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      Consumer Exposure to Antimicrobial Resistant Bacteria From Food at Swiss Retail Level

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          Abstract

          Background: Antimicrobial resistance (AMR) in bacteria is an increasing health concern. The spread of AMR bacteria (AMRB) between animals and humans via the food chain and the exchange of AMR genes requires holistic approaches for risk mitigation. The AMRB exposure of humans via food is currently only poorly understood leaving an important gap for intervention design.

          Method: This study aimed to assess AMRB prevalence in retail food and subsequent exposure of Swiss consumers in a systematic literature review of data published between 1996 and 2016 covering the Swiss agriculture sector and relevant imported food.

          Results: Data from 313 out of 9,473 collected studies were extracted yielding 122,438 food samples and 38,362 bacteria isolates of which 30,092 samples and 8,799 isolates were AMR positive. A median AMRB prevalence of >50% was observed for meat and seafood harboring Campylobacter, Enterococcus, Salmonella, Escherichia coli, Listeria, and Vibrio spp. and to a lesser prevalence for milk products harboring starter culture bacteria. Gram-negative AMRB featured predominantly AMR against aminoglycosides, cephalosporins, fluoroquinolones, penicillins, sulfonamides, and tetracyclines observed at AMR exposures scores of levels 1 (medium) and 2 (high) for Campylobacter, Salmonella, E. coli in meat as well as Vibrio and E. coli in seafood. Gram-positive AMRB featured AMR against glycoproteins, lincosamides, macrolides and nitrofurans for Staphylococcus and Enterococcus in meat sources, Staphylococcus in seafood as well as Enterococcus and technologically important bacteria (incl. starters) in fermented or processed dairy products. Knowledge gaps were identified for AMR prevalence in dairy, plant, fermented meat and novel food products and for the role of specific indicator bacteria ( Staphylococcus, Enterococcus), starter culture bacteria and their mobile genetic elements in AMR gene transfer.

          Conclusion: Raw meat, milk, seafood, and certain fermented dairy products featured a medium to high potential of AMR exposure for Gram-negative and Gram-positive foodborne pathogens and indicator bacteria. Food at retail, additional food categories including fermented and novel foods as well as technologically important bacteria and AMR genetics are recommended to be better integrated into systematic One Health AMR surveillance and mitigation strategies to close observed knowledge gaps and enable a comprehensive AMR risk assessment for consumers.

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          Most cited references16

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          From “one medicine” to “one health” and systemic approaches to health and well-being☆

          Faced with complex patterns of global change, the inextricable interconnection of humans, pet animals, livestock and wildlife and their social and ecological environment is evident and requires integrated approaches to human and animal health and their respective social and environmental contexts. The history of integrative thinking of human and animal health is briefly reviewed from early historical times, to the foundation of universities in Europe, up to the beginning of comparative medicine at the end of the 19th century. In the 20th century, Calvin Schwabe coined the concept of “one medicine”. It recognises that there is no difference of paradigm between human and veterinary medicine and both disciplines can contribute to the development of each other. Considering a broader approach to health and well-being of societies, the original concept of “one medicine” was extended to “one health” through practical implementations and careful validations in different settings. Given the global health thinking in recent decades, ecosystem approaches to health have emerged. Based on complex ecological thinking that goes beyond humans and animals, these approaches consider inextricable linkages between ecosystems and health, known as “ecosystem health”. Despite these integrative conceptual and methodological developments, large portions of human and animal health thinking and actions still remain in separate disciplinary silos. Evidence for added value of a coherent application of “one health” compared to separated sectorial thinking is, however, now growing. Integrative thinking is increasingly being considered in academic curricula, clinical practice, ministries of health and livestock/agriculture and international organizations. Challenges remain, focusing around key questions such as how does “one health” evolve and what are the elements of a modern theory of health? The close interdependence of humans and animals in their social and ecological context relates to the concept of “human-environmental systems”, also called “social-ecological systems”. The theory and practice of understanding and managing human activities in the context of social-ecological systems has been well-developed by members of The Resilience Alliance and was used extensively in the Millennium Ecosystem Assessment, including its work on human well-being outcomes. This in turn entails systems theory applied to human and animal health. Examples of successful systems approaches to public health show unexpected results. Analogous to “systems biology” which focuses mostly on the interplay of proteins and molecules at a sub-cellular level, a systemic approach to health in social-ecological systems (HSES) is an inter- and trans-disciplinary study of complex interactions in all health-related fields. HSES moves beyond “one health” and “eco-health”, expecting to identify emerging properties and determinants of health that may arise from a systemic view ranging across scales from molecules to the ecological and socio-cultural context, as well from the comparison with different disease endemicities and health systems structures.
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            Preservation and fermentation: past, present and future

            Preservation of food and beverages resulting from fermentation has been an effective form of extending the shelf-life of foods for millennia. Traditionally, foods were preserved through naturally occurring fermentations, however, modern large scale production generally now exploits the use of defined strain starter systems to ensure consistency and quality in the final product. This review will mainly focus on the use of lactic acid bacteria (LAB) for food improvement, given their extensive application in a wide range of fermented foods. These microorganisms can produce a wide variety of antagonistic primary and secondary metabolites including organic acids, diacetyl, CO2 and even antibiotics such as reuterocyclin produced by Lactobacillus reuteri. In addition, members of the group can also produce a wide range of bacteriocins, some of which have activity against food pathogens such as Listeria monocytogenes and Clostridium botulinum. Indeed, the bacteriocin nisin has been used as an effective biopreservative in some dairy products for decades, while a number of more recently discovered bacteriocins, such as lacticin 3147, demonstrate increasing potential in a number of food applications. Both of these lactococcal bacteriocins belong to the lantibiotic family of posttranslationally modified bacteriocins that contain lanthionine, beta-methyllanthionine and dehydrated amino acids. The exploitation of such naturally produced antagonists holds tremendous potential for extension of shelf-life and improvement of safety of a variety of foods.
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              Evolution and ecology of antibiotic resistance genes.

              A new perspective on the topic of antibiotic resistance is beginning to emerge based on a broader evolutionary and ecological understanding rather than from the traditional boundaries of clinical research of antibiotic-resistant bacterial pathogens. Phylogenetic insights into the evolution and diversity of several antibiotic resistance genes suggest that at least some of these genes have a long evolutionary history of diversification that began well before the 'antibiotic era'. Besides, there is no indication that lateral gene transfer from antibiotic-producing bacteria has played any significant role in shaping the pool of antibiotic resistance genes in clinically relevant and commensal bacteria. Most likely, the primary antibiotic resistance gene pool originated and diversified within the environmental bacterial communities, from which the genes were mobilized and penetrated into taxonomically and ecologically distant bacterial populations, including pathogens. Dissemination and penetration of antibiotic resistance genes from antibiotic producers were less significant and essentially limited to other high G+C bacteria. Besides direct selection by antibiotics, there is a number of other factors that may contribute to dissemination and maintenance of antibiotic resistance genes in bacterial populations.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                06 March 2018
                2018
                : 9
                : 362
                Affiliations
                [1] 1Laboratory of Food Biotechnology, Institute of Food Nutrition and Health, Department of Health Science and Technology, ETH Zurich , Zurich, Switzerland
                [2] 2Institute for Food Safety and Hygiene, University of Zurich , Zurich, Switzerland
                [3] 3SAFOSO AG , Liebefeld, Switzerland
                Author notes

                Edited by: David Rodriguez-Lazaro, University of Burgos, Spain

                Reviewed by: Beatrix Stessl, Veterinärmedizinische Universität Wien, Austria; Diego Florez-Cuadrado, Complutense University of Madrid, Spain

                *Correspondence: Christoph Jans christoph.jans@ 123456hest.ethz.ch

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2018.00362
                5845543
                29559960
                32e3b7f6-fd09-4688-8530-bd8bebdc5935
                Copyright © 2018 Jans, Sarno, Collineau, Meile, Stärk and Stephan.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 13 October 2017
                : 15 February 2018
                Page count
                Figures: 4, Tables: 4, Equations: 0, References: 37, Pages: 19, Words: 12062
                Funding
                Funded by: Bundesamt für Lebensmittelsicherheit und Veterinärwesen 10.13039/501100006454
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                antimicrobial resistance,antibiotic resistance,retail foods,food safety,exposure assessment,one health,prevalence

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