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. 2023 Aug 14;151:e143. doi: 10.1017/S0950268823001309

Table 1.

Characteristics of the included studies

Study Location Level Description of study aims (relevant to this review) Methods Relevant outcomes
Microbial subtyping studies
Hald, 2007 [33] Denmark National Attribute resistant salmonellosis cases to different animal reservoirs, using resistance profiles Typing: serotyping & antibiotyping (phenotypic); phage typing (for susceptible isolates)
Analysis: based on Hald model [49]
Attribution of all infections; % of resistant cases due to each source
Vieira, 2016 [32] United States National Evaluate the use of Salmonella Hadar retail contamination data and antibiotyping to attribute human illnesses to food sources, comparing four models Typing: PFGE (comparison) & antibiotyping (PT)
Analysis: used Dutch model [50]
Attribution (%)
Mughini-Gras, 2019 [31] Netherlands National Attribute ESBL- and pAmpC-producing E. coli carriage in the community to different sources based on gene, prevalence, and human exposure data Typing: ESBL & pAmpC gene occurrence
Analysis: based on modified Hald model [51]
Attribution (%)
Parisi, 2020 [47] Vietnam Sub-national Attribute invasive and non-invasive human non-typhoidal salmonellosis in Southern Vietnam to animal sources using serotyping and/or antibiotyping Typing: molecular serotyping (MLST) & antibiotyping (phenotypic)
Analysis: own, Bayesian multinomial mixture model
Attribution (% and total cases)
Duarte, 2021 [19] Europe Regional Demonstrate the use of metagenomics for the attribution of the human resistome to different animal reservoirs with three models differing on whether they include a human/unknown source and on whether they were country dependent or independent Typing: metagenomics
Analysis: own, random forests & dissimilarity analysis (SIMPER)
Different plots illustrating attribution
Mitchell, 2021 [46] India Sub-national Estimate the contribution of animals and water sources to resistant E. coli infections in children in rural India Typing: antibiotyping (phenotypic)
Analysis: SourceR [52]
Attribution (% and total cases)
Perestrelo, 2022 [30] Germany National Attribute human ESBL-producing E. coli colonisation to animal sources and nosocomial infections, using different combinations of three typing methods Typing: ESBL genotyping, phylogenetic grouping (PCR) & antibiotyping (phenotypic)
Analysis: based on Hald model [49]
Attribution (% and total cases)
Comparative exposure assessments
Carmo, 2014 [24] Denmark National Assess the relative contribution of different meat types to the consumer exposure to ESBL-/AmpC-producing E. coli Quantitative
Guideline: not specified
Exposure attribution (%)
Evers, 2017 [23] Netherlands National Quantify ESBL- & pAmpC-producing E. coli exposure in humans via meat consumption from pre-retail to exposure Quantitative
Guideline: based on swift QMRA [53]
Exposure/ portion; exposure attribution (total and %)
Lechner, 202 [22] Switzerland National Identify the most relevant AMR transmission pathways from animals to humans based on Swiss expert opinions Qualitative
Guideline: OIE framework for AMR [9]
Person days at risk; bubble chart relating exposure, release & person days at risk
Investigation of outbreaks
Holmberg, 1984 [29] United States National Describe animal sources of antibiotic-resistant Salmonella outbreaks between 1971 and 1983 Linked outbreak reports with resistance information Number of resistant outbreaks caused by each source
Sahin, 2012 [28] United States National Report of several outbreaks caused by Campylobacter jejuni clone SA as part of their investigation of its presence in human isolates Identified relevant outbreaks via the PulseNet database for Campylobacter Description of all clone SA outbreaks & their source
Brown, 2017 [27] United States National Compare foods associated with antibiotic-resistant Salmonella outbreaks from 2003 to 2012 Linked outbreak info to antibiotic susceptibility data Numbers of resistant (& multidrug-resistant) outbreaks caused by each source
Folster, 2017 [26] United States National Report the number of outbreaks caused by ceftriaxone-resistant Salmonella by source between 2011 and 2012 as part of a genetic analysis of the outbreak strains Tested outbreak samples for ceftriaxone-resistance & linked positive samples to source information Number of resistant outbreaks caused by each source
Waltenburg, 2021 [25] United States National Describe all salmonellosis outbreaks caused by reptiles or amphibians between 2009 and 2018, including a description of the sources by resistance profile Tested outbreak samples for resistance Number of resistant outbreaks caused by each pet species
Other source attribution studies
de Freitas Costa, 2022 [34] Netherlands National Develop a dynamic risk model that accounts for the multi-directional spread of ESBL-producing E. coli between populations over time and may be used for exploring the effects of different food chain interventions Source attribution
Analysis: discrete-time model
Attribution at equilibrium (%)
Risk assessments
Vose, 2000 [11] United States National Develop a model to assess the human health impact of fluoroquinolone-resistant Campylobacter attributed to chicken consumption that also allows for modelling future changes in the system Quantitative
Framework: own (FDA-CVM)
% and ‘1 in x’ of being affected for all citizens, cases, cases seeking care & care-seeking cases who are prescribed antibiotics
Alban, 2022 [44] Denmark National Assess whether dry-cured sausages produced with pork with Salmonella Typhimurium DT104 are a risk for consumers Quantitative
Framework: Codex [54]
Maximal observed number of diarrhoea cases per year within 100 years
Presi, 2009 [43] Switzerland National Compare the health risk for consumers arising from their exposure to resistant bacteria from meat of four different types Semi-Quantitative (Risk scoring)
Framework: own model
Ranking of different meat products according to high human health risk
Cox, 2014 [42] United States National Estimate the excess number of human MRSA infections attributable to MRSA ST398 from pigs and pork Quantitative
Framework: own model
Excess cases per year
Otto, 2014 [45] Canada Sub-national Estimate number of ceftiofur-resistant Salmonella enterica Heidelberg cases in humans in Québec and Ontario attributable to chicken consumption Quantitative
Framework: based on FDA-CVM [11]
Annual mean incidence due to chicken consumption
Doménech, 2015 [48] Spain Sub-national Characterise the human health risk due to different resistances in Salmonella from pork, beef, and poultry meat Qualitative
Framework: Codex AMR [55]
Level of risk for humans due to different resistances from different meats
Chereau, 2017 [20] South East Asia Regional Characterise the level of risk of the emergence and spread of AMR in the WHO Southeast Asian region Qualitative
Framework: WHO rapid risk assessment guideline [56]
High, medium, low & negligible risk transmission routes
Collineau, 2018 [41] Switzerland National Develop a framework to rank the human health importance of combinations of pathogens, resistance to antimicrobials, and different meat types Semi-Quantitative (Risk ranking)
Framework: Codex AMR & MCDA, identified via EFSA risk ranking review [55, 57]
List of meat-pathogen-resistance combinations with the highest human health risk
Collineau, 2020 [40] Canada National Define the baseline (2013) risk of human ceftiofur-resistant Salmonella Heidelberg infection due to chicken and compare it to alternative scenarios Qualitative
Framework: Based on Codex AMR & FAO/WHO model [55, 58]
% of illness per serving; number of cases per year
Costard, 2020 [39] United States National Estimate the risk for resistant non-typhoidal salmonellosis per beef meal using the yearly cases of resistant infections and number of meals made with beef and evaluate the change over time Quantitative
Framework: Based on [33] and USDA framework [10]
Annual incidence attributable to beef, cases per 1 million beef meals
Schoen, 2020 [38] United States National Assess the risk for MRSA colonisation from preparing contaminated pork meat Quantitative
Framework: not specified
Risk per preparation event
Opatowski, 2021 [21] South or South East Asia National Develop a model to combine annual ESBL-producing E. coli colonisation incidence due to five One Health transmission routes. Illustrate its application in hypothetical high- and low-income settings Quantitative
Framework: complementary to [20]
Incidence due to animal-based food and animal contact per 100 persons per year
Other studies
Bosch, 2016 [37] Netherlands National Describe changing characteristics of livestock-associated MRSA, including the percentage of cases reporting livestock contact / % of cases who were in contact with livestock
Larsen, 2017 [36] Denmark National Describe the emergence of livestock-associated MRSA CC398 in invasive human cases, including a summary of cases not reporting livestock contact / % of cases who were in contact with livestock
Booton, 2021 [35] Thailand National Develop a One Health model to predict the maximum impact of reducing different AMR drivers in Thailand on the human AMR burden between 2020 and 2040 Prediction model, One Health
Analysis: compartmental model of ordinary differential equations
Maximum human AMR reduction via elimination of animal-to-human transmission (%)

Abbreviations: Codex, Codex Alimentarius; EFSA, The European Food Safety Authority; ESBL, extended-spectrum β-lactamase; FAO, Food and Agriculture Organization; FDA-VCM, Food and Drug Administration Center for Veterinary Medicine; MRSA, methicillin-resistant S. aureus; OIE, World Organisation for Animal Health (now WOAH); (p)AmpC, (plasmid)-mediated AmpC β-lactamase; QMRA, quantitative microbial risk assessment; USDA, United States Department of Agriculture; WHO, World Health Organization.