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From farm to fork: global surveillance trends of animal-food-human antimicrobial resistance

From farm to fork: global surveillance trends of animal-food-human antimicrobial resistance Objectives: Global surveillance measures keep trending with antimicrobial resistance (AMR) from farm to the final consumer. It is intended to review these trends within the past few decades. Materials and Methods: This short communication showcases AMR surveillance basics, methods, processes, technicalities and milestones within recent decades in relationship to AMR emergence from farm to fork. Results and Conclusions: Antibiotics and antimicrobial agents contribute to AMR dynamics. Passive and active AMR surveillance strategies continuously render data-driven robust systems for monitoring resistance levels and thereof changes across all geographical regions. Key words: antimicrobial resistance; antibiotics; farm-to-fork; surveillance. Food crops and food-producing animals serve as reservoirs of Salmonella spp., Shigella spp., and Neisseria gonorrhoeae (WHO, pathogen and have the potential to transfer resistance to human. 2015b; Reed et al., 2019). Also, the magnitude of such transmission from animal reservoirs to As resistant microorganisms develop, they are carried and spread human probably varies among different bacterial species (WHO, either by food animals to people via food consumption, direct con- 2014). Furthermore, raw food of animal origin can get contam- tact with animals or by environment spread. When AMR organism inated with resistant enteric pathogens such as Salmonella spp., affects food supply of one country, it becomes a potential problem Campylobacter jejuni, and Campylobacter coli or resistant com- for another (Aidara-Kane, 2012). Indeed, AMR populations are pre- mensal bacteria such as Escherichia coli and Enterococcus spp. sent everywhere in all bacterial communities and expand through (Franklin et  al., 2001). Generally, antimicrobial resistance (AMR) complex pathways, for example through food and water (Acar and refers to the capacity of microorganism to resist the growth inhibi- Moulin, 2013). The mechanism of AMR can include enzymatic deg- tory or killing activity of an antimicrobial beyond the normal sus- radation of antibiotics, antibiotic target modification, changing bac- ceptibility of specific bacterial species—an inevitable consequence of terial cell wall permeability, and alternative pathways to escape the evolutionary adaptation of microbes (Silbergeld et al., 2008; Verraes activity (Verraes et  al., 2013). As AMR spreads from closed envir- et al., 2013). Often due to poor hygiene/infection control as well as onment into open communities, new resistance mechanisms equally unscrupulous use of antibiotics/antimicrobial compounds, AMR in get horizontally spread between different bacterial species (Acar foods has become a global burden with increasing cases of mortality and Röstel, 2001). In addition, the mechanism of horizontal gene (WHO, 2015a). Because large amounts of antimicrobial agents em- transfer, which involves conjugation (transfer of DNA that occurs ployed in food animal production gets exposed to healthy animals, between live bacterial cells and require direct contact between donor it can provide favourable conditions for the emergence, spread, and and recipient cell), transformation (naked DNA from environment persistence of AMR bacteria capable of causing infections in animals is taken up in bacterial cells), and transduction (bacteriophage- and humans (Aidara-Kane, 2012). Largely, the target microorgan- mediated transfer process), may as well occur in the food stuff. isms have involved E.  coli., Klebsiella pneumoniae, Acinetobacter Besides, AMR in food can be brought about by: 1. food contamin- baumannii, Staphylococcus aureus, Streptococcus pneumoniae, ation with AMR bacteria and AMR genes as well as 2. intentional © The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz041/5695641 by guest on 19 February 2020 2 T. J. Ashaolu addition of microorganisms (with AMR properties) to food as auxil- antimicrobial (or resistance) in defined population; 4. providing basis iary technical substance (Verraes et al., 2013). for policy recommendations for animal/public health; 5.  generating Events leading to development of resistance in bacterial life in- data to guide the design of further studies; 6.  identifying with the clude chromosomal mutations, plasmid-based mutations, and ac- need for potential interventions; and 7.  providing information for quisition of genes. Besides, the most studied location of resistance prescribing practices and prudent use of recommendations (Franklin emergence is the digestive tract of human and animals. Basically, et al., 2001). Considerations for surveillance would include: 1. moni- foodborne pathogens that bring about diarrheal diseases include toring of bacteria from animal-derived food collected at different steps Salmonella spp., Campylobacter spp., Escherichia coli, Yersinia of food chain, including packaging, processing, and retailing; 2.  the spp., Clostridia spp., and Listeria spp. (Acar and Röstel, 2001). basic exposure mechanisms of humans to resistant bacteria from food Notwithstanding that antibiotics critically help in reducing the would not (necessarily) differ across countries; and 3.  exposure of burden of communicable diseases, AMR still threatens the effect- humans to resistant bacteria can be either direct (through exposure iveness/efficacy of successful infection treatments (Ndihokubwayo to zoonotic pathogens, e.g. Campylobacter spp., Salmonella spp.) or et  al., 2013). With respect to food processing domains, the use of indirect (through exposure to resistant genes potentially transferable antibiotics potentially at some point, lead to bacterial resistance and from commensal animal bacteria) (Franklin et al., 2001). once developed, would not be bound to borders of different coun- Technically speaking, well-known surveillance methods include tries (Acar and Röstel, 2001). Indeed, the use of antibiotics in pri- culture-based procedures, main phenotypic methods (test-tube, mary agricultural production remains very vital to AMR selection microtitre plate, and congo red agar), Confocal Laser Scanning in bacteria, the latter that subsequently finds its way into foodstuffs. Microscopy (CLSM), quantitative polymerase chain reaction Nonetheless, the transfer of AMR (in food processing environment) (qPCR), Pulse-Field Gel Electrophoresis (PFGE), Multi-Locus can happen via influence of food processing/preservation techniques, Sequence Typing (MLST), and Whole/Partial Microbial Genomic influence of biofilms, cross-resistance to antibiotics, and chemical Sequencing. The latter, according to Stärk et  al. (2019), is among biocides (Verraes et al., 2013). the newer surveillance methods considered more robust with merits Although antimicrobial agents have always driven the development such as rapid dissemination of results, high resolution, accuracy, and of AMR (Felmingham, 2002), how resistance in bacteria develops precision, except with some demerits such as high (initial) cost, com- would on the other hand depend on the character of resistant gene(s) as plexity of bioinformatic processing, and its non-standardized quality well as characteristics of exposed bacterial populations (Franklin et al., assurance. On the other hand, ‘omics’-based approach, e.g. genome 2001). A  growing threat to effective treatment of an ever-increasing metabolic, can help us to improve AMR detection in foods. The range of infections caused by bacteria, parasites, viruses, and fungi, likes of metatranscriptomics, proteomics, and metabolomics (Caniça AMR remains a complex global public health challenge/crisis that et al., 2019) can form an integral part of next generation sequencing threatens the return of untreatable infections on a massive scale with (NGS) capable of monitoring environmental hygiene of newly pro- no single strategy to fully contain the emergence/spread of infectious duced foods and detecting any new antibiotic resistant organism. organisms that have attained resistance. The development and imple- Although AMR surveillance systems serve as a source of mentation of effective strategies to curtail the emergence and spread of multi-centric antimicrobial susceptibility data, an already existing AMR is imperative, which via evaluating effects of interventions would database—a merit especially with respect to clinical microbiology la- cumulatively depend on collecting accurate/representative information boratories (Monnet, 2000), they fundamentally help in determining that describes the degree/extent of the problem (Silbergeld et al. 2008; the level of resistance in specific geographical regions, as well as WHO, 2014). Indeed, the USA has demonstrated how critical AMR is monitoring changes in levels of resistance. Besides, the information by extending collaborative/cooperative relations with the EU in a bid provided about mechanisms of resistance, how such resistance de- to strategically curb AMR emanating from food products (The PCAST, velops, persists within a given population, and then spreads to other 2014). More so, the global and regional movement of food/food prod- populations are very vital, all of which are critical for developing/ ucts calls for robust susceptibility testing and accurate monitoring of monitoring intervention programmes that would help minimize re- any emerging AMR cases (Donaghy et  al., 2019). The international sistance spread (Felmingham, 2002). Yet, carrying out AMR sur- spread of AMR microorganisms therefore suggests such resistance veillance and at regular intervals to monitor prevalence changes of to be of a global scale that requires a common, unified, and united resistance bacteria of food origin remains a very critical aspect of strategy (Monnet, 2000) and this is where surveillance in the microbial strategy that helps us to limit (AMR) spread (Franklin et al., 2001). context plays a very vital function/role. Nonetheless, surveillance of resistance trends would continue to Surveillance according to Office of International des Epizootes focus on such different targets as: 1. evolving trends in antibiotic re- (OIE) refers to the continuous investigation of given population to sistance; 2. evolving trends in the incidence of particular mechanisms detect the occurrence of disease for control purposes, which may in- of resistance; 3. evolving trends in the incidence of particular resistant volve testing of a part of the (given) population (Franklin et al., 2001). clones; and 4.  evolving trends in the incidence of AMR infections With respect to AMR, surveillance is a systematic, on-going data col- (Cornaglia et al., 2004). Some challenges that confront AMR surveil- lection, analysis, and reporting process that quantitatively monitors lance can include: 1. lack of standardization of method used, the anti- temporal trends in the distribution and occurrence of resistance and microbial tested, and differences in quality of susceptibility testing susceptibility to antimicrobial agents, providing useful information results; 2. possible differences in frequency and distribution of sam- that guides disease control (and medical practice) activities (Cornaglia pling among countries/regions; 3. absence of consensus on minimum et  al., 2004). Surveillance, whether passive (samples submitted to set of data to be collected; 4. standardization of databases and level laboratory for testing by sources outside the programme) or active of stratification of reports; and 5. the presence of several (proposed) (programme-developed sampling scheme based on objectives of pro- measurement units to show level of AMR, yet no consensus on which gramme and actively obtained isolates), has the primary purpose to one should be applied/used (Monnet, 2000). Meanwhile, the per- generate data, which can involve such facets like: 1. risk analysis to tinence of on-site food safety surveillance against AMR led to the determine risk to human/animal health; 2. detecting emerging AMR; investigation of catering services by Garayoa et  al. (2017), who re- 3. determining trend in prevalence of reduced susceptibility to certain commended regular supervision of activities, continuous training of Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz041/5695641 by guest on 19 February 2020 Global surveillance trends 3 workers, and checking high-risk cross-contamination surfaces (such food chain (Aidara-Kane, 2012). By 2001, the Office International as cutting boards and handles) by supervisors, as the way forward. des Epizooties (OIE) 69th General Session adopted the resolution Most of these AMR surveillance advancements have evolved No. XXV, which would enable OIE Specialist Commissions develop within the past three to four decades. Importantly, some key global international standards within the AMR domains. Member coun- milestones of AMR surveillance associated with animal, food, and tries were encouraged to embrace new methodologies that would human within the past decades are shown in Figure 1. Historically, establish objective/science-based contaminant of AMR in animal interest to monitor AMR actually began about the mid-1960s. By bacteria (Acar and Röstel, 2001). late 1970s, some form of surveillance of resistant bacteria in human Fast forward to 2008, the WHO Advising Group on Integrated infections had begun in some countries like USA, UK, France, South Surveillance of Antimicrobial Resistance (WHO-AGISAR) was es- Africa, Australia, Thailand, and Venezuela (Acar and Moulin, 2013). tablished to minimize public health impact of AMR associated By the 1990s, World Health Organization of the United Nations with the use of antimicrobial agents in food animals. The WHO- (WHO) called on concerned sectors to work together to eliminate AGISAR comprised of over 20 internationally renowned experts in the burden of AMR arising from the use of antimicrobials in food disciplines broadly relevant to AMR (Aidara-Kane, 2012) that have producing animals (Aidara-Kane, 2012). Given that sampling of re- regularly convened, started with its 1st meeting 15–19 June 2009 tail foods was forming part of integrated monitoring of foodborne in Copenhagen-Denmark, 2nd meeting 5–7 June 2010 in Guelph- AMR bacteria, by 1996, the National Antimicrobial Resistance Canada, 3rd meeting 14–17 June 2011 in Oslo—Norway, 4th Monitoring System (NARMS) got established in the USA (Acar and meeting 24–25 June 2012 in Aix-en-Provence—France, 5th meeting Moulin, 2013). By 1998, the World Health Assembly in the view 3–5 September 2013 in Bogotá—Columbia, 6th meeting 10–12 June to encourage rational/reduced use of antimicrobial agents in animal 2015 in Seoul—Republic of Korea, and 7th meeting 17–20 October food production adopted resolution WHA51.17 on AMR. By 2000 in 2016 in Raleigh—NC (WHO, Food Safety webpage, accessed 24 Geneva, the WHO established the ‘Global principles for the contain- August 2019). Besides, the WHO has led some regional surveillance ment of antimicrobial resistance in animals intended for food’ which efforts of AMR, especially within the present decade. Not long ago, allowed for expert consultations jointly with Food and Agriculture WHO Regional Office for Africa (AFRO) published a guide to fa- Organization of the United Nations (FAO) and World Organization cilitate establishment of laboratory-based surveillance for priority for Animal Health (OIE), clearly demonstrating the select for AMR bacterial diseases. Besides, whilst health ministers of WHO South bacteria is required within antimicrobial use in food animals and East Asia Region have met (2011), to articulate (their) commitment their resistance determinants are transferrable to humans via the to combat AMR, the WHO Western Pacific Region is believed to be Figure 1. Milestones of AMR surveillance in foods, animals, and humans within recent decades (diagram courtesy of Itthanan Suthikhana). Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz041/5695641 by guest on 19 February 2020 4 T. J. Ashaolu Felmingham,  D. (2002). The need for antimicrobial resistance surveillance. growing in this process. On the other hand, ReLAVRA—the Latin The Journal of Antimicrobial Chemotherapy, 50 Suppl S1: 1–7. American Antimicrobial Resistance Surveillance Network has in- Franklin, A., et al.; Office International des Epizooties Ad hoc Group. (2001). creased their ability to detect, monitor, and manage antibacterial Antimicrobial resistance: harmonisation of national antimicrobial resist- resistance (ABR) data. Mindful of public threats posed by current ance monitoring and surveillance programmes in animals and in animal- trends in AMR, the Eastern Mediterranean Regional Committee in derived food. Revue Scientifique Et Technique (International Office of 2013, adopted resolutions addressing AMR. In addition, Foodborne Epizootics), 20: 859–870. and Waterborne Diseases and Zoonoses Network FWD-Net—a Garayoa,  R. Abundancia,  C., Díez-Leturia,  M., Vitas,  A.I. (2017). Essential European network coordinated by European Centre for Disease tools for food safety surveillance in catering services: on-site inspections Prevention and Control (ECDC), helps us to collect foodborne bac- and control of high risk cross-contamination surfaces. Food Control, 75: teria data, jointly with European Food Safety Authority (EFSA), on 48–54. HM Government. (2017). UK 5 Yead Antimicrobial Resistance (AMR) AMR in indicator/zoonotic bacteria as it affects animals, foodstuff, Strategy 2013–2018: Third Annual Progress Report, 2016. UK Depart- as well as human (WHO, 2014). In the UK, interestingly, surveillance ment of Health, London, UK. Retrieved from https://www.gov.uk/govern- measures have been people-oriented, an AMR strategy launched ment/publications/ progress-report-on-the-uk-5-year-amr-strategy-2016. in 2013 that focuses on public-private sector volunteering (HM Monnet, D. L. (2000). Toward multinational antimicrobial resistance surveil- Government, 2017; RUMA, 2017), which between 2013 and 2016 lance systems in Europe. International Journal of Antimicrobial Agents, substantially reduced antimicrobial use in broilers and pigs by 21% 15: 91–101. (Davies and Wales, 2019). Largely in Europe as well, data about Ndihokubwayo,  J.  B., et  al. (2013). Antimicrobial resistance in the African surveillance and control schemes of foodborne AMR have become Region: issues, challenges and actions proposed. The African Health increasingly available, which buttresses the emphasis on reducing the Monitor, 16: 27–30. use of antimicrobials (DANMAP, 2017). Reed, T. A. N., et al.; Cambodia Technical Working Group on Antimicrobial Resistance. (2019). Antimicrobial resistance in Cambodia: a review. Inter- national Journal of Infectious Diseases, 85: 98–107. Conflict of Interest Statement RUMA. (2017). Targets Task Force Report 2017. Responsible Use of Medi- None declared. cines in Agriculture Alliance. Retrieved from https://www.ruma.org.uk/ wp-content/uploads/2017/10/RUMA-TargetsTask-Force-Report-2017- FINAL.pdf. References Silbergeld, E. K., Graham, J., Price, L. B. (2008). Industrial food animal pro- Acar, J. F., Moulin, G. (2013). Integrating animal health surveillance and food duction, antimicrobial resistance, and human health. Annual Review of safety: the issue of antimicrobial resistance. Revue Scientifique Et Tech- Public Health, 29: 151–169. nique (International Office of Epizootics), 32: 383–392. Stärk, K. D. C., Pękala, A., Muellner, P. (2019). Use of molecular and genomic Acar,  J., Röstel,  B. (2001). Antimicrobial resistance: an overview. Revue data for disease surveillance in aquaculture: towards improved evidence Scientifique Et Technique (International Office of Epizootics), 20: 797– for decision making. Preventive Veterinary Medicine, 167: 190–195. The President’s Council of Advisors on Science and Technology (PCAST). Aidara-Kane, A. (2012). Containment of antimicrobial resistance due to use (2014). Report to the President on combating Antibiotic Resistance. Avail- of antimicrobial agents in animals intended for food: WHO perspective. able at: http://www.whitehouse.gov/sites/default/files/microsites/ostp/ Revue Scientifique Et Technique (International Office of Epizootics), 31: PCAST/pcast_carb_report_sept2014.pdf. Accessed 19 August 2019. 277–287. Verraes, C., et al. (2013). Antimicrobial resistance in the food chain: a review. Caniça, M., Manageiro, V., Abriouel, H., Moran-Gilad, J., Franz, C.M. A. P. International Journal of Environmental Research and Public Health, 10: (2019). Antibiotic resistance in foodborne bacteria. Trends in Food Sci- 2643–2669. ence and Technology, 84: 41–44. World Health Organization (WHO). (2014). Antimicrobial Resistance: Global Cornaglia, G., et al.; ESCMID Study Group for Antimicrobial Resistance Sur- Report on Surveillance. WHO Press, Geneva, Switzerland. pp. 256 (ISBN veillance. (2004). European recommendations for antimicrobial resistance 978 92 4 156474 8). surveillance. Clinical Microbiology and Infection, 10: 349–383. World Health Organization (WHO). (2015a). Global Action Plan on DANMAP. (2017). DANMAP 2016 – Use of Antimicrobial Agents and Occur- Antimicrobial Resistance. http://apps.who.int/iris/bitstream/han rence of Antimicrobial Resistance in Bacteria From Food Animals, Food dle/10665/193736/9789241509763_eng.pdf?sequence=1. Accessed 19 and Humans in Denmark. Natl. Food Inst. & Statens Serum Inst., Copen- August 2019, 05.00 h GMT. hagen, Denmark. Retrieved from http://www.danmap.org. World Health Organization (WHO). (2015b). Manual for Early Implemen- Davies,  R., Wales,  A. (2019). Antimicrobial resistance on farms: a review tation: Global Antimicrobial Resistance Surveillance System. https:// including biosecurity and the potential role of disinfectants in resistance apps.who.int/iris/bitstream/handle/10665/188783/9789241549400_eng. selection. Comprehensive Reviews in Food Science and Food Safety, 18: pdf?sequence=1. Accessed 19 August 2019, 05.00 h GMT. 753–774. World Health Organization (WHO). Food Safety: WHO Advisory Group on Donaghy,  J.  A., et  al. (2019). Relationship of sanitizers, disinfectants, and Integrated Surveillance Antimicrobial Resistance (AGISAR). https://www. cleaning agents with antimicrobial resistance. Journal of Food Protection, who.int/foodsafety/areas_work/antimicrobial-resistance/agisar/en/. Ac- 82: 889–902. cessed 24 August 2019, 17.04 h GMT. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Food Quality and Safety Oxford University Press

From farm to fork: global surveillance trends of animal-food-human antimicrobial resistance

Food Quality and Safety , Volume Advance Article – Jul 17, 2020

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© The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press.
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Abstract

Objectives: Global surveillance measures keep trending with antimicrobial resistance (AMR) from farm to the final consumer. It is intended to review these trends within the past few decades. Materials and Methods: This short communication showcases AMR surveillance basics, methods, processes, technicalities and milestones within recent decades in relationship to AMR emergence from farm to fork. Results and Conclusions: Antibiotics and antimicrobial agents contribute to AMR dynamics. Passive and active AMR surveillance strategies continuously render data-driven robust systems for monitoring resistance levels and thereof changes across all geographical regions. Key words: antimicrobial resistance; antibiotics; farm-to-fork; surveillance. Food crops and food-producing animals serve as reservoirs of Salmonella spp., Shigella spp., and Neisseria gonorrhoeae (WHO, pathogen and have the potential to transfer resistance to human. 2015b; Reed et al., 2019). Also, the magnitude of such transmission from animal reservoirs to As resistant microorganisms develop, they are carried and spread human probably varies among different bacterial species (WHO, either by food animals to people via food consumption, direct con- 2014). Furthermore, raw food of animal origin can get contam- tact with animals or by environment spread. When AMR organism inated with resistant enteric pathogens such as Salmonella spp., affects food supply of one country, it becomes a potential problem Campylobacter jejuni, and Campylobacter coli or resistant com- for another (Aidara-Kane, 2012). Indeed, AMR populations are pre- mensal bacteria such as Escherichia coli and Enterococcus spp. sent everywhere in all bacterial communities and expand through (Franklin et  al., 2001). Generally, antimicrobial resistance (AMR) complex pathways, for example through food and water (Acar and refers to the capacity of microorganism to resist the growth inhibi- Moulin, 2013). The mechanism of AMR can include enzymatic deg- tory or killing activity of an antimicrobial beyond the normal sus- radation of antibiotics, antibiotic target modification, changing bac- ceptibility of specific bacterial species—an inevitable consequence of terial cell wall permeability, and alternative pathways to escape the evolutionary adaptation of microbes (Silbergeld et al., 2008; Verraes activity (Verraes et  al., 2013). As AMR spreads from closed envir- et al., 2013). Often due to poor hygiene/infection control as well as onment into open communities, new resistance mechanisms equally unscrupulous use of antibiotics/antimicrobial compounds, AMR in get horizontally spread between different bacterial species (Acar foods has become a global burden with increasing cases of mortality and Röstel, 2001). In addition, the mechanism of horizontal gene (WHO, 2015a). Because large amounts of antimicrobial agents em- transfer, which involves conjugation (transfer of DNA that occurs ployed in food animal production gets exposed to healthy animals, between live bacterial cells and require direct contact between donor it can provide favourable conditions for the emergence, spread, and and recipient cell), transformation (naked DNA from environment persistence of AMR bacteria capable of causing infections in animals is taken up in bacterial cells), and transduction (bacteriophage- and humans (Aidara-Kane, 2012). Largely, the target microorgan- mediated transfer process), may as well occur in the food stuff. isms have involved E.  coli., Klebsiella pneumoniae, Acinetobacter Besides, AMR in food can be brought about by: 1. food contamin- baumannii, Staphylococcus aureus, Streptococcus pneumoniae, ation with AMR bacteria and AMR genes as well as 2. intentional © The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz041/5695641 by guest on 19 February 2020 2 T. J. Ashaolu addition of microorganisms (with AMR properties) to food as auxil- antimicrobial (or resistance) in defined population; 4. providing basis iary technical substance (Verraes et al., 2013). for policy recommendations for animal/public health; 5.  generating Events leading to development of resistance in bacterial life in- data to guide the design of further studies; 6.  identifying with the clude chromosomal mutations, plasmid-based mutations, and ac- need for potential interventions; and 7.  providing information for quisition of genes. Besides, the most studied location of resistance prescribing practices and prudent use of recommendations (Franklin emergence is the digestive tract of human and animals. Basically, et al., 2001). Considerations for surveillance would include: 1. moni- foodborne pathogens that bring about diarrheal diseases include toring of bacteria from animal-derived food collected at different steps Salmonella spp., Campylobacter spp., Escherichia coli, Yersinia of food chain, including packaging, processing, and retailing; 2.  the spp., Clostridia spp., and Listeria spp. (Acar and Röstel, 2001). basic exposure mechanisms of humans to resistant bacteria from food Notwithstanding that antibiotics critically help in reducing the would not (necessarily) differ across countries; and 3.  exposure of burden of communicable diseases, AMR still threatens the effect- humans to resistant bacteria can be either direct (through exposure iveness/efficacy of successful infection treatments (Ndihokubwayo to zoonotic pathogens, e.g. Campylobacter spp., Salmonella spp.) or et  al., 2013). With respect to food processing domains, the use of indirect (through exposure to resistant genes potentially transferable antibiotics potentially at some point, lead to bacterial resistance and from commensal animal bacteria) (Franklin et al., 2001). once developed, would not be bound to borders of different coun- Technically speaking, well-known surveillance methods include tries (Acar and Röstel, 2001). Indeed, the use of antibiotics in pri- culture-based procedures, main phenotypic methods (test-tube, mary agricultural production remains very vital to AMR selection microtitre plate, and congo red agar), Confocal Laser Scanning in bacteria, the latter that subsequently finds its way into foodstuffs. Microscopy (CLSM), quantitative polymerase chain reaction Nonetheless, the transfer of AMR (in food processing environment) (qPCR), Pulse-Field Gel Electrophoresis (PFGE), Multi-Locus can happen via influence of food processing/preservation techniques, Sequence Typing (MLST), and Whole/Partial Microbial Genomic influence of biofilms, cross-resistance to antibiotics, and chemical Sequencing. The latter, according to Stärk et  al. (2019), is among biocides (Verraes et al., 2013). the newer surveillance methods considered more robust with merits Although antimicrobial agents have always driven the development such as rapid dissemination of results, high resolution, accuracy, and of AMR (Felmingham, 2002), how resistance in bacteria develops precision, except with some demerits such as high (initial) cost, com- would on the other hand depend on the character of resistant gene(s) as plexity of bioinformatic processing, and its non-standardized quality well as characteristics of exposed bacterial populations (Franklin et al., assurance. On the other hand, ‘omics’-based approach, e.g. genome 2001). A  growing threat to effective treatment of an ever-increasing metabolic, can help us to improve AMR detection in foods. The range of infections caused by bacteria, parasites, viruses, and fungi, likes of metatranscriptomics, proteomics, and metabolomics (Caniça AMR remains a complex global public health challenge/crisis that et al., 2019) can form an integral part of next generation sequencing threatens the return of untreatable infections on a massive scale with (NGS) capable of monitoring environmental hygiene of newly pro- no single strategy to fully contain the emergence/spread of infectious duced foods and detecting any new antibiotic resistant organism. organisms that have attained resistance. The development and imple- Although AMR surveillance systems serve as a source of mentation of effective strategies to curtail the emergence and spread of multi-centric antimicrobial susceptibility data, an already existing AMR is imperative, which via evaluating effects of interventions would database—a merit especially with respect to clinical microbiology la- cumulatively depend on collecting accurate/representative information boratories (Monnet, 2000), they fundamentally help in determining that describes the degree/extent of the problem (Silbergeld et al. 2008; the level of resistance in specific geographical regions, as well as WHO, 2014). Indeed, the USA has demonstrated how critical AMR is monitoring changes in levels of resistance. Besides, the information by extending collaborative/cooperative relations with the EU in a bid provided about mechanisms of resistance, how such resistance de- to strategically curb AMR emanating from food products (The PCAST, velops, persists within a given population, and then spreads to other 2014). More so, the global and regional movement of food/food prod- populations are very vital, all of which are critical for developing/ ucts calls for robust susceptibility testing and accurate monitoring of monitoring intervention programmes that would help minimize re- any emerging AMR cases (Donaghy et  al., 2019). The international sistance spread (Felmingham, 2002). Yet, carrying out AMR sur- spread of AMR microorganisms therefore suggests such resistance veillance and at regular intervals to monitor prevalence changes of to be of a global scale that requires a common, unified, and united resistance bacteria of food origin remains a very critical aspect of strategy (Monnet, 2000) and this is where surveillance in the microbial strategy that helps us to limit (AMR) spread (Franklin et al., 2001). context plays a very vital function/role. Nonetheless, surveillance of resistance trends would continue to Surveillance according to Office of International des Epizootes focus on such different targets as: 1. evolving trends in antibiotic re- (OIE) refers to the continuous investigation of given population to sistance; 2. evolving trends in the incidence of particular mechanisms detect the occurrence of disease for control purposes, which may in- of resistance; 3. evolving trends in the incidence of particular resistant volve testing of a part of the (given) population (Franklin et al., 2001). clones; and 4.  evolving trends in the incidence of AMR infections With respect to AMR, surveillance is a systematic, on-going data col- (Cornaglia et al., 2004). Some challenges that confront AMR surveil- lection, analysis, and reporting process that quantitatively monitors lance can include: 1. lack of standardization of method used, the anti- temporal trends in the distribution and occurrence of resistance and microbial tested, and differences in quality of susceptibility testing susceptibility to antimicrobial agents, providing useful information results; 2. possible differences in frequency and distribution of sam- that guides disease control (and medical practice) activities (Cornaglia pling among countries/regions; 3. absence of consensus on minimum et  al., 2004). Surveillance, whether passive (samples submitted to set of data to be collected; 4. standardization of databases and level laboratory for testing by sources outside the programme) or active of stratification of reports; and 5. the presence of several (proposed) (programme-developed sampling scheme based on objectives of pro- measurement units to show level of AMR, yet no consensus on which gramme and actively obtained isolates), has the primary purpose to one should be applied/used (Monnet, 2000). Meanwhile, the per- generate data, which can involve such facets like: 1. risk analysis to tinence of on-site food safety surveillance against AMR led to the determine risk to human/animal health; 2. detecting emerging AMR; investigation of catering services by Garayoa et  al. (2017), who re- 3. determining trend in prevalence of reduced susceptibility to certain commended regular supervision of activities, continuous training of Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz041/5695641 by guest on 19 February 2020 Global surveillance trends 3 workers, and checking high-risk cross-contamination surfaces (such food chain (Aidara-Kane, 2012). By 2001, the Office International as cutting boards and handles) by supervisors, as the way forward. des Epizooties (OIE) 69th General Session adopted the resolution Most of these AMR surveillance advancements have evolved No. XXV, which would enable OIE Specialist Commissions develop within the past three to four decades. Importantly, some key global international standards within the AMR domains. Member coun- milestones of AMR surveillance associated with animal, food, and tries were encouraged to embrace new methodologies that would human within the past decades are shown in Figure 1. Historically, establish objective/science-based contaminant of AMR in animal interest to monitor AMR actually began about the mid-1960s. By bacteria (Acar and Röstel, 2001). late 1970s, some form of surveillance of resistant bacteria in human Fast forward to 2008, the WHO Advising Group on Integrated infections had begun in some countries like USA, UK, France, South Surveillance of Antimicrobial Resistance (WHO-AGISAR) was es- Africa, Australia, Thailand, and Venezuela (Acar and Moulin, 2013). tablished to minimize public health impact of AMR associated By the 1990s, World Health Organization of the United Nations with the use of antimicrobial agents in food animals. The WHO- (WHO) called on concerned sectors to work together to eliminate AGISAR comprised of over 20 internationally renowned experts in the burden of AMR arising from the use of antimicrobials in food disciplines broadly relevant to AMR (Aidara-Kane, 2012) that have producing animals (Aidara-Kane, 2012). Given that sampling of re- regularly convened, started with its 1st meeting 15–19 June 2009 tail foods was forming part of integrated monitoring of foodborne in Copenhagen-Denmark, 2nd meeting 5–7 June 2010 in Guelph- AMR bacteria, by 1996, the National Antimicrobial Resistance Canada, 3rd meeting 14–17 June 2011 in Oslo—Norway, 4th Monitoring System (NARMS) got established in the USA (Acar and meeting 24–25 June 2012 in Aix-en-Provence—France, 5th meeting Moulin, 2013). By 1998, the World Health Assembly in the view 3–5 September 2013 in Bogotá—Columbia, 6th meeting 10–12 June to encourage rational/reduced use of antimicrobial agents in animal 2015 in Seoul—Republic of Korea, and 7th meeting 17–20 October food production adopted resolution WHA51.17 on AMR. By 2000 in 2016 in Raleigh—NC (WHO, Food Safety webpage, accessed 24 Geneva, the WHO established the ‘Global principles for the contain- August 2019). Besides, the WHO has led some regional surveillance ment of antimicrobial resistance in animals intended for food’ which efforts of AMR, especially within the present decade. Not long ago, allowed for expert consultations jointly with Food and Agriculture WHO Regional Office for Africa (AFRO) published a guide to fa- Organization of the United Nations (FAO) and World Organization cilitate establishment of laboratory-based surveillance for priority for Animal Health (OIE), clearly demonstrating the select for AMR bacterial diseases. Besides, whilst health ministers of WHO South bacteria is required within antimicrobial use in food animals and East Asia Region have met (2011), to articulate (their) commitment their resistance determinants are transferrable to humans via the to combat AMR, the WHO Western Pacific Region is believed to be Figure 1. Milestones of AMR surveillance in foods, animals, and humans within recent decades (diagram courtesy of Itthanan Suthikhana). Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz041/5695641 by guest on 19 February 2020 4 T. J. Ashaolu Felmingham,  D. (2002). The need for antimicrobial resistance surveillance. growing in this process. On the other hand, ReLAVRA—the Latin The Journal of Antimicrobial Chemotherapy, 50 Suppl S1: 1–7. American Antimicrobial Resistance Surveillance Network has in- Franklin, A., et al.; Office International des Epizooties Ad hoc Group. (2001). creased their ability to detect, monitor, and manage antibacterial Antimicrobial resistance: harmonisation of national antimicrobial resist- resistance (ABR) data. Mindful of public threats posed by current ance monitoring and surveillance programmes in animals and in animal- trends in AMR, the Eastern Mediterranean Regional Committee in derived food. Revue Scientifique Et Technique (International Office of 2013, adopted resolutions addressing AMR. In addition, Foodborne Epizootics), 20: 859–870. and Waterborne Diseases and Zoonoses Network FWD-Net—a Garayoa,  R. Abundancia,  C., Díez-Leturia,  M., Vitas,  A.I. (2017). Essential European network coordinated by European Centre for Disease tools for food safety surveillance in catering services: on-site inspections Prevention and Control (ECDC), helps us to collect foodborne bac- and control of high risk cross-contamination surfaces. Food Control, 75: teria data, jointly with European Food Safety Authority (EFSA), on 48–54. 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Journal

Food Quality and SafetyOxford University Press

Published: Jul 17, 2020

References