Acta Alimentaria
Volume/Issue:
Volume 41: Issue 1
Use of RAPD-PCR, plasmid profiling, class 1 integron analysis, and antimicrobial resistance for molecular characterisation of Salmonella strains isolated from Turkey
Authors: N. Taşkale 1 and M. Akçelik 1
View More View Less
  • 1 Ankara University, Tandogan Department of Biology, Faculty of Science 06100 Ankara Turkey
DOI:
https://doi.org/10.1556/aalim.2011.0008
Page Count:
56–66
Publication Date:
01 Mar 2012
Online Publication Date:
04 Aug 2011
Article Category:
Research Article
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $878.00
Purchase Online Subscription

  • Purchase article

    USD  $25.00

  • 1 year subscription (Individual Only)

    USD  $878.00

Forty-one Salmonella strains, isolated from food samples collected from different parts of Turkey were characterized by various biochemical and genotypic tests. Among 41 isolates, 10 strains harboured at least one plasmid, sizes ranging from 3 kb to 400 kb. The antibiotic resistance profiles of Salmonella isolates were studied against 16 commonly used antibiotics. The highest level of resistance was observed against sulfonamide and neomycin, respectively. Moreover, resistance to multiple antibiotics (5) was also observed among 59% of isolates. Each isolate was also screened for the presence of class 1 integrons and nearly 88% of strains contained class 1 integron with different variable regions (VRs). Further examination of the Salmonella isolates was carried out by testing their clonal relation by RAPD-PCR analyses. With the amplification of primer P1254 the isolates classified into 15 groups and with primer P1283, they classified into 8 groups, on the basis of statistical analyses.

  • Aksakal, A. (2003): The occurrence and prevalence Salmonella species in faeces of certain fowls and their susceptibility to antibiotics (In Turkish). YYÜ. Vet. Fak. Derg., 14, 95–101.

    Aksakal A. , 'The occurrence and prevalence Salmonella species in faeces of certain fowls and their susceptibility to antibiotics (In Turkish) ' (2003 ) 14 YYÜ. Vet. Fak. Derg. : 95 -101.

    • Search Google Scholar

  • Bauer, A.W., Kirby, W.M.M., Sherris, J.C. & Turck, M. (1966): Antibiotic susceptibility testing by a standardized single disc method. Am. clin. Pathol., 45, 493–496.

    Turck M. , 'Antibiotic susceptibility testing by a standardized single disc method ' (1966 ) 45 Am. clin. Pathol. : 493 -496.

    • Search Google Scholar

  • Bennett, P.M. (2008): Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br. J. Pharmacol., 153, 347–357.

    Bennett P.M. , 'Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria ' (2008 ) 153 Br. J. Pharmacol. : 347 -357.

    • Search Google Scholar

  • Betancor, L., Schelotto, F., Martinez, A., Pereira, M., Algorta, G., Rodriguez, A., Vignoli, R. & Chabalgoity, J.A. (2004): Random amplified polymorphic DNA and phenotyping analysis of Salmonella enterica serovar Enteritidis isolates collected from humans and poultry in Uruguay from 1995 to 2002. J. clin. Microbiol., 42, 1155–1162.

    Chabalgoity J.A. , 'Random amplified polymorphic DNA and phenotyping analysis of Salmonella enterica serovar Enteritidis isolates collected from humans and poultry in Uruguay from 1995 to 2002 ' (2004 ) 42 J. clin. Microbiol. : 1155 -1162.

    • Search Google Scholar

  • Breuil, J., Brisabois, A., Casin, I., Armand, L.L., Fermy, S. & Collatz, E. (2000): Antimicrobial resistance in Salmonella isolated from humans and animals in France: comparative data from 1994 and 1997. J. antimicrob. Chemother., 46, 965–971.

    Collatz E. , 'Antimicrobial resistance in Salmonella isolated from humans and animals in France: comparative data from 1994 and 1997 ' (2000 ) 46 J. antimicrob. Chemother. : 965 -971.

    • Search Google Scholar

  • Cerro, A., Soto, S.M., Landeras, E., González-Hevia, M.A., Guijarro, J.A. & Mendoza, M.C. (2002): PCR-based procedures in detection and DNA-fingerprinting of Salmonella from samples of animal origin. Fd Microbiol., 19, 567–575.

    Mendoza M.C. , 'PCR-based procedures in detection and DNA-fingerprinting of Salmonella from samples of animal origin ' (2002 ) 19 Fd Microbiol. : 567 -575.

    • Search Google Scholar

  • Clinical and Laboratory Standards Institute (2005): Performance standards for antimicrobial susceptibility testing. Fifteenth informational supplement. M100-S15 (M2), Table 2A. Wayne, PA: CLSI; 2005.

    '', in Fifteenth informational supplement. M100-S15 (M2), Table 2A , (2005 ) -.

  • Del Tufo, J.P. & Tingey, S. (1994): RAPD assay. Methods mol. Biol., 28, 237–241.

    Tingey S. , 'RAPD assay ' (1994 ) 28 Methods mol. Biol. : 237 -241.

  • Genç, O. & Otlu, S. (2005): Salmonella isolations from different avian species in Kars distinct of Turkey (In Turkish). Kafkas Üniv. Vet. Fak. Derg., 11, 25–27.

    Otlu S. , 'Salmonella isolations from different avian species in Kars distinct of Turkey (In Turkish) ' (2005 ) 11 Kafkas Üniv. Vet. Fak. Derg. : 25 -27.

    • Search Google Scholar

  • Guerra, B., Soto, S., Cal, S. & Mendoza, M.C. (2000): Antimicrobial resistance and spread of class 1 integrons among Salmonella serotypes. Antımıcrob. Agents Chemother., 44, 2166–2169.

    Mendoza M.C. , 'Antimicrobial resistance and spread of class 1 integrons among Salmonella serotypes ' (2000 ) 44 Antımıcrob. Agents Chemother. : 2166 -2169.

    • Search Google Scholar

  • Guerra, B., Soto, S., Helmuth, R. & Mendoza, M.C. (2002): Characterisation of a self-transferable plasmid from Salmonella enterica serotype typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes. Antimicrob. Agents Chemother., 46, 2977–2981.

    Mendoza M.C. , 'Characterisation of a self-transferable plasmid from Salmonella enterica serotype typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes ' (2002 ) 46 Antimicrob. Agents Chemother. : 2977 -2981.

    • Search Google Scholar

  • Guerra, B., Junker, E., Miko, A., Helmuth, R. & Mendoza, M.C. (2004): Characterization and localization of drug resistance determinants in multi-resistant, integron carrying Salmonella enterica serotype Typhimurium strains. Microb. Drug Resist., 10, 83–91.

    Mendoza M.C. , 'Characterization and localization of drug resistance determinants in multi-resistant, integron carrying Salmonella enterica serotype Typhimurium strains ' (2004 ) 10 Microb. Drug Resist. : 83 -91.

    • Search Google Scholar

  • Hald, T., Vose, D., Wegner, H.C. & Koupeev, T. (2004): A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis. Risk Anal., 24, 255–269.

    Koupeev T. , 'A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis ' (2004 ) 24 Risk Anal. : 255 -269.

    • Search Google Scholar

  • Hall, R.M. & Stokes, H.W. (1993): Integrons: novel DNA elements which capture genes by site-specific recombination. Genetica, 90, 115–32.

    Stokes H.W. , 'Integrons: novel DNA elements which capture genes by site-specific recombination ' (1993 ) 90 Genetica : 115 -32.

    • Search Google Scholar

  • Hall, R.M. & Stokes, H.W. (2004): Integrons or super integrons. Microbiol. Comment, 150, 3–4.

    Stokes H.W. , 'Integrons or super integrons ' (2004 ) 150 Microbiol. Comment : 3 -4.

  • Havlickova, H., Hradecka, H., Bernardyova, I. & Rychlik, I. (2009): Distribution of integrons and SGI1 among antibiotic-resistant Salmonella enterica isolates of animal origin. Vet. Microbiol., 133, 193–198.

    Rychlik I. , 'Distribution of integrons and SGI1 among antibiotic-resistant Salmonella enterica isolates of animal origin ' (2009 ) 133 Vet. Microbiol. : 193 -198.

    • Search Google Scholar

  • Helmuth, R., Stephan, R., Bunge, C., Hoog, B., Steinbeck, A. & Bulling, E. (1985): Epidemiology of virulenceassociated plasmids and outer memrane protein patterns within seven common Salmonella serotypes. Infect. Immun., 48, 175–182.

    Bulling E. , 'Epidemiology of virulenceassociated plasmids and outer memrane protein patterns within seven common Salmonella serotypes ' (1985 ) 48 Infect. Immun. : 175 -182.

    • Search Google Scholar

  • Hilton, A.C. & Penn, C.W. (1998): Comparison of ribotyping and arbitrarily-primed PCR for molecular typing of Salmonella enterica and relationships between strains on the basis of these molecular markers. J. appl. Microbiol., 85, 933–940.

    Penn C.W. , 'Comparison of ribotyping and arbitrarily-primed PCR for molecular typing of Salmonella enterica and relationships between strains on the basis of these molecular markers ' (1998 ) 85 J. appl. Microbiol. : 933 -940.

    • Search Google Scholar

  • Hohmann, E.L. (2001): Nontyphoidal salmonellosis. Clin. Infect. Dis., 32, 263–269.

    Hohmann E.L. , 'Nontyphoidal salmonellosis ' (2001 ) 32 Clin. Infect. Dis. : 263 -269.

  • Holmberg, S.D., Wachsmuth, I.K., Hickman-Brenner, F.W. & Cohen, M.L. (1984): Comparison of plasmid profile analysis, Phage typing, and antimicrobial susceptibility testing in characterizing Salmonella typhimurium isolates from outbreaks. J. clin. Microbiol., 19, 100–104.

    Cohen M.L. , 'Comparison of plasmid profile analysis, Phage typing, and antimicrobial susceptibility testing in characterizing Salmonella typhimurium isolates from outbreaks ' (1984 ) 19 J. clin. Microbiol. : 100 -104.

    • Search Google Scholar

  • Kado, C.I. & Liu, S.T. (1981): Rapid procedure for detection and isolation of large and small plasmids. J. Bacteriol., 145, 1365–1373.

    Liu S.T. , 'Rapid procedure for detection and isolation of large and small plasmids ' (1981 ) 145 J. Bacteriol. : 1365 -1373.

    • Search Google Scholar

  • Lee, M.F., Chen, Y.H. & Peng, C.F. (2009): Molecular characterisation of class 1 integrons in Salmonella enterica serovars Choleraesuis isolates from Southern Taiwan. Int. J. Antimicrob. Ag., 33, 216–222.

    Peng C.F. , 'Molecular characterisation of class 1 integrons in Salmonella enterica serovars Choleraesuis isolates from Southern Taiwan ' (2009 ) 33 Int. J. Antimicrob. Ag. : 216 -222.

    • Search Google Scholar

  • Lin, A.W., Usera, M.A., Barrett, T.J. & Goldsby, R.A. (1996): Application of random amplified polymorphic DNA analysis to differentiate strains of Salmonella enteritidis. J. clin. Microbiol., 34, 870–876

    Goldsby R.A. , 'Application of random amplified polymorphic DNA analysis to differentiate strains of Salmonella enteritidis ' (1996 ) 34 J. clin. Microbiol. : 870 -876.

    • Search Google Scholar

  • Macedo-Vinas, M., Cordeiro, N.F., Bado, I., Herrera-Leon, S., Vola, M., Robino, L., Gonzalez-Sanz, R., Mateos, S., Schelotto, F., Algorta, G., Ayala, J.A., Echeita, A. & Vignoli, R. (2009): Surveillance of antibiotic resistance evolution and detection of class 1 and 2 integrons in human isolates of multi-resistant Salmonella Typhimurium obtained in Uruguay between 1976 and 2000. Int. J. Infect. Dis., 13, 342–348.

    Vignoli R. , 'Surveillance of antibiotic resistance evolution and detection of class 1 and 2 integrons in human isolates of multi-resistant Salmonella Typhimurium obtained in Uruguay between 1976 and 2000 ' (2009 ) 13 Int. J. Infect. Dis. : 342 -348.

    • Search Google Scholar

  • Madadgar, O., Zahraei Salehi, T., Tadjbakhsh, H., Mahzounieh, M. & Feizabadi, M.M. (2008): Genomic and phenotypic evaluation of Salmonella typhimurium and Salmonella enteritidis in Iran. Comp. clin. Pathol., 17, 229–235.

    Feizabadi M.M. , 'Genomic and phenotypic evaluation of Salmonella typhimurium and Salmonella enteritidis in Iran ' (2008 ) 17 Comp. clin. Pathol. : 229 -235.

    • Search Google Scholar

  • Maripandi, A. & Al-Salamah, A.A. (2010): Multiple-antibiotic resistance and plasmid profiles of Salmonella enteritidis isolated from retail chicken meats. Am. J. Fd Technol., 5, 260–268.

    Al-Salamah A.A. , 'Multiple-antibiotic resistance and plasmid profiles of Salmonella enteritidis isolated from retail chicken meats ' (2010 ) 5 Am. J. Fd Technol. : 260 -268.

    • Search Google Scholar

  • Miyamoto, T., Tian, H.Z., Okabe, T., Trevanich, S., Asoh, K., Tomoda, S., Honjoh, K. & Shoji, H. (1998): Application of randomly amplified polymorphic DNA analysis for detection of Salmonella spp. in foods. J. Fd Protect., 61, 785–791.

    Shoji H. , 'Application of randomly amplified polymorphic DNA analysis for detection of Salmonella spp. in foods ' (1998 ) 61 J. Fd Protect. : 785 -791.

    • Search Google Scholar

  • National Ant imicrobial Resistance Monitoring System (2007): Enteric Bacteria (NARMS) Annual Report.

  • Nayak, R. & Kenney, P.B. (2002): Screening of Salmonella isolates from a turkey production facility for antibiotic resistance, Poultry Sci., 81, 1496–1500.

    Kenney P.B. , 'Screening of Salmonella isolates from a turkey production facility for antibiotic resistance ' (2002 ) 81 Poultry Sci. : 1496 -1500.

    • Search Google Scholar

  • Oliveira, F.A., Frazzon, A.P.G., Brandelli, A. & Tondo, E.C. (2007): Use of PCR-ribotyping, RAPD and antimicrobial resistance for typing of Salmonella enteritidis involved in food-borne ourbreaks in Southern Brazil. J. Infect. Developing Countries, 1, 170–176.

    Tondo E.C. , 'Use of PCR-ribotyping, RAPD and antimicrobial resistance for typing of Salmonella enteritidis involved in food-borne ourbreaks in Southern Brazil ' (2007 ) 1 J. Infect. Developing Countries : 170 -176.

    • Search Google Scholar

  • Özbey, G., Kök, F. & Muz, A. (2007): Isolation of Salmonella spp. in camel sausages from retail markets in Aydın, Turkey, and polymerase chain reaction (PCR) confirmation. Turk. J. Vet. Anim. Sci., 31, 67–71.

    Muz A. , 'Isolation of Salmonella spp. in camel sausages from retail markets in Aydın, Turkey, and polymerase chain reaction (PCR) confirmation ' (2007 ) 31 Turk. J. Vet. Anim. Sci. : 67 -71.

    • Search Google Scholar

  • Perron, G.G., Bell, G. & Quessy, S. (2008): Parallel evolution of multidrug-resistance in Salmonella enterica isolated from swine. FEMS Microbiol. Lett., 281, 17–22.

    Quessy S. , 'Parallel evolution of multidrug-resistance in Salmonella enterica isolated from swine ' (2008 ) 281 FEMS Microbiol. Lett. : 17 -22.

    • Search Google Scholar

  • Poppe, C. (2000): Salmonella infections in the domestic fowl. —in: Wray, C. & Wray, A. (Eds) Salmonella in domestic animals. CAB International, New York, NY pp. 107–132.

    Poppe C. , '', in Salmonella in domestic animals , (2000 ) -.

  • Rodriguez, I.M., Rodicio, R., Herrera-Leon, S., Echeita, A. & Mendoza, M.C. (2008): Class 1 integrons in multidrug-resistant non-typhoidal Salmonella enterica isolated in Spain between 2002 and 2004. Int. J. Antimicrob. Ag., 32, 158–164.

    Mendoza M.C. , 'Class 1 integrons in multidrug-resistant non-typhoidal Salmonella enterica isolated in Spain between 2002 and 2004 ' (2008 ) 32 Int. J. Antimicrob. Ag. : 158 -164.

    • Search Google Scholar

  • Soto, S.M., Gonzalez-Hevia, M.A. & Mendoza, M.C. (2003): Antimicrobial resistance in clinical isolates of Salmonella enterica serotype Enteritidis: relationships between mutations conferring quinolone resistance, integrons, plasmids and genetic types. J. Antimicrob. Chemother., 51, 1287–1291.

    Mendoza M.C. , 'Antimicrobial resistance in clinical isolates of Salmonella enterica serotype Enteritidis: relationships between mutations conferring quinolone resistance, integrons, plasmids and genetic types ' (2003 ) 51 J. Antimicrob. Chemother. : 1287 -1291.

    • Search Google Scholar

  • Stepanauskas, R., Glenn, T.C., Jagoe, C.H., Tuckfield, R.C., Lindell, A.H., King, C.J. & McArthur, J.V. (2006): Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ. Microbiol., 8, 1510–1514.

    McArthur J.V. , 'Coselection for microbial resistance to metals and antibiotics in freshwater microcosms ' (2006 ) 8 Environ. Microbiol. : 1510 -1514.

    • Search Google Scholar

  • Thakur, Y.R. & Bajaj, B.K. (2006): Antibiotic resistance and molecular characterization of poultry isolates of Salmonella by RAPD-PCR. World. J. Microbiol. Biotechnol., 22, 1177–1183.

    Bajaj B.K. , 'Antibiotic resistance and molecular characterization of poultry isolates of Salmonella by RAPD-PCR ' (2006 ) 22 World. J. Microbiol. Biotechnol. : 1177 -1183.

    • Search Google Scholar

  • Thorns, C.J. (2000): Bacterial food-borne zoonoses. Rev. Sci. Tech., 19, 226–239.

    Thorns C.J. , 'Bacterial food-borne zoonoses ' (2000 ) 19 Rev. Sci. Tech. : 226 -239.

  • Tosini, F., Visca, P., Luzzi, I., Dionisi, A.M., Pezzella, C., Petrucca, A. & Carattoli, A. (1998): Class 1 integronborne multiple-antibiotic resistance carried by IncFI and IncL/M plasmids in Salmonella enterica serotype Typhimurium. Antimicrob. Agents Chemother., 42, 3053–3058.

    Carattoli A. , 'Class 1 integronborne multiple-antibiotic resistance carried by IncFI and IncL/M plasmids in Salmonella enterica serotype Typhimurium ' (1998 ) 42 Antimicrob. Agents Chemother. : 3053 -3058.

    • Search Google Scholar

  • Vo, A.T.T., Van Duijkeren, E., Fluit, A.C., Wannet, W.J.B., Verbruggen, A.J., Maas, H.M.E. & Gaastra, W. (2006): Antibiotic resistance, integrons and Salmonella genomic island 1 among non-typhoidal Salmonella serovars in The Netherlands. Int. J. Antimicrob. Agents, 28, 172–179.

    Gaastra W. , 'Antibiotic resistance, integrons and Salmonella genomic island 1 among non-typhoidal Salmonella serovars in The Netherlands ' (2006 ) 28 Int. J. Antimicrob. Agents : 172 -179.

    • Search Google Scholar

  • Welsh, J. & McClelland, M. (1990): Fingerprinting genomes using PCR with arbitrary primers. Nucleic. Acids Res., 18, 7213–7218.

    McClelland M. , 'Fingerprinting genomes using PCR with arbitrary primers ' (1990 ) 18 Nucleic. Acids Res. : 7213 -7218.

    • Search Google Scholar

  • White, D.G., Zhao, S., Sudler, R., Ayers, S., Friedman, S., Chen, S., McDermott, P.F., McDermott, S., Wagner, D.D. & Meng, J. (2001): The isolation of antibiotic-resistant Salmonella from retail ground meats. New Engl. J. Med., 345, 1147–1154.

    Meng J. , 'The isolation of antibiotic-resistant Salmonella from retail ground meats ' (2001 ) 345 New Engl. J. Med. : 1147 -1154.

    • Search Google Scholar

  • WHO (2001): World Health Organization Surveillance Programme for Control of Foodborne Infections and Intoxications in Europe. 7th Report, 1993–1998. Schmidt, K. & Tirado, C. (Eds) Published by the Federal Institute for Health Protection of Consumers and Veterinary Medicine (BgVV), Berlin, Germany. (FAO/WHO Collaborating Centre for Research and Training in Food Hygiene and Zoonoses), pp. 422–423.

  • Zhao, S., McDermott, P.F., Friedman, S., Qaiyumi, S., Abbott, J., Keissling, C., Ayers, S., Singh, R., Hubert, S., Sofos, J. & White, D.G. (2006): Characterization of antimicrobial-resistant Salmonella isolated from imported foods. J. Fd Protect., 69, 500–507.

    White D.G. , 'Characterization of antimicrobial-resistant Salmonella isolated from imported foods ' (2006 ) 69 J. Fd Protect. : 500 -507.

    • Search Google Scholar
Cover Acta Alimentaria
Acta Alimentaria
Print ISSN:
0139-3006
Online ISSN:
1588-2535
Keywords:
Salmonella ; multi-drug resistance; plasmid; RAPD-PCR; integron

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Nov 2020 2 19 5
Dec 2020 2 0 0
Jan 2021 2 0 0
Feb 2021 4 0 0
Mar 2021 0 0 0
Apr 2021 0 0 0
May 2021 0 0 0