Research article

Comparison of the Antibiotic-Resistant Enterobacteriaceae Content in Conventional, Organic and Fresh-Cut Vegetables Sold in Valencia (Spain)

  • Received: 14 January 2020 Accepted: 24 May 2020 Published: 05 June 2020
  • Bacterial content of fresh vegetables that are often eaten raw represents a risk factor for consumers, and the presence in these produce of antibiotic-resistant bacteria constitutes an additional food safety concern. We have compared the Enterobacteriaceae content, as well as the antibiotic resistances of bacterial isolates, in samples of different types of fresh vegetables (conventional an organic produce, fresh-cut vegetables and prepared salads) marketed in Valencia (Spain) in order to find possible differences among these vegetable types. Bacterial isolation, identification and resistance assays to eleven relevant chemotherapeutics agents were performed according to standard microbiological procedures. A total of 195 bacterial isolates (from 230 vegetable samples) were compared. All vegetable types carry a variety of opportunistic bacterial pathogens, with a significant frequency of resistant isolates to one or more (up to three, four or five antibiotics, depending on the vegetable type). Enterobacter spp. (mainly E. cloacae) and Klebsiella spp. (K. oxytoca and K. pneumoniae) were the most frequent in conventional, fresh-cut vegetables and prepared salads (60-77% of isolates), whereas in organic produce the most frequent species were Pantoea agglomerans (24%), Serratia marcescens (16%) and E. cloacae (13%). Fresh-cut produce had the highest content of bacterial burden and bacterial diversity, indicating that the sanitizing methods are not effective enough and should be improved. Organic vegetables showed a higher bacterial diversity and a lower frequency of antibiotic resistances, as compared with conventional produce, indicating that organic farming practices may favor microbial diversity and partially prevent selection and development of resistant bacteria. Therefore, it could be relevant to include the detection of antibiotic-resistant non-pathogenic Enterobacteriaceae species in fresh vegetables in the epidemiological surveillance routine to quantify dissemination of multi-resistances in non-hospital environment and to evaluate the potential role of consumption of fresh vegetables in spreading resistances into community.

    Citation: Hortensia Rico, Pilar Falomir. Comparison of the Antibiotic-Resistant Enterobacteriaceae Content in Conventional, Organic and Fresh-Cut Vegetables Sold in Valencia (Spain)[J]. AIMS Agriculture and Food, 2020, 5(2): 233-244. doi: 10.3934/agrfood.2020.2.233

    Related Papers:

  • Bacterial content of fresh vegetables that are often eaten raw represents a risk factor for consumers, and the presence in these produce of antibiotic-resistant bacteria constitutes an additional food safety concern. We have compared the Enterobacteriaceae content, as well as the antibiotic resistances of bacterial isolates, in samples of different types of fresh vegetables (conventional an organic produce, fresh-cut vegetables and prepared salads) marketed in Valencia (Spain) in order to find possible differences among these vegetable types. Bacterial isolation, identification and resistance assays to eleven relevant chemotherapeutics agents were performed according to standard microbiological procedures. A total of 195 bacterial isolates (from 230 vegetable samples) were compared. All vegetable types carry a variety of opportunistic bacterial pathogens, with a significant frequency of resistant isolates to one or more (up to three, four or five antibiotics, depending on the vegetable type). Enterobacter spp. (mainly E. cloacae) and Klebsiella spp. (K. oxytoca and K. pneumoniae) were the most frequent in conventional, fresh-cut vegetables and prepared salads (60-77% of isolates), whereas in organic produce the most frequent species were Pantoea agglomerans (24%), Serratia marcescens (16%) and E. cloacae (13%). Fresh-cut produce had the highest content of bacterial burden and bacterial diversity, indicating that the sanitizing methods are not effective enough and should be improved. Organic vegetables showed a higher bacterial diversity and a lower frequency of antibiotic resistances, as compared with conventional produce, indicating that organic farming practices may favor microbial diversity and partially prevent selection and development of resistant bacteria. Therefore, it could be relevant to include the detection of antibiotic-resistant non-pathogenic Enterobacteriaceae species in fresh vegetables in the epidemiological surveillance routine to quantify dissemination of multi-resistances in non-hospital environment and to evaluate the potential role of consumption of fresh vegetables in spreading resistances into community.


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    [1] Birt CA. (2017) Healthy diets and a healthy planet. Eur J Public Health 27: 790-791. doi: 10.1093/eurpub/ckx102
    [2] Smith-Spangler C, Brandeau ML, Hunter GE, et al. (2012) Are organic foods safer or healthier than conventional alternatives? A systematic review. Ann Intern Med 157: 348-366.
    [3] Francis GA, Gallone A, Nychas GJ, et al. (2012) Factors affecting quality and safety of fresh-cut produce. Crit Rev Food Sci Nutr 52: 595-610. doi: 10.1080/10408398.2010.503685
    [4] Ansah FA, Amodio ML, Colelli G (2018) Quality of fresh-cut products as affected by harvest and postharvest operations. J Sci Food Agric 98: 3614-3626. doi: 10.1002/jsfa.8885
    [5] 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. doi: 10.1017/S0950268808001969
    [6] Martínez-Vaz BM, Fink RC, Diez-González F, et al. (2014) Enteric pathogen-plant interactions: Molecular connections leading to colonization and growth and implications for food safety. Microbes Environ 29: 123-135. doi: 10.1264/jsme2.ME13139
    [7] Wadamori Y, Gooneratne R, Hussain MA (2017) Outbreaks and factors influencing microbiological contamination of fresh produce. J Sci Food Agric 97: 1396-1403. doi: 10.1002/jsfa.8125
    [8] Heaton JC, Jones K (2008) Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: A review. J Appl Microbiol 104: 613-626. doi: 10.1111/j.1365-2672.2007.03587.x
    [9] Olaimat AN, Holley RA (2012) Factors influencing the microbial safety of fresh produce: A review. Food Microbiol 32: 1-19. doi: 10.1016/j.fm.2012.04.016
    [10] Rajwar A, Srivastava P, Sahgal M (2016) Microbiology of fresh produce: route of contamination, detection methods, and remedy. Crit Rev Food Sci Nutr 56: 2383-2390. doi: 10.1080/10408398.2013.841119
    [11] Kaczmarek M, Avery SV, Singleton I (2019) Microbes associated with fresh produce: sources, types and methods to reduce spoilage and contamination. Adv Appl Microbiol 107: 29-82. doi: 10.1016/bs.aambs.2019.02.001
    [12] Venglovsky J, Sasakova N, Placha I (2009) Pathogens and antibiotic residues in animal manures and hygienic and ecological risks related to subsequent land application. Bioresour Technol 100: 5386-5391. doi: 10.1016/j.biortech.2009.03.068
    [13] Chee-Sanford LC, Mackie RI, Koike S, et al. (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38: 1086-1108. doi: 10.2134/jeq2008.0128
    [14] Marti R, Scott A, Tien YC, et al. (2013) Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl Environ Microbiol 79: 5701-5709. doi: 10.1128/AEM.01682-13
    [15] Araújo S, Silva I, Tacão M, et al. (2017) Characterization of antibiotic resistant and pathogenic Escherichia coli in irrigation water and vegetables in household farms. Int J Food Microbiol 257: 192-200. doi: 10.1016/j.ijfoodmicro.2017.06.020
    [16] Falomir MP, Rico H, Gozalbo D (2013) Enterobacter and Klebsiella species isolated from fresh vegetables marketed in Valencia (Spain) and their clinically relevant resistances to chemotherapeutic agents. Foodborne Pathog Dis 10: 1002-1007. doi: 10.1089/fpd.2013.1552
    [17] Falomir MP, González P, Rico H, et al. (2014) Resistances to chemotherapeutic agents in Enterobacteriaceae isolates from organic fresh vegetables marketed in Valencia (Spain). Int J Food Nutr Saf 5: 39-49.
    [18] Rico H, Gozalbo D, Sebastiá C, et al. (2013) Enterobacter cloacae in fresh vegetables: A potential carrier of antibiotic resistances to consumers. Food Studies: Interdiscipl J 2: 1-8.
    [19] Doyle ME (2015) Multidrug-resistant pathogens in the food supply. Foodborne Pathog Dis 12: 261-279. doi: 10.1089/fpd.2014.1865
    [20] Huijbers PM, Blaak H, de Jong MC, et al. (2015) Role of the environment in the transmission of antimicrobial resistance to humans: A review. Environ Sci Technol 49: 11993-12004. doi: 10.1021/acs.est.5b02566
    [21] Hölzel CS, Tetens JL, Schwaiger K (2018) Unraveling the role of vegetables in spreading antimicrobial-resistant bacteria: A need for quantitative risk assessment. Foodborne Pathog Dis 15: 671-688. doi: 10.1089/fpd.2018.2501
    [22] Walsh F (2013) The multiple roles of antibiotics and antibiotic resistance in nature. Front Microbiol 4: 255.
    [23] Blau K, Bettermann A, Jechalke S, et al. (2018) The transferable resistome of produce. MBio 9: pii: e01300-18.
    [24] Baquero F (2012) Metagenomic epidemiology: A public health need for the control of antimicrobial resistance. Clin Microbiol Infect 18: 67-73.
    [25] Arzanlou M, Chai WC, Venter H (2017) Intrinsic, adaptive and acquired antimicrobial resistance in Gram-negative bacteria. Essays Biochem 61: 49-59. doi: 10.1042/EBC20160063
    [26] Eichenberger EM, Thaden JT (2019) Epidemiology and mechanisms of resistance of extensively drug resistant Gram-negative bacteria. Antibiotics (Basel) 8: pii: E37.
    [27] Jung Y, Jang H, Matthews KR (2014) Effect of the food production chain from farm practices to vegetable processing on outbreak incidence. Microb Biotechnol 7: 517-527. doi: 10.1111/1751-7915.12178
    [28] Tyler HL, Triplett EW (2008) Plants as a habitat for beneficial and/or human pathogenic bacteria. Annu Rev Phytopathol 46: 53-63. doi: 10.1146/annurev.phyto.011708.103102
    [29] Hwang JH, Yoon JH, Bae YM, et al. (2017) Effect of the precutting process on sanitizing treatments for reducing pathogens in vegetables. Food Sci Biotechnol 26: 531-536. doi: 10.1007/s10068-017-0073-7
    [30] Yoon JH, Lee SY (2018) Review: Comparison of the effectiveness of decontaminating strategies for fresh fruits and vegetables and related limitations. Crit Rev Food Sci Nutr 58: 3189-3208. doi: 10.1080/10408398.2017.1354813
    [31] Uhlig E, Olsson C, He J, et al. (2017) Effects of household washing on bacterial load and removal of Escherichia coli from lettuce and 'ready-to-eat' salads. Food Sci Nutr 5: 1215-1220. doi: 10.1002/fsn3.514
    [32] Vestrheim DF, Lange H, Nygard K, et al. (2016) Are ready-to-eat salads ready to eat? An outbreak of Salmonella coeln linked to imported, mixed, pre-washed and bagged salad, Norway, November 2013. Epidemiol Infect 144: 1756-1760.
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