Insects in confined swine operations carry a large antibiotic resistant and potentially virulent enterococcal community
详细信息    查看全文
  • 作者:Aqeel Ahmad (1) (4)
    Anuradha Ghosh (2)
    Coby Schal (3)
    Ludek Zurek (1) (2)
  • 刊名:BMC Microbiology
  • 出版年:2011
  • 出版时间:December 2011
  • 年:2011
  • 卷:11
  • 期:1
  • 全文大小:869KB
  • 参考文献:1. Hall BG: Predicting the evolution of antibiotic resistance genes. / Nat Rev Microbiol 2004, 2: 430-35. CrossRef
    2. Cohen ML: Changing patterns of infectious disease. / Nature 2000, 406: 762-67. CrossRef
    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: 129-47.
    4. Levy SB: Factors impacting on the problem of antibiotic resistance. / J Antimicrob Chemother 2002, 49: 25-0. CrossRef
    5. Kummerer K: Resistance in the environment. / J Antimicrob Chemother 2004, 54: 311-20. CrossRef
    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; 2006:339-60.
    7. Mellon M, Benbrook C, Benbrook KL: Hogging It: Estimates of Antimicrobial Abuse in Livestock. [http://www.ucsusa.org/assets/documents/food_and_agriculture/hog_front.pdf] / Union of Concerned Scientists Cambridge MA; 2000.
    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; 2006:1-8.
    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. [http://www.environmentaldefense.org/documents/4301_AgEstimates.pdf] 2005.
    10. Aarestrup FM, Agers? 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: 127-37. CrossRef
    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: 3283-289. CrossRef
    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: 1628-635. CrossRef
    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: 6434-439. CrossRef
    14. Iversen A, Kühn I, Rahman M, Franklin A, Burman LG, Ollson-Liljequist B, Torrel E, M?llby R: Evidence for transmission between humans and the environment of nosocomial strain of Enterococcus faecium . / Environ Microbiol 2004, 6: 55-9. CrossRef
    15. De Leener E, Martel A, Decostere A, Haesebrouck F: Distribution of the erm (B) gene, tetracycline resistance genes, and Tn 1545-like transposons in macrolide- and lincosamide-resistant enterococci from pigs and humans. / Microb Drug Resist 2004, 10: 341-45. CrossRef
    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: 911-16. CrossRef
    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: 231-35. CrossRef
    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; 2008:1-6.
    19. Macovei L, Zurek L: Ecology of antibiotic resistance genes: characterization of enterococci from houseflies collected in food settings. / Appl Environ Microbiol 2006, 72: 4028-035. CrossRef
    20. Willems RJL, van Schalk W: Transition of Enterococcus faecium from commensal organism to nosicomial pathogen. / Future Microbiol 2009, 4: 1125-135. CrossRef
    21. Franz CAMP, Holzapfel WH, Stiles ME: Enterococci at the crossroads of food safety ? / Int J Food Microb 1999, 47: 1-4. CrossRef
    22. Klein G: Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. / Int J Food Microbiol 2003, 88: 123-31. CrossRef
    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: 7153-160. CrossRef
    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: 6740-747. CrossRef
    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: 154-547. CrossRef
    26. Kayser FH: Safety aspects of enterococci from the medical point of view. / Int J Food Microbiol 2003, 88: 255-62. CrossRef
    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; 2002:301-54.
    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: 269-90. CrossRef
    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: 1569-571. CrossRef
    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: 5709-718. CrossRef
    31. Mundy LM, Sahm DF, Gilmore MS: Relationship between enterococcal virulence and antimicrobial resistance. / Clin Microbiol Rev 2000, 13: 513-22. CrossRef
    32. Knudtson JM, Hartman PA: Antibiotic resistance among enterococcal isolates from environmental and clinical sources. / J Food Prot 1993, 56: 489-92.
    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, M?llby R: Comparison of enterococcal populations in animals, humans, and the environment - A European study. / Inter J Food Microbiol 2003, 88: 133-45. CrossRef
    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: 3255-260.
    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: 2112-115.
    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; 2002:55-9.
    37. Silbergeld EK, Graham J, Price LB: Industrial food animal production, antimicrobial resistance, and human health. / Annu Rev. Public Health 2008, 29: 151-69. CrossRef
    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. CrossRef
    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: 28-2. CrossRef
    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: 276-78. CrossRef
    41. Turnidge J: Antibiotic use in animals--prejudices, perceptions and realities. / J Antimicrob Chemother 2004, 53: 26-7. CrossRef
    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: 509-18. CrossRef
    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: 432-39.
    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: 924-28. CrossRef
    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: 993-97. CrossRef
    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: 609-21.
    47. Emerson PM, Lindsay SW, Walraven GEL, Faal H, Bogh C, Lowe K: Effect of fly control on trachoma and diarrhoea. / Lancet 1999, 353: 1401-403. CrossRef
    48. Graffar M, Mertens S: Le role des blattes dans la transmission des salmonelloses. / Ann Inst Past 1950, 79: 654-60.
    49. Tarshis IB: The cockroach - A new suspect in the spread of infectious hepatitis. / Am J Trop Med Hyg 1962, 11: 705-11.
    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: 263-67. CrossRef
    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: 2701-710. CrossRef
    52. Murray BE: The life and times of the Enterococcus. / Clin Microbiol Rev 1990, 3: 46-5.
    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: 365-66.
    54. Martin JD, Mundt JO: Enterococci in insects. / Appl Microbiol 1972, 24: 575-80.
    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: 172-88. CrossRef
    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: 2605-609.
    58. Van den Bogaard AE, Stobberingh EE: Epidemiology of resistance to antibiotics: Links between animals and humans. / Int J Antimicrb Agents 2000, 14: 327-35. CrossRef
    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: 151-58. CrossRef
    60. Teuber M, Meile L, Schwarz F: Acquired antibiotic resistance in lactic acid bacteria from food. / Antonie van Leeuwenhoek 1999, 76: 115-37. CrossRef
    61. Bertram J, Stratz M, Durre P: Natural transfer of conjugative transposon Tn 916 between Gram-positive and Gram-negative bacteria. / J Bacteriol 1991, 173: 443-48.
    62. Roberts MC: Resistance to tetracycline, macrolide-lincosamidestreptogramin, trimethoprim and sulfonamide drug classes. / Mol Biotechnol 2002, 20: 261-83. CrossRef
    63. Roberts MC: Update on acquired tetracycline resistance genes. / FEMS Microbiol Lett 2005, 245: 195-03. CrossRef
    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: 3152-155. CrossRef
    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: 2317-320. CrossRef
    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: 187-93. CrossRef
    67. Lester CH, Frimodt-M?ller N, S?rensen 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: 596-99. CrossRef
    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: 561-68. CrossRef
    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; 1998:140-47.
    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: 975-78. CrossRef
    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: 288-95. CrossRef
    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: 257-59. CrossRef
    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: 24-7.
    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: 3092-095.
    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: 1567-570. CrossRef
    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: 454-65. CrossRef
    78. Ng LK, Martin I, Alfa M, Mulvey M: Multiplex PCR for the detection of tetracycline resistant genes. / Mol Cell Probes 2001, 15: 209-15. CrossRef
    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: 878-82. CrossRef
    80. Sutcliffe J, Grebe T, Tait-Kamradt A, Wondrack L: Detection of erythromycin resistant determinants by PCR. / Antimicrob Agents Chemother 1996, 40: 2562-566.
    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: 4473-479. CrossRef
    82. Rice LB: Tn 916 family conjugative transposons and dissemination of antimicrobial resistance determinants. / Antimicrob Agents Chemother 1998, 42: 1871-877.
    83. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. / J Mol Biol 1990, 215: 403-10.
    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: 1089-097. CrossRef
  • 作者单位:Aqeel Ahmad (1) (4)
    Anuradha Ghosh (2)
    Coby Schal (3)
    Ludek Zurek (1) (2)

    1. Department of Entomology, Kansas State University, Manhattan, KS, USA
    4. Monsanto Company, 63167, St. Louis, MO, USA
    2. Department of Diagnostic Medicine and Pathobiology, Kansas State University, Manhattan, KS, USA
    3. Department of Entomology, North Carolina State University, Raleigh, NC, USA
  • ISSN:1471-2180
文摘
Background Extensive use of antibiotics as growth promoters in the livestock industry constitutes strong selection pressure for evolution and selection of antibiotic resistant bacterial strains. Unfortunately, the microbial ecology and spread of these bacteria in the agricultural, urban, and suburban environments are poorly understood. Insects such as house flies (Musca domestica) and German cockroaches (Blattella germanica) can move freely between animal waste and food and may play a significant role in the dissemination of antibiotic resistant bacteria within and between animal production farms and from farms to residential settings. Results Enterococci from the digestive tract of house flies (n = 162), and feces of German cockroaches (n = 83) and pigs (n = 119), collected from two commercial swine farms were isolated, quantified, identified, and screened for antibiotic resistance and virulence. The majority of samples (93.7%) were positive for enterococci with concentrations 4.2 ± 0.7 × 104 CFU/house fly, 5.5 ± 1.1 × 106 CFU/g of cockroach feces, and 3.2 ± 0.8 × 105 CFU/g of pig feces. Among all the identified isolates (n = 639) Enterococcus faecalis was the most common (55.5%), followed by E. hirae (24.9%), E. faecium (12.8%), and E. casseliflavus (6.7%). E. faecalis was most prevalent in house flies and cockroaches, and E. hirae was most common in pig feces. Our data showed that multi-drug (mainly tetracycline and erythromycin) resistant enterococci were common from all three sources and frequently carried antibiotic resistance genes including tet (M) and erm (B) and Tn 916/1545 transposon family. E. faecalis frequently harbored virulence factors gelE, esp, and asa1. PFGE analysis of selected E. faecalis and E. faecium isolates demonstrated that cockroaches and house flies shared some of the same enterococcal clones that were detected in the swine manure indicating that insects acquired enterococci from swine manure. Conclusions This study shows that house flies and German cockroaches in the confined swine production environment likely serve as vectors and/or reservoirs of antibiotic resistant and potentially virulent enterococci and consequently may play an important role in animal and public health.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700