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Spatial Epidemiology and Surveillance of Foodborne Pathogens

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A special issue of Pathogens (ISSN 2076-0817).

Deadline for manuscript submissions: closed (31 October 2021) | Viewed by 27507

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Special Issue Editor

Dr. Csaba Varga

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Guest Editor

Department of Pathobiology, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL 61802, USA
Interests: foodborne diseases; antimicrobial resistance; spatial epidemiology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Foodborne pathogens pose a substantial health burden to human populations worldwide. Despite consistent efforts of public health stakeholders in reducing the health burden of major foodborne pathogens, such as Salmonella spp., Campylobacter spp., E. coli (STEC), and Listeria monocytogenes, substantial work remains to better understand their incidence, risk factors, and spatial and temporal distribution. Since humans and animals share the same ecosystem, there is a need for a One Health approach to evaluate cases’ exposure sources at the human–animal–environment interface.

With the increase in GIS capabilities and disease mapping along with the emergence of novel spatial statistical methods, the time arrived to use these approaches to assess geographical differences in cases’ demographic, environmental, genetic, behavioral, and socioeconomic determinants. The main goal of this Special Issue is to describe and promote the use of spatial analytical techniques in analyzing foodborne disease surveillance and research data to aid public health stakeholders in creating effective disease prevention and control programs. Besides, we aim to attract research articles that showcase how integrating reportable foodborne disease surveillance data with auxiliary socioeconomic, environmental, agricultural, and climate data can be used in identifying area- and individual-level risk factors for foodborne diseases.

In this Special Issue, we aim to provide a platform for public health and animal health researchers to showcase their research on spatial epidemiology and surveillance of major foodborne pathogens in humans and animals, and we are encouraging you to send original research articles, communications, short notes, or review articles.

Potential topics include but are not limited to:

Spatial, temporal, and space-time clustering of foodborne diseases.
Integrating reportable foodborne disease surveillance data with auxiliary socioeconomic, environmental, agricultural, and climate data to identify novel risk factors.
Foodborne disease outbreak detection methods.
Molecular epidemiology of foodborne pathogens (i.e., whole-genome sequencing).
Surveillance of antimicrobial resistance of foodborne pathogens.
Transmission of foodborne pathogens at the human-animal-environment interface.

We look forward to your contribution that will generate knowledge to help public health stakeholders in mitigating the health burden of foodborne diseases.

Sincerely,

Dr. Csaba Varga
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Pathogens is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

Salmonella
Campylobacter
Listeria monocytogenes
Shiga-toxigenic E. coli
Spatial Epidemiology
Foodborne Diseases
Public Health
Spatio-temporal cluster analysis
One Health
Socioeconomic Factors
Geographic Information Systems

Published Papers (11 papers)

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Research

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18 pages, 3189 KiB

Open AccessArticle

Development of Single Nucleotide Polymorphism (SNP)-Based Triplex PCR Marker for Serotype-specific Escherichia coli Detection

by Md-Mafizur Rahman, Sang-Jin Lim and Yung-Chul Park

Pathogens 2022, 11(2), 115; https://doi.org/10.3390/pathogens11020115 - 19 Jan 2022

Cited by 7 | Viewed by 2694

Abstract

Single-nucleotide polymorphisms (SNPs) are one of the most common forms of genetic variation and as such are powerful tools for the identification of bacterial strains, their genetic diversity, phylogenetic analysis, and outbreak surveillance. In this study, we used 15 sets of SNP-containing primers to amplify and sequence the target Escherichia coli. Based on the combination of the 15-sequence primer sets, each SNP site encompassing forward and reverse primer sequences (620–919 bp) were aligned and an SNP-based marker was designed. Each SNP marker exists in at least two SNP sites at the 3′ end of each primer; one natural and the other artificially created by transition or transversion mutation. Thus, 12 sets of SNP primers (225–488 bp) were developed for validation by amplifying the target E. coli. Finally, a temperature gradient triplex PCR kit was designed to detect target E. coli strains. The selected primers were amplified in three genes (ileS, thrB, and polB), with fragment sizes of 401, 337, and 232 bp for E. coli O157:H7, E. coli, and E. coli O145:H28, respectively. This allele-specific SNP-based triplex primer assay provides serotype-specific detection of E. coli strains in one reaction tube. The developed marker would be used to diagnose, investigate, and control food-borne E. coli outbreaks. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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19 pages, 2783 KiB

Open AccessArticle

Temporal Study of Salmonella enterica Serovars Isolated from Fluff Samples from Ontario Poultry Hatcheries between 2009 and 2018

by Carolyn E. Murray, Csaba Varga, Rachel Ouckama and Michele T. Guerin

Pathogens 2022, 11(1), 9; https://doi.org/10.3390/pathogens11010009 - 22 Dec 2021

Cited by 5 | Viewed by 2563

Abstract

The objectives of this study were to determine the prevalence, temporal trends, seasonal patterns, and temporal clustering of Salmonella enterica isolated from fluff samples from poultry hatcheries in Ontario between 2009 and 2018. A scan statistic was used to identify clusters of common serovars and those of human health concern. A multi-level logistic regression model was used to identify factors (poultry commodity, year, season) associated with S. enterica presence. The period prevalence of S. enterica was 7.5% in broiler hatcheries, 1.6% in layer hatcheries, 7.6% in turkey hatcheries, 29.7% in waterfowl hatcheries, and 13.8% in game-bird hatcheries. An overall increasing trend in S. enterica prevalence was identified in waterfowl and game-bird hatcheries, while a decreasing trend was identified in broiler and turkey hatcheries. Overall, the most common S. enterica serovars were Kentucky, Enteritidis, Heidelberg, and Senftenberg. Salmonella enterica ser. Enteritidis was the most common serovar in waterfowl hatcheries. Temporal clusters were identified for all poultry commodities. Seasonal effects varied by commodity, with the highest odds of S. enterica occurring in the summer and fall. Our study offers information on the prevalence and temporality of S. enterica serovars that might guide prevention and control programs at the hatchery level. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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12 pages, 1690 KiB

Open AccessArticle

Unraveling the Contact Network Patterns between Commercial Turkey Operation in North Carolina and the Distribution of Salmonella Species

by Cameron Ellington, Claude Hebron, Rocio Crespo and Gustavo Machado

Pathogens 2021, 10(12), 1539; https://doi.org/10.3390/pathogens10121539 - 25 Nov 2021

Cited by 1 | Viewed by 2025

Abstract

Salmonellosis originating from poultry poses a significant threat to human health. Surveillance within production is thus needed to minimize risk. The objectives of this work were to investigate the distribution of Salmonella spp. from a commercial turkey operation and describe the animal movement patterns to investigate the association between contact network structure and Salmonella infection status. Four years of routine growout farm samples along with data on facility location, time since barns were built, production style, and bird movement data were utilized. From all of the surveillance samples collected, Salmonella serotyping was performed on positive samples and results showed that the most represented groups were C1 (28.67%), B (24.37%) and C2 (17.13%). The serovar Infantis (26.44%) was the most highly represented, followed by Senftenberg (12.76%) and Albany (10.93%). Results illustrated the seasonality of Salmonella presence with a higher number of positive samples being collected in the second half of each calendar year. We also demonstrated that Salmonella was more likely to occur in samples from older farms compared to farms built more recently. The contact network connectivity was low, although a few highly connected farms were identified. Results of the contact network showed that the farms which tested positive for Salmonella were not clustered within the network, suggesting that even though Salmonella dissemination occurs via transferring infected birds, for this study case it is unlikely the most important route of transmission. In conclusion, this study identified seasonality of Salmonella with significantly more cases in the second half of each year and also uncovered the role of between-farm movement of birds as not a major mode of Salmonella transmission. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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29 pages, 27801 KiB

Open AccessArticle

Informing Stewardship Measures in Canadian Food Animal Species through Integrated Reporting of Antimicrobial Use and Antimicrobial Resistance Surveillance Data—Part II, Application

by Agnes Agunos, Sheryl P. Gow, Anne E. Deckert and David F. Léger

Pathogens 2021, 10(11), 1491; https://doi.org/10.3390/pathogens10111491 - 16 Nov 2021

Cited by 6 | Viewed by 1939

Abstract

Using the methodology developed for integrated analysis and reporting of antimicrobial use (AMU) and antimicrobial resistance (AMR) data, farm-level surveillance data were synthesized and integrated to assess trends and explore potential AMU and AMR associations. Data from broiler chicken flocks (n = 656), grower–finisher pig herds (n = 462) and turkey flocks (n = 339) surveyed by the Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) at the farm-level (2015–2019) were used. The analyses showed a reduction in mean flock/herd level number of defined daily doses using Canadian standards (nDDDvetCA) adjusted for kg animal biomass that coincided with the decline in % resistance in the three species. This was noted in most AMU-AMR pairs studied except for ciprofloxacin resistant Campylobacter where resistance continued to be detected (moderate to high levels) despite limited fluoroquinolone use. Noteworthy was the significantly negative association between the nDDDvetCA/kg animal biomass and susceptible Escherichia coli (multispecies data), an early indication that AMU stewardship actions are having an impact. However, an increase in the reporting of diseases in recent years was observed. This study highlighted the value of collecting high-resolution AMU surveillance data with animal health context at the farm-level to understand AMR trends, enable data integration and measure the impact of AMU stewardship actions. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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13 pages, 1394 KiB

Open AccessArticle

A Snapshot of the Genetic Diversity of Salmonella Enteritidis Population Involved in Human Infections in Romania Taken in the European Epidemiological Context

by Codruta-Romanita Usein, Mihaela Oprea, Adriana Simona Ciontea, Sorin Dinu, Daniela Cristea, Lavinia Cipriana Zota and Saara Kotila

Pathogens 2021, 10(11), 1490; https://doi.org/10.3390/pathogens10111490 - 16 Nov 2021

Cited by 1 | Viewed by 2166

Abstract

In the absence of consistent national molecular typing data to enhance the surveillance of Salmonella Enteritidis, it was considered useful to collect baseline information on the genetic diversity and antibiotic susceptibility of strains isolated in Romania between January 2016 and April 2020 and compare them to strains described in major international outbreaks of the same period. A collection of 245 clinical isolates were genotyped by a standardised multiple-locus variable-number of tandem repeats analysis (MLVA) 5-loci protocol and screened for antimicrobial resistance against 15 compounds. Twenty strains were further subjected to whole genome sequencing (WGS) and compared to epidemiologically relevant high-throughput sequencing data available in European databases. Twenty-seven MLVA genotypes were identified, of which three, commonly reported in Europe between 2016–2020, covered 72% of the collection. Antibiotic resistance was detected in 30% of the strains, with resistance to nalidixic acid and ciprofloxacin as the most common phenotype, and also associated with two prevalent MLVA clones. WGS-derived multilocus sequence typing (MLST) revealed a single sequence type (ST11) further resolved into 10 core-genome MLST complex types. The minimum spanning tree constructed from the cgMLST data clustered Romanian and international strains, which shared more than 95% of the core genes, revealing links with a contemporaneous multi-country outbreak. This study could be regarded as a forerunner to the advent of using this integrative approach in the public health practice at a national level and thus contribute to the concerted actions at a European level to stop outbreaks. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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16 pages, 1939 KiB

Open AccessArticle

Identification of CTX-M Type ESBL E. coli from Sheep and Their Abattoir Environment Using Whole-Genome Sequencing

by Nigatu Aklilu Atlaw, Shivaramu Keelara, Maria Correa, Derek Foster, Wondwossen Gebreyes, Awa Aidara-Kane, Lyndy Harden, Siddhartha Thakur and Paula J. Fedorka Cray

Pathogens 2021, 10(11), 1480; https://doi.org/10.3390/pathogens10111480 - 14 Nov 2021

Cited by 6 | Viewed by 2706

Abstract

Widespread dissemination of extended-spectrum beta-lactamase (ESBL) Escherichia coli (E. coli) in animals, retail meats, and patients has been reported worldwide except for limited information on small ruminants. Our study focused on the genotypic characterization of ESBL E. coli from healthy sheep and their abattoir environment in North Carolina, USA. A total of 113 ESBL E. coli isolates from sheep (n = 65) and their abattoir environment (n = 48) were subjected to whole-genome sequencing (WGS). Bioinformatics tools were used to analyze the WGS data. Multiple CTX-M-type beta-lactamase genes were detected, namely bla_CTX-M-1, bla_CTX-M-14, bla_CTX-M-15, bla_CTX-M-27, bla_CTX-M-32, bla_CTX-M-55, and bla_CTX-M-65. Other beta-lactamase genes detected included bla_CMY-2, bla_TEM-1A/B/C, and bla_CARB-2. In addition, antimicrobial resistance (AMR) genes and/or point mutations that confer resistance to quinolones, aminoglycosides, phenicols, tetracyclines, macrolides, lincosamides, and folate-pathway antagonists were identified. The majority of the detected plasmids were shared between isolates from sheep and the abattoir environment. Sequence types were more clustered around seasonal sampling but dispersed across sample types. In conclusion, our study reported wide dissemination of ESBL E. coli in sheep and the abattoir environment and associated AMR genes, point mutations, and plasmids. This is the first comprehensive AMR and WGS report on ESBL E. coli from sheep and abattoir environments in the United States. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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15 pages, 299 KiB

Open AccessArticle

Demographic, Husbandry, and Biosecurity Factors Associated with the Presence of Campylobacter spp. in Small Poultry Flocks in Ontario, Canada

by Paige M. Schweitzer, Leonardo Susta, Csaba Varga, Marina L. Brash and Michele T. Guerin

Pathogens 2021, 10(11), 1471; https://doi.org/10.3390/pathogens10111471 - 12 Nov 2021

Cited by 4 | Viewed by 2207

Abstract

This study is part of a 2 year disease surveillance project conducted to establish the prevalence of poultry and zoonotic pathogens, including Campylobacter spp., among small poultry flocks in Ontario, Canada. For each post-mortem submission to the Animal Health Laboratory, a pooled sample of cecal tissue was cultured for Campylobacter spp., and a husbandry and biosecurity questionnaire was completed by the flock owner (n = 153). Using both laboratory and questionnaire data, our objective was to investigate demographic, husbandry, and biosecurity factors associated with the presence of Campylobacter spp. in small flocks. Two multivariable logistic regression models were built. In the farm model, the odds of Campylobacter spp. were higher in turkeys, and when birds were housed in a mixed group with different species and/or types of birds. The odds were lower when antibiotics were used within the last 12 months, and when birds had at least some free-range access. The effect of pest control depended on the number of birds at risk. In the coop model, the odds of Campylobacter spp. were lower when owners wore dedicated clothing when entering the coop. These results can be used to limit the transmission of Campylobacter spp. from small poultry flocks to humans. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

19 pages, 2162 KiB

Open AccessCommunication

Use of an Ecosystem-Based Approach to Shed Light on the Heterogeneity of the Contamination Pattern of Listeria monocytogenes on Conveyor Belt Surfaces in a Swine Slaughterhouse in the Province of Quebec, Canada

by Fanie Shedleur-Bourguignon, William P. Thériault, Jessie Longpré, Alexandre Thibodeau and Philippe Fravalo

Pathogens 2021, 10(11), 1368; https://doi.org/10.3390/pathogens10111368 - 22 Oct 2021

Cited by 5 | Viewed by 2269

Abstract

The role of the accompanying microbiota in the presence of Listeria monocytogenes on meat processing surfaces is not yet understood, especially in industrial production conditions. In this study, 300 conveyor belt samples from the cutting room of a swine slaughterhouse were collected during production. The samples were subjected to the detection of L. monocytogenes. Recovered strains were characterized by serogrouping-PCR, InlA Sanger sequencing and for their ability to form biofilm. A selection of isolates was compared with core genome multi-locus sequence typing analysis (cgMLST). The sequencing of the V4 region of the 16S RNA gene of the microorganisms harvested from each sample was carried out in parallel using the Illumina MiSeq platform. Diversity analyses were performed and MaAsLin analysis was used to assess the link between L. monocytogenes detection and the surrounding bacteria. The 72 isolates collected showed a low genetic diversity and important persistence characteristics. L. monocytogenes isolates were not stochastically distributed on the surfaces: the isolates were detected on three out of six production lines, each associated with a specific meat cut: the half carcasses, the bostons and the picnics. MaAsLin biomarker analysis identified the taxa Veillonella (p ≤ 0.0397) as a bacterial determinant of the presence of L. monocytogenes on processing surfaces. The results of this study revealed a heterogenous contamination pattern of the processing surfaces by L. monocytogenes and targeted a bacterial indicator of the presence of the pathogen. These results could lead to a better risk assessment of the contamination of meat products. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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10 pages, 1041 KiB

Open AccessArticle

Surveillance of Fresh Artisanal Cheeses Revealed High Levels of Listeria monocytogenes Contamination in the Department of Quindío, Colombia

by Elizabeth Jaramillo-Bedoya, Yenny Alexandra Trujillo-Alzate and Iván Darío Ocampo-Ibáñez

Pathogens 2021, 10(10), 1341; https://doi.org/10.3390/pathogens10101341 - 17 Oct 2021

Cited by 3 | Viewed by 2107

Abstract

Listeriosis is a foodborne disease caused by Listeria monocytogenes. Because outbreaks of listeriosis are associated with the ingestion of contaminated dairy products, surveillance of artisanal cheeses to detect the presence of this microorganism is necessary. We collected three types of artisanal non-acid fresh cheese (Campesino, Costeño, and Cuajada) from 12 municipalities of the Department of Quindío, Colombia. L. monocytogenes was identified using VIDAS^® and confirmed with API^® Listeria Rapid Kit. L. monocytogenes was detected in 104 (53.6%) of the 194 artisanal fresh-cheese samples analyzed. The highest percentages of contamination were detected in Salento (90.9%), Calracá (65.5%), Armenia (64.9%), and Filandia (50%). A significant association between municipality and contamination with L. monocytogenes was identified. However, no association could be established between the type of cheese and the occurrence of the bacterium. This is the first study on the presence of L. monocytogenes in artisanal fresh cheeses sold in the municipalities of the Department of Quindío, and the findings revealed very high percentages of contaminated samples. The presence of L. monocytogenes in artisanal cheeses remains a public health threat in developing countries, especially Colombia, where existing legislation does not require the surveillance of L. monocytogenes in food. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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16 pages, 2604 KiB

Open AccessArticle

Molecular Typing of Listeria monocytogenes IVb Serogroup Isolated from Food and Food Production Environments in Poland

by Beata Lachtara, Jacek Osek and Kinga Wieczorek

Pathogens 2021, 10(4), 482; https://doi.org/10.3390/pathogens10040482 - 15 Apr 2021

Cited by 13 | Viewed by 2809

Abstract

Listeria monocytogenes is one of the most important foodborne pathogens that may be present in food and in food processing environments. In the present study, 91 L. monocytogenes isolates of serogroup IVb from raw meat, ready-to-eat food and food production environments in Poland were characterized by whole genome sequencing (WGS). The strains were also compared, using core genome multi-locus sequence typing (cgMLST) analysis, with 186 genomes of L. monocytogenes recovered worldwide from food, environments, and from humans with listeriosis. The L. monocytogenes examined belonged to three MLST clonal complexes: CC1 (10; 11.0% isolates), CC2 (70; 76.9%), and CC6 (11; 12.1%). CC1 comprised of two STs (ST1 and ST515) which could be divided into five cgMLST, CC2 covered two STs (ST2 and ST145) with a total of 20 cgMLST types, whereas CC6 consisted of only one ST (ST6) classified as one cgMLST. WGS sequences of the tested strains revealed that they had several pathogenic markers making them potentially hazardous for public health. Molecular comparison of L. monocytogenes strains tested in the present study with those isolated from food and human listeriosis showed a relationship between the isolates from Poland, but not from other countries. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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Other

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35 pages, 9630 KiB

Open AccessProtocol

Informing Stewardship Measures in Canadian Food Animal Species through Integrated Reporting of Antimicrobial Use and Antimicrobial Resistance Surveillance Data—Part I, Methodology Development

by Agnes Agunos, Sheryl P. Gow, Anne E. Deckert, Grace Kuiper and David F. Léger

Pathogens 2021, 10(11), 1492; https://doi.org/10.3390/pathogens10111492 - 16 Nov 2021

Cited by 8 | Viewed by 2237

Abstract

This study explores methodologies for the data integration of antimicrobial use (AMU) and antimicrobial resistance (AMR) results within and across three food animal species, surveyed at the farm-level by the Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS). The approach builds upon existing CIPARS methodology and principles from other AMU and AMR surveillance systems. Species level data integration involved: (1) standard CIPARS descriptive and temporal analysis of AMU/AMR, (2) synthesis of results, (3) selection of AMU and AMR outcomes for integration, (4) selection of candidate AMU indicators to enable comparisons of AMU levels between species and simultaneous assessment of AMU and AMR trends, (5) exploration of analytic options for studying associations between AMU and AMR, and (6) interpretation and visualization. The multi-species integration was also completed using the above approach. In addition, summarized reporting of internationally-recognized indicators of AMR (i.e., AMR adjusted for animal biomass) and AMU (mg/population correction unit, mg/kg animal biomass) is explored. It is envisaged that this approach for species and multi-species AMU–AMR data integration will be applied to the annual CIPARS farm-level data and progressively developed over time to inform AMU–AMR integrated surveillance best practices for further enhancement of AMU stewardship actions. Full article

(This article belongs to the Special Issue Spatial Epidemiology and Surveillance of Foodborne Pathogens)

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