Sampling and pooling methods for capturing herd level antibiotic resistance in swine feces using qPCR and CFU approaches

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Schmidt, Gunilla Veslemøy ^a   Mellerup, Anders ^a   Christiansen, Lasse Engbo ^a   Ståhl, Marie ^a   Olsen, John Elmerdahl ^b   Angen, Øystein ^a,c  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ERYTHROMYCIN; SULFAMETHOXAZOLE; TETRACYCLINE; ANTIINFECTIVE AGENT; BACTERIAL DNA;

ACCURACY; AMPLICON; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; COLIFORM BACTERIUM; COLONY FORMING UNIT; CONTROLLED STUDY; COPY NUMBER VARIATION; FECES ANALYSIS; GENE AMPLIFICATION; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC RESISTANCE; NONHUMAN; PIG; ANIMAL; BACTERIAL COUNT; CHEMISTRY; DRUG EFFECTS; FECES; GENETICS; GRAM NEGATIVE BACTERIUM; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; SPECIMEN HANDLING; VETERINARY;

ANIMALIA; SUIDAE;

ANIMALS; ANTI-BACTERIAL AGENTS; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; DRUG RESISTANCE, MICROBIAL; FECES; GRAM-NEGATIVE BACTERIA; MICROBIAL SENSITIVITY TESTS; REAL-TIME POLYMERASE CHAIN REACTION; SPECIMEN HANDLING; SWINE;

EID: 84938387508     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131672     Document Type: Article

References (51)

1. Aarestrup FM. Association between the consumption of antimicrobial agents in animal husbandry and the occurrence of resistant bacteria among food animals. Int J Antimicrob Ag 1999; 12(4):279-285.
2. McGowan JE Jr. Economic Impact of Antimicrobial Resistance. Emerg Infect Dis 2001; 7(2):286. PMID: 11294725
3. World Health Organization. Surveillance standards for antimicrobial resistance. 2002;WHO/CDS/CSR/DRS/2001.5.
4. van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics links between animals and humans. Int J Antimicrob Agents 2000; 14(4):327-335. PMID: 10794955
5. Sunde M, Fossum K, Solberg A, Sørum H. Antibiotic resistance in Escherichia coli of the normal intestinal flora of swine. Microb Drug Resist 1998; 4(4):289-299. PMID: 9988047
6. Schwarz S, Kehrenberg C, Walsh TR. Use of antimicrobial agents in veterinary medicine and food animal production. Int J Antimicrob Agents 2001; 6; 17(6):431-437. PMID: 11397611
7. Alali WQ, Scott HM, Norby B, Gebreyes W, Loneragan GH. Quantification of the blaCMY-2 in feces from beef feedlot cattle administered three different doses of ceftiofur in a longitudinal controlled field trial. Foodborne Pathog Dis 2009; 6(8):917-924. doi: 10.1089/fpd.2009.0271 PMID: 19622032
8. Fluit AC, Visser MR, Schmitz FJ. Molecular Detection of Antimicrobial Resistance. Clin Microbiol Rev 2001; 14(4):836-871. PMID: 11585788
9. Yu Z, Michel FC Jr, Hansen G, Wittum T, Morrison M. Development and application of real-time PCR assays for quantification of genes encoding tetracycline resistance. Appl Environ Microbiol 2005; 71 (11):6926-6933. PMID: 16269727
10. Chen J, Yu Z, Michel FC Jr, Wittum T, Morrison M. Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Appl Environ Microbiol 2007; 73(14):4407-4416. PMID: 17496134
11. Knapp CW, Zhang W, Sturm BSM, Graham DW. Differential fate of erythromycin and beta-lactam resistance genes from swine lagoon waste under different aquatic conditions. Environ Poll 2010; 158 (5):1506-1512.
12. Skov MN, Carstensen B, Tornøe N, Madsen M. Evaluation of sampling methods for the detection of Salmonella in broiler flocks. J App Microbio 1999; 86:695-700.
13. Wegener HC, Hald T, Lo Fo Wong D, Madsen M, Korsgaard H, Bager F, et al. Salmonella Control Programs in Denmark. Emerg Infect Diseases 2003;(97:) :774-780.
14. Fødevareministeriet. Bekendtgørelse om salmonella hos svin. 2012;BEK 404 af 08/05/2012.
15. Caprioli A, Busani L, Martel JL, Helmuth R. Monitoring of antibiotic resistance in bacteria of animal origin: epidemiological and microbiological methodologies. Int J Antimicrob Agents 2000; 14(4):295-301. PMID: 10794950
16. DANMAP. DANMAP 2012-Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. 2013(ISSN 1600-2032).
17. Chen C, Nace GW, Irwin PL. A 6×6 drop plate method for simultaneous colony counting and MPN enumeration of Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli. J Microbiol Methods 2003;11; 55(2):475-479. PMID: 14529971
18. Hoelzel CS, Harms KS, Kcochenhoff H, Kunz A, Mcoller C, Meyer K, et al. Phenotypic and genotypic bacterial antimicrobial resistance in liquid pig manure is variously associated with contents of tetracyclines and sulfonamides. J Appl Microbiol 2010; 108(5):1642-1656. doi: 10.1111/j.1365-2672.2009.04570.x PMID: 19895649
19. Kazimierczak KA, Scott KP, Kelly D, Aminov RI. Tetracycline Resistome of the Organic Pig Gut. App Environ Microbiol 2009; 75(6):1717-1722.
20. CheeSanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, et al. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 2009; 38(3):1086-1108. doi: 10.2134/jeq2008.0128 PMID: 19398507
21. De Leener E, Martel A, Decostere A, Haesebrouck F. Distribution of the erm (B) Gene, tet racycline Resistance Genes, and Tn 1545-like Transposons in Macrolide-and Lincosamide-Resistant Enterococci from Pigs and Humans. Microbial Drug Resistance 2004; 10(4):341-345. PMID: 15650380
22. Garofalo C, Vignaroli C, Zandri G, Aquilanti L, Bordoni D, Osimani A, et al. Direct detection of antibiotic resistance genes in specimens of chicken and pork meat. Int J Food Microbiol 2007; 113(1):75-83. PMID: 17005283
23. Hammerum AM, Sandvang D, Andersen SR, Seyfarth AM, Porsbo LJ, FrimodtMoller N, et al. Detection of sul1, sul2 and sul3 in sulphonamide resistant Escherichia coli isolates obtained from healthy humans, pork and pigs in Denmark. Int J Food Microbiol 2006; 1; 106(2):235-237. PMID: 16216373
24. Byrne-Bailey KG, Gaze WH, Kay P, Boxall AB, Hawkey PM, Wellington EM. Prevalence of sulfonamide resistance genes in bacterial isolates from manured agricultural soils and pig slurry in the United Kingdom. Antimicrob Agents Chemother 2009; 53(2):696-702. doi: 10.1128/AAC.00652-07 PMID: 19064898
25. Moodley A, Guardabassi L. Transmission of IncN plasmids carrying blaCTX-M-1 between commensal Escherichia coli in pigs and farm workers. Antimicrob Agents Chemother 2009; 53(4):1709-1711. doi: 10.1128/AAC.01014-08 PMID: 19188380
26. Agerso Y, Aarestrup FM, Pedersen K, Seyfarth AM, Struve T, Hasman H. Prevalence of extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in Danish slaughter pigs and retail meat identified by selective enrichment and association with cephalosporin usage. J Antimicrob Chemother 2012; 67(3):582-588. doi: 10.1093/jac/dkr507 PMID: 22207594
27. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997;15; 25(24):4876-4882. PMID: 9396791
28. Aminov RI, Chee-Sanford JC, Garrigues N, Teferedegne B, Krapac IJ, White BA, et al. Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl Environ Microbiol 2002; 68(4):1786-1793. PMID: 11916697
29. Boeckelmann U, Doerries HH, Ayuso-Gabella MN, Salgot de Marcay M, Tandoi V, Levantesi C, et al. Quantitative PCR Monitoring of Antibiotic Resistance Genes and Bacterial Pathogens in Three Eurpean Artificial Groundwater Recharge Systems. Appl Environ Microbiol 2009; 75(1):154-163. doi: 10. 1128/AEM.01649-08 PMID: 19011075
30. Smith MS, Yang RK, Knapp CW, Niu YF, Peak N, Hanfelt MM, et al. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microbiol 2004; 70(12):7372-7377. PMID: 15574938
31. Jacoby GA. β-Lactamase Classification and Amino Acid Sequences for TEM, SHV and OXA Extended-Spectrum and Inhibitor Resistant Enzymes. Available at: http://www.lahey.org/Studies/. Accessed 15-08, 2013.
32. Birkett CI, Ludlam HA, Woodford N, Brown DF, Brown NM, Roberts MT, et al. Real-time TaqMan PCR for rapid detection and typing of genes encoding CTX-M extended-spectrum beta-lactamases. J Med Microbiol 2007; 56:52-55. PMID: 17172517
33. Guardabassi L, Dijkshoorn L, Collard JM, Olsen JE, Dalsgaard A. Distribution and in-vitro transfer of tetracycline resistance determinants in clinical and aquatic Acinetobacter strains. J Med Microbiol 2000; 49:929-936. PMID: 11023190
34. Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM. beta-Lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 2005; 56(1):115-121. PMID: 15941775
35. Archambault M, Petrov P, Hendriksen RS, Asseva G, Bangtrakulnonth A, Hasman H, et al. Molecular characterization and occurrence of extended-spectrum beta-lactamase resistance genes among Salmonella enterica serovar Corvallis from Thailand, Bulgaria, and Denmark. Microb Drug Resist 2006; 12 (3):192-198. PMID: 17002546
36. Angen O, Ahrens P, Tegtmeier C. Development of a PCR test for identification of Haemophilus somnus in pure and mixed cultures. Vet Microbiol 1998;28; 63(1):39-48. PMID: 9810620
37. Angen O, Ståhl M, Agerholm JS, Christoffersen AB, Agger JF. Dynamics of relationship between the presence of Coxiella burnetii DNA, antibodies, and intrinsic variables in cow milk and bulk tank milk from Danish dairy cattle. J Dairy Sci 2011;12; 94(12):5750-5759. doi: 10.3168/jds.2011-4197 PMID: 22118065
38. Harris S, Jones DB. Optimisation of the polymerase chain reaction. British Journal of Biomedical Science 1997; 54:166-173. PMID: 9499593
39. Bibbal D, Dupouy V, Ferre JP, Toutain PL, Fayet O, Prere MF, et al. Impact of three ampicillin dosage regimens on selection of ampicillin resistance in Enterobacteriaceae and excretion of blaTEM genes in swine feces. Appl Environ Microbiol 2007; 73(15):4785-4790. PMID: 17557857
40. Koike S, Krapac IG, Oliver HD, Yannarell AC, CheeSanford JC, Aminov RI, et al. Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Appl Environ Microbiol 2007; 73(15):4813-4823. PMID: 17545324
41. Gniadkowski M, Schneider I, Palucha A, Jungwirth R, Mikiewicz B, Bauernfeind A. Cefotaxime-resistant Enterobacteriaceae isolates from a hospital in Warsaw, Poland: identification of a new CTX-M-3 cefotaxime-hydrolyzing beta-lactamase that is closely related to the CTX-M-1/MEN-1 enzyme. Antimicrob Agents Chemother 1998; 42(4):827-832. PMID: 9559791
42. Heritage J, M'Zali FH, Gascoyne-Binzi D, Hawkey PM. Evolution and spread of SHV extended-spectrum beta-lactamases in Gram-negative bacteria. J Antimicrob Chemother 1999; 44(3):309-318. PMID: 10511397
43. Chanawong A, M'Zali FH, Heritage J, Lulitanond A, Hawkey PM. SHV-12, SHV-5, SHV-2a and VEB-1 extended-spectrum beta-lactamases in Gram-negative bacteria isolated in a university hospital in Thailand. J Antimicrob Chemother 2001; 48(6):839-852. PMID: 11733468
44. Navarro F, Perez-Trallero E, Marimon JM, Aliaga R, Gomariz M, Mirelis B. CMY-2-producing Salmonella enterica, Klebsiella pneumoniae, Klebsiella oxytoca, Proteus mirabilis and Escherichia coli strains isolated in Spain (October 1999-December 2000). J Antimicrob Chemother 2001; 48(3):383-389. PMID: 11533003
45. Baraniak A, Fiett J, Sulikowska A, Hryniewicz W, Gniadkowski M. Countrywide spread of CTX-M-3 extended-spectrum beta-lactamase-producing microorganisms of the family Enterobacteriaceae in Poland. Antimicrob Agents Chemother 2002; 46(1):151-159. PMID: 11751126
46. Li XZ, Mehrotra M, Ghimire S, Adewoye L. beta-Lactam resistance and beta-lactamases in bacteria of animal origin. Vet Microbiol 2007;15; 121(3-4):197-214. PMID: 17306475
47. Muñoz-Zanzi CA, Johnson WO, Thurmond MC, Hietala SK. Pooled-sample testing as a herd-screening tool for detection of bovine viral diarrhea virus persistently infected cattle. J Vet Diagn Invest 2000; 12 (3):195-203. PMID: 10826831
48. Muñoz-Zanzi C, Thurmond M, Hietala S, Johnson W. Factors affecting sensitivity and specificity of pooled-sample testing for diagnosis of low prevalence infections. Prev Vet Med 2006; 74(4):309-322. PMID: 16427711
49. Falk PG, Hooper LV, Midtvedt T, Gordon JI. Creating and Maintaining the Gastrointestinal Ecosystem: What We Know and Need to Know from Gnotobiology. Microbio Molec Bio Rev 1998; 62(4):1157-1170.
50. Dunlop RH, McEwen SA, Meek AH, Friendship RM, Black WD, Clarke RC. Sampling considerations for herd-level measurement of faecal Escherichia coli antimicrobial resistance in finisher pigs. Epi and Infect 1999; 122(3):485-496.
51. Broens EM, Graat EAM, Engel B, van Oosterom RAA, van de Giessen AW, van der Wolf PJ. Comparison of sampling methods used for MRSA-classification of herds with breeding pigs. Vet Microbiol 2011; 147(3-4):440-444. doi: 10.1016/j.vetmic.2010.07.021 PMID: 20727686