Antimicrobial resistance (the AMR project)

Funding period: 2016-2022
Participating Departments and Agencies: Agriculture and Agri-Food Canada, Canadian Food Inspection Agency, Health Canada, National Research Council of Canada, Public Health Agency of Canada
Lead: Ed Topp, AAFC
Total GRDI funding: $11,144,726

The development of resistance to antimicrobials by bacteria that were formerly sensitive is one of the most serious global health threats facing the world today. With no action, annual worldwide human deaths attributable to antimicrobial resistance could reach 10 million by 2050. The Antimicrobial Resistance project uses a genomics-based approach to understand how food production contributes to the development of antimicrobial resistance of human health concern, and explore strategies for reducing antimicrobial resistance in food production systems. It is a component of the Federal Action Plan for Antimicrobial Resistance and Use in Canada. The project involves scientists from 5 federal departments and agencies.

Highlights

  • 6 year collaboration
  • 23 scientists and their teams
  • 5 federal departments and agencies

Key Achievements

  • An understanding of the critical processes that contribute to AMR emergence in food production systems
  • A perspective on critical exposure pathways by which AMR bacteria of agricultural origin reach humans
  • Tools and an analytical infrastructure to elucidate the transmission of antimicrobial resistance
  • Alternatives to antibiotics

Benefits

  • Informed public health and food production decisions to address one of the most serious global health threats facing the world today
  • Reduced antimicrobial resistance in food production systems

Publications
  • Adator EH, Narvaez-Bravo C, Zaheer R, et al. 2020. A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant Escherichia coli from Beef Production, Sewage and Clinical Settings. Microorganisms. 8(6):E885. https://doi.org/10.3390/microorganisms8060885
  • Adator EH, Walker M, Narvaez-Bravo C, et al. 2020. Whole Genome Sequencing Differentiates Presumptive Extended Spectrum Beta-Lactamase Producing Escherichia coli along Segments of the One Health Continuum. Microorganisms. 8(3):448. https://doi.org/10.3390/microorganisms8030448
  • Banerjee S, Gill A, Pagotto F, Tamber S, Ronholm J. 2019. Changes detected in the genome sequences of Escherichia coli, Listeria monocyto genes, Vibrio parahaemolyticus, and Salmonella enterica after serial subculturing. Can J Microbiol. 29:1-9. https://doi.org/10.1139/cjm-2019-0235
  • Boyd D, Lefebvre B, Mataseje L, Gagnon S, Roger M, Savard P, Longtin J, Mulvey M. 2020. Enterobacter sp. N18-03635 harbouring blaFRI-6 class A carbapenemase, Canada. Antimicrobial Agents and Chemotherapy. 75: 486-488. https://doi.org/10.1093/jac/dkz438
  • Boyd D, Lisboa L, Rennie R, Zhanel GG, Dingle T, Mulvey M. 2019. Identification of a novel metallo-β-lactamase, CAM-1, in clinical Pseudomonas aeruginosa isolates from Canada. Journal of Antimicrobial Chemotherapy. 74:1563-1567. https://doi.org/10.1093/jac/dkz066
  • Boyd D, Mataseje L, Pelude L, Mitchell R, Bryce E, Roscoe D, Embree J. Katz K, Kibsey P, Lavallee C, Simor A, Taylor G, Turgeon N, Langley J, Amaratunga K, Mulvey M. 2019. Results from the Canadian Nosocomial Infection Surveillance Program for Detection of Carbapenemase Producing Acinetobacter spp. in Canadian hospitals, 2010-2016. Journal of Antimicrobial Chemotherapy. 74:315-320. https://doi.org/10.1093/jac/dky416
  • Carson C, Li X-Z, Agunos A, Loest D, Chapman B, Finley R, Mehrotra M, Sherk LM, Gaumond R, Irwin R. 2019. Ceftiofur-resistant Salmonella enterica serovar Heidelberg of poultry origin – a risk profile using the Codex framework. Epidemiol. Infect. 147:e296. https://doi.org/10.1017/s0950268819001778
  • Collineau L, Boerlin P, Carson CA, Chapman B, Fazil A, Hetman B, McEwen SA, Parmley EJ, Reid-Smith RJ, Taboada EN, Smith BA. 2019. Integrating whole-genome sequencing data into quantitative risk assessment of foodborne antimicrobial resistance: A review of opportunities and challenges. Front. Microbiol. 10:1107. https://doi.org/10.3389/fmicb.2019.01107
  • Collineau L, Chapman B, Bao X, Sivapathasundaram B, Carson CA, Fazil A, Reid-Smith RJ, Smith BA. 2020. A farm-to-fork quantitative risk assessment model for Salmonella Heidelberg resistant to third-generation cephalosporins in broiler chickens in Canada. International Journal of Food Microbiology. Volume 330. https://doi.org/10.1016/j.ijfoodmicro.2020.108559
  • Collineau L, Phillips C, Agunos A, Carson C, Chapman B, Fazil A, Reid-Smith R, Smith BA. 2020. A within-flock model of Salmonella Heidelberg transmission in broiler chickens. Prev. Vet. Med. 174:104823. https://doi.org/10.1016/j.prevetmed.2019.104823
  • Cooper AL, Carrillo CD, Deschênes M, Blais BW. 2020. Genomic markers for quaternary ammonium compound resistance as a persistence indicator for Listeria monocytogenes contamination in food manufacturing environments. J. Food. Prot. https://doi.org/10.4315/JFP-20-328
  • Cooper AL, Carter C, McLeod H, Wright M, Sritharan P, Tamber S, et al. 2021. Detection of carbapenem-resistance genes in bacteria isolated from wastewater in Ontario. FACETS. https://doi.org/10.1139/facets-2020-0101
  • Cooper AL, Low AJ, Koziol AG, Thomas MC, Leclair D, Tamber S, Wong A, Blais BW, Carrillo CD. 2020. Whole genome sequence-based predictions of serotype and antimicrobial resistance for Salmonella isolates from Canadian poultry. Frontiers in Microbiology. 11: 549. https://doi.org/10.3389/fmicb.2020.00549
  • Das Q, Lepp D, Yin X, Ross K, McCallum J L, Warriner K, Diarra M S. 2019. Transcriptional profiling of Salmonella enterica serovar Enteritidis exposed to ethanolic extract of organic cranberry pomace. PLoS One.3. 14(7):e0219163. https://doi.org/10.1371/journal.pone.0219163
  • Das Q, Islam MdR, Lepp D, Tang J, Yin X, Mats L, Liu H, Ross K, Kennes YM, Yacini H, Warriner K, Marcone MF, Diarra MS. 2020. Gut microbiota, blood metabolites and spleen immunity in broiler chickens fed berry pomaces and phenolic-enriched extractives. Frontiers Veterinary Science. 7:150. https://doi.org/10.3389/fvets.2020.00150
  • Das Q, Tang J, Yin X, Ross K, Warriner K, Marcone MF, Diarra MS. 2020. Organic cranberry pomace and its ethanolic extractives as feed supplement in broiler: impacts on serum immunoglobulin titers, liver and bursal immunity. Poultry Science. 100(2):517-526. https://doi.org/10.1016/j.psj.2020.09.044
  • Diarra MS, Hassan YI, Block GS, Drover JC-G, Delaquis P, Oomah BD. 2020. Antibacterial activities of a polyphenolic-rich extract prepared from American cranberry (Vaccinium macrocarpon) fruit pomace against Listeria spp. LWT - Food Science and Technology. 123:109056. https://doi.org/10.1016/j.lwt.2020.109056
  • Diarra MS, Zhao X, Butaye P. 2021. Editorial: Antimicrobial Use, Antimicrobial Resistance, and the Microbiome in Food Animals. Front. Vet. Sci. 7:638781. http://doi.org/10.3389/fvets.2020.638781
  • Eshaghi A, Zittermann S, Bharat A, Mulvey MR, Allen VG, Patel SN. 2019. Importation of extensively drug resistant (XDR) Salmonella Typhi cases in Ontario, Canada. Antimicrobial Agents and Chemotherapy. 64:e02581-19. https://doi.org/10.1128/AAC.02581-19
  • Hannon SJ, Brault SA, Otto SJG, Morley PS, McAllister TA, Booker CW, Gow SP. 2020. Feedlot Cattle Antimicrobial Use Surveillance Network: A Canadian Journey: Frontiers in Veterinary Science. 7:596042. https://doi.org/10.3389/fvets.2020.596042
  • Holman DB, Gzyl KE, Zaheer R, Jones TH, McAllister TA. 2019. Draft Genome Sequences of 43 Enterococcus faecalis and Enterococcus faecium Isolates from a Commercial Beef Processing Plant and Retail Ground Beef. Microbiol Resour Announc. 8(42):e00974-19. https://doi.org/10.1128/MRA.00974-19
  • Islam MdR, Hassan YI, Das Q, Lepp D, Hernandez M, Godfrey DV, Orban S, Ross K, Delaquis P, Diarra MS. 2020. Dietary organic cranberry pomace influences multiple blood biochemical parameters and cecal microbiota in pasture-raised broiler chickens. Journal of Functional Foods 72:104053. https://doi.org/10.1016/j.jff.2020.104053
  • Kahn LH, Bergeron G, Bourassa MW, De Vegt B, Gill J, Gomes F, Malouin F, Opengart K, Ritter GD, Singer R, Storrs C, Topp E. 2019. From farm management to bacteriophage therapy: established and emerging strategies to reduce antibiotic use in animal agriculture. N.Y. Acad. Sci. 1441(1): 31-39. https://doi.org/10.1111/nyas.14034
  • Laskey A, Devenish J, Kang M, Savic M, Chmara J, Dan H, Lin M, Robertson J, Bessonov K, Gurnik S, Liu K, Nash JHE, Topp E, Guan J. 2021. Mobility of β-lactam resistance under ampicillin treatment in gut microbiota suffering from pre-disturbance. Microb Genom. 7(12):000713. https://doi.org/10.1099/mgen.0.000713
  • Laskey A, Ottenbrite M, Devenish J, Kang M, Savic M, Nadin-Davis S, Chmara J, Lin M, Robertson J, Bessonov K, Gurnik S, Liu K, Nash JHE, Scott A, Topp E, Guan J. 2020. Mobility of β-Lactam resistance under bacterial co-infection and ampicillin treatment in a mouse model. Front. Microbiol. 11:1591. https://doi.org/10.3389/fmicb.2020.01591
  • Lau CH, DeJong EN, Dussault F, Carrillo C, Stogios PJ, Savchenko A, Topp E. 2020. A penicillin-binding protein that can promote advanced-generation cephalosporin resistance and genome adaptation in the opportunistic pathogen Pseudomonas aeruginosa. Int J Antimicrob Agents. 55(3):105896. https://doi.org/10.1016/j.ijantimicag.2020.105896
  • Lau CH-F, Tien Y-C, Stedtfeld RD, Topp E. 2020. Impacts of multi-year field exposure of agricultural soil to macrolide antibiotics on the abundance of antibiotic resistance genes and selected mobile genetic elements. Sci.Total Environ. 727:138520. https://doi.org/10.1016/j.scitotenv.2020.138520
  • Links MG, Dumonceaux TJ, McCarthy EL, Hemmingsen SM, Topp E, Town JR. 2021. CaptureSeq: Hybridization-based enrichment of cpn60 gene fragments reveals the community structures of synthetic and natural microbial ecosystems. Microorganisms 9(4): 816. https://doi.org/10.3390/microorganisms9040816
  • Liu X, Teixeira JS, Ner S, Ma K, Petronella N, Banerjee S, Ronholm J. 2020. Exploring the potential of the microbiome as a marker of the geographic origin of fresh seafood. Front. Microbiol. 11:e696. https://doi.org/10.3389/fmicb.2020.00696
  • Ma Y, Chen J, Fong K, Nadya S, Allen K, Laing C, Ziebell K, Topp E, Carroll LM, Wiedmann M, Delaquis P, Wang S. 2021. Antibiotic resistance in shiga toxigenic Escherichia coli isolates from surface waters and sediments in a mixed use urban agricultural landscape. Antibiotics. 10(3):237. https://doi.org/10.3390/antibiotics10030237
  • McDonald KL, Garland S, Carson CA, Gibbens K, Parmley EJ, Finley R, MacKinnon MC. 2021. Measures used to assess the burden of ESBL-producing Escherichia coli infections in humans: a scoping review. JAC Antimicrob Resist. 2021 Feb 14;3(1):dlaa104. https://doi.org/10.1093/jacamr/dlaa104
  • MacKinnon MC, Sargeant JM, Pearl DL, Reid-Smith RJ, Carson CA, Parmley EJ, McEwen SA. 2020. Evaluation of the health and healthcare system burden due to antimicrobial-resistant Escherichia coli infections in humans: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 9(1):200. https://doi.org/10.1186/s13756-020-00863-x
  • Maguire F, Rehman MA, Carrillo C, Diarra MS, Beiko RG. 2019. Identification of primary antimicrobial resistance drivers in agricultural nontyphoidal Salmonella enterica serovars by using machine learning. MSystems. 4: e00211-19. https://doi.org/10.1128/mSystems.00211-19
  • Maguire F, Rehman MA, Carrillo C, Diarra MS, Beiko RG. 2019. Identification of primary antimicrobial resistance drivers in agricultural nontyphoidal Salmonella enterica serovars by using machine learning. MSystems. 4: e00211-19. https://doi.org/10.1128/mSystems.00211-19
  • Manaia CM, Graham D, Topp E, Martinez JL, Collignon P, Gaze WH. 2020 Antibiotic Resistance in the Environment: Expert Perspectives. In: The Handbook of Environmental Chemistry. Springer, Berlin, Heidelberg. https://link.springer.com/chapter/10.1007/698_2020_472
  • Mangat C, Bekal S, Bharat A, Avery BP, Côté G, Daignault D, Doualla-Bell F, Finley R, Lefèbvre B, Parmley EJ, Reid-Smith RJ, Longtin J, Irwin RJ, Mulvey MR. 2019. Genomic investigation of the emergence of invasive multidrug resistant Salmonella Dublin in humans and animals in Canada. Antimicrobial Agents and Chemotherapy. pii: e00108-19. https://doi.org/10.1128/AAC.00108-19
  • Marano RBM… Scott A, Topp E, Cytryn E [74 authors]. 2020. A global multinational survey of cefotaxime-resistant coliforms in urban wastewater treatment plants. Environ. Intern. 144, 106035. https://doi.org/10.1016/j.envint.2020.106035
  • Martin-Laurent F, Topp E, Billet L, Batisson I, Malandain C, Besse-Hoggan P, Morin So, Artigas J, Bonnineau C, Kergoat L, Devers-Lamrani M, Pesce S. 2020. Environmental risk assessment of antibiotics in agroecosystems: Ecotoxicological effects on aquatic microbial communities and dissemination of antimicrobial resistances and antibiotic biodegradation potential along the soil-water continuum. Environ. Sci. Poll Res. 26(18):18930-18937. https://doi.org/10.1007/s11356-019-05122-0f
  • Martin-Laurent F, Topp E, Billet L, Batisson I, Malandain C, Besse-Hoggan P, Morin So, Artigas J, Bonnineau C, Kergoat L, Devers-Lamrani M, Pesce S. 2020. Environmental risk assessment of antibiotics in agroecosystems: Ecotoxicological effects on aquatic microbial communities and dissemination of antimicrobial resistances and antibiotic biodegradation potential along the soil-water continuum. Environ. Sci. Poll Res. 26(18):18930-18937. https://doi.org/10.1007/s11356-019-05122-0f
  • Mataseje LF, Boyd DA, Mulvey MR, Longtin Y. 2019. Two hypervirulent Klebsiella pneumoniae isolates producing a blaKPC-2 carbapenemase from a Canadian patient. Antimicrobial Agents and Chemotherapy. 63:pii: e00517-19. https://doi.org/10.1128/AAC.00517-19
  • Petrillo M, Fabbri M, Kagkli DM, et al. 2021. A roadmap for the generation of benchmarking resources for antimicrobial resistance detection using next generation sequencing. F1000Research 2021, 10:80 https://doi.org/10.12688/f1000research.39214.1
  • Poulin-Laprade D, Brouard J-S, Gagnon N, Turcotte A, Langlois A, Matte JJ, Carrillo CD, Zaheer R, McAllister TA, Topp E, Talbot G. 2021. Resistance determinants and their genetic context in enterobacteria from a longitudinal study of pigs reared under various husbandry conditions. Appl Environ Microbiol 87:e02612-20. https://doi.org/10.1128/AEM.02612-20
  • Rehman MA, Hasted T-L, Persaud-Lachhman MG, Yin X, Carrillo C, Diarra MS. 2019. Genome analysis and multiplex PCR method for the molecular detection of coresistance to cephalosporins and fosfomycin in Salmonella enterica serovar Heidelberg. J. Food. Prot. 82:1938-49. https://doi.org/10.4315/0362-028X.JFP-19-205
  • Rehman MA, Rempel H, Carrillo CD, Ziebell K, Allen K, Manges AR, Topp E, Diarra MS. 2022. Virulence genotype and phenotype of multiple antimicrobial resistant Escherichia coli isolates from broilers assessed in a "One-Health" Perspective. Journal of Food Protection, Vol. 85, No. 2, 2022, Pages 336–354. https://doi.org/10.4315/JFP-21-273
  • Robertson J, Bessonov K, Schonfeld J, Nash JHE. 2020. Universal whole-sequence-based plasmid typing and its utility to prediction of host range and epidemiological surveillance. Microbial Genomics 6(10). https://doi.org/10.1099/mgen.0.000435
  • Said LB, Emond-Rheault J-G, Soltani S, Telhig S, Zirah S, Rebuffat S, Diarra MS, Goodridge L, Levesque RC, Flis I. 2020. Phenomic and genomic approaches to studying the inhibition of multiresistant Salmonella enterica by microcin J25. Environ Microbiol. 22(7):2907-2920. https://doi.org/10.1111/1462-2920.15045
  • Sanderson H, Ortega-Polo R, Zaheer R, et al. 2020. Comparative genomics of multidrug-resistant Enterococcus spp. isolated from wastewater treatment plants. BMC Microbiol. 20(1):20. https://doi.org/10.1186/s12866-019-1683-4
  • Schonfeld J, Clark C, Robertson J, Arya G, Eagle SHC, Gurnik S, Johnson R, Labbe G, Liu K, Kernaghan S, Mazzocco A, MacKinnon J, Ziebell K, Nash JHE. 2021. Complete Genome Sequences for 36 Canadian Salmonella enterica Serovar Typhimurium and I 1, 4[5], 12: i:–Isolates from Clinical and Animal Sources. Microbiology Resource Announcements 10(1). https://doi.org/10.1128/MRA.00734-20
  • Scott A, Murray R, Tien Y-C, Topp E. 2022. Contamination of hay and haylage with enteric bacteria and selected antibiotic resistance genes following fertilization with dairy manure or biosolids. Can J Microbiol. 2022 68(4):249-257. https://doi.org/10.1139/cjm-2021-0326
  • Steinkey R, Moat J, Gannon V, Zovoilis A, Laing C. 2020. Application of artificial intelligence to the in silico assessment of antimicrobial resistance and risks to human and animal health presented by priority enteric bacterial pathogens. Can Commun Dis Rep. 46-6: 180-185. https://doi.org/10.14745/ccdr.v46i06a05
  • Subirats J, Murray R, Scott A, Lau CH-F, Topp E. 2020. Composting of chicken litter from commercial broiler farms reduces the abundance of viable enteric bacteria, Firmicutes, and selected antibiotic resistance genes. Sci. Tot. Environ. 746, 141113. htpps://doi.org/10.1016/j.scitotenv.2020.141113
  • Subirats J, Murray R, Yin X, Zhang T, Topp E. 2021. Impact of chicken litter pre-application treatment on the abundance, field persistence, and transfer of antibiotic resistant bacteria and antibiotic resistance genes to vegetables. Sci Total Environ. 801:149718. https://doi.org/10.1016/j.scitotenv.2021.149718
  • Taggar G, Rehman MA, Boerlin P, Diarra MS. 2020. Molecular epidemiology of carbapenemases in Enterobacteriales from humans, animals, food and the environment. Antibiotics 9:693. https://doi.10.3390/antibiotics9100693
  • Tran TT, Scott A, Tien YC, Murray R, Boerlin P, Pearl DL, Liu K, Robertson J, Nash JHE, Topp E. 2021. On-farm anaerobic digestion of dairy manure reduces the abundance of antibiotic resistance-associated gene targets, and the potential for plasmid transfer. Appl. Environ. Microbiol. 87(14). https://doi.org/10.1128/AEM.02980-20
  • Turcotte C, Thibodeau A, Quessy S, Topp E, Beauchamp G, Fravalo P, Archambault M, Gaucher M-L. 2020. Impacts of short-term antibiotic withdrawal and long-term judicious antibiotic use on resistance gene abundance and cecal microbiota composition on commercial broiler chicken farms in Québec. Front Vet Sci. 7: 547181. https://doi.org/10.3389/fvets.2020.547181
  • Tymensen L, Booker CW, Hannon SJ, et al. 2019. Plasmid Distribution among Escherichia coli from Livestock and Associated Wastewater: Unraveling Factors That Shape the Presence of Genes Conferring Third-Generation Cephalosporin Resistance. Environ Sci Technol. 53(20):11666-11674. https://doi.org/10.1021/acs.est.9b03486
  • Xu Q, Si W, Mba OI, Sienkiewicz O, Ngadi M, Ross K, Kithama M, Kiarie EG, Kennes Y-M, Diarra MS, Zhao X. 2021. Research Note: Effects of supplementing cranberry and blueberry pomaces on meat quality and anti-oxidative capacity in broilers. Poultry Science. 100(3):100900. https://doi.org/10.1016/j.psj.2020.11.069
  • Yang C, Diarra MS, Choi J, Rodas-Gonzalez A, Lepp D, Liu S, Lu P, Mogire M, Wang Q, Gong J, Yang C. 2021. Effects of encapsulated cinnamaldehyde on growth performance, intestinal digestive and absorptive functions, meat quality, and gut microbiota in broiler chicken. Transl. Anim. Sci. 5(3):txab099. https://doi.org/10.1093/tas/txab099
  • Yang C, Kennes YM, Lepp D, Yin X, Wang Q, Yu H, Yang C, Gong J, Diarra MS. 2020. Effects of encapsulated cinnamaldehyde and citral on the performance and cecal microbiota of in broilers vaccinated or not vaccinated against coccidiosis. Poult Sci. 99(2):936-948. https://doi.org/10.1016/j.psj.2019.10.036
  • Yang C, Rehman MA, Yin X, Carrillo CD, Wang Q, Gong J, Yang C, Diarra MS. 2021. Antimicrobial Resistance Phenotype and Genotype of Generic Escherichia coli from Encapsulated Cinnamaldehyde and Citral Fed-Broiler Chicken. Journal of Food Protection. 84(8):1385-1399. https://doi.org/10.4315/JFP-21-033
  • Yousfi K, Usongo V, Berry C, Khan RH, Tremblay DM, Moineau S, Mulvey MR, Doualla-Bell F, Fournier E, Nadon C, Goodridge L, Bekal S. 2020. Source Tracking Based on Core Genome SNV and CRISPR Typing of Salmonella enterica Serovar Heidelberg Isolates Involved in Foodborne Outbreaks in Québec, 2012. Front Microbiol 11:1317. https://doi.org/10.3389/fmicb.2020.01317
  • Zaheer R, Cook SR, Barbieri R, Goji N, Cameron A, Petkau A, Polo RO, Tymensen L, Stamm C, Song J, Hannon S, Jones T, Church D, Booker CW, Kingsley Amoako K, VanDomselaar G, Ron R. Read RR, McAllister TA. 2020. Surveillance of Enterococcus spp. reveals distinct species and antimicrobial resistance diversity across a One-Health continuum. Sci Rep 10:3937. https://doi.org/10.1038/s41598-020-61002-5
  • Zaheer R, Lakin SM, Polo RO, et al. 2019. Comparative diversity of microbiomes and Resistomes in beef feedlots, downstream environments and urban sewage influent. BMC Microbiol. 19(1):197. https://doi.org/10.1186/s12866-019-1548-x
  • Zaidi SZ, Zaheer R, Barbieri B, Cook SR, Hannon SJ, Booker CW, Church D, VanDomselaar G, Zovoilis A, McAllister TA. 2022. Genomic characterization of Enterococcus hirae from beef cattle feedlots and associated environmental continuum. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2022.859990
  • Zhang L, Said LB, Diarra MS, Fliss I. 2021. Inhibitory activity of natural synergetic antimicrobial consortia against Salmonella enterica on broiler chicken carcasses. Front. Microbiol. 12:656956. https://doi.org/10.3389/fmicb.2021.656956
  • Zhang T, Fukuda K, Topp E, Zhu Y-G, Smalla K, Tiedje JM, Larsson DGJ. 2020. Editorial: The environmental dimension of antibiotic resistance. FEMS Microbiol. Ecol., 96 (8):fiaa130. https://doi.org/10.1093/femsec/fiaa130
  • Zhang H, Yamamoto E, Murphy J, Carrillo C, Locas A. 2021. Shiga toxin-producing Escherichia coli (STEC) and STEC-associated virulence genes in raw ground pork in Canada. Journal of Food Protection. 84(11):1956–64. https://doi.org/10.4315/JFP-21-147
  • Zhang A-N, Gaston J, Dai C, Yin X, Li L-G, Poyet M, Groussin M, van Loosdrecht M, Topp E, Gillings M, Hanage W, Tiedje J, Moniz K, Alm E, Zhang T, Zhao S. 2021. An omics-based framework for assessing the health risk of antimicrobial resistance genes. Nat. Comm. 12(1):4765. https://doi.org/10.1038/s41467-021-25096-3

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