Insects in confined swine operations carry a large antibiotic resistant and potentially virulent enterococcal community

BMC Microbiology

Volumn 11, Issue , 2011, Pages

  Ahmad, Aqeel ^a,c   Ghosh, Anuradha ^a   Schal, Coby ^b   Zurek, Ludek ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c MONSANTO COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASA1 PROTEIN; BACTERIAL PROTEIN; CYLA PROTEIN; ERM(B) PROTEIN; ERYTHROMYCIN; ESP PROTEIN; GELE PROTEIN; TET(B) PROTEIN; TET(K) PROTEIN; TET(M) PROTEIN; TET(O) PROTEIN; TET(S) PROTEIN; TETRACYCLINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; BLATTA GERMANICA; COCKROACH; COLONY FORMING UNIT; CONTROLLED STUDY; ENTEROCOCCUS; ENTEROCOCCUS CASSELIFLAVUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS GALLINARUM; ENTEROCOCCUS HIRAE; ENTEROCOCCUS MUNDTII; FECES; GENOTYPE; HOUSE FLY; MICROBIAL COMMUNITY; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; PULSED FIELD GEL ELECTROPHORESIS; QUANTITATIVE ANALYSIS; SCREENING; SWINE; TRANSPOSON; ANIMAL; DRUG EFFECT; GENETICS; MICROBIOLOGY; MULTIDRUG RESISTANCE; PATHOGENICITY; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); BLATTARIA; BLATTELLA GERMANICA; ENTEROCOCCUS FAECALIS; HEXAPODA; MUSCA DOMESTICA; MUSCIDAE; SUIDAE;

ANIMALS; COCKROACHES; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; GENOTYPE; HOUSEFLIES; PHENOTYPE; SWINE; VIRULENCE;

EID: 79251535615     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-11-23     Document Type: Article

References (84)

1. Hall BG: Predicting the evolution of antibiotic resistance genes. Nat Rev Microbiol 2004, 2:430-435.
2. Cohen ML: Changing patterns of infectious disease. Nature 2000, 406:762-767.
3. Hardy B: The issue of antibiotic use in the livestock industry: What have we learned? Animal Biotechnology, Proceedings of the Conference on Antibiotics Use in Animal Agriculture 2002, 13:129-147.
4. Levy SB: Factors impacting on the problem of antibiotic resistance. J Antimicrob Chemother 2002, 49:25-30.
5. Kummerer K: Resistance in the environment. J Antimicrob Chemother 2004, 54:311-320.
6. Aarestrup FM: The origin, evolution, and local and global dissemination of antimicrobial resistance. In Antimicrobial resistance in bacteria of animal origin. Edited by: Aarestrup FM. Washington DC, ASM Press; 2006:339-360.
7. Mellon M, Benbrook C, Benbrook KL: Hogging It: Estimates of Antimicrobial Abuse in Livestock. Union of Concerned Scientists Cambridge MA; 2000 [http://www.ucsusa.org/assets/documents/food-and-agriculture/hog-front.pdf].
8. Guardabassi L, Courvalin P: Modes of antimicrobial action and mechanisms of bacterial resistance. In Antimicrobial Resistance in Bacteria of Animal Origin. Edited by: Aarestrup FM. Washington D.C., ASM Press; 2006:1-18.
9. Florini K, Denison R, Stiffler T, Fitzerald T, Goldburg R: Resistant bugs and antibiotic drugs: State and County estimates of antibiotics in animal feed and animal waste. 2005 [http://www.environmentaldefense.org/ documents/4301-AgEstimates.pdf].
10. Aarestrup FM, Agersø Y, Smith PG, Madsen M, Jensen LB: Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers and pigs in Denmark. Diagn Microbiol Infect Dis 2000, 37:127-137. (Pubitemid 30336326)
11. Garcia-Migura L, Pleydell E, Barnes S, Davies RH, Liebana E: Characterization of vancomycin-resistant Enterococcus faecium isolates from broiler poultry and pig farms in England and Wales. J Clin Microbiol 2005, 43:3283-3289. (Pubitemid 40981337)
12. Eaton TJ, Gasson MJ: Molecular screening of enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 2001, 67:1628-1635. (Pubitemid 33644933)
13. Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG Jr: Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci USA 2002, 99:6434-6439. (Pubitemid 34493329)
14. Iversen A, Kühn I, Rahman M, Franklin A, Burman LG, Ollson-Liljequist B, Torrel E, Möllby R: Evidence for transmission between humans and the environment of nosocomial strain of Enterococcus faecium. Environ Microbiol 2004, 6:55-59. (Pubitemid 38162027)
15. De Leener E, Martel A, Decostere A, Haesebrouck F: Distribution of the erm (B) gene, tetracycline resistance genes, and Tn1545-like transposons in macrolide- and lincosamide-resistant enterococci from pigs and humans. Microb Drug Resist 2004, 10:341-345. (Pubitemid 40096571)
16. Heuer OE, Hammerum AM, Collignon P, Wegener HC: Human health hazard from antimicrobial-resistant enterococci in animals and food. Clin Inf Dis 2006, 43:911-916. (Pubitemid 44435522)
17. Graczyk TK, Knight R, Gilman R, Cranfield M: The role of non-biting flies in the epidemiology of human infectious diseases. Microbes Infect 2001, 3:231-235. (Pubitemid 32453151)
18. Zurek L, Gorham JR: Insects as vectors of foodborne pathogens. In Wiley Handbook of Science and Technology for Homeland Security. Edited by: Voeller JG. Hoboken, N.J. John Wiley and Sons; 2008:1-16.
19. Macovei L, Zurek L: Ecology of antibiotic resistance genes: characterization of enterococci from houseflies collected in food settings. Appl Environ Microbiol 2006, 72:4028-4035. (Pubitemid 43894867)
20. Willems RJL, van Schalk W: Transition of Enterococcus faecium from commensal organism to nosicomial pathogen. Future Microbiol 2009, 4:1125-1135.
21. Franz CAMP, Holzapfel WH, Stiles ME: Enterococci at the crossroads of food safety?. Int J Food Microb 1999, 47:1-24. (Pubitemid 29225295)
22. Klein G: Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. Int J Food Microbiol 2003, 88:123-131.
23. Hayes JR, Enghish LL, Carter PJ, Proescholt T, Lee KY, Wagner DD, White DG: Prevalence and antimicrobial resistance of Enterococcus species isolated from retail meats. Appl Environ Microbiol 2003, 69:7153-7160. (Pubitemid 38585364)
24. Macovei L, Zurek L: Influx of enterococci and associated antibiotic resistance and virulence genes from ready-to-eat food to the human digestive tract. Appl Environ Microbiol 2007, 73:6740-6747. (Pubitemid 350076792)
25. Macovei L, Ghosh A, Thomas V, Hancock L, Mahmood S, Zurek L: Enterococcus faecalis with the gelatinase phenotype regulated by the fsr-operon and with biofilm forming capacity are common in the agricultural environment. Environ Microbiol 2009, 11:154-1547.
26. Kayser FH: Safety aspects of enterococci from the medical point of view. Int J Food Microbiol 2003, 88:255-262.
27. Gilmore MS, Coburn S, Nallapareddy SR, Murray BE: Enterococcal virulence. In The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance. Edited by: Gilmore MS. Washington DC, ASM Press; 2002:301-354.
28. Klare I, Konstabel C, Badstubner D, Werner G, Witte W: Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int J Food Microbiol 2003, 88:269-290. (Pubitemid 37329505)
29. Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal JK, Flannagan SE, Kolonay JF, Shetty J, Killgore GE, Tenover FC: Genetic analysis of a high-level vancomycin resistant isolate of Staphylococcus aureus. Science 2003, 302:1569-1571. (Pubitemid 37475701)
30. Nallapareddy SR, Wenxiang H, Weinstock GM, Murray E: Molecular characterization of a widespread, pathogenic, and antibiotic resistance receptive Enterococcus faecalis lineage and dissemination of its putative pathogenicity island. J Bacterial 2005, 187:5709-5718. (Pubitemid 41134307)
31. Mundy LM, Sahm DF, Gilmore MS: Relationship between enterococcal virulence and antimicrobial resistance. Clin Microbiol Rev 2000, 13:513-522.
32. Knudtson JM, Hartman PA: Antibiotic resistance among enterococcal isolates from environmental and clinical sources. J Food Prot 1993, 56:489-492.
33. Kühn I, Iversen A, Burman LG, Olsson-Liljequist B, Franklin A, Finn M, Aarestrup F, Seyfarth AM, Franklin A, Finn M, Blanch AR, Vilanova X, Taylor H, Caplin J, Moreno MA, Dominguez L, Herrero IA, Möllby R: Comparison of enterococcal populations in animals, humans, and the environment - A European study. Inter J Food Microbiol 2003, 88:133-145.
34. Nikolich MP, Hong G, Shoemaker NB, Salyers AA: Evidence for natural horizontal transfer of tetQ between bacteria that normally colonize humans and bacteria that normally colonize livestock. Appl Environ Microbiol 1994, 60:3255-3260. (Pubitemid 24272351)
35. Thal LA, Chow JW, Mahayni R, Bonilla H, Perri MB, Donabedian SA, Silverman J, Taber S, Zervos MJ: Characterization of antimicrobial resistance in enterococci of animal origin. Antimicrob Agents Chemother 1995, 39:2112-2115.
36. Aarestrup FM, Butaye P, Witte W: Non-human reservoirs of enterococci. In The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance. Edited by: Gilmore MS. Washington DC, ASM Press; 2002:55-99.
37. Silbergeld EK, Graham J, Price LB: Industrial food animal production, antimicrobial resistance, and human health. Annu Rev. Public Health 2008, 29:151-169. (Pubitemid 351600403)
38. Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, Nightingale C, Preston R, Waddell J: Antibiotic use in animals. J Antimicrob Chemother 2004, 53:885.
39. Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, Nightingale C, Preston R, Waddell J: Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemother 2004, 53:28-52. (Pubitemid 38072182)
40. Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, Nightingale C, Preston R, Waddell J: Does the use of antibiotics in food animals pose a risk to human health? A reply to critics. J Antimicrob Chemother 2004, 54:276-278. (Pubitemid 39029013)
41. Turnidge J: Antibiotic use in animals-prejudices, perceptions and realities. J Antimicrob Chemother 2004, 53:26-27.
42. Akhtar M, Hirt H, Zurek L: Horizontal transfer of the tetracycline resistance gene tetM mediated by pCF10 among Enterococcus faecalis in the house fly (Musca domestica L.) alimentary canal. Microb Ecol 2009, 58:509-518.
43. Macovei L, Miles B, Zurek L: The potential of house flies to contaminate ready-to-eat food with antibiotic resistant enterococci. J Food Protect 2008, 71:432-439.
44. Zurek L, Schal C, Watson DW: Diversity and contribution of the gastrointestinal bacterial community to the development of Musca domestica (Diptera: Muscidae) larvae. J Med Entomol 2000, 37:924-928.
45. Cohen D, Green M, Block C, Slepon R, Ambar R, Wasserman S, Levine MM: Reduction of transmission of shigellosis by control of houseflies (Musca domestica). Lancet 1991, 337:993-997.
46. Esrey SA: Effects of improved water supply and sanitation on ascariasis, diarrhoea, dracunculiasis, hookworm infection, schistosomiasis and trachoma. Bulletin of World Health Organisation 1991, 69:609-621.
47. Emerson PM, Lindsay SW, Walraven GEL, Faal H, Bogh C, Lowe K: Effect of fly control on trachoma and diarrhoea. Lancet 1999, 353:1401-1403. (Pubitemid 29192412)
48. Graffar M, Mertens S: Le role des blattes dans la transmission des salmonelloses. Ann Inst Past 1950, 79:654-660.
49. Tarshis IB: The cockroach - A new suspect in the spread of infectious hepatitis. Am J Trop Med Hyg 1962, 11:705-711.
50. Zurek L, Schal C: Evaluation of the German cockroach (Blattella germanica) as a vector for verotoxigenic Escherichia coli F18 in confined swine production. Vet Microbiol 2004, 101:263-267. (Pubitemid 38925302)
51. Graham JP, Price LB, Evans SL, Graczyk TK, Silbergeld EK: Antibiotic resistant Enterococci and staphylococci isolated from flies collected near confined feeding operations. Sci Tot Environ 2009, 407:2701-2710.
52. Murray BE: The life and times of the Enterococcus. Clin Microbiol Rev 1990, 3:46-65.
53. Butaye P, Devriese LA, Goosens H, Leven M, Haesebrousk F: Enterococci with acquired vancomycin resistance in pigs and chickens of different age groups. Antimicrob Agents Chemother 1999, 43:365-366. (Pubitemid 29079174)
54. Martin JD, Mundt JO: Enterococci in insects. Appl Microbiol 1972, 24:575-580.
55. FDA (U.S. Food and Drug Administration): FDA Approved Animal Drug Products (Green Book). Blacksburg, VA Drug Information Laboratory Virginia/Maryland Regional College of Veterinary Medicine; 2004.
56. Chakrabarti S, Kambhaampati Zurek L: Assessment of house fly dispersal between rural and urban habitats in Kansas, USA. J Kans Entomol Soc 2010, 83:172-188.
57. Coque TM, Tomayko JF, Ricke SC, Okhyusen PC, Murray BE: Vancomycin-resistant enterococci from nosocomial, community and animal sources in the United States. Antimicrob Agents Chemother 1996, 40:2605-2609. (Pubitemid 26367652)
58. Van den Bogaard AE, Stobberingh EE: Epidemiology of resistance to antibiotics: Links between animals and humans. Int J Antimicrb Agents 2000, 14:327-335.
59. Jensen LB, Frimodt-Moller N, Aarestrup FM: Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol Lett 1999, 170:151-158. (Pubitemid 29044087)
60. Teuber M, Meile L, Schwarz F: Acquired antibiotic resistance in lactic acid bacteria from food. Antonie van Leeuwenhoek 1999, 76:115-137. (Pubitemid 29440723)
61. Bertram J, Stratz M, Durre P: Natural transfer of conjugative transposon Tn916 between Gram-positive and Gram-negative bacteria. J Bacteriol 1991, 173:443-448.
62. Roberts MC: Resistance to tetracycline, macrolide- lincosamidestreptogramin, trimethoprim and sulfonamide drug classes. Mol Biotechnol 2002, 20:261-283.
63. Roberts MC: Update on acquired tetracycline resistance genes. FEMS Microbiol Lett 2005, 245:195-203.
64. Nakayama J, Kariyama R, Kumon H: Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl Environ Microbiol 2002, 68:3152-3155. (Pubitemid 34602046)
65. Roberts JC, Singh KV, Okhuysen PC, Murray BE: Molecular epidemiology of the fsr locus and of gelatinase production among different subsets of Enterococcus faecalis isolates. J Clin Microbiol 2004, 42:2317-2320. (Pubitemid 38637875)
66. Licht TR, Laugesen D, Jensen LB, Jacobsen BL: Transfer of the pheromone-inducible plasmid pCF10 among Enterococcus faecalis microorganisms colonizing the intestine of mini-pigs. Appl Environ Microbiol 2002, 68:187-193. (Pubitemid 34031179)
67. Lester CH, Frimodt-Møller N, Sørensen TL, Monnet DL, Hammerum AM: In vivo transfer of the vanA resistance gene from an Enterococcus faecium isolate of animal origin to an E. faecium isolate of human origin in the intestines of human volunteers. Antimicrob Agents Chemother 2005, 50:596-599.
68. Shoemaker NB, Vlamakis H, Hayes K, Salyers AA: Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol 2001, 67:561-568. (Pubitemid 32121342)
69. Acheson DWK, Linciome LL, Jacewicz MS, Keusch GT: Shiga toxin interaction with intestinal epithelial cells. In Escherichia coli 0157: H7 and other shiga-toxin producing E. coli strains. Edited by: Kaper JB, O'Brien AD. Washington DC, ASM Press; 1998:140-147.
70. Mater DDG, Langella P, Corthier G, Flores MJ: Evidence of vancomycin resistance gene transfer between enterococci of human origin in the gut of mice harbouring human microbiota. J Antimicrob Chemother 2005, 56:975-978. (Pubitemid 41631931)
71. Petridis M, Bagdasarian M, Waldor MK, Walker E: Horizontal transfer of shiga toxin and antibiotic resistance genes among Escherichia coli strains on house fly (Diptera; Muscidae) gut. J Med Entomol 2006, 43:288-295. (Pubitemid 44743539)
72. Devriese LA, Van de Kerckhove A, Kilpper-Balz R, Schleifer KH: Characterization and identification of Enterococcus species isolated from the intestines of animals. Int J Syst Bacteriol 1987, 37:257-259.
73. Dutka-Malen S, Evers S, Courvalin P: Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 1995, 33:24-27. (Pubitemid 24382391)
74. Kariyama R, Mitsuhata R, Chow JW, Clewell JB, Kumon H: Simple and reliable multiplex PCR assay for surveillance isolates of vancomycin-resistant enterococci. J Clin Microbiol 2000, 38:3092-3095. (Pubitemid 30640606)
75. Arias CA, Robredo B, Singh KV, Torres C, Panesso D, Murray BE: Rapid identification of Enterococcus hirae and Enterococcus durans by PCR and detection of a homologue of the E. hirae muramidase-2 gene in E. durans. J Clin Microbiol 2006, 44:1567-1570.
76. National Committee for Clinical Laboratory Standards: Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria. National Committee for Clinical Laboratory Standards, Wayne,PA; 2002.
77. Dunny GM, Craig R, Carron R, Clewell DB: Plasmid transfer in Streptococcus faecalis: production of multiple sex pheromones by recipients. Plasmid 1978, 2:454-465. (Pubitemid 9222363)
78. Ng LK, Martin I, Alfa M, Mulvey M: Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 2001, 15:209-215. (Pubitemid 32664617)
79. Villedieu A, Diaz-Torres ML, Hunt N, McNab R, Spratt DA, Wilson M, Mullany P: Prevalence of tetracycline resistance genes in oral bacteria. Antimicrob Agents Chemother 2003, 47:878-882. (Pubitemid 36254209)
80. Sutcliffe J, Grebe T, Tait-Kamradt A, Wondrack L: Detection of erythromycin resistant determinants by PCR. Antimicrob Agents Chemother 1996, 40:2562-2566. (Pubitemid 26367644)
81. Vankerckhoven V, Van Autgaerden T, Vael C, Lammens C, Chapelle S, Rossi R, Jabes D, Goossens H: Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J Clin Microbiol 2004, 42:4473-4479.
82. Rice LB: Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob Agents Chemother 1998, 42:1871-1877.
83. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
84. Amachawadi RG, Shelton NW, Jacob ME, Shi X, Narayanan S, Zurek L, Dritz SS, Nelssen JL, Tokach MD, Nagaraja TG: Occurrence of tcrB, a transferable copper resistance gene, in fecal enterococci of swine. Food Path Dis 2010, 7:1089-1097.