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Analysis of Salmonella Agona and Salmonella Weltevreden in Malaysia by PCR fingerprinting and antibiotic resistance profiling

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Abstract

Forty-eight strains of Salmonella enterica subsp. enterica serovar Agona and 33 strains of Salmonella enterica subsp. enterica serovar Weltevreden were characterized by random amplified polymorphic DNA (RAPD) fingerprinting using 3 different arbitrary primer, Enterobacterial Repetitive Intergenic Consensus-Polymerase Chain Reaction (ERIC-PCR) and antimicrobial susceptibility testing. By using RAPD, 81 strains (44 strains of S. Agona and 33 strains of S. Weltevreden) can be clustered into 14 groups and 6 single isolates whereas ERIC-PCR produced 7 clusters and 3 single isolates. Thirteen antimicrobial agents were used and all the isolates were resistant to erythromycin and showed Multiple Antimicrobial Resistance indexes, ranging from 0.08 to 0.62. Poultry still remain as the common reservoir for multi-drug-resistant Salmonella. On the other hand, vegetables contaminated with S. Weltevreden showed a gain in antimicrobial resistance. Besides that, consistent antibiograms were observed from S. Weltevreden isolated at Kajang wet market on 2000/08/02.

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References

  • Aarestrup FM, Lertworapreecha M, Evans MC, Bangtrakulnonth A, Chalermchaikit T, Hendriksen RS et al (2003) Antimicrobial susceptibility and occurrence of resistance genes among Salmonella enterica serovars Weltevreden from different countries. J Antimicrob Chemother 52:715–718. doi:10.1093/jac/dkg426

    Article  PubMed  CAS  Google Scholar 

  • Bahnson PB, Fedorka-Cray PJ, Ladedly SR, Mateus-Pinilla NE (2006) Herd-level risk factors for Salmonella enterica subsp. enterica in U.S. market pigs. Prev Vet Med 76:249–262. doi:10.1016/j.prevetmed.2006.05.009

    Article  PubMed  CAS  Google Scholar 

  • Bangtrakulnonth A, Pornruengwong S, Pulsrikarn C, Sawanpanyalert P, Hendriksen R, Wong D et al (2004) Salmonella serovars from humans and other sources in Thailand, 1993–2002. Emerg Infect Dis 10:131–136

    PubMed  Google Scholar 

  • Bender JB, Hedberg CW, Boxrud DJ, Besser JM, Winklund JH, Smith KE et al (2001) Use of molecular subtyping in surveillance for Salmonella enterica serotype typhimurium. N Engl J Med 344:189–194. doi:10.1056/NEJM200101183440305

    Article  PubMed  CAS  Google Scholar 

  • Boonmar S, Bangtrakulnonth A, Pornruangwong S (1998) Predominant serovars of Salmonella in humans and foods from Thailand. J Vet Med Sci 60:877–880. doi:10.1292/jvms.60.877

    Article  PubMed  CAS  Google Scholar 

  • Boyd D, Cloeckaert 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 46:1714–1722. doi:10.1128/AAC.46.6.1714-1722.2002

    Article  PubMed  CAS  Google Scholar 

  • Caprioli A, Busami L, Martel JL, Helmuth R (2000) Monitoring of antibiotic resistance bacteria of animal origin: epidemiological and microbiological methodologies. Int J Ant Antimicrob Agents 14:295–301. doi:10.1016/S0924-8579(00) 00140-0

    Article  CAS  Google Scholar 

  • Carraminana JJ, Rota C, Agustin I, Herrera A (2004) High prevalence of multiple resistant to antibiotics in Salmonella isolated from a poultry. Vet Microbiol 104:133–139. doi:10.1016/j.vetmic.2004.08.010

    Article  PubMed  CAS  Google Scholar 

  • Center for Disease Control and Prevention (CDC) (1998) Multistate outbreak of Salmonella serotype Agona infections linked to toasted oats cereal. United States. MMWWR Morb. Mortal. Wkly Rep. 47(April–May):462–464.

  • Cloeckaert A, Sidi Boumedine K, Flaujac G, Imberechts H, D’Hooghe I, Chaslus-Dancla E (2000) Occurrence of a Salmonella enterica serovar Typhimurium DT104-like antibiotic resistance gene cluster including the floR gene in S. enterica serovar Agona. Antimicrob Agents Chemother 44:1359–1361. doi:10.1128/AAC.44.5.1359-1361.2000

    Article  PubMed  CAS  Google Scholar 

  • Fadl AA, Nguyen AV, Khan MI (1995) Notes: analysis of Salmonella enteriditis isolates by arbitrarily primed PCR. J Clin Microbiol 33:987–989

    PubMed  CAS  Google Scholar 

  • Fuzihara TO, Fernandes SA, Franco BD (2000) Quantitative survival of native Salmonella serovars during storage of frozen pork. Int J Food Microbiol 54:19–25. doi:10.1016/S0168-1605(99) 00149-X

    Article  Google Scholar 

  • Gebreyes WA, Davies PR, Morrow WEM, Funk JA, Altier C (2000) Antimicrobial resistance of Salmonella isolates from swine. J Clin Microbiol 38:4633–4636

    PubMed  CAS  Google Scholar 

  • Hermans PEM, Saha SK, Van Leeuwen WJ, Verbrugh HA, Van Belkum A, Goessems WHF (1996) Molecular typing of Salmonella typhi strains from Dhaka (Bangladesh) and development of DNA probes identifying plasmid-encoded multidrug-resistant isolates. J Clin Microbiol 34:1373–1379

    PubMed  CAS  Google Scholar 

  • Hunter PR, Gaston MA (1988) Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol 26:2465–2466

    PubMed  CAS  Google Scholar 

  • Imberechts H, D’hooghe I, Pohl P (1998) Prevalence of Salmonella Agona in animal in Belgium. Salmonella Newsl 4:4

    Google Scholar 

  • Killalea D, Ward LR, Roberts D (1996) International epidemiological and microbiological study of outbreak of Salmonella Agona infection from a ready to eat savoury snack in England and Wales and the United States. BMJ 313:1105–1107

    PubMed  CAS  Google Scholar 

  • Krumperman PH (1983) Multiple antibiotic resistance indexing of Escherichis coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 46:165–170

    PubMed  CAS  Google Scholar 

  • Lim H, Lee KH, Hong C-H, Bahk G-J, Choi WS (2005) Comparison of four molecular typing methods for the differentiation of Salmonella spp. Int J Food Microbiol 105:411–418. doi:10.1016/j.ijfoodmicro.2005.03.019

    Article  PubMed  CAS  Google Scholar 

  • Lin AW, Usera MA, Barret TJ, Goldsby RA (1996) Application of random amplified polymorphic DNA analysis to differentiate strains of Salmonella enteriditis. J Clin Microbiol 34:870–876

    PubMed  CAS  Google Scholar 

  • Madden JM (1992) Microbial pathogens in fresh produce-the regulatory perspective. J Food Prot 55:821–823

    Google Scholar 

  • Maria J, Johara MY, Dahlia H, Siti Hajar I (2002) Salmonella serovars isolated in animals and livestock products in Malaysia (1996–2001). Proceedings; 12th federation of Asian veterinary association congress 2002 in conjunction with 14th veterinary association of Malaysia congress. 22–28 August 2002

  • Mead PS, Slutsker L, Dietz V, Macraig LF, Bresee JS, Shapiro C et al (1999) Food related illness and death in the United States. Emerg Infect Dis 5:607–634

    PubMed  CAS  Google Scholar 

  • Melloul A, Hassani L, Rafouk L (2001) Salmonella contamination of vegetables irrigated with untreated wastewater. World J Microbiol Biotechnol 17:207–209. doi:10.1023/A:1016686501953

    Article  Google Scholar 

  • Millemann Y, LesageDescauses MC, Lafont JP, Chaslus-Dancla E (1996) Comparison of random amplified polymorphic DNA analysis and enterobacterial repetitive intergenic consensus PCR for epidemiological studies of Salmonella. FEMS Immunol Med Microbiol 14:129–134. doi:10.1111/j.1574-695X.1996.tb00279.x

    Article  PubMed  CAS  Google Scholar 

  • Molbak K, Baggesen DL, Aarestrup FM, Ebbesen JM, Engberg J, Frydendahl K, Gerner-Smidt PetersonAM, Wegener HC (1999) An outbreak of multidrug-resistant quinolones-resistant Salmonella enterica serotype Typhimurium DT104. N Engl J Med 341:1420–1425. doi:10.1056/NEJM199911043411902

    Article  PubMed  CAS  Google Scholar 

  • National Committee for Clinical Laboratory Standards (1999) Performance standards for antimicrobial susceptibility testing, 9th international supplement document M100-S9. National committee for clinical laboratory standards. Ferraro, M.J.

  • National Committee for Clinical Laboratory Standards (2002) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, 2nd edn. Approved Standard M31-A2. Wayne, PA: NCCLS; 2002

  • Oliveira SDD, Flores FS, Santos LRD, Brandelli A (2005) Antimicrobioal resistance in Salmonella enteriditis strains isolated from broiler carcasses, food, human and poultry-related samples. Int J Food Microbiol 97:297–305. doi:10.1016/j.ijfoodmicro.2004.04.022

    Article  CAS  Google Scholar 

  • Ooi PL, Goh KT, Neo KS, Ngan CCL (1997) A shipyard outbreak of salmonellosis traced to contaminated fruits and vegetables. Ann Acad Med Singapore 26:539–543

    PubMed  CAS  Google Scholar 

  • Padungtod P, Kaneene BJ (2006) Salmonella in food animals and humans in northern Thailand. Int J Food Microbiol 108:346–254

    PubMed  Google Scholar 

  • Poirel L, Guibert M, Bellais S, Naas T, Nordmann P (1999) Integron and carbenicillinase-mediated reduced susceptibility to amoxicilin-clavulanic acid in isolates of multidrug-resistant Salmonella enterica serotype Typhimurium DT104 from French patients. Antimicrob Agents Chemother 43:1098–1104

    PubMed  CAS  Google Scholar 

  • Ponka A, Anderson Y, Siitonen A, de Jong B, Jahkota M, Haikappa O (1995) Salmonella in alfalfa sprouts. Lancet 345:462–463. doi:10.1016/S0140-6736(95) 90451-4

    Article  PubMed  CAS  Google Scholar 

  • Popoff MY, Bockemuhl J, Brenner FW (2000) Supplement 1998 (no. 42) to the Kauffmann-White scheme. Res Microbiol 151:63–65. doi:10.1016/S0923-2508(00) 00126-1

    Article  PubMed  CAS  Google Scholar 

  • Rowe B, Ward LR, Threfall EJ (1990) Spread of multiresistant Salmonella typhi. Lancet 337:1065. doi:10.1016/0140-6736(90)92532-M

    Article  Google Scholar 

  • Sahilah AM, Son R, Rusul G, Samuel L, Hassan Z, Lum KY et al (2000) Molecular typing of Salmonella weltevreden and Salmonella chincol by pulse-field gel electrophoresis (PFGE) and enterobacterial repetitive intergenic consensus- polymerase chain reaction (ERIC-PCR). World J Microbiol Biotechnol 16:621–624. doi:10.1023/A:1008967914499

    Article  CAS  Google Scholar 

  • Shabarinath S, Kumar HS, Khushiramani R, Karunasagar I, Karunasagar I (2007) Detection and characterization of Salmonella associated with tropical seafood. Int J Food Microbiol 114:227–233. doi:10.1016/j.ijfoodmicro.2006.09.012

    Article  PubMed  CAS  Google Scholar 

  • Shahada F, Chuma T, Tobata T, Okamoto K, Sueyoshi M, Takase K (2006) Molecular epidemiology of antimicrobial resistance among Salmonella enterica serovars Infantis from poultry in Kagoshima, Japan. Int J Ant Antimicrob Agents 28:302–307. doi:10.1016/j.ijantimicag.2006.07.003

    Article  CAS  Google Scholar 

  • Shangkuan YH, Lin HC (1998) Application of randomly amplified polymorphic DNA analysis to differentiate strains of Salmonella typhi and other Salmonella spp. J Appl Microbiol 85:693–702. doi:10.1111/j.1365-2672.1998.00582.x

    Article  PubMed  CAS  Google Scholar 

  • Swanenburg M, Urlings HAP, Keuzenkamp DA, Snijders JMA (1998) Validation of ERIC-PCR as a tool in epidemiologic research of Salmonella in slaughter pigs. J Ind Microbiol Biotechnol 21:141–144. doi:10.1038/sj.jim.2900568

    Article  CAS  Google Scholar 

  • Tavechio AT, Ghilardi ACR, Peresi JTM, Fuzihara TO, Yonamine EK, Jakabi M et al (2002) Salmonella serotypes isolated from nonhuman sources in Sao Paulo, Brazil from 1996 through 2000. J Food Prot 65:1041–1044

    PubMed  Google Scholar 

  • Thong KL, Goh YL, Radu S, Noorzaleha S, Yasin R, Koh YT et al (2002) Genetic diversity if clinical and environmental strains of Salmonella enterica serotype Weltevreden isolated in Malaysia. J Clin Microbiol 40:2498–2503. doi:10.1128/JCM.40.7.2498-2503.2002

    Article  PubMed  CAS  Google Scholar 

  • Threlfall EJ, Powell NG, Rowe B (1994) Differentiation of salmonellas by molecular methods. PHLS Microbiol Dig 11:199–202

    Google Scholar 

  • Threlfall EJ, Teale CJ, Davies RH, Ward LR, Skinner JA, Graham A et al (2003) A comparison of antimicrobial susceptibilities in nontyphoidal salmonellas from humans and food animals in England and Wales in 2000. Microb Drug Resist 9:183–189. doi:10.1089/107662903765826787

    Article  PubMed  CAS  Google Scholar 

  • Van Lith LAJT, Aarts HJM (1994) Polymerase chain reaction identification of Salmonella serotypes. Appl Microbiol Lett 19:273–276. doi:10.1111/j.1472-765X.1994.tb00962.x

    Article  CAS  Google Scholar 

  • Verdet C, Arlet G, Barnaud G, Lagrange PH, Philippon (2000) A novel integron in Salmonella enterica serovar Enteriditis, carrying the bla DHA-1 gene and its regulator gene ampR, originated from Morganella morganii. Antimicrob Agents Chemother 44:222–225

    Article  PubMed  CAS  Google Scholar 

  • Versalovic LJ, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831. doi:10.1093/nar/19.24.6823

    Article  PubMed  CAS  Google Scholar 

  • White DG, Zhao S, Sudler R, Ayers S, Friedman S, Chen S et al (2001) The isolation of antibiotic-resistant salmonella from retail ground meats. N Engl J Med 345:1147–1154. doi:10.1056/NEJMoa010315

    Article  PubMed  CAS  Google Scholar 

  • World Health Organisation (2005) Global Salm-Surv Strategic Plan. Report of a WHO meeting. Copenhagen, Denmark

  • Yan SS, Pendrak ML, Abela-Ridder B, Punderson JW, Fedorko DP, Foley SL (2003) An overview of Salmonella typing Public health perspectives. Clin Appl Immunol Rev 4:189–204

    Google Scholar 

  • Zansky S, Wallace B, Schoonmaker-Bopp D, Smith P, Ramsey F, Painter J et al (2002) From Centers of Disease Control and Prevention. Outbreak of multidrug-resistant Salmonella Newport-United States. MMWR Morb Mortal Wkly Rep 51:545–548

    Google Scholar 

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Acknowledgments

The authors thank the Department of Chemistry, Malaysia for the collaboration and providing samples for this study. This work was supported by funds provided by the fundamental research grants from the Ministry of Higher Education, Malaysia.

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Authors and Affiliations

  1. Department of Biomedical Science, Faculty of Medicine and Health Sciences, University Putra Malaysia, UPM Serdang, Selangor Darul Ehsan, 43400, Malaysia

    Lee Learn-Han, Cheah Yoke-Kqueen, Sabrina Sukardi, Sim Jiun-Horng & Khoo Chai-Hoon

  2. Unit Microbiology, Department of Chemistry Malaysia, Jalan Sultan, Petaling Jaya, Selangor, 46661, Malaysia

    Noorzaleha Awang Salleh

  3. Department of Food Science, Faculty of Food Science and Technology, University Putra Malaysia, UPM Serdang, Selangor Darul Ehsan, 43400, Malaysia

    Son Radu

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  1. Lee Learn-Han
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Correspondence to Cheah Yoke-Kqueen.

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Learn-Han, L., Yoke-Kqueen, C., Salleh, N.A. et al. Analysis of Salmonella Agona and Salmonella Weltevreden in Malaysia by PCR fingerprinting and antibiotic resistance profiling. Antonie van Leeuwenhoek 94, 377–387 (2008). https://doi.org/10.1007/s10482-008-9254-y

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