Development and validation of a resistance and virulence gene microarray targeting Escherichia coli and Salmonella enterica

Journal of Microbiological Methods

Volumn 82, Issue 1, 2010, Pages 36-41

  Davis, Margaret A ^a   Lim, Ji Youn ^b   Soyer, Yesim ^c   Harbottle, Heather ^d   Chang, Yung Fu ^c   New, Daniel ^a   Orfe, Lisa H ^a   Besser, Thomas E ^a   Call, Douglas R ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Enterobacteriaceae; Microarray; Resistance genes; Validation

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; CEFTAZIDIME; CHLORAMPHENICOL; COTRIMOXAZOLE; GENTAMICIN; KANAMYCIN; NALIDIXIC ACID; STREPTOMYCIN; SULFAFURAZOLE; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; ESCHERICHIA COLI; GENOTYPE; INTERRATER RELIABILITY; INTRARATER RELIABILITY; MICROARRAY ANALYSIS; NONHUMAN; OLIGONUCLEOTIDE PROBE; PRIORITY JOURNAL; SALMONELLA ENTERICA; SENSITIVITY AND SPECIFICITY; STANDARDIZATION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; MICROBIAL SENSITIVITY TESTS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SALMONELLA ENTERICA; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; SALMONELLA ENTERICA;

EID: 77953542246     PISSN: 01677012     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mimet.2010.03.017     Document Type: Article

References (60)

1. Bauer A.W., Kirby M.M.W., Sherris J.C., Turck M. Antibiotic susceptibility testing by a standard single disk method. Am. J. Clin. Pathol. 1966, 45:493-496.
2. Bewick V., Cheek L., Ball J. Statistics review 13: receiver operating characteristic curves. Crit. Care 2004, 8:508-512.
3. Boerlin P., Reid-Smith R.J. Antimicrobial resistance: its emergence and transmission. Anim. Health Res. Rev. 2008, 9:115-126.
4. Brazma A. Minimum Information About a Microarray Experiment (MIAME)-successes, failures, challenges. Sci. World J. 2009, 9:420-423.
5. Bruant G., Maynard C., Bekal S., Gaucher I., Masson L., Brousseau R., Harel J. Development and validation of an oligonucleotide microarray for detection of multiple virulence and antimicrobial resistance genes in Escherichia coli. Appl. Environ. Microbiol. 2006, 72:3780-3784.
6. Burland V., Shao Y., Perna N.T., Plunkett G., Sofia H.J., Blattner F.R. The complete DNA sequence and analysis of the large virulence plasmid of Escherichia coli O157:H7. Nucleic Acids Res. 1998, 26:4196-4204.
7. Bush K. Extended-spectrum beta-lactamases in North America, 1987-2006. Clin. Microbiol. Infect. 2008, 14(Suppl 1):134-143.
8. Call D.R. Challenges and opportunities for pathogen detection using DNA microarrays. Crit. Rev. Microbiol. 2005, 31:91-99.
9. Call D.R., Bakko M.K., Krug M.J., Roberts M.C. Identifying antimicrobial resistance genes with DNA microarrays. Antimicrob. Agents Chemother. 2003, 47:3290-3295.
10. Canales R.D., Luo Y., Willey J.C., Austermiller B., Barbacioru C.C., Boysen C., Hunkapiller K., Jensen R.V., Knight C.R., Lee K.Y., Ma Y., Maqsodi B., Papallo A., Peters E.H., Poulter K., Ruppel P.L., Samaha R.R., Shi L., Yang W., Zhang L., Goodsaid F.M. Evaluation of DNA microarray results with quantitative gene expression platforms. Nat. Biotechnol. 2006, 24:1115-1122.
11. Canton R., Coque T.M. The CTX-M beta-lactamase pandemic. Curr. Opin. Microbiol. 2006, 9:466-475.
12. Cassone M., Del Grosso M., Pantosti A., Giordano A., Pozzi G. Detection of genetic elements carrying glycopeptide resistance clusters in Enterococcus by DNA microarrays. Mol. Cell Probes 2008, 22:162-167.
13. Cattoir V., Nordmann P. Plasmid-mediated quinolone resistance in gram-negative bacterial species: an update. Curr. Med. Chem. 2009, 16:1028-1046.
14. Cattoir V., Poirel L., Rotimi V., Soussy C.J., Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J. Antimicrob. Chemother. 2007, 60:394-397.
15. Chen J.J., Hsueh H.M., Delongchamp R.R., Lin C.J., Tsai C.A. Reproducibility of microarray data: a further analysis of microarray quality control (MAQC) data. BMC Bioinform. 2007, 8:412.
16. Chen S., Zhao S., McDermott P.F., Schroeder C.M., White D.G., Meng J. A DNA microarray for identification of virulence and antimicrobial resistance genes in Salmonella serovars and Escherichia coli. Mol. Cell Probes 2005, 19:195-201.
17. Cleven B.E., Palka-Santini M., Gielen J., Meembor S., Kronke M., Krut O. Identification and characterization of bacterial pathogens causing bloodstream infections by DNA microarray. J. Clin. Microbiol. 2006, 44:2389-2397.
18. Performance Standards for Antimicrobial Disk and Dilution Suscptibility Tests for Bacteria Isolated from Animals; Approved Standard. CLSI document M31-A3 2008, CLSI, Clinical and Laboratory Standards Institute, Wayne, PA. Third Edition.
19. Fan J., Niu Y. Selection and validation of normalization methods for c-DNA microarrays using within-array replications. Bioinformatics 2007, 23:2391-2398.
20. Fan X., Shi L., Fang H., Harris S., Perkins R., Tong W. Investigation of reproducibility of differentially expressed genes in DNA microarrays through statistical simulation. BMC Proc. 2009, 3(Suppl 2):S4.
21. Fleiss J.L. Statistical Methods for Rates and Proportions 1981, John Wiley & Sons, New York.
22. Frye J.G., Jesse T., Long F., Rondeau G., Porwollik S., McClelland M., Jackson C.R., Englen M., Fedorka-Cray P.J. DNA microarray detection of antimicrobial resistance genes in diverse bacteria. Int. J. Antimicrob. Agents 2006, 27:138-151.
23. Frye J.G., Lindsey R.L., Rondeau G., Porwollik S., Long F., McClelland M., Jackson C.R., Englen M.D., Meinersmann R.J., Berrang M.E., Davis J.A., Barrett J.B., Turpin J.B., Thitaram S.N., Fedorka-Cray P.J. Development of a DNA microarray to detect antimicrobial resistance genes identified in the National Center for Biotechnology Information database. Microb. Drug Resist. 2010, 16:9-19.
24. Grimm V., Ezaki S., Susa M., Knabbe C., Schmid R.D., Bachmann T.T. Use of DNA microarrays for rapid genotyping of TEM beta-lactamases that confer resistance. J. Clin. Microbiol. 2004, 42:3766-3774.
25. Guo L., Lobenhofer E.K., Wang C., Shippy R., Harris S.C., Zhang L., Mei N., Chen T., Herman D., Goodsaid F.M., Hurban P., Phillips K.L., Xu J., Deng X., Sun Y.A., Tong W., Dragan Y.P., Shi L. Rat toxicogenomic study reveals analytical consistency across microarray platforms. Nat Biotechnol. 2006, 24:1162-1169.
26. Hopkins K.L., Batchelor M.J., Anjum M., Davies R.H., Threlfall E.J. Comparison of antimicrobial resistance genes in nontyphoidal salmonellae of serotypes enteritidis, hadar, and virchow from humans and food-producing animals in England and wales. Microb Drug Resist. 2007, 13:281-288.
27. Irizarry R.A., Warren D., Spencer F., Kim I.F., Biswal S., Frank B.C., Gabrielson E., Garcia J.G., Geoghegan J., Germino G., Griffin C., Hilmer S.C., Hoffman E., Jedlicka A.E., Kawasaki E., Martinez-Murillo F., Morsberger L., Lee H., Petersen D., Quackenbush J., Scott A., Wilson M., Yang Y., Ye S.Q., Yu W. Multiple-laboratory comparison of microarray platforms. Nat. Methods. 2005, 2:345-350.
28. Kadota K., Nakai Y., Shimizu K. Ranking differentially expressed genes from Affymetrix gene expression data: methods with reproducibility, sensitivity, and specificity. Algorithms Mol. Biol. 2009, 4:7.
29. Kang M.S., Besser T.E., Call D.R. Variability in the region downstream of the blaCMY-2 beta-lactamase gene in Escherichia coli and Salmonella enterica plasmids. Antimicrob. Agents Chemother. 2006, 50:1590-1593.
30. Lee Y., Lee C.S., Kim Y.J., Chun S., Park S., Kim Y.S., Han B.D. Development of DNA chip for the simultaneous detection of various beta-lactam antibiotic-resistant genes. Mol. Cells 2002, 14:192-197.
31. Ma M., Wang H., Yu Y., Zhang D., Liu S. Detection of antimicrobial resistance genes of pathogenic Salmonella from swine with DNA microarray. J. Vet. Diagn. Investig. 2007, 19:161-167.
32. Majtan T., Majtanova L., Timko J., Majtan V. Oligonucleotide microarray for molecular characterization and genotyping of Salmonella spp. strains. J. Antimicrob. Chemother. 2007, 60:937-946.
33. Malorny B., Bunge C., Guerra B., Prietz S., Helmuth R. Molecular characterisation of Salmonella strains by an oligonucleotide multiprobe microarray. Mol. Cell Probes 2007, 21:56-65.
34. Mao S., Wang C., Dong G. Evaluation of inter-laboratory and cross-platform concordance of DNA microarrays through discriminating genes and classifier transferability. J. Bioinform. Comput. Biol. 2009, 7:157-173.
35. Martinez G., Bruant G., Brousseau R., Masson L., Harel J. Development of a new integrated diagnostic test for identification and characterization of pathogens. Dev. Biol. (Basel) 2006, 126:213-218.
36. McClelland M., Sanderson K.E., Spieth J., Clifton S.W., Latreille P., Courtney L., Porwollik S., Ali J., Dante M., Du F., Hou S., Layman D., Leonard S., Nguyen C., Scott K., Holmes A., Grewal N., Mulvaney E., Ryan E., Sun H., Florea L., Miller W., Stoneking T., Nhan M., Waterston R., Wilson R.K. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 2001, 413:852-856.
37. Michael G.B., Butaye P., Cloeckaert A., Schwarz S. Genes and mutations conferring antimicrobial resistance in Salmonella: an update. Microbes Infect. 2006, 8:1898-1914.
38. Nordmann P., Poirel L., Mak J.K., White P.A., McIver C.J., Taylor P. Multidrug-resistant Salmonella strains expressing emerging antibiotic resistance determinants. Clin. Infect. Dis. 2008, 46:324-325.
39. Perna N.T., Plunkett G., Burland V., Mau B., Glasner J.D., Rose D.J., Mayhew G.F., Evans P.S., Gregor J., Kirkpatrick H.A., Posfai G., Hackett J., Klink S., Boutin A., Shao Y., Miller L., Grotbeck E.J., Davis N.W., Lim A., Dimalanta E.T., Potamousis K.D., Apodaca J., Anantharaman T.S., Lin J., Yen G., Schwartz D.C., Welch R.A., Blattner F.R. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 2001, 409:529-533.
40. Perreten V., Vorlet-Fawer L., Slickers P., Ehricht R., Kuhnert P., Frey J. Microarray-based detection of 90 antibiotic resistance genes of gram-positive bacteria. J. Clin. Microbiol. 2005, 43:2291-2302.
41. Peterson, G., Bai, J., Nagaraja, T.G., Narayanan, S., Diagnostic microarray for human and animal bacterial diseases and their virulence and antimicrobial resistance genes. J Microbiol Methods. 80, 223-230.
42. Pitout J.D. Multiresistant Enterobacteriaceae: new threat of an old problem. Expert Rev. Anti Infect. Ther. 2008, 6:657-669.
43. Pitout J.D., Laupland K.B. Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect. Dis. 2008, 8:159-166.
44. Pritchett L.C., Konkel M.E., Gay J.M., Besser T.E. Identification of DT104 and U302 phage types among Salmonella enterica serotype typhimurium isolates by PCR. J. Clin. Microbiol. 2000, 38:3484-3488.
45. Randegger C.C., Hachler H. Real-time PCR and melting curve analysis for reliable and rapid detection of SHV extended-spectrum beta-lactamases. Antimicrob. Agents Chemother. 2001, 45:1730-1736.
46. Sato F., Tsuchiya S., Terasawa K., Tsujimoto G. Intra-platform repeatability and inter-platform comparability of microRNA microarray technology. PLoS One 2009, 4:e5540.
47. Shi L., Jones W.D., Jensen R.V., Harris S.C., Perkins R.G., Goodsaid F.M., Guo L., Croner L.J., Boysen C., Fang H., Qian F., Amur S., Bao W., Barbacioru C.C., Bertholet V., Cao X.M., Chu T.M., Collins P.J., Fan X.H., Frueh F.W., Fuscoe J.C., Guo X., Han J., Herman D., Hong H., Kawasaki E.S., Li Q.Z., Luo Y., Ma Y., Mei N., Peterson R.L., Puri R.K., Shippy R., Su Z., Sun Y.A., Sun H., Thorn B., Turpaz Y., Wang C., Wang S.J., Warrington J.A., Willey J.C., Wu J., Xie Q., Zhang L., Zhang L., Zhong S., Wolfinger R.D., Tong W. The balance of reproducibility, sensitivity, and specificity of lists of differentially expressed genes in microarray studies. BMC Bioinform. 2008, 9(Suppl 9):S10.
48. Shi L., Perkins R.G., Fang H., Tong W. Reproducible and reliable microarray results through quality control: good laboratory proficiency and appropriate data analysis practices are essential. Curr. Opin. Biotechnol. 2008, 19:10-18.
49. Shi L., Reid L.H., Jones W.D., Shippy R., Warrington J.A., Baker S.C., Collins P.J., de Longueville F., Kawasaki E.S., Lee K.Y., Luo Y., Sun Y.A., Willey J.C., Setterquist R.A., Fischer G.M., Tong W., Dragan Y.P., Dix D.J., Frueh F.W., Goodsaid F.M., Herman D., Jensen R.V., Johnson C.D., Lobenhofer E.K., Puri R.K., Schrf U., Thierry-Mieg J., Wang C., Wilson M., Wolber P.K., Zhang L., Amur S., Bao W., Barbacioru C.C., Lucas A.B., Bertholet V., Boysen C., Bromley B., Brown D., Brunner A., Canales R., Cao X.M., Cebula T.A., Chen J.J., Cheng J., Chu T.M., Chudin E., Corson J., Corton J.C., Croner L.J., Davies C., Davison T.S., Delenstarr G., Deng X., Dorris D., Eklund A.C., Fan X.H., Fang H., Fulmer-Smentek S., Fuscoe J.C., Gallagher K., Ge W., Guo L., Guo X., Hager J., Haje P.K., Han J., Han T., Harbottle H.C., Harris S.C., Hatchwell E., Hauser C.A., Hester S., Hong H., Hurban P., Jackson S.A., Ji H., Knight C.R., Kuo W.P., LeClerc J.E., Levy S., Li Q.Z., Liu C., Liu Y., Lombardi M.J., Ma Y., Magnuson S.R., Maqsodi B., McDaniel T., Mei N., Myklebost O., Ning B., Novoradovskaya N., Orr M.S., Osborn T.W., Papallo A., Patterson T.A., Perkins R.G., Peters E.H., Peterson R., Philips K.L., Pine P.S., Pusztai L., Qian F., Ren H., Rosen M., Rosenzweig B.A., Samaha R.R., Schena M., Schroth G.P., Shchegrova S., Smith D.D., Staedtler F., Su Z., Sun H., Szallasi Z., Tezak Z., Thierry-Mieg D., Thompson K.L., Tikhonova I., Turpaz Y., Vallanat B., Van C., Walker S.J., Wang S.J., Wang Y., Wolfinger R., Wong A., Wu J., Xiao C., Xie Q., Xu J., Yang W., Zhang L., Zhong S., Zong Y., Slikker W. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat. Biotechnol. 2006, 24:1151-1161.
50. Shi L., Tong W., Fang H., Scherf U., Han J., Puri R.K., Frueh F.W., Goodsaid F.M., Guo L., Su Z., Han T., Fuscoe J.C., Xu Z.A., Patterson T.A., Hong H., Xie Q., Perkins R.G., Chen J.J., Casciano D.A. Cross-platform comparability of microarray technology: intra-platform consistency and appropriate data analysis procedures are essential. BMC Bioinform. 2005, 6(Suppl 2):S12.
51. Sim J., Wright C.C. The kappa statistic in reliability studies: use, interpretation, and sample size requirements. Phys. Ther. 2005, 85:257-268.
52. Spence R.P., Wright V., Ala-Aldeen D.A., Turner D.P., Wooldridge K.G., James R. Validation of virulence and epidemiology DNA microarray for identification and characterization of Staphylococcus aureus isolates. J. Clin. Microbiol. 2008, 46:1620-1627.
53. Tong W., Lucas A.B., Shippy R., Fan X., Fang H., Hong H., Orr M.S., Chu T.M., Guo X., Collins P.J., Sun Y.A., Wang S.J., Bao W., Wolfinger R.D., Shchegrova S., Guo L., Warrington J.A., Shi L. Evaluation of external RNA controls for the assessment of microarray performance. Nat. Biotechnol. 2006, 24:1132-1139.
54. van Hoek H.A.M., Scholtens I.M.J., Cloeckaert A., Aarts H.J.M. Detection of antibiotic resistance genes in different Salmonella serovars by oligonucleotide microarray analysis. J. Microbiol. Methods 2005, 62:13-23.
55. Volokhov D., Chizhikov V., Chumakov K., Rasooly A. Microarray analysis of erythromycin resistance determinants. J. Appl. Microb. 2003, 95:787-798.
56. Weiss N.S. Clinical Epidemiology: The Study of the Outcome of Illness 1986, Oxford university Press, New York.
57. Yu X., Susa M., Knabbe C., Schmid R.D., Bachmann T.T. Development and validation of a diagnostic DNA microarray to detect quinolone-resistant Escherichia coli among clinical isolates. J. Clin. Microbiol. 2004, 42:4083-4091.
58. Zhu J., Bozdech Z., DeRisi J. ArrayOligoSelector 2003, http://arrayoligosel.sourceforge.net/. Accessed November, 2005.
59. Zhu L.X., Zhang Z.W., Wang C., Yang H.W., Jiang D., Zhang Q., Mitchelson K., Cheng J. Use of a DNA microarray for simultaneous detection of antibiotic resistance genes among staphylococcal clinical isolates. J. Clin. Microbiol. 2007, 45:3514-3521.
60. Zou W., Frye J.G., Chang C.W., Liu J., Cerniglia C.E., Nayak R. Microarray analysis of antimicrobial resistance genes in Salmonella enterica from preharvest poultry environment. J. Appl. Microbiol. 2009, 107:906-914.