Stenotrophomonas
maltophilia from animals and their environment. PhD thesis, Ankara
University Health Science Institute, Ankara.
Clinical and Laboratory Standards Institute (CLSI) (2020) Document.
Performance Standards for Antimicrobial Disk and Dilution Suscep
tibility Tests for Bacteria Isolated from Animals, Approved Standard,
M100-30rd ed., Wayne, USA.
Cruz-Córdova A, Mancilla-Rojano J, Luna-Pineda VM, Escalona-Ven
egas G, Cázares-Domínguez V, Ormsby C, Franco-Hernández I,
Zavala-Vega S, Hernández MA, Medina-Pelcastre M, Parra-Ortega
I, Rosa-Zamboni DDl, Ochoa SA and Xicohtencatl-Cortes J (2020)
Molecular epidemiology, antibiotic resistance, and virulence traits of
Stenotrophomonas maltophilia strains associated with an outbreak in
a Mexican tertiary care. Hospital Front Cell Infect. Microbiol. 10:50.
Denton M and Kerr KG (1998) Microbiological and clinical aspects of
infection associated with Stenotrophomonas maltophilia. Clin. Mi
crobiol. Rev. 11:57-80.
Edwards U, Rogall T, Blöcker H, Emde M and Böttger EC (1989) Iso
lation and direct complete nucleotide determination of entire genes.
Characterization of a gene coding for 16S ribosomal RNA. Nucleic
Acids Res. 17:7843-7853.
Falagas ME, Kastoris AC, Vouloumanou EK and Dimopoulos G (2009)
Community-acquired Stenotrophomonas maltophilia infections: a
systematic review. Eur. J. Clin. Microbiol. Infect. Dis. 28:719-730.
Fouhy Y, Scanlon K, Schouest K, Spillane C, Crossman L, Avison MB,
Ryan RP and Dow JM (2007) Diffusible signal factor-dependent cell
cell signaling and virulence in the nosocomial pathogen Stenotro
phomonas maltophilia. J. Bacteriol. 189:4964-4968.
Gallo SW, Figueiredo TP, Bessa MC, Pagnussatti VE, Ferreira CAS
and Oliveira SD (2016) Isolation and characterization of Stenotro
phomonas maltophilia isolates from a Brazilian hospital. Microb.
Drug Resist. 22:688-695.
Goldstein C, Lee MD, Sanchez S, Hudson C, Phillips B, Register B,
Grady M, Liebert C, Summers AO, White DG and Maurer JJ (2001)
Incidence of class 1 and 2 integrases in clinical and commensal bac
teria from livestock, companion animals, and exotics. Antimicrob.
Agents Chemother. 45:723-726.
Gozel MG, Celik C and Elaldi N (2015) Stenotrophomonas maltophilia
infections in adults: primary bacteremia and pneumonia. Jundishapur
J. Microbiol. 8:e23569.
Jayol A, Corlouer C, Haenni M, Darty M, Maillard K, Desroches M,
Lamy B, Jumas-Bilak E, Madec J and Decousser J (2018) Are ani
mals a source of Stenotrophomonas maltophilia in human infections?
Contributions of a nationwide molecular study. Eur. J. Clin. Microbi
ol. Infect. Dis. 37:1039-1045.
Johnson EH, Al-Busaidy R and Hameed MS (2003) An outbreak of
lymphadenitis associated with Stenotrophomonas (Xanthomonas)
maltophilia in Omani goats. J. Vet. Med. 50:102-104.
Kerr KG, Denton M, Todd N, Corps CM, Kumari P and Hawkwy PM
(1996) A new selective differential medium for isolation of Stenotro
phomonas maltophilia. Eur. J. Clin. Microbiol. Infect. Dis. 15:607
Kralova-Kovarikova S, Husnik R, Honzak D, Kohout P. and Fictum P
(2012) Stenotrophomonas maltophilia urinary tract infections in three
dogs: a case report. Vet. Med. 57:380-383.
Krumpernam PH (1983) Multiple antibiotic resistance indexing Esche
richia coli to identify risk sources of faecal contamination of foods.
Appl. Environ. Microbiol. 46:165-170.
Madi H, Lukic J, Vasiljevic Z, Biočanin M, Kojić M., Jovčić, B and Loz
J (2016) Genotypic and phenotypic characterization of Stenotro
phomonas maltophilia strains from a pediatric tertiary care hospital
in Serbia. PLoS One. 31:11, e0165660.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske
CG, Harbart S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Pater
son DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT
and Monnet DL (2012) Multidrug-resistant, extensively drug resis
tant and pandrug resistant bacteria: an international expert proposal
for interim standard definitions for acquired resistance. Clin. Micro
biol. Infect. 18:268-281.
Maniatis T and Sambrook J (1989) Molecular Cloning, A Laboratory
Manual, Cold Spring Harbor Laboratory Press, USA.
Muir P, Oldenhoff WE, Hudson AP, Manley PA, Schaefer SL, Markel MD
and Hao Z (2007) Detection of DNA from a range of bacterial spe
cies in the knee joints of dogs with inflammatory knee arthritis and
associated degenerative anterior cruciate ligament rupture. Microb.
Pathog. 42:47-55.
Murray PR (2007) Manual of Clinical Microbiology. 9th ed. Washington,
DC: ASM Press.
Nam HM, Lim SK, Kang HM, Kim JM, Moon JS, Jang KC, Kim JM, Joo
YS and Jung SC (2009) Prevalence and antimicrobial susceptibility
of gram-negative bacteria isolated from bovine mastitis between 2003
and 2008 in Korea. J. Dairy Sci. 92:2020-2026.
Nicoletti M, Iacobino A, Prosseda G, Fiscarelli E, Zarrilli R, De Carolis E,
Petrucca A, Nencioni L, Colonna B and Casalino M (2011) Stenotro
phomonas maltophilia strains from cystic fibrosis patients: genomic
variability and molecular characterization of some virulence determ-nants. Int. J. Med. Microbiol. 301:34-43.
Ohnishi M, Sawada T, Marumo K, Harada K, Hirose K., Shimizu A, Ha
yashimoto M, Sato R, Uchida N and Kato H (2012) Antimicrobial
susceptibility and genetic relatedness of bovine Stenotrophomonas
maltophilia isolates from a mastitis outbreak. Lett. Appl. Microbiol.
:572-576.
Okuno NT, Freire IR, Segundo RTRS, Silva CR and Marin VA (2018)
Polymerase chain reaction assay for detection of Stenotrophomonas
maltophilia in cheese samples based on the smeT gene. Curr. Micro
biol. 75:1555-1559.
Olsen I (2015) Biofilm-specific antibiotic tolerance and resistance. Eur. J.
Clin. Microbiol. Infect. Dis. 34:877-886.
Pavel BA and Vasile CI (2012) PyElph - a software tool for gel images
analysis and phylogenetics. B.M.C. Bioinform. 13:1-6.
Petridou E, Filioussis G, Karavanis E and Kritas SK (2010) Stenotro
phomonas maltophilia as a causal agent of pyogranulomatous hepa
titis in a buffalo (Bubalus bubalis). J. Vet. Diagn. Invest. 22:772-774.
Pompilio A, Pomponio S, Crocetta V, Gherardi G, Verginelli F., Fiscarelli
E, Dicuonzo G, Savini V, D’Antonio D. and Bonaventura G (2011)
Phenotypic and genotypic characterization of Stenotrophomonas
maltophilia isolates from patients with cystic fibrosis: genome diver
sity, biofilm formation, and virulence. B.M.C. Microbiol. 11:159.
Quinn PJ, Markey B.K., Leonard FC, FitzPatrick ES, Fanning S and Har
tigan PJ (2011) Veterinary Microbiology and Microbial Disease. Sec
ond Edition, Blackwell Science Ltd, Oxford, UK.
Sader HS, Pignatari AC, Frei R., Hollis RJ and Jones RN (1994) Pulsed
f
ield gel electrophoresis of restriction-digested genomic DNA and
antimicrobial susceptibility of Xanthomonas maltophilia strains from
Brazil, Switzerland and the USA. J. Antimicrob. Chemother. 33:615
Schable B, Villarino ME, Favero MS and Miller JM (1991). Application
of multilocus enzyme electrophoresis to epidemiologic investiga
tions of Xanthomonas maltophilia. Infect. Control Hosp. Epidemiol.
:63-67.
Stepanovic S, Vukovic D, Dakic I, Savic B and Svabic-Vlahovic MA
(2000) Modified microtiter-plate test for quantification of staphylo
coccal biofilm formation. J. Microbiol. Methods. 40:175-179.
Stephanie WG and Locosque RP (2013) A specific polymerase chain re
action method to identify Stenotrophomonas maltophilia. Mem. Inst.
Oswaldo Cruz. 108:390-391.
Ucan US, Mohammed BO and Yigit M (2019) Antibiotic resistance of
Stenotrophomonas maltophilia strains isolated from horses. Kocatepe
Vet. J. 12:384-388.
Versalovic J, Koeuth T and Lupski JR (1991) Distribution of repetitive
DNA sequences in eubacteria and application to fingerprinting of bac
terial genomes. Nucleic Acids Res. 19:6823-68231.
Wilson LA and Sharp PM (2006) Enterobacterial repetitive intergenic
consensus (ERIC) sequences in Escherichia coli: Evolution and im
plications for ERIC-PCR. Mol. Biol. Evol. 23:1156-1156.
Zhang L, Li XZ and Pool K (2001) SmeDEF multidrug efflux pump con
tributes to intrinsic multidrug resistance in Stenotrophomonas malto
philia. Antimicrob. Agents Chemother. 45:3497-3503.
Zheng D, Alm EW, Stahl DA and Raskin L (1996) Characterization of
universal small-subunit rRNA hybridization probes for quantitative
molecular microbial ecology studies. Appl. Environ. Microbiol.
:4504-4513.
Zhuo C, Zhao QY and Xiao SN (2014) The impact of spgM, rpfF, rmlA
gene distribution on biofilm formation in Stenotrophomonas malto
philia. PLoS One. 9:e108409.
Τα περισσότερο διαβασμένα άρθρα του ίδιου συγγραφέα(s)