https://doi.org/10.4081/ijfs.2023.11134
Food risk associated with vegetable consumption, exposure to antimicrobial-resistant strains and pesticide residues
Submitted: 30 December 2022
Accepted: 13 March 2023
Published: 8 June 2023
Accepted: 13 March 2023
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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This preliminary study aimed to detect biological and chemical contaminants in vegetables sold in Sicily for human consumption, assess the spread of antimicrobial-resistant (AMR) strains in these foods, and characterize their antimicrobial-resistance genes. A total of 29 fresh and ready-to-eat samples were analyzed. Microbiological analyses were performed for the detection of Salmonella spp. and the enumeration of Enterococci, Enterobacteriaceae, and Escherichia coli. Antimicrobial resistance was assessed by the Kirby-Bauer method, according to the Clinical and Laboratory Standards Institute guidelines. Pesticides were detected by high-performance liquid chromatography and gas chromatography coupled with mass spectrometry. No samples were contaminated by Salmonella spp., E. coli was detected in 1 sample of fresh lettuce at a low bacterial count (2 log cfu/g). 17.24% of vegetables were contaminated by Enterococci and 65.5% by Enterobacteriaceae (bacterial counts between 1.56 log cfu/g and 5.93 log cfu/g and between 1.6 log cfu/g and 5.48 log cfu/g respectively). From 86.2% of vegetables, 53 AMR strains were isolated, and 10/53 isolates were multidrug resistant. Molecular analysis showed that the blaTEM gene was detected in 12/38 β-lactam-resistant/intermediate-resistant isolates. Genes conferring tetracycline resistance (tetA, tetB, tetC, tetD, tetW) were detected in 7/10 isolates. The qnrS gene was detected in 1/5 quinolone-resistant isolates, the sulI gene was detected in 1/4 sulfonamide-resistant/intermediate-resistant isolates and the sulIII gene was never detected. Pesticides were detected in 27.3% of samples, all of which were leafy vegetables. Despite the satisfactory hygienic status of samples, the high percentage of AMR bacteria detected stresses the need for an effective monitoring of these foods as well as adequate strategies to counteract the spread of AMR bacteria along the agricultural chain. Also, the chemical contamination of vegetables should not be underestimated, especially considering that leafy vegetables are commonly consumed raw and that no official guidelines about maximum residue limits of pesticides in ready-to-eat vegetables are available.
Ahmed AM, Shimamoto T, Shimamoto T, 2013. Molecular characterization of multidrug-resistant avian pathogenic Escherichia coli isolated from septicemic broilers. Int J Med Microbiol 303:475-83.
DOI: https://doi.org/10.1016/j.ijmm.2013.06.009
Al-Kharousi ZS, Guizani N, Al-Sadi AM, Al-Bulushi IM, 2019. Antibiotic resistance of enterobacteriaceae isolated from fresh fruits and vegetables and characterization of their AmpC β-lactamases. J Food Prot 82:1857-63.
DOI: https://doi.org/10.4315/0362-028X.JFP-19-089
Alduina R, 2020. Antibiotics and environment. Antibiotics 9:202.
DOI: https://doi.org/10.3390/antibiotics9040202
AOAC, 2007. Pesticide residues in foods by acetonitrile extraction and partitioning with magnesium sulfate gas chromatography/mass spectrometry and liquid chromatography/tandem mass spectrometry first action. Available from: https://nucleus.iaea.org/sites/fcris/Shared%20Documents/SOP/AOAC_2007_01.pdf.
Arienzo M, Cataldo D, Ferrara L, 2013. Pesticide residues in fresh-cut vegetables from integrated pest management by ultra performance liquid chromatography coupled to tandem mass spectrometry. Food Control 31:108-15.
DOI: https://doi.org/10.1016/j.foodcont.2012.09.021
Calvaruso E, Cammilleri G, Pulvirenti A, Lo Dico GM, Lo Cascio G, Giaccone V, Vitale Badaco V, Ciprì V, Alessandra MM, Vella A, Macaluso A, Di Bella C, Ferrantelli V, 2020. Residues of 165 pesticides in citrus fruits using LC-MS/MS: a study of the pesticides distribution from the peel to the pulp. Nat Prod Res 34:34-8.
DOI: https://doi.org/10.1080/14786419.2018.1561682
Choubbane H, Ouakhssase A, Chahid A, Taourirte M, Aamouche A, 2022. Pesticides in fruits and vegetables from the Souss Massa region, Morocco. Food Addit Contam Part B Surveill 15:79-88.
DOI: https://doi.org/10.1080/19393210.2022.2028196
CLSI, 2021. M100 – performance standards for antimicrobial susceptibility testing. 31st ed. Malvern (PA), USA: Clinical and Laboratory Standards Institute.
Coy MR, Hoffmann M, Kingdom Gibbard HN, Kuhns EH, Pelz-Stelinski KS, Stelinski LL, 2014. Nested-quantitative PCR approach with improved sensitivity for the detection of low titer levels of Candidatus Liberibacter asiaticus in the Asian citrus psyllid, Diaphorina citri Kuwayama. J Microbiol Methods 102:15-22.
DOI: https://doi.org/10.1016/j.mimet.2014.04.007
Elgueta S, Fuentes M, Valenzuela M, Zhao G, Liu S, Lu H, Correa A, 2019. Pesticide residues in ready-to-eat leafy vegetables from markets of Santiago, Chile, and consumer’s risk. Food Addit Contam Part B Surveill 12:259-67.
DOI: https://doi.org/10.1080/19393210.2019.1625975
European Commission, 2005a. Regulation of the European Parliament and of the Council of 15 November 2005 on microbiological criteria for foodstuffs, 2073/2005/CE. In: Official Journal, L 338, 22/12/2005.
European Commission, 2005b. Regulation of the European Parliament and of the Council of 23 February 2005 on maximum residue levels of pesticides in or on food and feed of plant and animal origin, 396/2005/CE. In: Official Journal, L 70, 16/3/2005.
Ferri M, Ranucci E, Romagnoli P, Giaccone V, 2017. Antimicrobial resistance: a global emerging threat to public health systems. Crit Rev Food Sci Nutr 57:2857-76.
DOI: https://doi.org/10.1080/10408398.2015.1077192
Fontana C, Patrone V, Lopez CM, Morelli L, Rebecchi A, 2021. Incidence of tetracycline and erythromycin resistance in meat-associated bacteria: impact of different livestock management strategies. Microorganisms 9:2111.
DOI: https://doi.org/10.3390/microorganisms9102111
Garcês A, Pires I, Rodrigues P, 2020. Teratological effects of pesticides in vertebrates: a review. J Environ Sci Health B 55:75-89.
DOI: https://doi.org/10.1080/03601234.2019.1660562
ISO, 2010. Microbiology of food and animal feeding stuffs- horizontal method for the enumeration of beta-glucuronidase-positive escherichia coli-part 2: colony count technique at 44 degrees C using 5-bromo-4-chloro-3indolyl beta-D-glucuronide. ISO Norm 16649-2:2010. Geneva: International Organization for Standardization Publications.
ISO, 2017a. Microbiology of the food chain — horizontal method for the detection, enumeration and serotyping of salmonella — part 1: detection of Salmonella spp. ISO Norm 6579-1:2017. Geneva: International Organization for Standardization Publications.
ISO, 2017b. Microbiology of the food chain — horizontal method for the detection and enumeration of enterobacteriaceae — part 2: colony-count technique. ISO Norm 21528-2:2017. Geneva: International Organization for Standardization Publications.
Kiwango PA, Kassim N, Kimanya ME, 2018. The risk of dietary exposure to pesticide residues and its association with pesticide application practices among vegetable farmers in arusha, tanzania. JFR 7:86.
DOI: https://doi.org/10.5539/jfr.v7n2p86
Losio MN, Pavoni E, Bilei S, Bertasi B, Bove D, Capuano F, Farneti S, Blasi G, Comin D, Cardamone C, Decastelli L, Delibato E, De Santis P, Di Pasquale S, Gattuso A, Goffredo E, Fadda A, Pisanu M, De Medici D, 2015. Microbiological survey of raw and ready-to-eat leafy green vegetables marketed in Italy. Int J Food Microbiol 210:88-91.
DOI: https://doi.org/10.1016/j.ijfoodmicro.2015.05.026
Lynne AM, Rhodes-Clark BS, Bliven K, Zhao S, Foley SL, 2008. Antimicrobial resistance genes associated with Salmonella enterica Serovar Newport isolates from food animals. Antimicrob Agents Chemother 52:353-6.
DOI: https://doi.org/10.1128/AAC.00842-07
Marti E, Balcázar JL, 2013. Real-time PCR Assays for quantification of qnr genes in environmental water samples and chicken feces. Appl Environ Microbiol 79:1743-5.
DOI: https://doi.org/10.1128/AEM.03409-12
Morrison L, Zembower TR, 2020. Antimicrobial resistance. Gastrointest Endosc Clin N Am 30:619-35.
DOI: https://doi.org/10.1016/j.giec.2020.06.004
O’Flaherty E, Solimini AG, Pantanella F, De Giusti M, Cummins E, 2019. Human exposure to antibiotic resistant-Escherichia coli through irrigated lettuce. Environ Int 122:270-80.
DOI: https://doi.org/10.1016/j.envint.2018.11.022
Pesavento G, Calonico C, Ducci B, Magnanini A, Lo Nostro A, 2014. Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol 41:1-7.
DOI: https://doi.org/10.1016/j.fm.2014.01.008
Pihlström T, Fernández-Alba AR, Ferrer Amate C, Poulsen ME, Hardebusch B, Anastassiades M, 2021. Guidance SANTE 11312/2021 – analytical quality control and method validation procedures for pesticide residues analysis in food and feed. Available from: https://food.ec.europa.eu/system/files/2022-02/pesticides_mrl_guidelines_wrkdoc_2021-11312.pdf.
Romyasamit C, Sornsenee P, Chimplee S, Yuwalaksanakun S, Wongprot D, Saengsuwan P, 2021. Prevalence and characterization of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolated from raw vegetables retailed in Southern Thailand. PeerJ 9:e11787.
DOI: https://doi.org/10.7717/peerj.11787
Sabarwal A, Kumar K, Singh RP, 2018. Hazardous effects of chemical pesticides on human health–cancer and other associated disorders. Environ Toxicol Pharmacol 63:103-14.
DOI: https://doi.org/10.1016/j.etap.2018.08.018
Santarelli GA, Migliorati G, Pomilio F, Marfoglia C, Centorame P, D’Agostino A, D’Aurelio R, Scarpone R, Battistelli N, Di Simone F, Aprea G, Iannetti L, 2018. Assessment of pesticide residues and microbial contamination in raw leafy green vegetables marketed in Italy. Food Control 85:350-8.
DOI: https://doi.org/10.1016/j.foodcont.2017.09.035
Sucato A, Vecchioni L, Savoca D, Presentato A, Arculeo M, Alduina R, 2021. A comparative analysis of aquatic and polyethylene-associated antibiotic-resistant microbiota in the mediterranean sea. Biology 10:200.
DOI: https://doi.org/10.3390/biology10030200
Tasiopoulou S, Chiodini AM, Vellere F, Visentin S, 2007. Results of the monitoring program of pesticide residues in organic food of plant origin in Lombardy (Italy). J Environ Sci Health B 42:835-41.
DOI: https://doi.org/10.1080/03601230701555054
Tudi M, Ruan HD, Wang L, Lyu J, Sadler R, Connell D, Chu C, Phung DT, 2021. Agriculture development, pesticide application and its impact on the environment. Int J Environ Res Public Health 18:1112.
DOI: https://doi.org/10.3390/ijerph18031112
UNI EN, 2018. Foods of plant origin - multimethod for the determination of pesticide residues using GC- and LC-based analysis following acetonitrile extraction/partitioning and clean-up by dispersive SPE - Modular QuEChERS-method. UNI EN Norm 15662:2018. Available from: https://standards.iteh.ai/catalog/standards/cen/167a30bc-edf9-4cf8-b96b-cabd932f2f02/en-15662-2018.
World Health Organization, 2021. Antimicrobial resistance. Available from: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance. Accessed: 17 December 2022.
Zhang YJ, Hang-Wei H, Qing-Lin C, Brajesh KS, Hui Y, Deli C, Ji-Zheng H, 2019. Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes. Environ Int 130:104912.
DOI: https://doi.org/10.1016/j.envint.2019.104912
How to Cite
1.
Castello A, Lo Cascio G, Ferraro C, Pantano L, Costa A, Butera G, Oliveri G, Rizzuto ML, Alduina R, Cardamone C. Food risk associated with vegetable consumption, exposure to antimicrobial-resistant strains and pesticide residues. Ital J Food Safety [Internet]. 2023 Jun. 8 [cited 2024 Dec. 22];12(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/11134
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