Antimicrobial resistance in United States retail ground beef with and without label claims regarding antibiotic use

Author(s):  
John W. Schmidt ◽  
Amit Vikram ◽  
Enrique Doster ◽  
Kevin Thomas ◽  
Margaret D Weinroth ◽  
...  

Antibiotics used during food-animal production account for approximately 77% of U.S. antimicrobial consumption by mass. Ground beef products labeled as raised without antibiotics (RWA) are perceived to harbor lower antimicrobial resistance (AMR) levels than conventional (CONV) products with no label claims regarding antimicrobial use. Retail ground beef samples were obtained from 6 U. S. cities. Samples with a RWA or USDA Organic claim ( N = 299) were assigned to the RWA production system. Samples lacking these claims ( N = 300) were assigned to the CONV production system. Each sample was cultured for the detection of five antimicrobial resistant bacteria. Genomic DNA was isolated from each sample and qPCR was used to determine the abundance of ten antimicrobial resistance genes (ARGs). Tetracycline-resistant Escherichia coli (CONV = 46.3%; RWA = 34.4%, P < 0.01) and erythromycin-resistant Enterococcus (CONV = 48.0%; RWA = 37.5%, P = 0.01) were more frequently detected in CONV. Salmonella were detected in 1.2% of samples. The ARG bla CTX-M (CONV = 4.1 log 10 normalized abundance, RWA = 3.8 log 10 normalized abundance, P < 0.01) was more abundant in CONV ground beef. The ARGs mecA (CONV = 4.4 log 10 normalized abundance, RWA = 4.9 log 10 normalized abundance, P = 0.05), tet (A) (CONV = 3.9 log 10 normalized abundance, RWA = 4.5 log 10 normalized abundance, P < 0.01), tet (B) (CONV = 3.9 log 10 normalized abundance, RWA = 4.5 log 10 normalized abundance, P < 0.01), and tet (M) (CONV = 5.4 log 10 normalized abundance, RWA = 5.8 log 10 normalized abundance, P < 0.01) were more abundant in RWA ground beef. Although these results suggest that antimicrobial use during U. S. cattle production does not increase human exposure to AMR via ground beef quantitative microbiological risk assessments are required for authoritative assessments regarding the human health impacts of antimicrobial uses during beef production.

2019 ◽  
Vol 3 (2) ◽  
Author(s):  
J. W. Schmidt ◽  
A. Vikram ◽  
K. Thomas ◽  
T. M. Arthur ◽  
M. Weinroth ◽  
...  

ObjectivesThe occurrences of human bacterial infections complicated by antimicrobial resistance (AMR) have increased in recent decades. Concerns have been raised that food-animal production practices that incorporate antimicrobials contribute significantly to human AMR exposures since food-animal production accounts for approximately 81% of U.S. antimicrobial consumption by mass. Although empirical studies comparing AMR levels in meat products, including ground beef, are scant ground beef products with Raised without Antibiotics (RWA) label claims are perceived to harbor less AMR than “conventional” (CONV) products with no label claims regarding antimicrobial use. The objective of this research was to determine AMR levels in retail ground beef with and without an RWA label claims.Materials and MethodsRetail ground beef samples were obtained from 6 U.S. cities. Samples were obtained on the following dates: 9/18/2017, 10/30/2017, 11/27/2017. 1/29/2018. 3/5/2018, and 6/11/2018. A total of 599 samples were obtained. Samples with a “Raised without Antibiotics” or USDA Organic claim (N = 299) were assigned to the RWA production system. Samples lacking a “Raised without Antibiotics” claim (N = 300) were assigned to the CONV production system. Each sample was cultured for the detection of five antimicrobial resistant bacteria (ARB). Genomic DNA was isolated from each sample and qPCR was used to determine the abundance of ten antimicrobial resistance genes (ARGs). The impacts of production system and city on ARB detection were assessed by the Likelihood-ratio chi-squared test. The impacts of production system and city on ARG abundance was assessed by two-way ANOVA.ResultsTetracycline-resistant Escherichia coli (CONV = 46.3%; RWA = 34.4%) and erythromycin-resistant Enterococcus (CONV = 48.0%; RWA = 37.5%) were more frequently (P < 0.01) detected in CONV. Detection of third generation cephalosporin-resistant E. coli (CONV = 5.7%; RWA = 1.0%), vancomycin-resistant Enterococcus (CONV = 0.0%; RWA = 0.0%) and methicillin-resistant Staphylococcus aureus (CONV = 1.3%; RWA = 0.7%) did not differ (P = 1.00). The blaCTX-M ARG was more abundant in CONV (2.4 vs. 2.1 log copies/gram, P = 0.01) but the tet(A) (2.4 vs. 2.5 log copies/gram, P = 0.02) and tet(M) (3.6 vs. 3.9 log copies/gram, P < 0.01) ARGs were more abundant in RWA. aadA1, blaCMY-2, mecA, erm(B), and tet(B) abundances did not differ significantly (Fig. 5) (P > 0.05). Abundances of aac (6’)-Ie-aph (2”)-Ia and blaKPC-2 were not analyzed since they were quantified in less than 5% of the samples.ConclusionU.S. retail CONV and RWA ground beef harbor generally similar levels of AMR since only 5 of 15 AMR measurements were statistically different between production systems. Three AMR measurements were higher in CONV, while 2 AMR measurements were higher in RWA. These results are in general agreement with a recently published study authored by our group that examined antimicrobial resistance in CONV and RWA ground beef obtained from U.S. foodservice suppliers (Vikram et al., J. Food Prot. 81:2007–2018. 2018.). Together these studies suggest that antimicrobial use during U.S. cattle production has minimal to no impact on human exposure to AMR via ground beef.Figure 5.


2018 ◽  
Vol 81 (12) ◽  
pp. 2007-2018 ◽  
Author(s):  
AMIT VIKRAM ◽  
ERIC MILLER ◽  
TERRANCE M. ARTHUR ◽  
JOSEPH M. BOSILEVAC ◽  
TOMMY L. WHEELER ◽  
...  

ABSTRACTU.S. ground beef with “raised without antibiotics” (RWA) label claims are perceived as harboring fewer bacteria with antimicrobial resistance (AMR) than are found in conventional (CONV) ground beef with no such label claim. A total of 370 ground beef samples from CONV (n = 191) and RWA (n = 179) production systems were collected over 13 months from three food service suppliers. The following bacteria were cultured: Escherichia coli, tetracycline-resistant (TETr) E. coli, third-generation cephalosporin-resistant (3GCr) E. coli, Salmonella enterica, TETr S. enterica, 3GCr S. enterica, nalidixic acid–resistant S. enterica, Enterococcus spp., erythromycin-resistant Enterococcus spp., TETr Enterococcus spp., Staphylococcus aureus, and methicillin-resistant S. aureus. TETr E. coli was more frequently detected in CONV ground beef (CONV, 54.2%; RWA, 35.2%; P &lt; 0.01), but supplier (P &lt; 0.01) and production system × suppler interaction (P &lt; 0.01) effects were also significant. Metagenomic DNA was isolated from each sample, and equal amounts of metagenomic DNA were pooled by supplier, month, and production system for 75 pooled samples (38 CONV, 37 RWA). The abundance of aac(6′)-Ie-aph(2″)-Ia, aadA1, blaCMY-2, blaCTX-M, blaKPC-2, erm(B), mecA, tet(A), tet(B), and tet(M) genes was assessed by quantitative PCR. The tet(A) (2.9-log2-fold change, P = 0.04) and tet(B) (5.6-log2-fold change) (P = 0.03) genes were significantly more abundant in RWA ground beef. Phylogenetic analyses revealed that ground beef microbiomes differed more by supplier than by production system. These results were consistent with prior research suggesting antimicrobial use in U.S. beef cattle has minimal impact on the AMR of bacteria found in these products. These results should spur a reevaluation of assumptions regarding the impact of antimicrobial use during U.S. beef production on the AMR of bacteria in ground beef.


Author(s):  
Dominic Poulin-Laprade ◽  
Jean-Simon Brouard ◽  
Nathalie Gagnon ◽  
Annie Turcotte ◽  
Alexandra Langlois ◽  
...  

Pigs are major reservoirs of resistant Enterobacteriaceae that can reach humans through consumption of contaminated meat or vegetables grown in manure-fertilized soil. Samples were collected from sows during lactation and their piglets at five time points spanning the production cycle. Cefotaxime-resistant bacteria were quantified and isolated from feed, feces, manures and carcasses of pigs reared with penicillin-using or antibiotic-free husbandries. The isolates were characterized by antibiotic susceptibility testing, whole genome sequencing and conjugation assays. The extended spectrum β-lactamase (ESBL) phenotype was more frequent in isolates originating from antibiotic-free animals, while the bacteria isolated from penicillin-using animals were on average resistant to a greater number of antibiotics. The ESBL-encoding genes identified were blaCTX-M-1, blaCTX-M-15 and blaCMY-2 and they co-localised on plasmids with various genes encoding resistance to ß-lactams, co-trimoxazole, phenicols and tetracycline, all antibiotics used in pig production. Groups of genes conferring the observed resistance and the mobile elements disseminating multidrug resistance were determined. The observed resistance to ß-lactams was mainly due to the complementary actions of penicillin-binding proteins, an efflux pump and ß-lactamases. Most resistance determinants were shared by animals raised with or without antimicrobials. This suggests a key contribution of indigenous enterobacteria maternally transmitted along the sow lineage, regardless of antimicrobial use. It is unclear if the antimicrobial resistance observed in the enterobacteria populations of the commercial pig herds studied were present before the use of antibiotics, or the extent to which historical antimicrobial use exerted a selective pressure defining the resistant bacterial populations in farms using penicillin prophylaxis. Importance: Antimicrobial resistance is a global threat that needs to be fought on numerous fronts along the One Health continuum. Vast quantities of antimicrobials are used in agriculture to ensure animal welfare and productivity, and are arguably a driving force for the persistence of environmental and food-borne resistant bacteria. This study evaluated the impact of conventional, organic and other antibiotic-free husbandry practices on the frequency and nature of antimicrobial resistance genes and multidrug resistant enterobacteria. It provides knowledge about the relative contribution of specific resistance determinants to observed antibiotic resistance. It also showed the clear co-selection of genes coding for extended-spectrum beta-lactamases and genes coding for the resistance to antibiotics commonly used for prophylaxis or in curative treatments in pig operations.


2021 ◽  
Author(s):  
Lajos Kalmar ◽  
Srishti Gupta ◽  
Iain R. L. Kean ◽  
Xiaoliang Ba ◽  
Nazreen Hadjirin ◽  
...  

AbstractShotgun metagenomics is a powerful tool to identify antimicrobial resistance (AMR) genes in microbiomes but has the limitation that extrachromosomal DNA, such as plasmids, cannot be linked with the host bacterial chromosome. Here we present a laboratory and bioinformatics pipeline HAM-ART (Hi-C Assisted Metagenomics for Antimicrobial Resistance Tracking) optimised for the generation of metagenome-assembled genomes including both chromosomal and extrachromosomal AMR genes. We demonstrate the performance of the pipeline in a study comparing 100 pig faecal microbiomes from low- and high-antimicrobial use pig farms (organic and conventional farms). We found significant differences in the distribution of AMR genes between low- and high-antimicrobial use farms including a plasmid-borne lincosamide resistance gene exclusive to high-antimicrobial use farms in three species of Lactobacilli.Author SummaryAntimicrobial resistance (AMR) is one of the biggest global health threats humanity is facing. Understanding the emergence and spread of AMR between different bacterial species is crucial for the development of effective countermeasures. In this paper we describe a user-friendly, affordable and comprehensive (laboratory and bioinformatics) workflow that is able to identify, associate and track AMR genes in bacteria. We demonstrate the efficiency and reliability of the method by comparing 50 faecal microbiomes from pig farms with high-antibiotic use (conventional farms), and 50 faecal microbiomes from pig farms with low-antibiotic use (organic farms). Our method provides a novel approach to resistance gene tracking, that also leads to the generation of high quality metagenomic assembled genomes that includes genes on mobile genetic elements, such as plasmids, that would not otherwise be included in these assembled genomes.


Microbiome ◽  
2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Oscar Mencía-Ares ◽  
Raúl Cabrera-Rubio ◽  
José Francisco Cobo-Díaz ◽  
Avelino Álvarez-Ordóñez ◽  
Manuel Gómez-García ◽  
...  

Abstract Background The global threat of antimicrobial resistance (AMR) is a One Health problem impacted by antimicrobial use (AMU) for human and livestock applications. Extensive Iberian swine production is based on a more sustainable and eco-friendly management system, providing an excellent opportunity to evaluate how sustained differences in AMU impact the resistome, not only in the animals but also on the farm environment. Here, we evaluate the resistome footprint of an extensive pig farming system, maintained for decades, as compared to that of industrialized intensive pig farming by analyzing 105 fecal, environmental and slurry metagenomes from 38 farms. Results Our results evidence a significantly higher abundance of antimicrobial resistance genes (ARGs) on intensive farms and a link between AMU and AMR to certain antimicrobial classes. We observed differences in the resistome across sample types, with a higher richness and dispersion of ARGs within environmental samples than on those from feces or slurry. Indeed, a deeper analysis revealed that differences among the three sample types were defined by taxa-ARGs associations. Interestingly, mobilome analyses revealed that the observed AMR differences between intensive and extensive farms could be linked to differences in the abundance of mobile genetic elements (MGEs). Thus, while there were no differences in the abundance of chromosomal-associated ARGs between intensive and extensive herds, a significantly higher abundance of integrons in the environment and plasmids, regardless of the sample type, was detected on intensive farms. Conclusions Overall, this study shows how AMU, production system, and sample type influence, mainly through MGEs, the profile and dispersion of ARGs in pig production.


mSystems ◽  
2021 ◽  
Vol 6 (4) ◽  
Author(s):  
Adelumola Oladeinde ◽  
Zaid Abdo ◽  
Maximilian O. Press ◽  
Kimberly Cook ◽  
Nelson A. Cox ◽  
...  

The reported increase in antibiotic-resistant bacteria in humans has resulted in a major shift away from antibiotic use in food animal production. This shift has been driven by the assumption that removing antibiotics will select for antibiotic susceptible bacterial taxa, which in turn will allow the currently available antibiotic arsenal to be more effective.


2021 ◽  
Vol 104 (4) ◽  
pp. 003685042110502
Author(s):  
Fernanda Loayza-Villa ◽  
Alejandro Torres ◽  
Lixin Zhang ◽  
Gabriel Trueba

The use of antimicrobials in the food animal industry has caused an increased prevalence of antimicrobial-resistant bacteria and antimicrobial resistance genes, which can be transferred to the microbiota of humans through the food chain or the environment. To reduce the development and spread of antimicrobial resistance, restrictions on antimicrobial use in food animals have been implemented in different countries. We investigated the impact of an antimicrobial restriction intervention during two generations of pigs. Fecal samples were collected in five growth phases. The frequency of antimicrobial-resistant coliforms and antimicrobial-resistant bacteria or antimicrobial resistance genes was analyzed. No differences in the richness or abundance of antimicrobial-resistant coliforms or antimicrobial resistance genes were found when animals fed with or without prophylactic antimicrobials were compared. Withholding antimicrobial supplementation did not negatively affect weight gain in pigs. Withdrawal of prophylactic antimicrobial consumption during two generations of pigs was not enough to reduce the prevalence of antimicrobial resistance genes, as measured by richness and abundance markers. This study indicates that the fitness costs associated with bacterial carriage of some antimicrobial resistance genes are low.


Author(s):  
Dana Trevas ◽  
Angela M Caliendo ◽  
Kimberly Hanson ◽  
Jaclyn Levy ◽  
Christine C Ginocchio

Abstract Uptake of existing diagnostics to identify infections more accurately could minimize unnecessary antibiotic use and decrease the growing threat of antibiotic resistance. The Infectious Diseases Society of America (IDSA) and the Presidential Advisory Council on Combating Antibiotic-Resistant Bacteria (PACCARB) agree that, to improve uptake of existing diagnostics, healthcare providers, health systems, and payors all need better clinical and economic outcomes data to support use of diagnostic tests over empiric use of antibiotics, providers need better tools and education about diagnostic tests, and diagnostics developers need federal funding in the absence of a viable diagnostics market. Recommendations from PACCARB and the IDSA are amplified. Incentives for—and challenges to—diagnostics research, development, and uptake are summarized. Advocacy opportunities are given for infectious disease professionals to join the fight against antimicrobial resistance.


2013 ◽  
Vol 4 (4) ◽  
pp. 5 ◽  
Author(s):  
Usman Hadi ◽  
Kuntaman Kuntaman ◽  
Mariyatul Qiptiyah ◽  
Hari Paraton

Background: Based on the results Antimicrobial Resistance in Indonesia: prevalence and prevention-study (AMRIN-study), the Ministry of Health of Indonesia in 2005 began a program antibiotic resistance control (PPRA) in some government hospitals, and is currently developing to all government teaching hospitals in Indonesia. Aim: The core activities of the PPRA are to implement standardized surveillance emergence of antibiotic resistant bacteria, and the surveillance of antibiotic use in terms of quantity and quality. Method: Our research in the years 2003 showed the proportion of antibiotic use 84% of patients in a hospital. The use of inappropriate antibiotics was very high, 42% no indication. Result: In 2012 the results of surveillance showed decline of inappropriate use of antibiotic, but prevalence extended-spectrum b-lactamase (ESBL)-producing K.pneumoniae (58%), and E.coli (52%) andmethicillin-resistant S.aures (MRSA) (24%) were increasing. Conclusion: It was needed to implement the most appropriate programs to prevent the growth and development of bacteria resistant to antibiotics.


2021 ◽  
Author(s):  
Wenjuan Cong ◽  
Ak Narayan Poudel ◽  
Nour Alhusein ◽  
Hexing Wang ◽  
Guiqing Yao ◽  
...  

AbstractBackgroundAs the numbers of people with COVID-19 continue to increase globally, concerns have been raised regarding the widespread use of antibiotics for the treatment of COVID-19 patients and its consequences for antimicrobial resistance during the pandemic and beyond. The scale and determinants of antibiotic use in the early phase of the pandemic, and whether antibiotic prescribing is beneficial to treatment effectiveness in COVID-19 patients, are still unknown. Unwarranted treatment of this viral infection with antibiotics may exacerbate the problem of antibiotic resistance, while antibiotic resistance may render presumptive treatment of secondary infections in COVID-19 patients ineffective.MethodsThis rapid review was undertaken to identify studies reporting antimicrobial use in the treatment of hospitalised COVID-19 patients. The review was conducted to comply with PRISMA guidelines for Scoping Reviews (http://www.prisma-statement.org/Extensions/ScopingReviews) and the protocol was registered with the Open Science Framework (OSF): http://osf.io/vp6t5. The following databases: Web of Science, EMBASE, PubMed, CNKI & VIP were searched to identify the relevant studies from 1 Dec 2019 up to 15 June 2020; no limits were set on the language or the country where studies were conducted. The search terms used were: ((“Covid-19” or “SARS-CoV-2” or “Coronavirus disease 2019” or “severe acute respiratory syndrome coronavirus-2”) and ((“antibiotic prescribing” or “antibiotic use” or “antibiotic*”) or “antimicrobial *” or “antimicrobial therapy” or “antimicrobial resistance” or “antimicrobial stewardship”)). A total of 1216 records were identified through database searching and 118 clinical studies met the inclusion criteria and were taken into data extraction. A bespoke data extraction form was developed and validated through two independent, duplicate extraction of data from five Records. As all the included studies were descriptive in nature, we conducted descriptive synthesis of data and reported pooled estimates such as mean, percentage and frequency. We created a series of scenarios to capture the range of rationales for antibiotic prescribing presented in the included studies.ResultsOur results show that during the early phase of the pandemic, 8501 out of 10 329 COVID-19 patients (82·3%) were prescribed antibiotics; antibiotics were prescribed for COVID-19 patients regardless of reported severity, with a similar mean antibiotic prescribing rate between patients with severe or critical illness (75·4%) and patients with mild or moderate illness (75·1%). The top five frequently prescribed antibiotics for hospitalised COVID-19 patients were azithromycin (28·0 % of studies), ceftriaxone (17·8%), moxifloxacin (14·4%), meropenem (14·4%) and piperacillin/tazobactam (12·7%). The proportion of patients prescribed antibiotics without clinical justification was 51·5% vs 41·9 % for patients with mild or moderate illness and those with severe or critical illness respectively. Comparison of patients who were provided antibiotics with a clinical justification with those who were given antibiotics without clinical justification showed lower mortality rates (9·5% vs 13·1%), higher discharge rates (80·9% vs 69·3%) and shorter length of hospital of stay (9·3 days vs 12·2 days). Only 9·7% of patients in our included studies were reported to have secondary infections.ConclusionsAntibiotics were prescribed indiscriminately for hospitalised COVID-19 patients regardless of severity of illness during the early phase of the pandemic. COVID-19 related concerns and lack of knowledge drove a large proportion of antibiotic use without specific clinical justification. Although we are still in the midst of the pandemic, the goals of antimicrobial stewardship should remain unchanged for the treatment of COVID-19 patients.


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