Food safety is important to prevent infection by contaminating foodborne microbes, and is becoming increasingly to prevent infection with drug-resistant foodborne microbes. The use of antibiotics in agriculture has increased antibiotic-resistant microbes in associated foodstuffs. Fortunately, governmental institutions like the Food and Drug Administration (FDA), the Center for Disease Control and Protection (CDC), and the U.S. Department of Agriculture (USDA) have many programs in place to prevent contamination as well as detect it when it does occur. A new study in Antimicrobial Agents and Chemotherapy reports how a routine surveillance program identified drug-resistant Salmonella contamination of grocery-store pork products.
AACJournal: Identification of plasmid-mediated quinolone resistance in Salmonella isolated from swine ceca and retail pork chops in the United States.
Map of where Salmonella containing one of two drug-resistance plasmid have been found in the United States. Source.
The National Antimicrobial Resistance Monitoring System (NARMS) surveillance program tracks changes in drug susceptibility in gut bacteria from ill people, retail meats, and food animals in the U.S. From 2002 to 2015, all Salmonella isolates were susceptible to ciprofloxacin, but 2013 to 2015 saw the emergence and increase of nonsusceptibility to 8% of isolates. To understand why, the research team led by first author Gregory Tyson and senior scientist Patrick McDermott sequenced the genome of 30 cipro-nonsusceptible isolates. This is how they happened to identify the plasmid-mediated quinolone resistance genes being carried by 27 of the 30 sequenced samples. Plasmids containing quinolone-resistance genes were isolated from swine cecal contents or retail pork samples in nine states (see right).
Fluoroquinolone-resistant Salmonella are considered a serious threat to public health by the CDC. People sickened with fluoroquinolone-resistant enteric gram-negative bacteria have longer hospital stays and more complications. Additionally, plasmid-mediated drug resistance is more easily passed between bacterial species via horizontal gene transfer than genome-encoded resistance – meaning even people not sickened by these contaminating Salmonella could develop resistance in other members of their gut bacteria.
Vegetarians might think they can rest easy, but a second report in the same Antimicrobial Agents and Chemotherapy issue described drug-resistant E. coli contamination among vegetables for sale in China. Similar to the study described above, the scientific team tested fresh vegetable samples for surveillance purposes, looking for the presence of extended-spectrum beta-lactamase (ESBL) production. Once identified, the ESBL-producing Enterobacteriaceae were screened for mcr-1, a gene that confers colistin resistance. Six of the 244 ESBL-producing isolates contained plasmid-borne mcr-1.
AACJournal: Emergence of mcr-1 in Raoultella ornithinolytica and Escherichia coli isolates from retail vegetables in China
The discovery of mcr-1 on fresh tomatoes and lettuce in China doesn’t mean only the Chinese need worry. Globalization means bacteria can travel between countries as easily as cargo ships or planes can, and our interconnected trading systems (including food trade) mean health systems of different countries can very quickly be similarly affected. The fact that these resistance determinants are all found on plasmids also bodes poorly for their containment. It’s worth noting that both reports found a second type of resistance after screening for a primary resistance unrelated to those reported, underscoring the problem of multiple drug resistance in our agriculture, foodstuffs, and other everyday interactions. The best recourse is to follow good food preparation techniques by thoroughly washing produce and cooking animal products to avoid exposure to these potentially dangerous pathogens.
1. Boyce JM. Community-associated methicillin-resistant Staphylococcus aureus as a cause of health care-associated infection. Clin Infect Dis. 2008;46:795–8.[PubMed]
2. Popovich KJ, Weinstein RA. The graying of methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol. 2009;30:9–12.[PubMed]
3. Aminov RI, Mackie RI. Evolution and ecology of antibiotic resistance genes. FEMS Microbiol Lett. 2007;271:147–61.[PubMed]
4. Courvalin P. Predictable and unpredictable evolution of antibiotic resistance. J Intern Med. 2008;264:4–16.[PubMed]
5. Spellberg B, Powers JH, Brass EP, Miller LG, Edwards JE., Jr Trends in antimicrobial drug development: implications for the future. Clin Infect Dis. 2004;38:1279–86.[PubMed]
6. Talbot GH, Bradley J, Edwards JE, Jr, Gilbert D, Scheld M, Bartlett JG. Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America. Clin Infect Dis. 2006;42:657–68.[PubMed]
7. Norrby SR, Nord CE, Finch R European Society of Clinical Microbiology and Infectious Diseases. Lack of development of new antimicrobial drugs: a potential serious threat to public health. Lancet Infect Dis. 2005;5:115–9.[PubMed]
8. Avorn JL, Barrett JF, Davey PG, McEwen SA, O'Brien TF, Levy SB. Geneva: World Health Organization; 2001. [cited 2010 Nov 10]. Antibiotic resistance: synthesis of recommendations by expert policy groups. Also available from: URL: http://whqlibdoc.who.int/hq/2001/WHO_CDS_CSR_DRS_2001.10.pdf.
9. Belongia EA, Knobloch MJ, Kieke BA, Davis JP, Janette C, Besser RE. Impact of statewide program to promote appropriate antimicrobial drug use. Emerg Infect Dis. 2005;11:912–20.[PMC free article][PubMed]
10. 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;113:75–83.[PubMed]
11. Cui S, Ge B, Zheng J, Meng J. Prevalence and antimicrobial resistance of Campylobacter spp. and Salmonella serovars in organic chickens from Maryland retail stores. Appl Environ Microbiol. 2005;71:4108–11.[PMC free article][PubMed]
12. Gundogan N, Citak S, Yucel N, Devren A. A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Sci. 2005;69:807–10.[PubMed]
13. Kim SH, Wei CI, Tzou YM, An H. Multidrug-resistant Klebsiella pneumoniae isolated from farm environments and retail products in Oklahoma. J Food Prot. 2005;68:2022–9.[PubMed]
14. Parveen S, Taabodi M, Schwarz JG, Oscar TP, Harter-Dennis J, White DG. Prevalence and antimicrobial resistance of Salmonella recovered from processed poultry. J Food Prot. 2007;70:2466–72.[PubMed]
15. Ramchandani M, Manges AR, DebRoy C, Smith SP, Johnson JR, Riley LW. Possible animal origin of human-associated multidrug-resistant, uropathogenic Escherichia coli. Clin Infect Dis. 2005;40:251–7.[PubMed]
16. Mena C, Rodrigues D, Silva J, Gibbs P, Teixeira P. Occurrence, identification, and characterization of Campylobacter species isolated from Portuguese poultry samples collected from retail establishments. Poult Sci. 2008;87:187–90.[PubMed]
17. Diarrassouba F, Diarra MS, Bach S, Delaquis P, Pritchard J, Topp E, et al. Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. J Food Prot. 2007;70:1316–27.[PubMed]
18. McEwen SA, Fedorka-Cray PJ. Antimicrobial use and resistance in animals. Clin Infect Dis. 2002;34(Suppl 3):S93–106.[PubMed]
19. Institute of Medicine; National Research Council; Panel on Animal Health, Food Safety and Public Health; Committee on Drug Use in Food Animals. Washington: National Academy Press; 1999. The use of drugs in food animals: benefits and risks.
20. Department of Agriculture (US) Fort Collins (CO): USDA, Animal and Plant Health Inspection Service, Veterinary Services, National Animal Health Monitoring System; 2008. Sep, [cited 2010 Nov 11]. Dairy 2007 part III: reference of dairy cattle health and management practices in the United States, 2007. Also available from: URL: http://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_dr_PartIII_rev.pdf.
21. Department of Agriculture (US) Fort Collins (CO): USDA, Animal and Plant Health Inspection Service, Veterinary Services, National Animal Health Monitoring System; 2000. Dec, [cited 2011 Sep 12]. Feedlot 1999 part III: health management and biosecurity in U.S. feedlots, 1999. Also available from: URL: http://www.aphis.usda.gov/animal_health/nahms/feedlot/downloads/feedlot99/Feedlot99_dr_PartIII.pdf.
22. Department of Agriculture (US) Fort Collins (CO): USDA, Animal and Plant Health Inspection Service, Veterinary Services, National Animal Health Monitoring System; 2008. Mar, [cited 2011 Sep 12]. Swine 2006 part III: reference of swine health, productivity, and general management in the United States, 2006. Also available from: URL: http://www.aphis.usda.gov/animal_health/nahms/swine/downloads/swine2006/Swine2006_dr_PartIII.pdf.
23. Raymond MJ, Wohrle RD, Call DR. Assessment and promotion of judicious antibiotic use on dairy farms in Washington State. J Dairy Sci. 2006;89:3228–40.[PubMed]
24. Sawant AA, Sordillo LM, Jayaro BM. A survey on antibiotic usage in dairy herds in Pennsylvania. J Dairy Sci. 2005;88:2991–9.[PubMed]
25. Sarmah AK, Meyer MT, Boxall AB. A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere. 2006;65:725–59.[PubMed]
26. Mellon M, Benbrook C, Benbrook KL. Cambridge (MA): Union of Concerned Scientists; 2001. Jan, [cited 2010 Nov 11]. Hogging it' Estimates of antimicrobial abuse in livestock. Also available from: URL: http://www.ucsusa.org/food_and_agriculture/science_and_impacts/impacts_industrial_agriculture/hogging-it-estimates-of.html.
27. Institute of Medicine. Washington: National Academy Press; 1989. Human health risks with the subtherapeutic use of penicillin or tetracyclines in animal feed.
28. World Health Organization. Critically important antimicrobials for human medicine: categorization for the development of risk management strategies to contain antimicrobial resistance due to non-human antimicrobial use. Report of the Second WHO Expert Meeting; 29-31 May 2007; Copenhagen. [cited 2010 Nov 11]. Available from: URL: http://www.who.int/foodborne_disease/resistance/antimicrobials_human.pdf.
29. Collingnon P, Powers JH, Chiller TM, Aidara-Kane A, Aarestrup FM. World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clin Infec Dis. 2009;49:132–41.[PubMed]
30. Callaway TR, Edrington TS, Rychlik JL, Genovese KJ, Poole TL, Jung YS, et al. Ionophores: their use as ruminant growth promotants and impact on food safety. Curr Issues Intest Microbiol. 2003;4:43–51.[PubMed]
31. Greenland S, Rothman KJ, Lash TL. Measures of effect and measures of association. In: Rothman KJ, Greenland S, Lash TL, editors. Modern epidemiology. 3rd ed. Philadelphia: Wolters Kluwer/ Lippincott Williams & Wilkins; 2008. pp. 51–70.
32. Department of Health and Human Services (US), Food and Drug Administration, Center for Veterinary Medicine. Guidance for industry #152: evaluating the safety of antimicrobial new animal drugs with regard to their microbiological effects on bacteria of human health concern. 2003. Oct 23, [cited 2010 Nov 11]. Available from: URL: http://www.fda.gov/downloads/AnimalVeterinary/-GuidanceComplianceEnforcement/GuidanceforIndustry/UCM052519.pdf.
33. World Health Organization. WHO global principles for the containment of antimicrobial resistance in animals intended for food: report of a WHO consultation with the participation of the Food and Agriculture Organization of the United Nations and the Office International des Epizooties, 5–9 Jun 2000, Geneva. [cited 2010 Nov 11]. Available from: URL: http://whqlibdoc.who.int/hq/2000/who_cds_csr_aph_2000.4.pdf.
34. Interagency Task Force on Antimicrobial Resistance (US) Atlanta: Centers for Disease Control and Prevention (US), Food and Drug Administration (US), National Institutes of Health; 2008. Jun, [cited 2010 Nov 11]. A public health action plan to combat antimicrobial resistance: part 1: domestic issues. Also available from: URL: http://www.cdc.gov/drugresistance/actionplan/aractionplan.pdf.
35. Spellberg B, Guidos R, Gilbert D, Bradley J, Boucher HW, Scheld WM, et al. The epidemic of antibiotic-resistant infections: a call to action for the medical community from the Infectious Diseases Society of America. Clin Infect Dis. 2008;46:155–64.[PubMed]
36. Dorsey ER, de Roulet J, Thompson JP, Reminick JI, Thai A, White-Stellato Z, et al. Funding of US biomedical research, 2003–2008. JAMA. 2010;303:137–43.[PMC free article][PubMed]
37. Roberts RM, Smith GW, Bazer FW, Cibelli J, Seidel GE, Jr, Bauman DE, et al. Research priorities: farm animal research in crisis. Science. 2009;324:468–9.[PubMed]
38. Peters NK, Dixon DM, Holland SM, Fauci AS. The research agenda of the National Institute of Allergy and Infectious Diseases for antimicrobial resistance. J Infect Dis. 2008;197:1087–93.[PubMed]