Diversity, distribution and antibiotic resistance of Enterococcus spp. recovered from tomatoes, leaves, water and soil on U.S. Mid-Atlantic farms

Food Microbiology

Volumn 36, Issue 2, 2013, Pages 465-474

  Micallef, Shirley A ^a,c   Rosenberg Goldstein, Rachel E ^a   George, Ashish ^a   Ewing, Laura ^b   Tall, Ben D ^b   Boyer, Marc S ^b   Joseph, Sam W ^a   Sapkota, Amy R ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Amplified fragment length polymorphism; Antibiotic resistance; Enterococcus faecalis; Enterococcus spp.; Food safety; Pre harvest tomatoes; Soil; Water

Indexed keywords

ENTEROCOCCUS; ENTEROCOCCUS CASSELIFLAVUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS GALLINARUM; ENTEROCOCCUS HIRAE; ENTEROCOCCUS RAFFINOSUS; LYCOPERSICON ESCULENTUM;

ANTIINFECTIVE AGENT; GROUND WATER; WATER;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANTIBIOTIC RESISTANCE; ARTICLE; BIODIVERSITY; CLASSIFICATION; DRUG EFFECT; ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS SPP.; FOOD SAFETY; FRUIT; GENETICS; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PLANT LEAF; PRE-HARVEST TOMATOES; SOIL; TOMATO; UNITED STATES;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANTIBIOTIC RESISTANCE; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS SPP.; FOOD SAFETY; PRE-HARVEST TOMATOES; SOIL; WATER;

ANTI-BACTERIAL AGENTS; BIODIVERSITY; ENTEROCOCCUS; FRUIT; GROUNDWATER; LYCOPERSICON ESCULENTUM; MICROBIAL SENSITIVITY TESTS; MID-ATLANTIC REGION; PLANT LEAVES; SOIL MICROBIOLOGY;

EID: 84884165786     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2013.04.016     Document Type: Article

References (35)

1. Abriouel H., Omar N.B., Molinos A.C., López R.L., Grande M.J., Martínez-Viedma P., Ortega E., Cañamero M.M., Galvez A. Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal populations from raw fruit and vegetable foods, water and soil, and clinical samples. International Journal of Food Microbiology 2008, 123:38-49.
2. Ailes E.C., Leon J.S., Jaykus L.-A., Johnston L.M., Clayton H.A., Blanding S., Kleinbaum D.G., Backer L.C., Moe C.L. Microbial concentrations on fresh produce are affected by postharvest processing, importation, and season. Journal of Food Protection 2008, 71:2389-2397.
3. Arias C.A., Murray B.E. The rise of the Enterococcus: beyond vancomycin resistance. Nature Reviews Microbiology 2012, 10:266-278.
4. Aznar E., Buendía B., García-Peñuela E., Escudero E., Alarcón T., López-Brea M. Community-acquired urinary tract infection caused by vancomycin-resistant Enterococcus faecalis clinical isolate. Revista Española de Quimioterapia 2004, 17:263-265.
5. Badgley B.D., Thomas F.I.M., Harwood V.J. The effects of submerged aquatic vegetation on the persistence of environmental populations of Enterococcus spp. Environmental Microbiology 2010, 12:1271-1281.
6. Burtscher M.M., Köllner K.E., Sommer R., Keiblinger K., Farnleitner A.H., Mach R.L. Development of a novel amplified fragment length polymorphism (AFLP) typing method for enterococci isolates from cattle faeces and evaluation of the single versus pooled faecal sampling approach. Journal of Microbiological Methods 2006, 67:281-293.
7. Cevallos-Cevallos J.M., Danyluk M.D., Gu G., Vallad G.E., van Bruggen A.H.C. Dispersal of Salmonella Typhimurium by rain splash onto tomato plants. Journal of Food Protection 2012, 75:472-479.
8. CLSI Performance Standards for Antimicrobial Susceptibility Testing; Twentieth Informational Supplement 2010, Clinical and Laboratory Standards Institute, Wayne, PA, CLSI Document M100-S20. Clinical and Laboratory Standards Institute (Ed.).
9. EPA Method 1600: Enterococci in Water by Membrane Filtration Using Membrane-Enterococcus Indoxyl-B-D-Glucoside Agar (mEI) 2002, Office of Water. U.S. Environmental Protection Agency, Washington, DC.
10. Fazal B., Turett G., Chilimuri S., Mendoza C., Telzak E. Community-acquired enterococcal meningitis in an adult. Clinical Infectious Diseases 1995, 20:725-726.
11. FDA, Center for Food Safety and Applied Nutrition (CFSAN) Guidance for Industry: Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits and Vegetables 1998.
12. Fisher K., Phillips C. The ecology, epidemiology and virulence of Enterococcus. Microbiology 2009, 155:1749-1757.
13. Franz C.M.A.P., Stiles M.E., Schleifer K.H., Holzapfel W.H. Enterococci in foods-A conundrum for food safety. International Journal of Food Microbiology 2003, 88:105-122.
14. Gascon F., Castano M., Gonzalez A., Cordon M. Endocarditis due to Enterococcus casseliflavus. Enfermedades Infecciosas y Microbiología Clínica 2003, 21:275-276.
15. Giraffa G. Enterococci from foods. FEMS Microbiology Reviews 2002, 26:163-171.
16. Graham J.P., Evans S.L., Price L.B., Silbergeld E.K. Fate of antimicrobial-resistant enterococci and staphylococci and resistance determinants in stored poultry litter. Environmental Research 2009, 109:682-689.
17. Iaria C., Stassi G., Costa G., Di Leo R., Toscano A., Cascio A. Enterococcal meningitis caused by Enterococcus casseliflavus. BMC Infectious Diseases 2005, 5:3. First case report.
18. Jackson C.R., Fedorka-Cray P.J., Barrett J.B. Use of a genus- and species-specific multiplex PCR for identification of enterococci. Journal of Clinical Microbiology 2004, 42:3558-3565.
19. Johnston L.M., Jaykus L.-A. Antimicrobial resistance of Enterococcus species isolated from produce. Applied and Environmental Microbiology 2004, 70:3133-3137.
20. Johnston L.M., Jaykus L.-A., Moll D., Anciso J., Mora B., Moe C.L. Afield study of the microbiological quality of fresh produce of domestic and Mexican origin. International Journal of Food Microbiology 2006, 112:83-95.
21. Kariyama R., Mitsuhata R., Chow J.W., Clewell D.B., Kumon H. Simple and reliable multiplex PCR assay for surveillance isolates of vancomycin-resistant enterococci. Journal of Clinical Microbiology 2000, 38:3092-3095.
22. Kubota H., Tsuji H., Matsuda K., Kurakawa T., Asahara T., Nomoto K. Detection of human intestinal catalase-negative, Gram-positive cocci by rRNA-targeted reverse transcription-PCR. Applied and Environmental Microbiology 2010, 76:5440-5451.
23. Kwan C.W., Onyett H. Community-acquired urinary tract pathogens and their resistance patterns in hospitalized children in Southeastern Ontario between 2002 and 2006. Paediatrics & Child Health 2008, 13:759-762.
24. McGowan L.L., Jackson C.R., Barrett J.B., Hiott L.M., Fedorka-Cray P.J. Prevalence and antimicrobial resistance of enterococci isolated from retail fruits, vegetables, and meats. Journal of Food Protection 2006, 69:2976-2982.
25. McGowan-Spicer L.L., Fedorka-Cray P.J., Frye J.G., Meinersmann R.J., Barrett J.B., Jackson C.R. Antimicrobial resistance and virulence of Enterococcus faecalis isolated from retail food. Journal of Food Protection 2008, 71:760-769.
26. Micallef S.A., Shiaris M.P., Colón-Carmona A. Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. Journal of Experimental Botany 2009, 60:1729-1742.
27. Micallef S.A., Rosenberg Goldstein R.E., George A., Kleinfelter L., Boyer M.S., McLaughlin C.R., Estrin A., Ewing L., Jean-Gilles Beaubrun J., Hanes D.E., Kothary M.H., Tall B.D., Razeq J.H., Joseph S.W., Sapkota A.R. Occurrence and antibiotic resistance of multiple Salmonella serotypes recovered from water, sediment and soil on Mid-Atlantic tomato farms. Environmental Research 2012, 114:31-39.
28. Müller T., Ulrich A., Ott E.M., Müller M. Identification of plant-associated enterococci. Journal of Applied Microbiology 2001, 91:268-278.
29. Ntahimpera N., Wilson L.L., Ellis M.A., Madden L.V. Comparison of rain effects on splash dispersal of three Colletotrichum species infecting strawberry. Phytopathology 1999, 89:555-563.
30. Pappas G., Liberopoulos E., Tsianos E., Elisaf M. Enterococcus casseliflavus bacteremia. Case report and literature review. Journal of Infection 2004, 48:206-208.
31. Raja N.S., Karunakaran R., Ngeow Y.F., Awang R. Community-acquired vancomycin-resistant Enterococcus faecium: a case report from Malaysia. Journal of Medical Microbiology 2005, 54:901-903.
32. Ronconi M.C., Merino L.A., Fernández G. Detection of Enterococcus with high-level aminoglycoside and glycopeptide resistance in Lactuca sativa (lettuce). Enfermedades Infecciosas y Microbiología Clínica 2002, 20:380-383.
33. Tang Chen-Wei, Cheng Cheng-Kuo, Lee T.-S. Community-acquired bleb-related endophthalmitis caused by vancomycin-resistant enterococci. Canadian Journal of Ophthalmology 2007, 42:477-478.
34. USEPA Method 1106.1: Enterococci in Water by Membrane Filtration Using Membrane-Enterococcus-Esculin Iron Agar (mE-EIA) 2002, EPA 821-R-02-021, U.S. Environmental Protection Agency Office of Water, Washington, DC.
35. Willems R.J.L., Hanage W.P., Bessen D.E., Feil E.J. Population biology of gram-positive pathogens: high-risk clones for dissemination of antibiotic resistance. FEMS Microbiology Reviews 2011, 35:872-900.