Antimicrobial Resistance in Poultry Production

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Poultry".

Deadline for manuscript submissions: closed (15 July 2020) | Viewed by 42506

Special Issue Editors


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Guest Editor
Department of Comparative Biomedicine and Food Science, University of Padua, Legnaro, 35020 Padua, PD, Italy
Interests: molecular microbiology; food-borne zoonoses; antimicrobial use; antimicrobial resistance; microbiome; resistome
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Guest Editor
Department of Comparative Biomedicine and Food Science, University of Padua, Viale dell’Università 16, 35020 Legnaro (PD), Italy

Special Issue Information

Dear Colleagues,

In recent years, antimicrobial resistance has become a serious concern both for animal and human health. The emergence of resistant pathogens in poultry may pose serious economic and health problems because of a decreased responsiveness of diseased birds to antimicrobial therapy. In addition, the emergence of resistance in poultry is a public health risk due to the potential transfer of resistant bacteria or genetic determinants to humans. Indeed, poultry is considered an important reservoir and source of resistant zoonotic and commensal bacteria for humans due to the large use of antimicrobials to prevent and treat diseases. Improving our knowledge on antimicrobial use and resistance epidemiology in the poultry industry is fundamental to the development of intervention measures aimed at preserving the efficacy of antimicrobial agents in poultry and at controlling human exposure to resistance determinants through the food chain.

In this Special Issue, we welcome original research papers and reviews dealing with the current issues related to antimicrobial use and resistance in the poultry industry. Since it is still uncertain whether there is a relationship between antimicrobial use in poultry, the emergence and spread of resistant bacteria along the food chain, and resistant infections in humans, studies providing insights using a quantitative and/or high-throughput approach will be highly appreciated. Additional data and research studies are strongly needed to better understand this challenging issue for poultry and public health.

Dr. Alessandra Piccirillo
Dr. Ilias Apostolakos
Guest Editors

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Published Papers (7 papers)

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Research

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17 pages, 1253 KiB  
Article
Antibiotic Resistance of Escherichia coli Isolated from Conventional, No Antibiotics, and Humane Family Owned Retail Broiler Chicken Meat
by Helen M. Sanchez, Victoria A. Whitener, Vanessa Thulsiraj, Alicia Amundson, Carolyn Collins, Mckenzie Duran-Gonzalez, Edwin Giragossian, Allison Hornstra, Sarah Kamel, Andrea Maben, Amelia Reynolds, Elizabeth Roswell, Benjamin Schmidt, Lauren Sevigny, Cindy Xiong and Jennifer A. Jay
Animals 2020, 10(12), 2217; https://doi.org/10.3390/ani10122217 - 26 Nov 2020
Cited by 8 | Viewed by 2966
Abstract
The use of antibiotics for therapeutic and especially non-therapeutic purposes in livestock farms promotes the development of antibiotic resistance in previously susceptible bacteria through selective pressure. In this work, we examined E. coli isolates using the standard Kirby-Bauer disk diffusion susceptibility protocol and [...] Read more.
The use of antibiotics for therapeutic and especially non-therapeutic purposes in livestock farms promotes the development of antibiotic resistance in previously susceptible bacteria through selective pressure. In this work, we examined E. coli isolates using the standard Kirby-Bauer disk diffusion susceptibility protocol and the CLSI standards. Companies selling retail chicken products in Los Angeles, California were grouped into three production groupings—Conventional, No Antibiotics, and Humane Family Owned. Humane Family Owned is not a federally regulated category in the United States, but shows the reader that the chicken is incubated, hatched, raised, slaughtered, and packaged by one party, ensuring that the use of antibiotics in the entire production of the chicken is known and understood. We then examined the antibiotic resistance of the E. coli isolates (n = 325) by exposing them to seven common antibiotics, and resistance was seen to two of the antibiotics, ampicillin and erythromycin. As has been shown previously, it was found that for both ampicillin and erythromycin, there was no significant difference (p > 0.05) between Conventional and USDA (United States Department of Agriculture)-certified No Antibiotics chicken. Unique to this work, we additionally found that Humane Family Owned chicken had fewer (p ≤ 0.05) antibiotic-resistant E. coli isolates than both of the previous. Although not considered directly clinically relevant, we chose to test erythromycin because of its ecological significance to the environmental antibiotic resistome, which is not generally done. To our knowledge, Humane Family Owned consumer chicken has not previously been studied for its antibiotic resistance. This work contributes to a better understanding of a potential strategy of chicken production for the overall benefit of human health, giving evidentiary support to the One Health approach implemented by the World Health Organization. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Poultry Production)
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11 pages, 2092 KiB  
Article
Occurrence and Molecular Characteristics of Mcr-1-Positive Escherichia coli from Healthy Meat Ducks in Shandong Province of China
by Fengzhi Liu, Ruihua Zhang, Yupeng Yang, Hanqing Li, Jingyu Wang, Jingjing Lan, Pengfei Li, Yanli Zhu, Zhijing Xie and Shijin Jiang
Animals 2020, 10(8), 1299; https://doi.org/10.3390/ani10081299 - 29 Jul 2020
Cited by 12 | Viewed by 2378
Abstract
Colistin has been used as a growth promotant in livestock feed for many years. In China, mcr-1-positive Escherichia coli strains have been isolated from humans, chickens, and pigs. To date, there are few reports about the prevalence and molecular characteristics of fecal [...] Read more.
Colistin has been used as a growth promotant in livestock feed for many years. In China, mcr-1-positive Escherichia coli strains have been isolated from humans, chickens, and pigs. To date, there are few reports about the prevalence and molecular characteristics of fecal E. coli bearing mcr-1 in the meat ducks. In this study, the prevalence of mcr-1 gene was investigated among 120 fecal E. coli strains isolated from healthy meat ducks in Shandong province of China between October 2017 and February 2018. A total of nine mcr-1-containing E. coli strains were identified and two were identified as extra-intestinal pathogenic E. coli (ExPEC) among them. The clonal relationship of the nine E. coli strains was determined by multilocus sequencing typing (MLST) and pulsed field gel electrophoresis (PFGE), and the results indicated that all mcr-1-carrying isolates were clonally unrelated. Two different genetic contexts of mcr-1 were identified among these isolates. Colistin-resistant phenotype of all the isolates was successfully transferred to the recipient strains by conjugation experiments and seven transconjugants carried a single plasmid. The mcr-1 was located on three replicon plasmids: IncI2 (n = 4), IncFII (n = 2) and IncN (n = 1). Complete sequence analysis of a representative plasmid pTA9 revealed that it was strikingly similar with plasmid pMCR1-IncI2 of E. coli, plasmid pHNSHP45 of E. coli, and plasmid pWF-5-19C of Cronobacter sakazakii, implying that pTA9-like plasmids may be epidemic plasmids that mediate the spread of mcr-1 among Enterobacteriaceae. These results highlight that healthy meat duck is a potential reservoir for multidrug resistant mcr-1-containing E. coli strains. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Poultry Production)
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12 pages, 429 KiB  
Article
Antimicrobial Susceptibility of Escherichia coli and ESBL-Producing Escherichia coli Diffusion in Conventional, Organic and Antibiotic-Free Meat Chickens at Slaughter
by Laura Musa, Patrizia Casagrande Proietti, Raffaella Branciari, Laura Menchetti, Sara Bellucci, David Ranucci, Maria Luisa Marenzoni and Maria Pia Franciosini
Animals 2020, 10(7), 1215; https://doi.org/10.3390/ani10071215 - 17 Jul 2020
Cited by 26 | Viewed by 4076
Abstract
As a result of public health concerns regarding antimicrobial resistance in animal-based food products, conventional poultry companies have turned to ‘raised without antibiotics’ (ABF) and organic farming systems. In this work, we evaluated the influence of rearing systems on antimicrobial susceptibility in E. [...] Read more.
As a result of public health concerns regarding antimicrobial resistance in animal-based food products, conventional poultry companies have turned to ‘raised without antibiotics’ (ABF) and organic farming systems. In this work, we evaluated the influence of rearing systems on antimicrobial susceptibility in E. coli and extended-spectrum β-lactamase (ESLB) E. coli diffusion in conventional (C), organic (O) and antibiotic free (ABF) chicken samples collected from cloacal swabs and skin samples in slaughterhouse. The E. coli isolates from conventional (135), antibiotic-free (131) and organic (140) samples were submitted to the Kirby–Bauer method and ESBL E. coli were analyzed by the microdilution test. Conventional samples showed the highest number of strains resistant to ampicillin (89.6%; p < 0.01), cefotaxime (43.7%; p < 0.01), nalidixic acid (57.8%; p < 0.01), ciprofloxacin (44.4%; p < 0.001), and trimethoprim/sulfamethoxazole (62.2%; p < 0.01), with patterns of multi-resistance to three (35.1%) and to four antimicrobials (31.3%), whereas most of the E. coli isolated from antibiotic-free and organic chicken samples revealed a co-resistance pattern (29.2% and 39%, respectively). The highest number of ESBL E. coli was observed in conventional, in both cloacal and skin samples and the lowest in organic (p < 0.001). Our results are consistent with the effect of conventional farming practices on E. coli antimicrobial resistance and ESBL E. coli number, due to the use of antimicrobials and close contact with litter for most of the production cycle. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Poultry Production)
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15 pages, 878 KiB  
Article
Phenotypic and Genotypic Characterization of Virulence Factors and Susceptibility to Antibiotics in Salmonella Infantis Strains Isolated from Chicken Meat: First Findings in Chile
by Lisette Lapierre, Javiera Cornejo, Sebastián Zavala, Nicolás Galarce, Fernando Sánchez, María Belén Benavides, Miguel Guzmán and Leonardo Sáenz
Animals 2020, 10(6), 1049; https://doi.org/10.3390/ani10061049 - 18 Jun 2020
Cited by 39 | Viewed by 4668
Abstract
Salmonella Infantis is a zoonotic pathogen that causes gastroenteritis in humans and animals, with poultry being its main reservoir. In Chile, there are no data to characterize S. Infantis strains in poultry production. In this study, 87 S. Infantis strains were isolated from [...] Read more.
Salmonella Infantis is a zoonotic pathogen that causes gastroenteritis in humans and animals, with poultry being its main reservoir. In Chile, there are no data to characterize S. Infantis strains in poultry production. In this study, 87 S. Infantis strains were isolated from chicken meat for sale in supermarkets in Santiago, Chile, and characterized according to their virulence genes, biofilm formation abilities, antibiotic susceptibility, and resistance genes. Through polymerase chain reaction or PCR, the strains were analyzed to detect the presence of 11 virulence genes, 12 antibiotic resistance genes, and integrase genes. Moreover, disc diffusion susceptibility to 18 antimicrobials and the ability to form biofilm in vitro were evaluated. Results demonstrated six different virulence gene profiles. Ninety-four percent of the strains were multi-resistant to antibiotics with weak biofilm formation abilities, 63.2% of the strains were broad spectrum β- lactam resistant, and the bla CTX-M-65 gene was amplified in 13 strains. Only 3.4% of the strains were fluoroquinolone resistant, and the qnrB gene was amplified in two strains. Colistin resistance was exhibited in 28.7% of the strains, but mrc genes were not amplified in any strain under study. The isolated S. Infantis strains are pathogenic and antibiotic multi-resistant, and thus, this Salmonella serotype should be under surveillance in the poultry food production chain with the aim of protecting public health. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Poultry Production)
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15 pages, 940 KiB  
Article
Antimicrobial Resistance and Virulence Properties of Campylobacter Spp. Originating from Domestic Geese in Poland
by Beata Wysok, Joanna Wojtacka, Agnieszka Wiszniewska-Łaszczych and Joanna Szteyn
Animals 2020, 10(4), 742; https://doi.org/10.3390/ani10040742 - 24 Apr 2020
Cited by 16 | Viewed by 2599
Abstract
A total of 240 samples were evaluated for the presence of Campylobacter spp. Campylobacter was found in 83.3% of the cecum contents samples and 52.5% of the neck skin samples from carcasses. The prevailing species was C. jejuni, accounting for 87.7% of [...] Read more.
A total of 240 samples were evaluated for the presence of Campylobacter spp. Campylobacter was found in 83.3% of the cecum contents samples and 52.5% of the neck skin samples from carcasses. The prevailing species was C. jejuni, accounting for 87.7% of all Campylobacter isolates, and the remaining 12.3% of isolates were C. coli. All Campylobacter isolates, independent of the sample origin and species, were positive for 6 out of 15 tested genes (flaA, flhA, cadF, racR, ciaB, and cdtA genes). The prevalence of dnaJ, docA, pldA, cdtB, cdtC, and iam genes was also very common (ranging from 86.5% to 98.8%). The lowest prevalence was noted for virB11 and wlaN genes, both in Campylobacter isolates from cecum (12% and 19%) and carcasses (11.1% and 17.5%). None of the isolates tested, regardless of the sample origin, carried the cgtB gene. The highest resistance rates were observed for quinolones (90.8%) and tetracyclines (79.8%). Simultaneously, only single Campylobacter isolate was resistant to macrolides (0.6%) and none of the isolates showed resistance to aminoglycosides and amphenicols. The common presence of Campylobacter on geese carcasses as well as the detection of multidrug-resistant isolates indicate that consuming goose meat might cause a potential risk, therefore leading to human campylobacteriosis. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Poultry Production)
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Review

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17 pages, 579 KiB  
Review
Overview of Quantitative Methodologies to Understand Antimicrobial Resistance via Minimum Inhibitory Concentration
by Alec Michael, Todd Kelman and Maurice Pitesky
Animals 2020, 10(8), 1405; https://doi.org/10.3390/ani10081405 - 12 Aug 2020
Cited by 22 | Viewed by 4031
Abstract
The development of antimicrobial resistance (AMR) represents a significant threat to humans and food animals. The use of antimicrobials in human and veterinary medicine may select for resistant bacteria, resulting in increased levels of AMR in these populations. As the threat presented by [...] Read more.
The development of antimicrobial resistance (AMR) represents a significant threat to humans and food animals. The use of antimicrobials in human and veterinary medicine may select for resistant bacteria, resulting in increased levels of AMR in these populations. As the threat presented by AMR increases, it becomes critically important to find methods for effectively interpreting minimum inhibitory concentration (MIC) tests. Currently, a wide array of techniques for analyzing these data can be found in the literature, but few guidelines for choosing among them exist. Here, we examine several quantitative techniques for analyzing the results of MIC tests and discuss and summarize various ways to model MIC data. The goal of this review is to propose important considerations for appropriate model selection given the purpose and context of the study. Approaches reviewed include mixture models, logistic regression, cumulative logistic regression, and accelerated failure time–frailty models. Important considerations in model selection include the objective of the study (e.g., modeling MIC creep vs. clinical resistance), degree of censoring in the data (e.g., heavily left/right censored vs. primarily interval censored), and consistency of testing parameters (e.g., same range of concentrations tested for a given antibiotic). Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Poultry Production)
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39 pages, 2386 KiB  
Review
A Review of Antimicrobial Resistance in Poultry Farming within Low-Resource Settings
by Hayden D. Hedman, Karla A. Vasco and Lixin Zhang
Animals 2020, 10(8), 1264; https://doi.org/10.3390/ani10081264 - 24 Jul 2020
Cited by 107 | Viewed by 20320
Abstract
The emergence, spread, and persistence of antimicrobial resistance (AMR) remain a pressing global health issue. Animal husbandry, in particular poultry, makes up a substantial portion of the global antimicrobial use. Despite the growing body of research evaluating the AMR within industrial farming systems, [...] Read more.
The emergence, spread, and persistence of antimicrobial resistance (AMR) remain a pressing global health issue. Animal husbandry, in particular poultry, makes up a substantial portion of the global antimicrobial use. Despite the growing body of research evaluating the AMR within industrial farming systems, there is a gap in understanding the emergence of bacterial resistance originating from poultry within resource-limited environments. As countries continue to transition from low- to middle income countries (LMICs), there will be an increased demand for quality sources of animal protein. Further promotion of intensive poultry farming could address issues of food security, but it may also increase risks of AMR exposure to poultry, other domestic animals, wildlife, and human populations. Given that intensively raised poultry can function as animal reservoirs for AMR, surveillance is needed to evaluate the impacts on humans, other animals, and the environment. Here, we provide a comprehensive review of poultry production within low-resource settings in order to inform future small-scale poultry farming development. Future research is needed in order to understand the full extent of the epidemiology and ecology of AMR in poultry within low-resource settings. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Poultry Production)
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