#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Quantitative dynamics of Salmonella and E. coli in feces of feedlot cattle treated with ceftiofur and chlortetracycline


Autoři: Naomi Ohta aff001;  Bo Norby aff002;  Guy H. Loneragan aff003;  Javier Vinasco aff001;  Henk C. den Bakker aff004;  Sara D. Lawhon aff001;  Keri N. Norman aff005;  Harvey M. Scott aff001
Působiště autorů: Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, United States of America aff001;  Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, Michigan, United States of America aff002;  School of Veterinary Medicine, Texas Tech University, Amarillo, Texas, United States of America aff003;  Center for Food Safety, University of Georgia, Griffin, Georgia, United States of America aff004;  Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225697

Souhrn

Antibiotic use in beef cattle is a risk factor for the expansion of antimicrobial-resistant Salmonella populations. However, actual changes in the quantity of Salmonella in cattle feces following antibiotic use have not been investigated. Previously, we observed an overall reduction in Salmonella prevalence in cattle feces associated with both ceftiofur crystalline-free acid (CCFA) and chlortetracycline (CTC) use; however, during the same time frame the prevalence of multidrug-resistant Salmonella increased. The purpose of this analysis was to quantify the dynamics of Salmonella using colony counting (via a spiral-plating method) and hydrolysis probe-based qPCR (TaqMan® qPCR). Additionally, we quantified antibiotic-resistant Salmonella by plating to agar containing antibiotics at Clinical & Laboratory Standards Institute breakpoint concentrations. Cattle were randomly assigned to 4 treatment groups across 16 pens in 2 replicates consisting of 88 cattle each. Fecal samples from Days 0, 4, 8, 14, 20, and 26 were subjected to quantification assays. Duplicate qPCR assays targeting the Salmonella invA gene were performed on total community DNA for 1,040 samples. Diluted fecal samples were spiral plated on plain Brilliant Green Agar (BGA) and BGA with ceftriaxone (4 μg/ml) or tetracycline (16 μg/ml). For comparison purposes, indicator non-type-specific (NTS) E. coli were also quantified by direct spiral plating. Quantity of NTS E. coli and Salmonella significantly decreased immediately following CCFA treatment. CTC treatment further decreased the quantity of Salmonella but not NTS E. coli. Effects of antibiotics on the imputed log10 quantity of Salmonella were analyzed via a multi-level mixed linear regression model. The invA gene copies decreased with CCFA treatment by approximately 2 log10 gene copies/g feces and remained low following additional CTC treatment. The quantities of tetracycline or ceftriaxone-resistant Salmonella were approximately 4 log10 CFU/g feces; however, most of the samples were under the quantification limit. The results of this study demonstrate that antibiotic use decreases the overall quantity of Salmonella in cattle feces in the short term; however, the overall quantities of antimicrobial-resistant NTS E. coli and Salmonella tend to remain at a constant level throughout.

Klíčová slova:

Antibiotic resistance – Antibiotics – Cattle – Livestock care – Ribosomal RNA – Salmonella – Tetracyclines


Zdroje

1. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17(1):7–15. doi: 10.3201/eid1701.P11101 21192848

2. NARMS 2015 Integrated Report [Internet]. 2017. https://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoringSystem/UCM581468.pdf.

3. Pires SM, Vieira AR, Hald T, Cole D. Source attribution of human salmonellosis: an overview of methods and estimates. Foodborne Pathog Dis. 2014;11(9):667–76. Epub 2014/06/03. doi: 10.1089/fpd.2014.1744 24885917.

4. Clinton NA, Weaver RW, Hidalgo RJ. Transmission of Salmonella typhimurium among feedlot cattle after oral inoculation. The Journal of applied bacteriology. 1981;50(1):149–55. doi: 10.1111/j.1365-2672.1981.tb00879.x 7014545.

5. Dargatz DA, Strohmeyer RA, Morley PS, Hyatt DR, Salman MD. Characterization of Escherichia coli and Salmonella enterica from cattle feed ingredients. Foodborne Pathog Dis. 2005;2(4):341–7. doi: 10.1089/fpd.2005.2.341 16366856.

6. Fegan N, Vanderlinde P, Higgs G, Desmarchelier P. Quantification and prevalence of Salmonella in beef cattle presenting at slaughter. J Appl Microbiol. 2004;97(5):892–8. doi: 10.1111/j.1365-2672.2004.02380.x 15479403.

7. Fegan N, Vanderlinde P, Higgs G, Desmarchelier P. A study of the prevalence and enumeration of Salmonella enterica in cattle and on carcasses during processing. J Food Prot. 2005;68(6):1147–53. Epub 2005/06/16. doi: 10.4315/0362-028x-68.6.1147 15954700.

8. Brichta-Harhay DM, Arthur TM, Bosilevac JM, Guerini MN, Kalchayanand N, Koohmaraie M. Enumeration of Salmonella and Escherichia coli O157:H7 in ground beef, cattle carcass, hide and faecal samples using direct plating methods. J Appl Microbiol. 2007;103(5):1657–68. doi: 10.1111/j.1365-2672.2007.03405.x 17953577.

9. Kunze DJ, Loneragan GH, Platt TM, Miller MF, Besser TE, Koohmaraie M, et al. Salmonella enterica burden in harvest-ready cattle populations from the southern high plains of the United States. Appl Environ Microbiol. 2008;74(2):345–51. doi: 10.1128/AEM.02076-07 18024678

10. Arthur TM, Brichta-Harhay DM, Bosilevac JM, Kalchayanand N, Shackelford SD, Wheeler TL, et al. Super shedding of Escherichia coli O157:H7 by cattle and the impact on beef carcass contamination. Meat Sci. 2010;86(1):32–7. doi: 10.1016/j.meatsci.2010.04.019 20627603.

11. Wheeler TL, Kalchayanand N, Bosilevac JM. Pre- and post-harvest interventions to reduce pathogen contamination in the U.S. beef industry. Meat Sci. 2014;98(3):372–82. Epub 2014/07/17. doi: 10.1016/j.meatsci.2014.06.026 25027798.

12. Brichta-Harhay DM, Arthur TM, Koohmaraie M. Enumeration of Salmonella from poultry carcass rinses via direct plating methods. Letters in applied microbiology. 2008;46(2):186–91. doi: 10.1111/j.1472-765X.2007.02289.x 18069983.

13. Koohmaraie M, Scanga JA, De La Zerda MJ, Koohmaraie B, Tapay L, Beskhlebnaya V, et al. Tracking the sources of salmonella in ground beef produced from nonfed cattle. J Food Prot. 2012;75(8):1464–8. doi: 10.4315/0362-028X.JFP-11-540 22856570.

14. Leekha S, Terrell CL, Edson RS. General principles of antimicrobial therapy. Mayo Clin Proc. 2011;86(2):156–67. Epub 2011/02/02. doi: 10.4065/mcp.2010.0639 21282489

15. FDA. Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals 2015

16. Ohta N, Norman KN, Norby B, Lawhon SD, Vinasco J, den Bakker H, et al. Population dynamics of enteric Salmonella in response to antimicrobial use in beef feedlot cattle. Sci Rep. 2017;7(1):14310. doi: 10.1038/s41598-017-14751-9 29085049

17. Singer RS, Patterson SK, Wallace RL. Effects of therapeutic ceftiofur administration to dairy cattle on Escherichia coli dynamics in the intestinal tract. Appl Environ Microbiol. 2008;74(22):6956–62. doi: 10.1128/AEM.01241-08 18820057

18. Daniels JB, Call DR, Hancock D, Sischo WM, Baker K, Besser TE. Role of ceftiofur in selection and dissemination of blaCMY-2-mediated cephalosporin resistance in Salmonella enterica and commensal Escherichia coli isolates from cattle. Appl Environ Microbiol. 2009;75(11):3648–55. doi: 10.1128/AEM.02435-08 19376926

19. Schmidt JW, Griffin D, Kuehn LA, Brichta-Harhay DM. Influence of therapeutic ceftiofur treatments of feedlot cattle on fecal and hide prevalences of commensal Escherichia coli resistant to expanded-spectrum cephalosporins, and molecular characterization of resistant isolates. Appl Environ Microbiol. 2013;79(7):2273–83. doi: 10.1128/AEM.03592-12 23354706

20. Agga GE, Schmidt JW, Arthur TM. Effects of In-Feed Chlortetracycline Prophylaxis in Beef Cattle on Animal Health and Antimicrobial-Resistant Escherichia coli. Appl Environ Microbiol. 2016;82(24):7197–204. doi: 10.1128/AEM.01928-16 27736789

21. Cassin MH, Lammerding AM, Todd EC, Ross W, McColl RS. Quantitative risk assessment for Escherichia coli O157:H7 in ground beef hamburgers. International journal of food microbiology. 1998;41(1):21–44. Epub 1998/06/19. doi: 10.1016/s0168-1605(98)00028-2 9631335.

22. McCullough NB, Eisele CW. Experimental human salmonellosis. I. Pathogenicity of strains of Salmonella meleagridis and Salmonella anatum obtained from spray-dried whole egg. The Journal of infectious diseases. 1951;88(3):278–89. Epub 1951/05/01. doi: 10.1093/infdis/88.3.278 14850755.

23. Mirzaagha P, Louie M, Sharma R, Yanke LJ, Topp E, McAllister TA. Distribution and characterization of ampicillin- and tetracycline-resistant Escherichia coli from feedlot cattle fed subtherapeutic antimicrobials. BMC Microbiol. 2011;11:78. doi: 10.1186/1471-2180-11-78 21504594.

24. Kadykalo SV, Anderson MEC, Alsop JE. Passive surveillance of antimicrobial resistance in Salmonella and Escherichia coli isolates from Ontario livestock, 2007–2015. The Canadian veterinary journal La revue veterinaire canadienne. 2018;59(6):617–22. Epub 2018/06/19. 29910475

25. Douard G, Praud K, Cloeckaert A, Doublet B. The Salmonella genomic island 1 is specifically mobilized in trans by the IncA/C multidrug resistance plasmid family. PLoS One. 2010;5(12):e15302. doi: 10.1371/journal.pone.0015302 21187963

26. Kanwar N, Scott HM, Norby B, Loneragan GH, Vinasco J, McGowan M, et al. Effects of ceftiofur and chlortetracycline treatment strategies on antimicrobial susceptibility and on tet(A), tet(B), and bla CMY-2 resistance genes among E. coli isolated from the feces of feedlot cattle. PloS one. 2013;8(11):e80575. doi: 10.1371/journal.pone.0080575 24260423

27. CLSI. Performance standards for antimicrobial disk susceptibility tests; Approved standard-Twelfth Edition. Clinical and Laboratory Standards Institute, Wayne, PA. 2015.

28. NARMS. Antibiotics tested by NARMS [updated March 15, 2019]. https://www.cdc.gov/narms/antibiotics-tested.html.

29. Lowrance TC, Loneragan GH, Kunze DJ, Platt TM, Ives SE, Scott HM, et al. Changes in antimicrobial susceptibility in a population of Escherichia coli isolated from feedlot cattle administered ceftiofur crystalline-free acid. American Journal of Veterinary Research. 2007;68(5):501–7. doi: 10.2460/ajvr.68.5.501 17472449

30. Kanwar N, Scott HM, Norby B, Loneragan GH, Vinasco J, Cottell JL, et al. Impact of treatment strategies on cephalosporin and tetracycline resistance gene quantities in the bovine fecal metagenome. Scientific reports. 2014;4:5100. doi: 10.1038/srep05100 24872333

31. Fey A, Eichler S, Flavier S, Christen R, Hofle MG, Guzman CA. Establishment of a real-time PCR-based approach for accurate quantification of bacterial RNA targets in water, using Salmonella as a model organism. Appl Environ Microbiol. 2004;70(6):3618–23. doi: 10.1128/AEM.70.6.3618-3623.2004 15184165

32. Brankatschk R, Bodenhausen N, Zeyer J, Burgmann H. Simple absolute quantification method correcting for quantitative PCR efficiency variations for microbial community samples. Appl Environ Microbiol. 2012;78(12):4481–9. Epub 2012/04/12. doi: 10.1128/AEM.07878-11 22492459

33. Galan JE, Ginocchio C, Costeas P. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol. 1992;174(13):4338–49. Epub 1992/07/01. doi: 10.1128/jb.174.13.4338-4349.1992 1624429

34. Rahn K, De Grandis SA, Clarke RC, McEwen SA, Galan JE, Ginocchio C, et al. Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Molecular and cellular probes. 1992;6(4):271–9. Epub 1992/08/01. doi: 10.1016/0890-8508(92)90002-f 1528198.

35. Gonzalez-Escalona N, Hammack TS, Russell M, Jacobson AP, De Jesus AJ, Brown EW, et al. Detection of live Salmonella sp. cells in produce by a TaqMan-based quantitative reverse transcriptase real-time PCR targeting invA mRNA. Appl Environ Microbiol. 2009;75(11):3714–20. doi: 10.1128/AEM.02686-08 19376910

36. Steinman CR, Muralidhar B, Nuovo GJ, Rumore PM, Yu D, Mukai M. Domain-directed polymerase chain reaction capable of distinguishing bacterial from host DNA at the single-cell level: characterization of a systematic method to investigate putative bacterial infection in idiopathic disease. Anal Biochem. 1997;244(2):328–39. Epub 1997/01/15. doi: 10.1006/abio.1996.9896 9025950.

37. Pires AF, Funk JA, Lim A, Bolin SR. Enumeration of salmonella in feces of naturally infected pigs. Foodborne Pathog Dis. 2013;10(11):933–7. doi: 10.1089/fpd.2013.1547 23944750.

38. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55(4):611–22. Epub 2009/02/28. doi: 10.1373/clinchem.2008.112797 19246619.

39. Y. M. Multiple-imputation analysis using Stata’s mi command. 2010 [cited 2018 3-29-2018]. https://www.stata.com/meeting/boston10/boston10_marchenko.pdf.

40. Yulia V. Marchenko WE. A note on how to perform multiple-imputation diagnostics in Stata [cited 2018 3-29-2018]. https://www.stata.com/users/ymarchenko/midiagnote.pdf.

41. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature. 2013;502(7469):96–9. doi: 10.1038/nature12503 23995682

42. Schmidt JW, Agga GE, Bosilevac JM, Brichta-Harhay DM, Shackelford SD, Wang R, et al. Occurrence of Antimicrobial-Resistant Escherichia coli and Salmonella enterica in the Beef Cattle Production and Processing Continuum. Appl Environ Microbiol. 2015;81(2):713–25. doi: 10.1128/AEM.03079-14 25398858

43. McCall MN, McMurray HR, Land H, Almudevar A. On non-detects in qPCR data. Bioinformatics. 2014;30(16):2310–6. Epub 2014/04/26. doi: 10.1093/bioinformatics/btu239 24764462

44. Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. Bmj. 2009;338:b2393. Epub 2009/07/01. doi: 10.1136/bmj.b2393 19564179

45. Boyer TC, Hanson T, Singer RS. Estimation of low quantity genes: a hierarchical model for analyzing censored quantitative real-time PCR data. PLoS One. 2013;8(5):e64900. Epub 2013/06/07. doi: 10.1371/journal.pone.0064900 23741414

46. Hulsen T, de Vlieg J, Alkema W. BioVenn—a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC genomics. 2008;9:488. Epub 2008/10/18. doi: 10.1186/1471-2164-9-488 18925949


Článek vyšel v časopise

PLOS One


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

plice
INSIGHTS from European Respiratory Congress
nový kurz

Současné pohledy na riziko v parodontologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#