Comparative analysis of the bacterial flora of vegetables collected directly from farms and from supermarkets in Germany

International Journal of Environmental Health Research

Volumn 21, Issue 3, 2011, Pages 161-172

  Schwaiger, Karin ^a   Helmke, Katharina ^a   Hölzel, Christina Susanne ^a   Bauer, Johann ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

bacteria; farm; fresh produce; supermarket; vegetables

Indexed keywords

BACTERIUM; COLIFORM BACTERIUM; COMPARATIVE STUDY; DISEASE PREVALENCE; FARM; FOOD MARKET; HEALTH RISK; MICROBIAL ACTIVITY; PATHOGEN; VEGETABLE;

AGRICULTURAL LAND; ANIMAL; ARTICLE; BACTERIAL FLORA; BACTERIUM ISOLATION; BULBOUS VEGETABLE; CEREAL; COMPARATIVE STUDY; ENTEROBACTER CLOACAE; ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS GALLINARUM; ESCHERICHIA COLI; FOOD INDUSTRY; FRUIT VEGETABLE; GERMANY; LISTERIA; LISTERIA INNOCUA; LISTERIA MONOCYTOGENES; MARKET; NONHUMAN; PREVALENCE; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; ROOT VEGETABLE; SALMONELLA; SALMONELLA ENTERICA; VEGETABLE;

BACTERIA; ENTEROCOCCUS; ESCHERICHIA COLI; FOOD CONTAMINATION; FOOD SUPPLY; GERMANY; HUMANS; PSEUDOMONAS; SALMONELLA; VEGETABLES;

BAVARIA; GERMANY;

ANIMALIA; BACTERIA (MICROORGANISMS); ENTEROBACTER CLOACAE; ENTEROCOCCUS; ESCHERICHIA COLI; LISTERIA; LISTERIA MONOCYTOGENES; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; SALMONELLA; SALMONELLA ENTERICA;

EID: 79957594900     PISSN: 09603123     EISSN: 13691619     Source Type: Journal    
DOI: 10.1080/09603123.2010.515672     Document Type: Article

References (62)

1. Altman SJ, McGrath LK, Souza CA, Murton JK, Camper AK. 2009. Integration and decontamination of Bacillus cereus in Pseudomonas fluorescens biofilms. J Appl Microbiol. 107:287-299.
2. Ammon A, Schmidt K, Braunig J. 2000. Lebensmittelinfektionen in Deutschland. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 43:751-757.
3. Bari ML, Inatsu Y, Isobe S, Kawamoto S. 2008. Hot water treatments to inactivate Escherichia coli O157:H7 and Salmonella in mung bean seeds. J Food Prot. 71:830-834. (Pubitemid 351500009)
4. Bejuk D, Begovac J, Gamberger D, Kucisec-Tepes N. 2000. Evaluation of phenotypic characteristics for differentiation of enterococcal species using an example based algorithm. Diagnost Microbiol Infect Dis. 38:2001-2005.
5. Bell KS, Sebaihia M, Pritchard L, Holden MTG, Hyman LJ, Holeva MC, Thomson NR, Bentley SD, Churcher LJ, Mungall K, Atkin R, Bason N, Brooks K, Chillingworth T, Clark K, Doggett J, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Norbertczak H, Ormond D, Price C, Quail MA, Sanders M, Walker D, Whitehead S, Salmond GP, Birch PR, Parkhill J, Toth IK. 2004. Genome sequence of the enterobacterial phytopathogen Erwinia carotovera subsp. atroseptica and characterization of virulence factors. PNAS. 27(101):11105-11110. (Pubitemid 38989591)
6. Boehme S, Werner G, Klare I, Reissbrodt R, Witte W. 2004. Occurrence of antibiotic-resistant enterobacteria in agricultural foodstuffs. Molec Nutrit Food Res. 48:522-531. (Pubitemid 39643695)
7. Bradford SA, Segal E. 2009. Fate of indicator microorganisms under nutrient management plan conditions. J Environ Qual. 38:1728-1738.
8. Brandl MT. 2006. Fitness of human enteric pathogens on plants and implications for food safety. Ann Rev Phytopathol. 44:1-26.
9. Buffet-Bataillon S, Rabier V, Betremieux P, Beuchee A, Bauer M, Pladys P, Le Gall E, Cormier M, Jolivet-Gougeon A. 2009. Outbreak of Serratia marcescens in a neonatal intensive care unit: Contaminated unmedicated liquid soap and risk factors. J Hosp Infect. 72:17-22.
10. Carpenter RJ, Hartzell JD, Forsberg JA, Babel BS, Ganesan A. 2008. Pseudomonas putida war wound infection in a US Marine: A case report and review of the literature. J Infect. 56:234-240.
11. Davis O, Wall BM. 2006. 'Broom straw peritonitis' secondary to Cedecea lapagei in a liver transplant recipient. Perit Dial Int. 26:512-513. (Pubitemid 44339990)
12. DIN EN 11290-1. 2005. Microbiology of food and animal feeding stuffs-Horizontal method for the detection and enumeration of Listeria monocytogenes-Part 1: Detection method. ISO 11290-1:1996\+ AMD 1: 2004. Berlin: Beuth-Verlag.
13. DIN EN 12824. 1998. Microbiology of Food and Animal Feeding Stuffs-Horizontal Method for the Detection of Salmonella (ISO 6579:1993, modified). German Version EN 12824:1997. Berlin: Beuth-Verlag.
14. Eugster W. 2006. Method and device for cleaning grain. WO/2006/114006. [Internet]. c2004-2010. Niederuzwil (CH): FreePatentsOnline.com. Accessed 29 March 2010 from the website: http://www.freepatentsonline.com/WO2006114006.html.
15. European Commission (EC). 2002. Regulation (EC) No. 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Available from: http://eur-lex.europa.eu/pri/en/oj/dat/2002/l-031/l- 03120020201en00010024.pdf.
16. European Commission. 2005. Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs [cited 2010 May]. Available from: http://eur-lex.europa.eu/LexUriServ/Lex-UriServ.douriCELEX:32005R2073:en:NOT.
17. European Community. 1996. Council Regulation (EC) No. 2200/96 on the common organization of the market in fruit and vegetables. CELEX-EUR Official Journal L. 297:1-28.
18. Farmer JJ, 3rd, Fanning GR, Huntley-Carter GP, Holmes B, Hickman FW, Richard C, Brenner DJ. 1981. Kluyvera, a new (redefined) genus in the family Enterobacteriaceae: Identification of Kluyvera ascorbata sp. nov. and Kluyvera cryocrescens sp. nov. in clinical specimens. J Clin Microbiol. 13:919-933. (Pubitemid 11094082)
19. Farmer JJ. 2005. Kluyvera. In: Brenner DJ, Krieg NR, Staley JT, editors. Bergey's manual of systematic bacteriology. Vol. 2, Part B. USA: Springer.
20. Freitag NE, Port GC, Miner MD. 2009. Listeria monocytogenes-from saprophyte to intracellular pathogen. Nat Rev Microbiol. 7:623-628.
21. Gedek B. 1995. Feed and feeding hygiene. In: Abel HJ, Flachowsky G, Jeroch H, Molnar S, editors. Livestock nutrition. Potentials, responsibility, perspectives. Jena/Stuttgart: G. Fischer. p. 354-374.
22. Gedek B. 1974. [Possibilities and limitations of microbiological animal feed control]. Dtsch Tierarztl Wochenschr. 81:37-40.
23. Grenier A-M, Duport G, Pages S, Condemine G, Rahbe Y. 2006. The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl Environ Microbiol. 72:1956-1965.
24. Hamilton-Miller JMT, Shah S. 2001. Identity and antibiotic susceptibility of enterobacterial flora of salad vegetables. Int J Antimicrob Agents. 18:81-83. (Pubitemid 32703872)
25. Hanning IB, Johnson MG, Ricke SC. 2008. Precut prepackaged lettuce: A risk for listeriosis? Foodborne Pathog Dis. 5:731-746.
26. Harrell LJ, Cameron ML, O'Hara CM. 1989. Rahnella aquatilis, an unusual gram-negative rod isolated from the bronchial washing of a patient with acquired immunodeficiency syndrome. J Clin Microbiol. 27:1671-1672.
27. Heesemann J. 2001. The family Enterobacteriaceae. In: Kohler W, Eggers HJ, Fleischner R, Marre H, Pfister G, Pulverer G, editors. Medical microbiology. 8th ed. Munich (Jena): Urban and Fischer.
28. Holzel C, Bauer J. 2008. Salmonella spp. in Bavarian liquid pig manure: Occurrence and relevance for the distribution of antibiotic resistance. Zoonoses Public Health. 55:133-138. (Pubitemid 351362060)
29. Holzel CS, Harms KS, Kuchenhoff H, Kunz A, Muller C, Meyer K, Schwaiger K, Bauer J. 2009. Phenotypic and genotypic bacterial antimicrobial resistance in liquid pig manure is variously associated with contents of tetracyclines and sulfonamides. J Appl Microbiol. 108:1642-1656.
30. Jensen LB, Baloda S, Boye M, Aarestrup FM. 2001. Antimicrobial resistance among Pseudomonas spp. and the Bacillus cereus group isolated from Danish agricultural soil. Environ Int. 26:581-587. (Pubitemid 32677473)
31. Johnston LM, Jaykus L-A. 2004. Antimicrobial resistance of Enterococcus species isolated from produce. Appl Environ Microbiol. 70:3133-3137. (Pubitemid 38657834)
32. Karlowsky JA, Kelly LJ, Thornsberry C, Jones ME, Sahm DF. 2002. Trends in antimicrobial resistance among urinary tract infection isolates of Escherichia coli from female outpatients in the United States. Antimicrob Agents Chemother. 47:1672-1680.
33. Khoo CH, Cheah YK, Lee LH, Sim JH, Salleh NA, Sidik SM, Radu S, Sukardi S. 2009. Virulotyping of Salmonella enterica subsp. enterica isolated from indigenous vegetables and poultry meat in Malaysia using multiplex-PCR. Antonie Van Leeuwenhoek. 96:441-457.
34. Kuhn I, Iversen A, Burman LG, Olsson-Liljequist B, Franklin A, Finn M, Aarestrup F, Seyfarth AM, Blanch AR, Vilanova X, Taylor H, Caplin J, Moreno MA, Dominguez L, Herrero IA, Mollby R. 2003. Comparison of enterococcal populations in animals, humans, and the environment-a European study. Int J Food Microbiol. 88:133-145. (Pubitemid 37329492)
35. Landgren M, Oden H, Kuhn I, Osterlund A, Kahlmeter G. 2005. Diversity among 2481 Escherichia coli from women with community-acquired lower urinary tract infections in 17 countries. J Antimicrob Chemother. 55:928-937. (Pubitemid 40883178)
36. Lee B, Sir JJ, Park SW, Kwak CH, Kim SM, Kim SB, Kwak YG, Whang DH, Cho WH, Choi SK. 2009. A case of Leclercia adecarboxylata endocarditis in a woman with endometrial cancer. Am J Med Sci. 337:146-147.
37. Lee YL, Cesario T, Wang Y, Shanbrom E, Thrupp L. 2003. Antibacterial activity of vegetables and juices. Nutrition. 19:994-996. (Pubitemid 37421207)
38. Leuschner RG, Ielsch V. 2003. Antimicrobial effects of garlic, clove and red hot chilli on Listeria monocytogenes in broth model systems and soft cheese. Int J Food Sci Nutr. 54:127-133. (Pubitemid 36267079)
39. Liao C-H, Fett WF. 2001. Analysis of native microflora and selection of strains antagonistic to human pathogens on fresh produce. J Food Prot. 64:1110-1115. (Pubitemid 32763547)
40. Liberto MC, Matera G, Puccio R, Lo Russo T, Colosimo E, Foca E. 2009. Six cases of sepsis caused by Pantoea agglomerans in a teaching hospital. New Microbiol. 32:119-123.
41. Lynch MF, Tauxe RV, Hedberg CW. 2009. The growing burden of foodborne outbreaks due to contaminated fresh produce: Risks and opportunities. Epidemiol Infect. 137:307-315. Review.
42. Mena KD, Gerba CP. 2009. Risk assessment of Pseudomonas aeruginosa in water. Rev Environ Contam Toxicol. 201:71-115.
43. Morris CE, Monier JM. 2003. The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol. 41:429-453. Review. (Pubitemid 37399689)
44. Muller T, Ulrich A, Ott E-M, Muller M. 2001. Identification of plant-associated enterococci. J Appl Microbiol. 91:268-278. (Pubitemid 32682049)
45. Noorzaleha AS, Gulam R, Zaiton H, Abdul R, Siti HI, Nishibuchi M, Son R. 2003. Incidence of Salmonella spp. in raw vegetables in Selangor, Malaysia. Food Control. 14:475-479. (Pubitemid 36880871)
46. Osterblad M, Pensala O, Peterzens M, Heleniusc H, Huovinen P. 1999. Antimicrobial susceptibility of Enterobacteriaceae isolated from vegetables. J Antimicrob Chemother. 43:503-509. (Pubitemid 29182299)
47. Ott E-M, Mueller T, Mueller M, Franz CM, Ulrich A, Gabel M, Seyfarth W. 2001. Population dynamics and antagonistic potential of enterococci colonizing the phyllosphere of grasses. J Appl Microbiol. 91:54-66. (Pubitemid 32623350)
48. Palaniswamy C, Selvaraj DR, Selvaraj T. 2009. Gangrenous cholecystitis caused by Hafnia alvei: A case report and review of literature. J Am Med Dir Assoc. 10:361-363.
49. Palleroni NJ. 2005. Pseudomonas. In: Garrity G, editor. Bergey's manual of systematic bacteriology. 2nd ed. Vol. 2, Part B-The Gammaproteobacteria. USA: Sringer.
50. Paterson DL, Ko WC, Von Gottberg A, Mohapatra S, Casellas JM, Goossens H, Mulazimoglu L, Trenholme G, Klugman KP, Bonomo RA, Rice LB, Wagener MM, McCormack JG, Yu VL. 2004. Antibiotic therapy for Klebsiella pneumoniae bacteremia: Implications of production of extended-spectrum beta-lactamases. Clin Infect Dis. 39:31-37. (Pubitemid 38879546)
51. Peters J, Mac K, Wichmann-Schauer H, Klein G, Ellerbroek L. 2003. Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany. Int J Food Microbiol. 88:311-314. (Pubitemid 37329508)
52. Pound MW, Tart SB, Okoye O. 2007. Multidrug-resistant Ewingella americana: A case report and review of the literature. Ann Pharmacother. 41:2066-2070. (Pubitemid 350230578)
53. Quiroz-Santiago C, Rodas-Suarez OR, Carlos RV, Fernandez FJ, Quinones-Ramirez EI, Vazquez-Salinas C. 2009. Prevalence of Salmonella in vegetables from Mexico. J Food Prot. 72:1279-1282.
54. Rossignol G, Merieau A, Guerillon J, Veron W, Lesouhaitier O, Feuilloley MG, Orange N. 2008. Involvement of a phospholipase C in the hemolytic activity of a clinical strain of Pseudomonas fluorescens. BMC Microbiol. 8:189.
55. Samonis G, Karageorgopoulos DE, Kofteridis DP, Matthaiou DK, Sidiropoulou V, Maraki S, Falagas ME. 2009. Citrobacter infections in a general hospital: Characteristics and outcomes. Eur J Clin Microbiol Infect Dis. 28:61-68.
56. Schleifer K-H, Ehrmann M, Beimfohr C, Brockmann E, Ludwig W, Amann R. 1995. Application of molecular methods for the classification and identification of lactic acid bacteria. Int Dairy J. 5:1081-1094.
57. Schmid MW, Ng EY, Lampidis R, Emmerth M, Walcher M, Kreft J, Goebel W, Wagner M, Schleifer KH. 2005. Evolutionary history of the genus Listeria and its virulence genes. Syst Appl Microbiol. 28:1-18.
58. Schwaiger K, Schmied E-M, Bauer J. 2008. Comparative analysis of antibiotic resistance characteristics of Gram-negative bacteria isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses Public Health. 55:331-341.
59. Schwaiger K, Schmied E-M, Bauer J. 2009. Comparative analysis on antibiotic resistance characteristics of Listeria spp. and Enterococcus spp. isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses Public Health. 57:171-180.
60. Warburton DW, Harrison B, Crawford C, Foster R, Fox C, Gour L, Purvis U. 1998. Current microbiological status of 'health foods' sold in Canada. Int J Food Microbiol. 42:1-7. (Pubitemid 28370325)
61. Wegener HC. 2003. Antibiotics in animal feed and their role in resistance development. Curr Opin Microbiol. 6:439-445 (Pubitemid 37345407)
62. ZMP. 2003. Central Market and Price Report Office. Bonn: Marktbilanz/Gemuse.