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.