Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest

Applied and Environmental Microbiology

Volumn 79, Issue 18, 2013, Pages 5701-5709

  Marti, Romain ^a   Scott, Andrew ^a   Tien, Yuan Ching ^a   Murray, Roger ^a   Sabourin, Lyne ^a   Zhang, Yun ^a   Topp, Edward ^b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; FERTILIZERS; GENES; HARVESTING; MANURES; POLYMERASE CHAIN REACTION; SOILS; STABILIZATION; VEGETABLES;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; ANTIBIOTIC-RESISTANT BACTERIA; BACTERIA-RESISTANT; FERTILIZED SOILS; HUMAN CONSUMPTION; PLASMID INCOMPATIBILITY; STABILIZATION PROCESS;

ANTIBIOTICS;

ANTIBIOTIC RESISTANCE; CONCENTRATION (COMPOSITION); DETECTION METHOD; FERTILIZER APPLICATION; FREQUENCY ANALYSIS; GROWTH RATE; HARVESTING; MANURE; SOIL MICROORGANISM; STABILIZATION;

CUCUMIS SATIVUS; DAUCUS CAROTA; LACTUCA; LYCOPERSICON ESCULENTUM; RAPHANUS SATIVUS; SUIDAE;

BACTERIAL DNA;

AGRICULTURE; ANIMAL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL LOAD; BACTERIUM; CATTLE; DRUG EFFECT; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MANURE; METHODOLOGY; MICROBIOLOGY; POLYMERASE CHAIN REACTION; SWINE; VEGETABLE;

AGRICULTURE; ANIMALS; BACTERIA; BACTERIAL LOAD; CATTLE; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; GENES, BACTERIAL; HUMANS; MANURE; POLYMERASE CHAIN REACTION; SOIL MICROBIOLOGY; SWINE; VEGETABLES;

EID: 84884239313     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01682-13     Document Type: Article

References (49)

1. Health Canada. 25 April 2013, accession date. Canada's Food Guide. Health Canada, Ottawa, ON, Canada. http://www.hc-sc.gc.ca/fn-an/food -guide-aliment/basics-base/index-eng.php.
2. Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, Frankel G. 2010. Minireview: fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ. Microbiol. 12:2385-2397.
3. Newell DG, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, Opsteegh M, Langelaar M, Threfall J, Scheutz F, van der Giessen J, Kruse H. 2010. Food-borne diseases-the challenges of 20 years ago still persist while new ones continue to emerge. Int. J. Food Microbiol. 139(Suppl):S3-S15.
4. Kozak GK, MacDonald D, Landry L, Farber JM. 2013. Foodborne outbreaks in Canada linked to produce: 2001 through 2009. J. Food Prot. 76:173-183.
5. Food and Drug Administration. 25 April 2013, accession date. Food safety standards. FDA, Washington, DC. http://www.fda.gov/Food/GuidanceR egulation/FSMA/ucm304045.htm.
6. Codex Alimentarius. 26 April 2013, accession date. Code of hygienic practice for fresh fruits and vegetables. World Health Organization, Geneva, Switzerland. http://www.codexalimentarius.org/download/standards/10200/CXP_0 53e.pdf.
7. Canadian Food Inspection Agency. 2009, posting date. Code of Practice for minimally processed ready-to-eat vegetables. Canadian Food Inspection Agency, Ottawa, ON, Canada. http://www.inspection.gc.ca/english /fssa/frefra/safsal/minproe.shtml#s2.
8. Yost CK, Diarra MS, Topp E. 2011. Animals and humans as sources of fecal indicator bacteria, p 67-92. In Sadowsky MJ, Whitman RL (ed), The fecal bacteria. ASM Press, Washington, DC.
9. Hawkey PM, Jones AM. 2009. The changing epidemiology of resistance. J. Antimicrob. Chemother. 64:i3-i10.
10. McEwen SA. 2012. Quantitative human health risk assessments of antimicrobial use in animals and selection of resistance: a review of publicly available reports. Rev. Sci. Tech. 31:261-276.
11. Lanthier M, Scott A, Lapen D, Zhang Y, Topp E. 2010. Frequency of virulence genes and antibiotic resistances in Enterococcus spp. isolates from wastewater and feces of domesticated mammals and birds, and wildlife. Can. J. Microbiol. 56:715-729.
12. Chen B, Zheng W, Yu Y, Huang W, Zheng S, Zhang Y, Guan X, Zhuang Y, Chen N, Topp E. 2011. Class 1 integrons, selected virulence genes, and antibiotic resistance in Escherichia coli isolates from the Minjiang River, Fujian Province, China. Appl. Environ. Microbiol. 77:148-155.
13. Kristiansson E, Fick J, Janzon A, Grabic R, Rutgersson C, Weijdegård B, Söderström H, Larsson DGJ. 2011. Pyrosequencing of antibioticcontaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One 6:e17038. doi:10.1371/journal.pone.0017038.
14. Jury KL, Khan SJ, Vancov T, Stuetz RM, Ashbolt NJ. 2011. Are sewage treatment plants promoting antibiotic resistance? Crit. Rev. Environ. Sci. Technol. 41:243-270.
15. Pruden A, Arabi M, Storteboom HN. 2012. Correlation between upstream human activities and riverine antibiotic resistance genes. Environ. Sci. Technol. 46:11541-11549.
16. Suzuki S, Hoa PTP. 2012. Distribution of quinolones, sulfonamides, tetracyclines in aquatic environment and antibiotic resistance in Indochina. Front. Microbiol. 3:67.
17. Jechalke S, Kopmann C, Rosendahl I, Groeneweg J, Weichelt V, Krögerrecklenfort E, Brandes N, Nordwig M, Ding G-C, Siemens J, Heuer H, Smalla K. 2013. Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Appl. Environ. Microbiol. 79:1704-1711.
18. Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall ABA, Wellington EMH. 2011. Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J. 5:1253-1261.
19. Heuer H, Schmitt H, Smalla K. 2011. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14:236-243.
20. Wellington EMH, Boxall ABA, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP. 2013. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect. Dis. 13: 155-165.
21. Gaze WH, Krone SM, Larsson DGJ, Li X-Z, Robinson J, Simonet P, Smalla K, Timinouni M, Topp E, Wellington EM, Wright GD, Zhu Y-G. 2013. Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg. Infect. Dis. doi:10.3201/eid1907.120871.
22. Line JE. 2001. Development of a selective differential agar for isolation and enumeration of Campylobacter spp. J. Food Prot. 64:1711-1715.
23. Kiess AS, Parker HM, McDaniel CD. 2010. Evaluation of different selective media and culturing techniques for the quantification of Campylobacter ssp. from broiler litter. Poult. Sci. 89:1755-1762.
24. Government of Canada. 2010. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2007. Public Health Agency of Canada, Guelph, ON, Canada.
25. Boehme S, Werner G, Klare I, Reissbrodt R, Witte W. 2004. Occurrence of antibiotic-resistant enterobacteria in agricultural foodstuffs. Mol. Nutr. Food Res. 48:522-531.
26. Rodríguez C, Lang L, Wang A, Altendorf K, García F, Lipski A. 2006. Lettuce for human consumption collected in Costa Rica contains complex communities of culturable oxytetracycline-and gentamicin-resistant bacteria. Appl. Environ. Microbiol. 72:5870-5876.
27. Bezanson GS, MacInnis R, Potter G, Hughes T. 2008. Presence and potential for horizontal transfer of antibiotic resistance in oxidasepositive bacteria populating raw salad vegetables. Int. J. Food Microbiol. 127:37-42.
28. Ruimy R, Brisabois A, Bernede C, Skurnik D, Barnat S, Arlet G, Momcilovic S, Elbaz S, Moury F, Vibet M-A, Courvalin P, Guillemot D, Andremont A. 2010. Organic and conventional fruits and vegetables contain equivalent counts of Gram-negative bacteria expressing resistance to antibacterial agents. Environ. Microbiol. 12:608-615.
29. Hassan SA, Altalhi AD, Gherbawy YA, El-Deeb BA. 2011. Bacterial load of fresh vegetables and their resistance to the currently used antibiotics in Saudi Arabia. Foodborne Pathog. Dis. 8:1011-1018.
30. Raphael E, Wong LK, Riley LW. 2011. Extended-spectrum betalactamase gene sequences in Gram-negative saprophytes on retail organic and nonorganic spinach. Appl. Environ. Microbiol. 77:1601-1607.
31. Schwaiger K, Helmke K, Hölzel CS, Bauer J. 2011. Antibiotic resistance in bacteria isolated from vegetables with regards to the marketing stage (farm vs. supermarket). Int. J. Food Microbiol. 148:191-196.
32. Walia S, Rana SW, Maue D, Rana J, Kumar A, Walia SK. 2013. Prevalence of multiple antibiotic-resistant Gram-negative bacteria on bagged, ready-toeat baby spinach. Int. J. Environ. Health Res. 23:108-118.
33. D'Costa VM, McGrann KM, Hughes DW, Wright GD. 2006. Sampling the antibiotic resistome. Science 311:374-377.
34. Wright GD. 2010. Antibiotic resistance in the environment: a link to the clinic? Curr. Opin. Microbiol. 13:589-594.
35. Davies J, Davies D. 2010. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74:417-433.
36. Bhullar K, Waglechner N, Pawlowski A, Koteva K, Banks ED, Johnston MD, Barton HA, Wright GD. 2012. Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS One 7:e34953. doi:10.1371/journal .pone.0034953.
37. D'Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD. 2011. Antibiotic resistance is ancient. Nature 477:457-461.
38. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107-1111.
39. Sannes MR, Belongia EA, Kieke B, Smith K, Kieke A, Vandermause M, Bender J, Clabots C, Winokur P, Johnson JR. 2008. Predictors of antimicrobial-resistant Escherichia coli in the feces of vegetarians and newly hospitalized adults in Minnesota and Wisconsin. J. Infect. Dis. 197: 430-434.
40. Zhang L, Kinkelaar D, Huang Y, Li Y, Li X, Wang HH. 2011. Acquired antibiotic resistance: are we born with it? Appl. Environ. Microbiol. 77: 7134-7141.
41. Ashbolt NJ, Aézquita A, Backhaus T, Borriello SP, Brandt KK, Collignon P, Coors A, Finley R, Gaze WH, Heberer T, Lawrence JR, Larsson DGJ, McEwen SA, Ryan JJ, Schönfeld J, Silley P, Snape JR, Van den Eede C, Topp E. 2013. Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspect. doi:10.1289/ehp.1206316.
42. Robinson CJ, Bohannan BJM, Young VB. 2010. From structure to function: the ecology of host-associated microbial communities. Microbiol. Mol. Biol. Rev. 74:453-476.
43. Human Microbiome Project. 2012. A framework for human microbiome research. Nature 486:215-221.
44. Sing D, Sing CF. 2010. Impact of direct soil exposures from airborne dust and geophagy on human health. Int. J. Environ. Res. Public Health 7:1205-1223.
45. Topp E, Scott A, Lapen DR, Lyautey E, Duriez P. 2009. Livestock waste treatment systems for reducing environmental exposure to hazardous enteric pathogens: some considerations. Bioresour. Technol. 100:5395-5398.
46. Ma Y, Wilson CA, Novak JT, Riffat R, Aynur S, Murthy S, Pruden A. 2011. Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons. Environ. Sci. Technol. 45:7855-7861.
47. Pruden A, Larsson DGJ, Amézquita A, Collignon P, Brandt KK, Graham DW, Lazorchak JR, Suzuki S, Silley P, Snape JR, Topp E, Zhang T, Zhu YG. Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environment. Health Persp. doi:10.1289/ehp.1206446.
48. Ingham SC, Fanslau MA, Engel RA, Breuer JR, Wright TH, Reith-Rozelle JK, Zhu J. 2005. Evaluation of fertilization-to-planting and fertilization-to-harvest intervals for safe use of noncomposted bovine manure in Wisconsin vegetable production. J. Food Prot. 68:1134-1142.
49. Merchant LE, Rempel H, Forge T, Kannangara T, Bittman S, Delaquis P, Topp E, Ziebell KA, Diarra MS. 2012. Characterization of antibioticresistant and potentially pathogenic Escherichia coli from soil fertilized with litter of broiler chickens fed antimicrobial-supplemented diets. Can. J. Microbiol. 58:1084-1098.