Presence and potential for horizontal transfer of antibiotic resistance in oxidase-positive bacteria populating raw salad vegetables

Bezanson, G. S.; MacInnis, R.; Pötter, Gabrielle; Hughes, Thomas A.

doi:10.1016/j.ijfoodmicro.2008.06.008

Cited by 63 publications

(53 citation statements)

References 40 publications

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“…Presumably, the difference is accounted for by washing soil off the vegetables, as would be expected in normal culinary preparation. These results are entirely consistent with previous studies that have detected antibiotic-resistant bacteria on vegetable products at harvest or at the retail level (25)(26)(27)(28)(29)(30)(31)(32). Variation in laboratory methods, sampling strategy, and sample handling practices makes it difficult to compare studies, especially quantitatively.…”

Section: Discussionsupporting

confidence: 87%

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

Marti

Scott

Tien

et al. 2013

Appl Environ Microbiol

401

236

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bConsumption of vegetables represents a route of direct human exposure to bacteria found in soil. The present study evaluated the complement of bacteria resistant to various antibiotics on vegetables often eaten raw (tomato, cucumber, pepper, carrot, radish, lettuce) and how this might vary with growth in soil fertilized inorganically or with dairy or swine manure. Vegetables were sown into field plots immediately following fertilization and harvested when of marketable quality. Vegetable and soil samples were evaluated for viable antibiotic-resistant bacteria by plate count on Chromocult medium supplemented with antibiotics at clinical breakpoint concentrations. DNA was extracted from soil and vegetables and evaluated by PCR for the presence of 46 gene targets associated with plasmid incompatibility groups, integrons, or antibiotic resistance genes. Soil receiving manure was enriched in antibiotic-resistant bacteria and various antibiotic resistance determinants. There was no coherent corresponding increase in the abundance of antibiotic-resistant bacteria enumerated from any vegetable grown in manure-fertilized soil. Numerous antibiotic resistance determinants were detected in DNA extracted from vegetables grown in unmanured soil. A smaller number of determinants were additionally detected on vegetables grown only in manured and not in unmanured soil. Overall, consumption of raw vegetables represents a route of human exposure to antibiotic-resistant bacteria and resistance determinants naturally present in soil. However, the detection of some determinants on vegetables grown only in freshly manured soil reinforces the advisability of pretreating manure through composting or other stabilization processes or mandating offset times between manuring and harvesting vegetables for human consumption.

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Section: Discussionsupporting

confidence: 87%

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

Marti

Scott

Tien

et al. 2013

Appl Environ Microbiol

401

236

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“…Exposure is still possible because of cross-contamination in the kitchen (71). However, the present study and also other studies have revealed an antibiotic resistance pool in food-borne commensal bacteria in many readyto-consume food products (23,49,72). Because many of these foods (including fresh produce such as lettuce) are directly consumed without further processing, AR bacteria can be directly transmitted to humans through daily food intake (70).…”

Section: Discussionmentioning

confidence: 57%

“…Because many of these foods (including fresh produce such as lettuce) are directly consumed without further processing, AR bacteria can be directly transmitted to humans through daily food intake (70). As there is a potential to pass resistance to other bacteria, including those normally present in the human gastrointestinal tract, ready-to-eat foods such as fresh produce may serve as a vehicle for expanding the pool of antibiotic resistances available to (pathogenic or other) bacteria inhabiting humans (72). If these resistance genes are transferred to human-pathogenic bacteria, infections may become more difficult to treat.…”

Section: Discussionmentioning

confidence: 99%

Moderate Prevalence of Antimicrobial Resistance in Escherichia coli Isolates from Lettuce, Irrigation Water, and Soil

Holvoet

Sampers

Callens

et al. 2013

Appl Environ Microbiol

104

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cFresh produce is known to carry nonpathogenic epiphytic microorganisms. During agricultural production and harvesting, leafy greens can become contaminated with antibiotic-resistant pathogens or commensals from animal and human sources. As lettuce does not undergo any inactivation or preservation treatment during processing, consumers may be exposed directly to all of the (resistant) bacteria present. In this study, we investigated whether lettuce or its production environment (irrigation water, soil) is able to act as a vector or reservoir of antimicrobial-resistant Escherichia coli. Over a 1-year period, eight lettuce farms were visited multiple times and 738 samples, including lettuce seedlings (leaves and soil), soil, irrigation water, and lettuce leaves were collected. From these samples, 473 isolates of Escherichia coli were obtained and tested for resistance to 14 antimicrobials. Fiftyfour isolates (11.4%) were resistant to one or more antimicrobials. The highest resistance rate was observed for ampicillin (7%), followed by cephalothin, amoxicillin-clavulanic acid, tetracycline, trimethoprim, and streptomycin, with resistance rates between 4.4 and 3.6%. No resistance to amikacin, ciprofloxacin, gentamicin, or kanamycin was observed. One isolate was resistant to cefotaxime. Among the multiresistant isolates (n ‫؍‬ 37), ampicillin and cephalothin showed the highest resistance rates, at 76 and 52%, respectively. E. coli isolates from lettuce showed higher resistance rates than E. coli isolates obtained from soil or irrigation water samples. When the presence of resistance in E. coli isolates from lettuce production sites and their resistance patterns were compared with the profiles of animal-derived E. coli strains, they were found to be the most comparable with what is found in the cattle reservoir. This may suggest that cattle are a potential reservoir of antimicrobial-resistant E. coli strains in plant primary production.

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“…Previous studies have reported appreciable numbers of antibiotic resistant members on the consumer-ready vegetables, such as lettuce and spinach leaves [17,46,47]. Root endophytes can be recruited from common soil bacteria and survived in the interior of the root [48,49], which allow ARGs transferring from soil into plant.…”

Section: Discussionmentioning

confidence: 99%

“…Phyllosphere, normally referring to the aerial leaf surfaces, is a special niche harboring diverse species of microbes, especially bacteria [52]. Therefore, vegetables grown in manureamended soil, particularly that are eaten raw or only subjected to minimal processing before consumption, could serve as vehicles for expanding the pool of antibiotic resistance available to bacteria (pathogens or otherwise) [47]. Recent outbreaks of infectious disease have prompted increased interest in the microbiologic safety [53].…”

Section: Discussionmentioning

confidence: 99%

Antibiotic resistance genes in manure-amended soil and vegetables at harvest

Wang

Qiao

Chen

et al. 2015

Journal of Hazardous Materials

286

110

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Presence and potential for horizontal transfer of antibiotic resistance in oxidase-positive bacteria populating raw salad vegetables

Cited by 63 publications

References 40 publications

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

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

Moderate Prevalence of Antimicrobial Resistance in Escherichia coli Isolates from Lettuce, Irrigation Water, and Soil

Antibiotic resistance genes in manure-amended soil and vegetables at harvest

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