The transfer of antibiotic resistance from food to humans: Facts, implications and future directions

OIE Revue Scientifique et Technique

Volumn 31, Issue 1, 2012, Pages 249-260

  Wang, H ^a   McEntire, J C ^b   Zhang, L ^a   Li, X ^a   Doyle, M ^c  

^a OHIO STATE UNIVERSITY   (United States)

^b Leavitt Partners   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Antibiotic resistance; Commensal bacteria; Food chain; Gut microbiota; Horizontal gene transfer; Targeted mitigation

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 84864051158     PISSN: 02531933     EISSN: 16080645     Source Type: Journal    
DOI: 10.20506/rst.31.1.2117     Document Type: Article

References (71)

1. Bacon R.T., Ransom J.R., Sofos J.N., Kendall RA., Belk K.E. & Smith G.C. (2003). - Thermal inactivation of susceptible and multiantimicrobial- resistant Salmonella strains grown in the absence or presence of glucose. Appl. environ. Microbiol., 69, 4123-4128. (Pubitemid 36870074)
2. Baker-Austin C., McArthur J.V, Tuckfield R.C., Najarro M., Lindell A.H., Gooch J. & Stepanauskas R. (2008). -Antibiotic resistance in the shellfish pathogen Vibrio parahaemolyticus isolated from the coastal water and sediment of Georgia and South Carolina, USA. J. Food Frot., 71 (12), 2552-2558.
3. Barrangou R. & Horvath R (2009). - The CRISPR system protects microbes against phages, plasmids. Microbe, 4, 224-230.
4. Bezanson G.S., Maclnnis R., Potter G. & Hughes T. (2008). -Presence and potential for horizontal transfer of antibiotic resistance in oxidase-positive bacteria populating raw salad vegetables. Int.J. Food Microbiol., 127 (1-2), 37-42.
5. Bhargava K., Wang X., Donabedian S., Zervos M., de Rocha L. & Zhang Y. (2011). - MethiciUin-resistant Staphylococcus aureus in retail meat, Detroit, Michigan, USA. Emerg. inject. Dis., 17 (6), 1135-1137.
6. Boehme S., Werner G., Klare I., Reissbrodt R. & Witte W (2004). - Occurrence of antibiotic-resistant enterobacteria in agricultural foodstuffs. Mol. Nutr. Food Res., 48 (7), 522-531. (Pubitemid 39643695)
7. Centers for Disease Control and Prevention (CDC) (2011). -Investigation announcement: multistate outbreak of human Salmonella Heidelberg infections. CDC, Atlanta. Available at: www.cdc.gOv/Salmonella/heidelberg/080111/ (accessed on 4 January 2012).
8. Chee-Sanford J.C., Aminov R.I., Krapac I.J., Garrigues-Jeanjean N. & Mackie R.I. (2001). - Occurrence and diversity of tetracychne resistance genes in lagoons and groundwater underlying two swine production facilities. Appl. environ. Microbiol, 67, 1494-1502. (Pubitemid 33644914)
9. Chen J., Michel EC. Jr, Sreevatsan S., Morrison M. & Yu Z. (2010). - Occurrence and persistence of erythromycin resistance genes (erm) and tetracychne resistance genes (tet) in waste treatment systems on swine farms. Microb. Ecol, 60 (3), 479-486.
10. Çitak S., Yucel N. & Orhan S. (2004). - Antibiotic resistance and incidence of Enterococcus species in Turkish white cheese. Int.J. Dairy Technol, 57, 27-31. (Pubitemid 38197400)
11. Codex Alimentarius Commission (CAC) (2011). - Guidelines for risk analysis of foodbome antimicrobial resistance. CAC, Rome. Available at; wwwcodexalimentarius.net/download/ standards/11776/CXG-077e.pdf (accessed on 4 January 2012).
12. Comunian R., Daga E., Dupre I., Paba A., Devirgiliis C., Piccioni v., Perozzi G., Zonenschain D., Rebecchi A., Morelli L., De Lorentiis A. & Giraffa G. (2010). -Susceptibility to tetracycline and erythromycin of Lactobacillus paracasei strains isolated from traditional Italian fermented foods. Int.J. Food Microbiol., 138, 151-156.
13. Devirgiliis C., Caravelh A., Coppola D., Barile S. & Perozzi G. (2008). - Antibiotic resistance and microbial composition along the manufacturing process of Mozzarella di Búfala Campana. Int.J Food Microbial., 128 (2), 378-384.
14. Doyle M.R, Busta E, Cords B.R., Davidson RM., Hawke J., Scott Hurd H., Isaacson R.E., Matthews K., Maurer J., MengJ., Montville TJ., Shryock T.R., Sofos J.N., Vidaver A.K. & Vogel L. (2006). - Antibiotic resistance; implications for the food system. Comp. Rev. Food Sci. Food Sajety, 5, 71-137.
15. Duran G.M. & Marshall D.L. (2005). - Ready-to-eat shrimp as an intemational vehicle of antibiotic-resistant bacteria. J. Food Protec., 68, 2395-2401. (Pubitemid 41628416)
16. Feld L., Bielak E., Hammer K. & Wilcks A. (2009). -Characterization of a small erythromycin resistance plasmid pLEEl from the food-isolate Lactobacillus plantarum M345. Plasmid, 61 (3), 159-170.
17. EeiSler A.T, Kadlec K., Hassel M., Hauschild T, Eidam C., Ehricht R., Monecke S. & Schwarz S. (2011). -Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany Appl. environ. Microbial, 77 (20), 7151-7157.
18. Food and Dmg Administration (2009). - Retail Meat Annual Report. National Antimicrobial Resistance Monitoring System. Available at; wvm.fda.gov/ downloads/Animal Veterinary/SafetyHealth/AntimicrobialResistance/National AntimicrobialResistanceMonitoringSystem/UCM257593.pdf (accessed on 26 September 2011).
19. GRID-Arendal (2009). - World capture fisheries and aquaculture production. In The environmental food crisis; the environment's role in averting future food crises. GRID-Arendal, Arendal, Norway Available at; http;//maps.grida. no/go/graphic/world-capture-fisheries-and-aquaculture- production (accessed on 4 January 2012).
20. Gueimonde M., Salminen S. & Isolauri E. (2006). - Presence of specific antibiotic (tet) resistance genes in infant faecal microbiota. FEMS Immunol med. Microbiol, 48, 21-25. (Pubitemid 44379216)
21. Hammad A.M., Ishida Y. & Shimamoto T. (2009). -Prevalence and molecular characterization of ampicilhn-resistant Enterobacteriaceae isolated from traditional Egyptian Domiati cheese. J. Food Protec., 72 (3), 624-630.
22. Hayes E (2003). - Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science, 301, 1496-1499.
23. Horby RW, O'Brien S.J., Adak G.K., Graham C., Hawker J.I., Hunter E, Lane C., Lawson A.J., Mitchell R.T, Reacher M.H., Threlfall E.J. & Ward L.R. (2003). - A national outbreak of multi-resistant Salmonella enterica serovar Typhimurium definitive phage type (DT) 104 associated with consumption of lettuce. Epidemiol. Infect., 130 (2), 169-178. (Pubitemid 36511954)
24. Johnsen RJ., Österhus J.L, Sletvold H., Sorum M., Kruse H., Nielsen K., Simonsen G.S. & Sundsfjord A. (2005). -Persistence of animal and human glycopeptide-resistant enterococci on two Norwegian poultry farms formerly exposed to avoparcin is associated with a widespread plasmid-mediated vanA element within a polyclonal Enterococcus faecium population. Appl. environ. Microbiol, 71, 159-168. (Pubitemid 40116263)
25. Johnston L.M. & Jaykus L.A. (2004). - Antimicrobial resistance of Enterococcus species isolated from produce. Appl environ. Microbiol 70 (5), 3133-3137. (Pubitemid 38657834)
26. Kadlec K., von Czapiewski E., Kaspar H., Wallmann J., Michael G.B., Steinacker U. & Schwarz S. (2011). -Molecular basis of sulfonamide and trimethoprim resistance in fish-pathogenic Aeromonas isolates. Appl environ. Microbiol, 77 (20), 7147-7150.
27. Khan A.A., Ponce E., Nawaz M.S., Cheng C.M., Khan J.A. & West C.S. (2009). - Identification and characterization of Class 1 integron resistance gene cassettes among Salmonella strains isolated from imported seafood. Appl environ. Microbiol, 75 (4), 1192-1196.
28. Lachmayr K.L., Kerkhof LJ., Dirienzo A.G., Cavanaugh C.M. & Eord T.E. (2009). - Quantifying nonspecific TEM beta-lactamase (blajEi) genes in a wastewater stream. Appl environ. Microbiol, 75, 203-211.
29. Lee TS., Lee S.W, Seok WS., Yoo M.Y., Yoon J.W, Park B.K., Moon K.D. & Oh D.H. (2004). - Prevalence, antibiotic susceptibihty, and virulence factors of Yersinia enterocolitica and related species from ready-to-eat vegetables available in Korea. J. Food Protec., 67 (6), 1123-1127.
30. Lehman M. (2006). - Assessment of antibiotic resistant commensal bacteria in food. MSc Thesis. The Ohio State University, Columbus, Ohio.
31. Levy S.B., EitzGerald G.B. & Macone A.B. (1976). - Changes in intestinal flora of farm personnel after introduction of a tetracycline- supplemented feed on a farm. N. Engl J. Med., 295, 583-588.
32. U X.H., Alvarez A., Harper WJ. & Wang H.H. (2011). -Persistent, toxin-antitoxin system-independent tetracychne resistance-encoding plasmid from a dairy Enterococcus faecium isolate. Appl environ. Microbiol, 77 (20), 7096-7103.
33. U X.H., Li Y.L., Alvarez A., Harper WJ. & Wang H.H. (2011). - Antibiotic resistance mitigation in dairy fermentation. Appl. environ. Microbiol. 11 (20), 7093-7095.
34. U XJ., Sun K., Zhang L., Li Y.L. 61 Wang H H. (2010). - The involvement of animal host in the enrichment of antibiotic resistance. Institute of Food Technologists Annual Meeting, 18-20 July Chicago, Abstract No. 37-45.
35. Li XJ. & Wang H.H. (2010). - Profiles of antibiotic resistant commensal bacteria from representative ready-to-consume deh and restaurant foods. J. Food Protec., 13 (10), 1841-1848.
36. López A.C., de Ortúzar R.V & Alippi A.M. (2008). -Tetracychne and oxytetracychne resistance determinants detected in Bacillus cereus strains isolated from honey samples. Rev Argent. Microbiol., 40 (4), 231-237.
37. Luo H., Wan K. & Wang H.H. (2005). - A high frequency conjugation system facilitated biofilm formation and pAMbl transmission in Lactococcus lactis. Appl. environ. Microbiol, 11, 2970-2978. (Pubitemid 40807201)
38. Luo N., Pereira S., Sahin O., Un J., Huang S., Michel L. & Zhang Q. (2005). - Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. natl Acad. Sci. USA, 102, 541-546. (Pubitemid 40282701)
39. Manuzon M.Y, Hanna S.E., Luo H., Yu Z., Harper WJ. & Wang H.H. (2007). - Quantitative assessment of the tetracycline resistance gene pool in cheese samples by real-time TaqMan PCR. Appl environ. Microbiol, 13, 1676-1677. (Pubitemid 46417896)
40. Moritz E.M. & Hergenrother RJ. (2007). - Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycin-resistant enterococci. Proc. natl Acad. Sd. USA, 104, 311-316. (Pubitemid 46068028)
41. Nandi S., Maurer JJ., Hofacre C. & Summers A.O. (2004). -Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance intégrons in poultry Utter. Proc. natl Acad. Sd. USA, 101, 7118-7122. (Pubitemid 38596452)
42. Oh E.G., Son K.T, Yu H., Lee TS, Lee HJ., Shin S., Kwon J.Y, Park K. & Kim J. (2011). - Antimicrobial resistance of Vibrio parahaemolyticus and Vibrio alginolyticus strains isolated from farmed fish in Korea from 2005 through 2007. J. Food Protec., 74 (3), 380-386.
43. Peak N., Knapp C.W, Yang R.K., Hanfelt M.M., Smith M.S., Aga D.S. & Graham D.W (2007). - Abundance of six tetracychne resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ. Microbiol, 9, 143-151. (Pubitemid 46059005)
44. Perreten V, Schwarz E, Cresta L., Boeglin M., Dasen G. & Teuber M. (1997). - Antibiotic resistance spread in food. Nature, 389 (6653), 801-802.
45. Perreten V, Schwarz E, Teuber M. & Levy S.B. (2001). -Mdt(A), a new efflux protein conferring multiple antibiotic resistance in Lactococcus lactis and Escherichia coli. Antimicrob. Agents Chemother., 45 (4), 1109-1114. (Pubitemid 32230990)
46. Potenski C.J., Gandhi M. & Matthews K R. (2003). -Exposure of Salmonella Enteritidis to chlorine or food preservatives decreases (corrected] susceptibihty to antibiotics. FEMS Microbiol. Lett., 220, 181-186. (Pubitemid 36378970)
47. Ready D., Bedi R., Spratt D.A., Mullany R & Wilson M. (2003). - Prevalence, proportions, and identities of antibiotic-resistant bacteria in the oral microflora of healthy children. Microb. Drug Resist., 9, 367-372. (Pubitemid 38168193)
48. Resch M., Nagel V & Hertel C. (2008). - Antibiotic resistance of coagulase-negative staphylococci associated with food and used in starter cultures. Int. J. Food Microbiol., 127 (1-2), 99-104.
49. Rizzotti L., La Gioia E, Dellagho E & Torriani S. (2009). -Characterization of tetracycline-resistant Streptococcus thermophilus isolates from Italian soft cheeses. Appl. environ. Microbial., 75 (12), 4224-4229.
50. Salyers A.A., Gupta A. Wang Y. (2004). - Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol, 12, 412-416. (Pubitemid 39178592)
51. Shen Z., Pu X. & Zhang Q. (2011). - Salicylate functions as an efflux pump inducer and promotes the emergence of fluoroquinolone-resistant mutants in Campylobacter jejuni mutants. Appl environ. Microbiol, 77 (20), 7128-7133.
52. Shoemaker N.B., Vlamakis Hayes H.K. & Salyers A.A. (2001). - Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl environ. Microbiol, 67, 561-568. (Pubitemid 32121342)
53. Smith M.S., Yang RK., Knapp C.W, Niu Y, Peak N., Hanfelt M.M., Galland J.C. & Graham D.W (2004). -Quantification of tetracychne resistance genes in feedlot lagoons by real-time PCR. Appl environ. Microbiol, 70, 7372-7377. (Pubitemid 39643803)
54. Sorum M., Johnsen PJ., Aasnes B., Rosvoll T, Kruse H., Sundsfjord A. & Simonsen G.S. (2006). - Prevalence, persistence, and molecular characterization of glycopeptide-resistant enterococci in Norwegian poultry and poultry farmers 3 to 8 years after the ban on avoparcin. Appl environ. Microbiol, 72, 516-521.
55. Stanton TS., Humphrey S.B. & Stoffregen WC. (2011). -Chlortetracycline-resistant intestinal bacteria in organically raised and feral swine. Appl environ. Microbiol, 77 (20), 7167-7170.
56. Surendraraj A., Thampuran N. & Joseph TC. (2010). -Molecular screening, isolation, and characterization of enterohemorrhagic Escherichia coh 0157:H7 from retail shrimp. J. Food Protec., 73 (1), 97-103.
57. Teuber M., Schwarz E & Perreten V (2003). - Molecular structure and evolution of the conjugative multiresistance plasmid pRE25 of Enterococcus faecalis isolated from a raw-fermented sausage. Int.J. Food Microbial, 88, 325-329. (Pubitemid 37329510)
58. Togay S.O., Keskin A.C., Acik L. & Temiz A. (2010). -Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus jaecéis and Enterococcus faecium from naturally fermented Turkish foods. J, appl. Microbial., 74, 6085-6090.
59. Toomey N., Bolton D. & Fanning S. (2010). -Characterisation and transferabihty of antibiotic resistance genes from lactic acid bacteria isolated from Irish pork and beef abattoirs. Res. Microbiol., 161 (2), 127-135.
60. Tran Q.T., Nawaz M.S., Deck J., Nguyen K.T. & Cernigha C.E. (2011). - Plasmid-mediated quinolone resistance in Pseudomonas putida isolates from imported shrimp. Appl. environ. Microbiol, 77 (5), 1885-1887.
61. United States Census Bureau (2011). - World POPClock Projection. Available at: www.census.gov/population/ popclockworld.html (accessed on 27 September 2011).
62. United States Department of Agriculture (USDA) (2001). -FY-2005 Annual Report: Manure and Byproduct Utilization. National Program 206. USDA Agricultural Research Services, Beltsville, MD. Available at: www.ars.usda.gov/research/ programs/programs. htm?np-code=206&docid= 13337 (accessed on 27 September 2011).
63. Villedieu A., Diaz-Torres M.L., Roberts A.R, Hunt N., McNab R., Spratt D.A., Wilson M. & Mullany R (2004). -Genetic basis of erythromycin resistance in oral bacteria. Antimicrob. Agents Chemother., 48, 2298-2301. (Pubitemid 38691636)
64. Wang H.H. (2009). - Commensal bacteria, microbial ecosystems and horizontal gene transmission: adjusting our focus for strategic breakthroughs against antibiotic resistance. In Foodbome microbes: shaping the host ecosystems (L. Jaykus, H.H. Wang & L.S. Schlesinger, eds). ASM Press, Washington, DC, 267-281.
65. Wang H.H., Manuzon M., Lehman M., Wan K., Luo H., Wittum T.E., Yousef A. & Bakaletz L.O. (2006). - Food commensal microbes as a potentially important avenue in transmitting antibiotic resistance genes. FEMS Microbiol Lett., 254, 226-231.
66. Wang H.H. & Schaffner D.W (2011). - Antibiotic resistance: how much do we know and where to go from here? Appl environ. Microbiol., 77 (20), 7093-7095.
67. Wang H.H., Sofos J.N., Stanton T.B., Buckley T.J., Doyle M.P, Schaffner D.W, Shryock T.R., Torrence M.E., Zhang Q., Medeiros L.C., Raymond R. & Salyers A. (2010). - Antibiotic resistance mitigation: a comphcated issue begging for targeted investigation. Microbe, 5, 504-505.
68. Waters A.E., Contente-Cuomo T., Buchhagen J., Liu C.M., Watson L., Pearce K., Foster J.T., Bowers J., Driebe E.M., Engelthaler D.M., Keim RS. & Price L.B. (2011). - Multidrug-resistant Staphylococcus aureus in US meat and poultry Clin, infect. Dis., 52 (10), 1227-1230.
69. Zhang L. (2011). - Establishment and development of antibiotic resistant bacteria in human gastrointestinal tract: food, drug, or are we bom with it? PhD Thesis. The Ohio State University Columbus, Ohio.
70. Zhang L., Kinkelaar D., Huang Y., U Y., Li X.J. & Wang H.H. (2011). - Acquired antibiotic resistance: are we bom with it? Appl environ. Microbiol, 77 (20), 7134-7141.
71. Zhang L, McEntire J.C., Newsome R.L. & Wang H.H. (2011). - Antimicrobial resistance. In Food microbiology: fundamentals and frontiers, 4th Ed. (M.P. Doyle & R.L. Buchanan, eds). ASM Press, Washington, DC.