Antibiotic resistance and distribution of SodCI, sopE, sefA genes among Salmonella enteric serotype Enteritidis isolates from poultry


L. V. EKATERINIADOU (Λ.Β. ΑΙΚΑΤΕΡΙΝΙΑΔΟΥ)
E. BOUKOUVALA (Ε. ΜΠΟΥΚΟΥΒΑΛΑ)
R. M. PAPI (Ρ.Μ. ΠΑΠΗ)
A. ZDRAGAS (Α. ΖΔΡΑΓΚΑΣ)
V. GIANTZI (Β. ΓΙΑΝΤΖΗ)
D. A. KYRIAKIDIS (Δ.Α. ΚΥΡΙΑΚΙΔΗΣ)
Abstract

Present work aimed to examine the antibiotic resistance of the Salmonella enterica serotype Enteritidis (SE) isolates from poultry, to study the plasmid-mediated ampicillin resistance and to detect and determine the distribution of sodCI, sopE and sefA genes. Thirty-five SE isolates from one-day chicks, layers and broilers were studied for susceptibility/resistance to sixteen antimicrobial agents; 23 (65.7%) of them showed resistance to ampicillin, 5 (14.3%) to ampicillin and tetracycline, 4 (11.45%) to tetracycline and 1 (2.9%) isolate showed multi-drug resistance. Ampicillin (AmpR) and ampicillin/tetracycline (AmpRTeR) resistance was easily transferred by conjugation, and all isolates except two possessed a common band. The molecular mass of the plasmid carrying ampicillin resistance was approximately determined at 41kb after DNA digestion with BamHI, HindIII, EcoRI, EcoRV and PstI restriction enzymes and ligation of EcoRI fragments to pET29c. For the detection of TEM-1 or/and TEM-2 ß-lactamases, two pairs of primers were used in a polymerase chain reaction (PCR). The PCR products showed the presence of blaTEM-1 gene in all isolates. The presence of SodCI, sopE, sefA genes was also examined by PCR. Twenty-two (62,8%) isolates carried the sodCI gene, thirty-four (97,2%) isolates carried the sopE gene and all isolates carried the sefA fimbrial locus.

Article Details
  • Rubrik
  • Research Articles
Downloads
Keine Nutzungsdaten vorhanden.
Literaturhinweise
Abbassi-Ghossi I, Jaquani A, Aissa RB, Martinez-Urtaza J, Boudabous A, Gtari M (2011) Antimicrobial resistance and molecular analysis of non-typhoidal salmonella isolates from human in Tunisia. Pathol Biol 59: 207-212.
Altekruse SF, Bauer N, Chanlongbutra A, DeSagun R, Naugle A, Schlosser W, Umholtz R, White P (2006) Salmonella Enteritidis in broiler chickens, United States, 2000–2005. Emerg Infect Dis 12: 1848–1852.
Anğu-Küçüker M, Tolun V, Helmuth R, Rabsch W, Büyükbaba- Boral O, Törümküney-Akbulut D. Susever S, Anğ O (2000) Phage types, antibiotic susceptibilities and plasmid profiles of Salmonella typhimurium and Salmonella Enteritidis strains isolated in Istanbul, Turkey. Clin Microbiol & Infect 6 (11): 593-599.
Antunes P, Mourão J, Machadoc J, Peixe L (2011) First description of qnrS1-IncN plasmid in a ST11 Salmonella Enteritidis clinical
isolate from Portugal Diagnostic Microbiol Inf Dis 69:463–465.
Arvanitidou M, Tsakris A, Sofianou D, Katsouyannopoulos V (1998) Antimicrobial resistance and R-factor transfer of salmonellae isolated from chicken carcasses in Greek hospitals. In. J Food Microbiol 14(40): 197-201.
Bakshi CS, Sing VP, Malik M, Singh RK, Sharma B (2003) 55 kb plasmid and virulence-associatedgenes are positively correlated with Salmonella enteritidis pathogenicity in mice and chickens. Vet Res Commun 27(6): 425-32
Balis E, Vatopoulos AC, Kanelopoulou M, Mainas E, Hatzoudis G, Kontogianni V, Malamou-Lada H, Kitsou-Kyriakopoulou S, Kalapothaki V (1996) Indications on In Vivo Transfer of an Epidemic R Plasmid from Salmonella Enteritidis to Escherichia coli of the Normal Human Gut Flora. J Clin Microbiol 34(4): 1977-979
.
Boyd D, Cloechaert A, Chaslus-Dancla E, Mulvey MR (2002) Characterization of Variant Salmonella Genomic Island 1 Multidrug Resistance Regions from Serovars Typhimurium DT104 and Agona. Antimicrob Agents Chemother 46(6): 1714-22.
Braden CR (2006) Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis 43: 512–517.
Brown DJ, Threlfall EJ, Hampton MD, Rowe B (1993) Molecular characterization of plasmids in Salmonella Enteritidis phage
types.Epidemiol Infect 110(2): 209-216.
C.D.S.C. (Communicable Disease Surveillance Centre), Health Protection Agency (2004) Salmonella Enteritidis in humans faecal & unknown reports England and Wales, 1981 – 2003 report. CDSC 4: 204-208.
Centers for Disease Control and Prevention.Surveillance for foodborne disease outbreaks--United States, 2009-2010 (2013) MMWR Morb Mortal Wkly Rep CDC 62(3): 41-7.
Chu C, Wong DW, Wang MH, Lin HH, Chen YS , Tien N, Shih MC, Chen TH, Chiu CH (2009) Genotyping, Plasmid Analysis, and
Antimicrobial Susceptibility of Salmonella enterica Serotype Enteritidis Isolates from Humans and Chickens in Central Taiwan.J Formos Med Assoc 108 (10): 765-771.
Clinical and Laboratory Standards Institute, CLSI (2008) Development of In Vitro Susceptibility Testing Criteria and Quality Control Parameters; Approved Guideline, 3nd Edition M23-A3: 28 (27).
Clinical and Laboratory Standards Institute, CLSI (2009) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard- Eight Edition M7-A8: 26 (2).
Dione MM, Ikumapayi U, Saha D, Mohammed NI, Adegbol RA, Geerts S, Ieven M, Antonio M (2011) Antimicrobial resistance and virulence genes of non-typhoidal Salmonella isolates in The Gambia and Senegal.J Infect Dev Ctries 5(11): 765-775.
Dogru KA, Ayaz NA, Cencay YE (2010) Serotype identification and antimicrobial resistance profiles of Salmonella spp. isolated from chicken carcasses. Trop Anim Health Prod 42: 893–897.
Ekateriniadou LV, Papoutsopoulou SV, Kyriakidis DA (1994) High production of xanthan gum by a strain of Xanthomonas campestris conjugated with Lactococcus lactis. Bacteriology Letters 16 (5): 517-522.
Fang FC, Degroote MA, Foster JW, Baumler AJ, Ochsner U, Testerman T, Bearson S, Giard JC, Xu Y, Cambell G, Laessing T
(1999) Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc Natl Acad Sci 96: 7502–7507.
Foley SL, Lynne AM (2008) Food animal-associated Salmonella challenges: Pathogenicity and antimicrobial resistance. J Anim Sci 86 (E. Suppl.): E173–E187.
Glynn MK, Bopp C, Dewitt W, Dabney P, Mokhtar M, Angulo FJ (1998) Emergence of multidrug-resostanceSalmonella enterica serotype typhimurium DT104 infections in the United States. N Engl J Med 338(19): 1333-8.
Henriques A, Sereno R, Almeida A (2013).Reducing Salmonella horizontal transmission during egg incubation by phage therapy. Foodborne Pathog Dis.
Hopkins KL and Threlfall EJ (2004) Frequency and polymorphism of sopE in isolates of Salmonella enterica belonging to the ten most prevalent serotypes in England and Wales. J Medical Microbiol 53: 539–543
Jain S and Chen J (2006) Antibiotic resistance profiles and cell surface components of salmonellae. J Food Prot 69: 1017–1023.
Hur J, Kim JH, Park JO, Lee YJ, Lee JH (2011) Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strains isolated from poultry. Vet J 189:306–311.
Ιordanidis P and Georgopoulou I (1998) Study of the resistance in Salmonella strains against antimicrobial drugs. JHVMS 49(2): 134-136.
Karasova D, Havlickova H, Sisak F, Rychlik I (2009) Deletion of sodCI and spvBC in Salmonella enterica serovar Enteritidis reduced its virulence to the natural virulence of serovars Agona, Hadar and Infantis for mice but not for chickens early after infection. Vet Microbiol 139: 304-309.
Linam WM and Gerber MA (2007) Changing epidemiology and prevention of Salmonella infections. Pediatr Infect Dis J 26: 747–748.
Llanes EC, Kirchgesner V, Plesiat P (1999) Propagation of TEMand PSE- Type β- Lactamases among Amoxicillin-Resistant Salmonella spp. Isolated in France. Antim Ag Chem 43(10): 2430-36.
Lopes VC, Velayudham BT, Halvorson DA, Nagaraja KV (2006) Preliminary evaluation of the use of the sefAfibrial gene to elicit immune response against Salmonella enterica serotype Enteritidis in chickens. Avian Dis 50(2): 185-190.
Lu S, Manges AR, Xu Y, Fang FC, Riley LW (1999) Analysis of Virulence of Clinical Isolates of Salmonella Enteritidis In Vivo and In Vitro. Infect & Immun 67: 5651-5657.
Maripandi A and Al-Salamah AA (2010) Multiple-Antibiotic Resistance and Plasmid Profiles of Salmonella Enteritidis Isolated from Retail Chicken Meats. American Journal of Food Technology 5(4): 260-268.
Markogiannakis A, Tassios PT, Lambiri M, Ward LR, Kourea- Kremastinou J, Legakis NJ, Vatopoulos AC (2000) Multiple clones within multigrug-resistant Salmonella enterica serotype typhimurium phage type DT104. The Greek Nontyphoidal Salmonella Study Group. J Clin Microbiol 38(3): 1269-71.
Melendez SN, Hanning I, Han J, Nayak R, Clement AR, Wooming A, Hererra P, Jones FT, Foley SL, Ricke, SC (2010) Salmonella enterica isolates from pasture-raised poultry exhibit antimicrobial resistance and class I integrons. Appl Microbiol 109: 1957–1966.
Metzer E, Agmon V, Andersen N, Cohen D (1998) Emergence of multidrug-resostanceSalmonella enterica serotype typhimurium DT104 among Salmonellae causing enteridites in Israel. Epidemiol Infect 121(3): 555-9.
Mirmomeni MH, Hosseinzadeh-Colagar A, Ghazaey S (2007) Molecular study of Salmonella Enteritidis in poultry by PCR, plasmid curing, antibiotic resistance and protein pattern analysis. Pakistan J Biol Sci 10: 1562-1570.
Morshed R and Peighambari SM (2010) Drug resistance, plasmid profile and random amplified polymorphic DNA analysis of Iranian isolates of Salmonella Enteritidis.New Microbiologic 33: 47-56.
MurugkarHV, Rahman H, Dutta PK (2003) Distribution of virulence genes in Salmonella serovars isolated from man & animals. Indian J Med Res 117: 66-70.
Nastasi A, Mammina C, Cannova I (2000) Antimicrobial Resistance in Salmonella enteritidis, Southern Italy, 1990 – 1998. Emerg Infect Dis 6(4): 401-403.
Ogunniyi AD, Kotlarski I, Morona R, Manning PA (1997) Role of SefA subunit protein of SEF14 fimbriae in the pathogenesis of
Salmonella enterica serovar Enteritidis. Infect Immun 65: 708-717.
Papadopoulou C, Davies RH, Carrique-Mas JJ, Evans SJ (2009) Salmonella serovars and their antimicrobial resistance in British
turkey flocks in 1995 to 2006. Avian Pathology38: 349-357.
Rahman H, Streckel W, Prager R, Tschape H (2004) Presence of sopE gene & its phenotypic expression among different serovars of Salmonella isolated from man & animals. Indian J Med Res 120: 35-38.
Rychlik ,IGregorova D, Hradecka H (2006) Distribution and function of plasmids in Salmonella enterica, Review Vet Microbiol 112: 1–10.
Sakaridis I, Soultos N, Iossifidou E, Koidis P, Ambrosiadis I (2011) Prevalence and antimicrobial resistance of salmonella serovars from chicken carcasses in Northen Greece. Journal of Food Safety 31: 203-210.
Sambrook J and Ruussell DW (2001) Molecular Cloning: a laboratory manual. 3rd ed. N.Y., Cold Spring Harbor Laboratory, Cold
Spring Harbor Laboratory Press.
Sarna M, Dowse G, Evans G, Guest C (2002) An outbreak of Salmonella typhimurium PT135 gastroenteritis associated with a minimally cooked dessert containing raw eggs. Commun dis Intell 26: 32-37.
Smith KP, George J, Cadle KM, Kumar S, Aragon SJ, Hernadez RL, Jones SE, Floyd JL, Varela MF (2010) Elucidation of Antimicrobial Susceptibility Profiles and Genotyping of Salmonellaenterica Isolates from Clinical Cases of Salmonellosis
in New Mexico in 2008. World J Microbiol Biotechnol 26: 1025-1031.
Smith LD, Harris DH, Johnston AJ, Silbergeld EK, Morris JJr (2002) Animal antibiotic use has an early but important impact on the emergency of antibiotics resistance in human commensal bacteria. PNAS 99: 6434-6439.
Snow LC, Davies RH, Christiansen KH, Carrique-Mas JJ,Wales AD, O’Connor JL, Cook AJC, Evans SJ (2007) Survey of the prevalence of Salmonella species on commercial laying farms in the United Kingdom. Vet Rec 161: 471-476.
Suh DK and Song JC (2006) Analysis of Salmonella enterica serotype Enteritidis isolated from human and chicken by repetitive
sequence-PCR fingerpringing, antibiotic resistance and plasmid profiles. J Ve Sci 7: 37-41.
Tassios PT, Markogiannakis A, Vatopoulos AC, Katsanikou E, Velonakis EN, Koures-Kremastinou J, Legakis NJ (1997) Molecular epidemiology of antibiotic resistance of Salmonella enteritidis during a 7-year period in Greece.J Clin Microbiol35 :1316-21.
Tassios PT, Gazouli M, Tzelepi E, Milch H, Kozlova N, Sidorenko S, Legakis NJ, Tzouvelekis LS (1999) Spread of Salmonella typhimurium clone resistant to expanded – spectrum cephalosporins in three European countries. J Clin Microbiol 37: 3774-7.
Threlfall EJ, Rowe B, Ward LR (1993) A comparison of multiple drug resistance in salmonellae from humans and animals in England and Wales, 1981 and 1990.Epidemiol Infect 111: 189-197.
Threlfall EJ, Fisher IST, Berghold C, Gemer-Smidt P, Tschape H, Corrnican M, Luzzi I, Schnieder F, Wannet W, Machado J, Edwards G (2003) Antimicrobial drug resistance in isolates of Salmonella enterica from cases of salmonellosis in humans in Europe in 2000: results of international multi-centre surveillance. Eurosurveillance 8: 41-45.
Turcotte C and Woodward MJ (1993) Cloning, DNA nucleotide sequence and distribution of the gene encoding the SEF14 fibrial antigen of Salmonella Enteritidis. J General Microbiol 139: 1477-1485.
Van de Giessen AW, Bouwknegt M, Dam-Deisz WD, van Pelt W,Wannet WJ, Visser G (2006) Surveillance of Salmonella spp. and Campylobacter spp. in poultry production flocks in The Netherlands. Epidemiol Infect 134: 1266-75.
Vassiliadis P (1983) The Rappaport – Vassiliadis enrichment media for the isolation of Salmonellas: an overview. J ApplBact 37: 411-418.
Vatopoulos AC, Mainas E, Balis E, Threlfall EJ, Kanelopoulou M, Kalapothaki V, Malamou-Lada H, Legakis NJ (1994) Molecular epidemiology of ampicillin-resistant clinical isolates of Salmonella enteritidis.J Clin Microbiol 32 : 1322-1325.
Villa L, Mammina C, Miriagou V, Tzouvelekis LS, Tassios PT, Nastasi A, Carattoli A (2002) Multidrug and broad-spectrum cephalosporin resistance among Salmonella enterica serotype Enteritidis clinicalisolates in Southern Italy. J Clin Microbiol 40 : 2662-2665.
Yang SJ, Park KY, So SH, Kyoung Min-No, Besser TE, Yoo HS, Kim SH, Lee BK, Park YH (2002) Antimicrobioal resistance in Salmonella enterica serovars Enteritidis and typhimurium isolated from animals in Korea: copmarison of phenotypic and genotypic resistance characterization. Vet Microbiol 86: 295-301.
Yates C and Amyes S (2005) Extended-spectrum β-lactamases in non-typhoid Salmonella spp. isolated in the U.K. are now a reality: why the late arrival? J Antimicrob Chemoth 56: 262-264.
Zdragas Α (2001).Serological study of poultry salmonellosis with emphasis to those that caused by Salmonella Enteritidis. PhD
Thesis, Thessaloniki.
Zdragas A, Mazaraki K, Vafeas G, Giantzi V, Papadopoulos T, Ekateriniadou L (2012) Prevalence, seasonal occurrence and antimicrobial resistance of Salmonella in poultry retail products in Greece. Lett App lMicrobiol 55(4):308-13.
Zhu CH, Wu J, Chen WW, Hassan HM, Zhu GO (2010) Difference and variation of the sef14 operon gene clusters in Salmonella pullorum. J Basic Microbiol 50: Suppl 1, S120-3. www.efsa.europa.eu/en/efsajournal/2597.pdf, pp14
Am häufigsten gelesenen Artikel dieser/dieses Autor/in