Antimicrobial resistance of Enterococcus faecium strains isolated from commercial probiotic products used in cattle and swine1,2

Amachawadi, Raghavendra G.; Giok, Felicia; Shi, Xiaorong; Soto, J.; Narayanan, Sanjeev; Tokach, Mike D; Apley, Mike; Nagaraja, T. G.

doi:10.1093/jas/sky056

Cited by 21 publications

(16 citation statements)

References 39 publications

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“…Besides contamination at the processing facility, additional explanations for the observed close relationships between isolates include the possibility that chickens were purchased from common chicken vendors that distribute fertilized eggs, which in turn originate from common breeding flocks that are often treated with antibiotics (42). The use of commercial probiotics in chicken rearing may also have a role, particularly since it has been noted that E. faecium strains used as probiotics for agriculture can contain antimicrobial resistance (AMR) genes (43). Finally, we do not know the locations where the chickens were farmed, and it is possible that additional links exist between the geographies of the source farms.…”

Section: Discussionmentioning

confidence: 99%

Chicken Meat-Associated Enterococci: Influence of Agricultural Antibiotic Use and Connection to the Clinic

McGuire

Tyne

Straub

et al. 2019

Appl Environ Microbiol

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Industrial farms are unique, human-created ecosystems that provide the perfect setting for the development and dissemination of antibiotic resistance. Agricultural antibiotic use amplifies naturally occurring resistance mechanisms from soil ecologies, promoting their spread and sharing with other bacteria, including those poised to become endemic within hospital environments. To better understand the role of enterococci in the movement of antibiotic resistance from farm to table to clinic, we characterized over 300 isolates of Enterococcus cultured from raw chicken meat purchased at U.S. supermarkets by the Consumers Union in 2013. Enterococcus faecalis and Enterococcus faecium were the predominant species found, and antimicrobial susceptibility testing uncovered striking levels of resistance to medically important antibiotic classes, particularly from classes approved by the FDA for use in animal production. While nearly all isolates were resistant to at least one drug, bacteria from meat labeled as raised without antibiotics had fewer resistances, particularly for E. faecium. Whole-genome sequencing of 92 isolates revealed that both commensal- and clinical-isolate-like enterococcal strains were associated with chicken meat, including isolates bearing important resistance-conferring elements and virulence factors. The ability of enterococci to persist in the food system positions them as vehicles to move resistance genes from the industrial farm ecosystem into more human-proximal ecologies. IMPORTANCE Bacteria that contaminate food can serve as a conduit for moving drug resistance genes from farm to table to clinic. Our results show that chicken meat-associated isolates of Enterococcus are often multidrug resistant, closely related to pathogenic lineages, and harbor worrisome virulence factors. These drug-resistant agricultural isolates could thus represent important stepping stones in the evolution of enterococci into drug-resistant human pathogens. Although significant efforts have been made over the past few years to reduce the agricultural use of antibiotics, continued assessment of agricultural practices, including the roles of processing plants, shared breeding flocks, and probiotics as sources for resistance spread, is needed in order to slow the evolution of antibiotic resistance. Because antibiotic resistance is a global problem, global policies are needed to address this threat. Additional measures must be taken to mitigate the development and spread of antibiotic resistance elements from farms to clinics throughout the world.

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Section: Discussionmentioning

confidence: 99%

Chicken Meat-Associated Enterococci: Influence of Agricultural Antibiotic Use and Connection to the Clinic

McGuire

Tyne

Straub

et al. 2019

Appl Environ Microbiol

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“…The bacteria liquid was evenly coated onto the surface of un-supplemented Mueller-Hinton (Oxoid, UK) agar plates using cotton swab. Each plate was pasted with five different antimicrobial disks (Beijing Tiantan, China), and then incubated at 37 °C for 24 h. The diameter of inhibition zones was measured to the nearest millimeter and interpreted according to the CLSI standards and previous studies [22, 23]. The E. faecalis reference strain ATCC 29212 was used as the quality control.…”

Section: Methodsmentioning

confidence: 99%

Horizontal transfer of vanA between probiotic Enterococcus faecium and Enterococcus faecalis in fermented soybean meal and in digestive tract of growing pigs

Liu

et al. 2019

J Animal Sci Biotechnol

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Background The aim of this study was to investigate the intergeneric transfer of vancomycin resistance gene vanA between probiotic enterococci in the fermentation progress of soybean meal and in the digestive tract of growing pigs. One vanA genotype vancomycin resistant E. faecium strain, E fm 4, and one chloramphenicol-resistant E. faecalis strain, E fs 2, were isolated from twenty-nine probiotic basis feed material / additive samples. For in vitro conjugation, E fm 4 and E fs 2 were used as starter to ferment soybean meal. For in vivo conjugation, thirty growing pigs were randomly assigned to five groups ( n = 6), treated with a basic diet, or supplemented with 10% fermented soybean meal, 1% E fm 4, 5% E fs 2 or a combination of 1% E fm 4 + 5% E fs 2 for 7 d, respectively. Fecal samples of pigs in each group were collected daily for the isolation and dynamic analysis of E fm 4, E fs 2 and transconjugants. The sequence types (STs) of E fm 4, E fs 2 and transconjugants were analyzed by multilocus sequence typing (MLST). The vanA harboring plasmid in E fm 4 and transconjugants was analyzed by S1-pulsed field gel electrophoresis (PFGE) and further verified by multiple alignments. Results The results showed that, in FSBM, transconjugants were detected 1 h after the fermentation, with a conjugation frequency of ~ 10 − 3 transconjugants / recipient. Transconjugants proliferated with E fm 4 and E fs 2 in the first 8 h and maintained steadily for 10 d till the end of the experiment. Additionally, in vivo experiment showed that transcojugants were recovered in one of six pigs in both FSBM and E fm 4 + E fs 2 groups, with conjugation frequency of ~ 10 − 5 and ~ 10 − 4 , respectively. MLST revealed the ST of E fm 4, E fs 2 and transconjugants was ST1014, ST69 and ST69, respectively. S1-PFGE confirmed the existence of the vanA -harboring, 142,988-bp plasmid, which was also a multi-drug resistant plasmid containing Tn1546 -like transposon. Conclusions The findings revealed the potential safety hazard existing in the commercial probiotic enterococci in China, because the horiz...

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“…In addition, a probiotic‐containing Bacillus licheniformis and Bacillus subtilis spores could improve productive performance and carcass quality in pigs 15 . However, probiotic microorganisms such as Enterococcus faecium and B. subtilis might serve as a reservoir for antimicrobial resistance (AMR) determinants 16 , 17 . Subtherapeutic antibiotics have been widely used to improve growth performance and food efficiency of weaned piglets.…”

Section: Introductionmentioning

confidence: 99%

Dynamics of the fecal microbiome and antimicrobial resistome in commercial piglets during the weaning period

Suriyaphol

Chiu

Yimpring

et al. 2021

Sci Rep

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This study aimed to characterize the alteration of the fecal microbiome and antimicrobial resistance (AMR) determinants in 24 piglets at day 3 pre-weaning (D. − 3), weaning day (D.0), days 3 (D.3) and 8 post-weaning (D.8), using whole-genome shotgun sequencing. Distinct clusters of microbiomes and AMR determinants were observed at D.8 when Prevotella (20.9%) was the major genus, whereas at D. − 3–D.3, Alistipes (6.9–12.7%) and Bacteroides (5.2–8.5%) were the major genera. Lactobacillus and Escherichia were notably observed at D. − 3 (1.2%) and D. − 3–D.3 (0.2–0.4%), respectively. For AMR, a distinct cluster of AMR determinants was observed at D.8, mainly conferring resistance to macrolide–lincosamide–streptogramin (mefA), β-lactam (cfxA6 and aci1) and phenicol (rlmN). In contrast, at D. − 3–D.3, a high abundance of determinants with aminoglycoside (AMG) (sat, aac(6')-aph(2''), aadA and acrF), β-lactam (fus-1, cepA and mrdA), multidrug resistance (MDR) (gadW, mdtE, emrA, evgS, tolC and mdtB), phenicol (catB4 and cmlA4), and sulfonamide patterns (sul3) was observed. Canonical correlation analysis (CCA) plot associated Escherichia coli with aac(6')-aph(2''), emrA, mdtB, catB4 and cmlA4 at D. − 3, D.0 and/or D.3 whereas at D.8 associations between Prevotella and mefA, cfxA6 and aci1 were identified. The weaning age and diet factor played an important role in the microbial community composition.

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Antimicrobial resistance of Enterococcus faecium strains isolated from commercial probiotic products used in cattle and swine1,2

Cited by 21 publications

References 39 publications

Chicken Meat-Associated Enterococci: Influence of Agricultural Antibiotic Use and Connection to the Clinic

Chicken Meat-Associated Enterococci: Influence of Agricultural Antibiotic Use and Connection to the Clinic

Horizontal transfer of vanA between probiotic Enterococcus faecium and Enterococcus faecalis in fermented soybean meal and in digestive tract of growing pigs

Dynamics of the fecal microbiome and antimicrobial resistome in commercial piglets during the weaning period

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