Prevalence and Characterization of Beta-Lactam and Carbapenem-Resistant Bacteria Isolated from Organic Fresh Produce Retailed in Eastern Spain

Jiménez-Belenguer, Ana; Ferrús, María Antonia; Cedillo-Hernandez, Manuel; García-Hernández, Jorge; Moreno, Yolanda; Castillo, M.A.

doi:10.3390/antibiotics12020387

Cited by 13 publications

(7 citation statements)

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“…We observed higher ESBL-PE percentages in samples from organic versus conventionally raised products, both in chicken meat and greens samples. A recent study from Spain supports organic fresh fruits and vegetables as important reservoirs for β-lactam-and even carbapenem-resistant bacteria (Jimenez-Belenguer et al, 2023). Comparable differences in detection rates of ESBL-PE between organic and non-organic grown vegetables have also been previously reported from the Netherlands , and between organic and non-organic chicken meat samples from Germany (Kola et al, 2012) and the Netherlands (Cohen Stuart et al, 2012).…”

Section: Discussionmentioning

confidence: 55%

Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland

Gómez-Sanz,

Bagutti,

García-Martín

et al. 2023

Front. Microbiol.

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BackgroundThe involvement of non-human-to-human transmission of extended-spectrum β-lactamase-producing Enterobacterales (ESBL-PE) remains elusive. Foodstuffs may serve as reservoirs for ESBL-PE and contribute to their spread.AimWe aimed to systematically investigate the presence and spatiotemporal distribution of ESBL-PE in diverse unprocessed foodstuffs of different origin purchased in a central European city.MethodsChicken and green (herbs, salad, sprouts, vegetables) samples were collected monthly for two consecutive years, from June 2017 to June 2019, from large supermarket chains and small local food retailers, representing all ten postcode areas of the City of Basel (Switzerland), and the kitchen of the University Hospital Basel (Basel, Switzerland). After enrichment, presumptive ESBL-PE were isolated by selective culture methods and identified by Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. ESBL production was confirmed by phenotypic testing.ResultsAmong 947 food samples, 14.8% were positive for ESBL-PE isolate/s belonging to eight different ESBL-producing bacterial species. Escherichia coli and Serratia fonticola were predominant across samples (9 and 2%, respectively). Higher ESBL-PE prevalence was observed in chicken (25.9%) than in green (3.8%) samples (p < 0.001). Among greens, ESBL-PE were most frequently isolated from sprouts (15.2%). High ESBL-PE species diversity was observed among chicken samples, with E. coli as predominant (17.6%). ESBL-producing Enterobacter cloacae was detected among different greens. Yet, ESBL-producing Klebsiella pneumoniae was predominant in sprouts (12.1%). In total, 20.5% of samples from organic farming and 14.2% of samples from conventionally raised animals harbored an ESBL-producing isolate. Detection of ESBL-PE across samples differed between organic and non-organic when stratified by food source (p < 0.001), particularly among greens (12.5% organic, 2.4% conventional). High proportion of organic chicken samples was positive for ESBL-E. coli (33.3%), while the detection of several species characterized the conventional chicken samples. No significant differences in ESBL-PE frequences were detected between national (13.4%) and international samples (8.0%) (p = 0.122). Instead, differences were observed between regions of food production and countries (p < 0.001). No significant differences were found when comparing the proportion of ESBL-PE positive samples across districts, shop sizes and the hospital kitchen. The percentage of ESBL-PE positive samples did not differ monthly across the two-year sampling period (p = 0.107).ConclusionOur findings indicate moderate dissemination of ESBL-PE in foodstuffs, especially between chicken products and sprouts. Chicken meat represents a source for several ESBL-producing Enterobacterales, especially E. coli, while greens are more prone to carry ESBL-K. pneumoniae and E. cloacae. We disclose the importance of food type, food production system and production origin when assessing the risk of contamination with different ESBL-PE species.

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Section: Discussionmentioning

confidence: 55%

Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland

Gómez-Sanz,

Bagutti,

García-Martín

et al. 2023

Front. Microbiol.

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“… 166 In addition, bla NDM (50%) and bla KPC-2 (50%) were the most prevalent carbapenemase genes in CRBs isolated from Chinese rivers. 167 In Spain, Jiménez-Belenguer et al, 168 rather reported bla VIM (26.7%), bla IMP (23.6%), bla OXA-48 (17.4%), bla CMY-2 (8.1%), and bla KPC (4.3%) in CRBs isolated from fresh vegetables. Interestingly, SHV-type carbapenemases, which are often neglected in humans, are well represented (third rank) in animal-environment-food, with 19 variants in this study.…”

Section: Discussionmentioning

confidence: 98%

Carbapenem Resistance in Animal-Environment-Food from Africa: A Systematic Review, Recommendations and Perspectives

Dossouvi,

Ametepe

2024

IDR

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Background The World Health Organization (WHO) has classified carbapenem-resistant Enterobacteriaceae, Pseudomonas aeruginosa ( P. aeruginosa ), and Acinetobacter baumannii ( A. baumannii ) as high-priority pathogens, and carbapenem-resistant bacteria (CRB) have been reported to spread between humans, animals, and the environment. Objective This study aimed to conduct a systematic review of carbapenem resistance in animals, foods, and the environment on the African continent and to provide recommendations and perspectives for better prevention and control of carbapenem resistance in Africa. Results A total of 137 research articles collected from 2009 to 2023 were selected for this review, including articles reporting carbapenem-resistant bacteria in animals (81/137; 59.1%), the environment (66/137; 48.2%), and foods (26/137; 19%). Carbapenem-resistant bacterial species belonged to 31 genera and 17 families, including mainly Escherichia spp. (68/127; 53.5%); Klebsiella spp. (45/127; 35.4%); Pseudomonas spp. (20/127; 15.7%), Enterobacter spp. (19/127; 15%) and Acinetobacter spp. (15/127; 11.8%). The prevalence of CRBs by country ranged from 1.1% to 48.5%, and the pooled prevalence of CRBs isolated from animal-environment-food in Africa was 19.1% (2804/14,684; Standard Deviation = 15). Twenty carbapenemase families belonging to A, B, C, and D Ambler classes were reported, including mainly carbapenemase genes from bla OXA (44/84; 52.4%), bla NDM (34/84; 40.5%), bla SHV (23/84; 27.4%), bla KPC (22/84; 26.2%), bla VIM (19/84; 22.6%), and bla IMP (12/84; 14.3%) families. The reported mobile genetic elements (MGE) carrying carbapenemase-encoding genes included plasmids (16/19; 84.2%), integrons (3/19; 15.8%), transposons (3/19; 15.8%), and insertion sequences (2/19; 10.5%). bla OXA-48 was often carried by (60kb-65kb) IncL/M-type pOXA-48 plasmids, while bla NDM-5 was often carried by (45–50kb) IncX-type plasmids. Moreover, 25 articles investigated and reported virulent and hypervirulent CRBs that carried multiple virulence factors. Conclusion Animal-environment-food ecosystems would constitute reservoirs of CRBs involved in human infections. The One Health approach and constant collaboration between governments are necessary to drastically reduce the mortality rates linked to antimicrobial resistance.

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“…These isolates exhibited the highest phenotypic antimicrobial resistance towards ampicillin, tetracycline, and trimethoprim-sulfamethoxazole. The use of antibiotics in animal feed and as veterinary drugs is increasing, which poses a threat to the entire agriculture ecosystem, including raw vegetable production systems, soil, and groundwater quality [ 35 ]. Our findings suggest that fresh produce vegetables could also serve as a source for multidrug-resistant E. coli .…”

Section: Discussionmentioning

confidence: 99%

Contamination Levels and Phenotypic and Genomic Characterization of Antimicrobial Resistance in Escherichia coli Isolated from Fresh Salad Vegetables in the United Arab Emirates

et al. 2023

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Contaminated fresh produce has been identified as a vehicle for human foodborne illness. The present study investigated the counts, antimicrobial resistance profile, and genome-based characterization of Escherichia coli in 11 different types of fresh salad vegetable products (n = 400) sampled from retailers in Abu Dhabi and Dubai in the United Arab Emirates. E. coli was detected in 30% of the tested fresh salad vegetable items, with 26.5% of the samples having an unsatisfactory level (≥100 CFU/g) of E. coli, notably arugula and spinach. The study also assessed the effect of the variability in sample conditions on E. coli counts and found, based on negative binominal regression analysis, that samples from local produce had a significantly higher (p-value < 0.001) E. coli count than imported samples. The analysis also indicated that fresh salad vegetables from the soil-less farming system (e.g., hydroponic and aeroponic) had significantly (p-value < 0.001) fewer E. coli than those from traditional produce farming. The study also examined the antimicrobial resistance in E. coli (n = 145) recovered from fresh salad vegetables and found that isolates exhibited the highest phenotypic resistance toward ampicillin (20.68%), tetracycline (20%), and trimethoprim-sulfamethoxazole (10.35%). A total of 20 (13.79%) of the 145 E. coli isolates exhibited a multidrug-resistant phenotype, all from locally sourced leafy salad vegetables. The study further characterized 18 of the 20 multidrug-resistant E. coli isolates using whole-genome sequencing and found that the isolates had varying numbers of virulence-related genes, ranging from 8 to 25 per isolate. The frequently observed genes likely involved in extra-intestinal infection were CsgA, FimH, iss, and afaA. The β-lactamases gene blaCTX-M-15 was prevalent in 50% (9/18) of the E. coli isolates identified from leafy salad vegetable samples. The study highlights the potential risk of foodborne illness and the likely spread of antimicrobial resistance and resistance genes associated with consuming leafy salad vegetables and emphasizes the importance of proper food safety practices, including proper storage and handling of fresh produce.

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Prevalence and Characterization of Beta-Lactam and Carbapenem-Resistant Bacteria Isolated from Organic Fresh Produce Retailed in Eastern Spain

Cited by 13 publications

References 58 publications

Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland

Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland

Carbapenem Resistance in Animal-Environment-Food from Africa: A Systematic Review, Recommendations and Perspectives

Contamination Levels and Phenotypic and Genomic Characterization of Antimicrobial Resistance in Escherichia coli Isolated from Fresh Salad Vegetables in the United Arab Emirates

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