Dissemination of carbapenemase-producing Enterobacteriaceae and associated resistance determinants through global food systems.
antimicrobial resistance
carbapenem resistance
carbapenemase-producing Enterobacteriaceae
food systems
foodborne
molecular epidemiology
Journal
Comprehensive reviews in food science and food safety
ISSN: 1541-4337
Titre abrégé: Compr Rev Food Sci Food Saf
Pays: United States
ID NLM: 101305205
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
revised:
27
03
2023
received:
29
11
2022
accepted:
01
04
2023
medline:
17
7
2023
pubmed:
21
4
2023
entrez:
21
04
2023
Statut:
ppublish
Résumé
Antimicrobial agents are a critical component of modern healthcare systems, fulfilling a core function in patient care and improving individual patient outcomes and consequently overall public health. However, the efficacy of antimicrobial interventions is being consistently eroded by the emergence and dissemination of various antimicrobial resistance (AMR) mechanisms. One highly valued class of antimicrobial compounds is carbapenems, which retain efficacy in treating most multidrug-resistant infections and are considered "last line" agents. Therefore, recent trends in proliferation of carbapenem resistance (CR) via dissemination of carbapenemase-encoding genes among members of the Enterobacteriaceae family pose a significant threat to public health. While much of the focus relating to this has been on nosocomial environments, community-acquired carbapenemase-producing Enterobacteriaceae (CPE) infections and their associated transmission routes are less well studied. Among these community-associated vectors, the role of food chains and contaminated foods is important, since Enterobacteriaceae occupy niches within these settings. This review examines foodborne CPE transmission by exploring how interactions within and between food, the food chain, and agriculture not only promote and disseminate CPE, but also create reservoirs of mobile genetic elements that may lead to further carbapenemase gene proliferation both within and between microbial communities. Additionally, recent developments regarding the global occurrence and molecular epidemiology of CPEs in food chains will be reviewed.
Identifiants
pubmed: 37083194
doi: 10.1111/1541-4337.13159
doi:
Substances chimiques
Anti-Bacterial Agents
0
Carbapenems
0
Types de publication
Review
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2706-2727Informations de copyright
© 2023 The Authors. Comprehensive Reviews in Food Science and Food Safety published by Wiley Periodicals LLC on behalf of Institute of Food Technologists.
Références
Abdelraouf, K., Kabbara, S., Ledesma, K. R., Poole, K., & Tam, V. H. (2011). Effect of multidrug resistance-conferring mutations on the fitness and virulence of Pseudomonas aeruginosa. Journal of Antimicrobial Chemotherapy, 66(6), 1311-1317. https://doi.org/10.1093/jac/dkr105
Abraham, S., O'Dea, M., Trott, D. J., Abraham, R. J., Hughes, D., Pang, S., & Gottlieb, T. (2016). Isolation and plasmid characterization of carbapenemase (IMP-4) producing Salmonella enterica Typhimurium from cats. Scientific Reports, 6, 35527. https://doi.org/10.1038/srep35527
Abraham, S., Wong, H. S., Turnidge, J., Johnson, J. R., & Trott, D. J. (2014). Carbapenemase-producing bacteria in companion animals: A public health concern on the horizon. Journal of Antimicrobial Chemotherapy, 69(5), 1155-1157. https://doi.org/10.1093/jac/dkt518
AbuOun, M., O'Connor, H. M., Stubberfield, E. J., Nunez-Garcia, J., Sayers, E., Crook, D. W., & Anjum, M. F. (2020). Characterizing antimicrobial resistant Escherichia coli and associated risk factors in a cross-sectional study of pig farms in Great Britain. Frontiers in Microbiology, 11, 861-861. https://doi.org/10.3389/fmicb.2020.00861
Albiger, B., Glasner, C., Struelens, M. J., Grundmann, H., Monnet, D. L., & The European Survey of Carbapenemase-Producing Enterobacteriaceae (EuSCAPE) working group. (2015). Carbapenemase-producing Enterobacteriaceae in Europe: Assessment by national experts from 38 countries, May 2015. Eurosurveillance, 20(45), 30062. https://doi.org/10.2807/1560-7917.ES.2015.20.45.30062
Al-Marzooq, F., Mohd Yusof, M. Y., & Tay, S. T. (2015). Molecular analysis of antibiotic resistance determinants and plasmids in Malaysian isolates of multidrug resistant Klebsiella pneumoniae. PLoS ONE, 10(7), e0133654. https://doi.org/10.1371/journal.pone.0133654
Amador, P., Fernandes, R., Prudêncio, C., & Duarte, I. (2019). Prevalence of antibiotic resistance genes in multidrug-resistant Enterobacteriaceae on Portuguese livestock manure. Antibiotics, 8(1), 23.
Ambler, R. P., Baddiley, J., & Abraham, E. P. (1980). The structure of β-lactamases. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 289(1036), 321-331. https://doi.org/10.1098/rstb.1980.0049
Anjum, M. F., Choudhary, S., Morrison, V., Snow, L. C., Mafura, M., Slickers, P., & Woodward, M. J. (2011). Identifying antimicrobial resistance genes of human clinical relevance within Salmonella isolated from food animals in Great Britain. Journal of Antimicrobial Chemotherapy, 66(3), 550-559. https://doi.org/10.1093/jac/dkq498
Armstrong, T., Fenn, S. J., & Hardie, K. R. (2021). JMM profile: Carbapenems: A broad-spectrum antibiotic. Journal of Medical Microbiology, 70(12), 001462. https://doi.org/10.1099/jmm.0.001462
Barlow, R. S., McMillan, K. E., Duffy, L. L., Fegan, N., Jordan, D., & Mellor, G. E. (2015). Prevalence and antimicrobial resistance of Salmonella and Escherichia coli from Australian cattle populations at slaughter. Journal of Food Protection, 78(5), 912-920. https://doi.org/10.4315/0362-028x.jfp-14-476
Bennett, P. M. (2008). Plasmid encoded antibiotic resistance: Acquisition and transfer of antibiotic resistance genes in bacteria. British Journal of Pharmacology, 153(S1), S347-S357. https://doi.org/10.1038/sj.bjp.0707607
Bergenholtz, R. D., Jørgensen, M. S., Hansen, L. H., Jensen, L. B., & Hasman, H. (2009). Characterization of genetic determinants of extended-spectrum cephalosporinases (ESCs) in Escherichia coli isolates from Danish and imported poultry meat. Journal of Antimicrobial Chemotherapy, 64(1), 207-209. https://doi.org/10.1093/jac/dkp168
BMEL. (2020). Facts and figures on German agricultural exports. https://www.bmel.de/EN/topics/international-affairs/foreign-trade-policy/facts-figures-german-agricultural-exports.html
Bonardi, S., & Pitino, R. (2019). Carbapenemase-producing bacteria in food-producing animals, wildlife and environment: A challenge for human health. Italian Journal of Food Safety, 8(2), 7956-7956. https://doi.org/10.4081/ijfs.2019.7956
Borowiak, M., Szabo, I., Baumann, B., Junker, E., Hammerl, J. A., Kaesbohrer, A., & Fischer, J. (2017). VIM-1-producing Salmonella Infantis isolated from swine and minced pork meat in Germany. Journal of Antimicrobial Chemotherapy, 72(7), 2131-2133. https://doi.org/10.1093/jac/dkx101
Briñas, L., Zarazaga, M., Sáenz, Y., Ruiz-Larrea, F., & Torres, C. (2002). β-Lactamases in ampicillin-resistant Escherichia coli isolates from foods, humans, and healthy animals. Antimicrobial Agents and Chemotherapy, 46(10), 3156-3163. https://doi.org/10.1128/AAC.46.10.3156-3163.2002
Brodzicki, T. (2020). Agri-food exports of China. https://ihsmarkit.com/research-analysis/agrifood-exports-of-china.html
Brunton, L. A., Duncan, D., Coldham, N. G., Snow, L. C., & Jones, J. R. (2012). A survey of antimicrobial usage on dairy farms and waste milk feeding practices in England and Wales. Veterinary Record, 171(12), 296.
Calbo, E., Freixas, N., Xercavins, M., Riera, M., Nicolás, C., Monistrol, O., & Garau, J. (2011). Foodborne nosocomial outbreak of SHV1 and CTX-M-15-producing Klebsiella pneumoniae: Epidemiology and control. Clinical Infectious Diseases, 52(6), 743-749. https://doi.org/10.1093/cid/ciq238
Card, R., Vaughan, K., Bagnall, M., Spiropoulos, J., Cooley, W., Strickland, T., & Anjum, M. F. (2016). Virulence characterisation of Salmonella enterica isolates of differing antimicrobial resistance recovered from UK livestock and imported meat samples. Frontiers in Microbiology, 7, 640-640. https://doi.org/10.3389/fmicb.2016.00640
Castanheira, M., Deshpande, L. M., Mathai, D., Bell, J. M., Jones, R. N., & Mendes, R. E. (2011). Early dissemination of NDM-1- and OXA-181-producing Enterobacteriaceae in Indian hospitals: Report from the SENTRY Antimicrobial Surveillance Program, 2006-2007. Antimicrobial Agents and Chemotherapy, 55(3), 1274-1278. https://doi.org/10.1128/AAC.01497-10
Centers for Disease Control and Prevention (CDC). (2019). Carbapenem-resistant Enterobacterales (CRE). https://www.cdc.gov/hai/organisms/cre/index.html
Chekabab, S. M., Paquin-Veillette, J., Dozois, C. M., & Harel, J. (2013). The ecological habitat and transmission of Escherichia coli O157:H7. FEMS Microbiology Letters, 341(1), 1-12. https://doi.org/10.1111/1574-6968.12078
Chen, L., Mathema, B., Chavda, K. D., DeLeo, F. R., Bonomo, R. A., & Kreiswirth, B. N. (2014). Carbapenemase-producing Klebsiella pneumoniae: Molecular and genetic decoding. Trends in Microbiology, 22(12), 686-696. https://doi.org/10.1016/j.tim.2014.09.003
Cohen Stuart, J., van den Munckhof, T., Voets, G., Scharringa, J., Fluit, A., & Hall, M. L.-V. (2012). Comparison of ESBL contamination in organic and conventional retail chicken meat. International Journal of Food Microbiology, 154(3), 212-214. https://doi.org/10.1016/j.ijfoodmicro.2011.12.034
Cuzon, G., Naas, T., Truong, H., Villegas, M. V., Wisell, K. T., Carmeli, Y., & Nordmann, P. (2010). Worldwide diversity of Klebsiella pneumoniae that produce beta-lactamase blaKPC-2 gene. Emerging Infectious Diseases, 16(9), 1349-1356. https://doi.org/10.3201/eid1609.091389
D'Agostino, M., & Cook, N. (2016). Foodborne pathogens. In B. Caballero, P. M. Finglas, & F. Toldrá (Eds.), Encyclopedia of food and health (pp. 83-86). Academic Press. https://doi.org/10.1016/B978-0-12-384947-2.00326-3
Davies, J., & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74(3), 417-433. https://doi.org/10.1128/mmbr.00016-10
Davis, G. S., & Price, L. B. (2016). Recent research examining links among Klebsiella pneumoniae from food, food animals, and human extraintestinal infections. Current Environmental Health Reports, 3(2), 128-135. https://doi.org/10.1007/s40572-016-0089-9
D'Costa, V. M., King, C. E., Kalan, L., Morar, M., Sung, W. W. L., Schwarz, C., & Wright, G. D. (2011). Antibiotic resistance is ancient. Nature, 477(7365), 457-461. https://doi.org/10.1038/nature10388
Department for Environment, Food and Rural Affairs (DEFRA). (2012). Sales of antimicrobial products authorized for use as veterinary medicines in the UK in 2011. Author.
Department for Environment, Food and Rural Affairs (DEFRA). (2019). Agriculture in the United Kingdom. https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/950618/AUK-2019-07jan21.pdf
Department for Environment, Food and Rural Affairs (DEFRA). (2020). Food statistics in your pocket: Global and UK supply. https://www.gov.uk/government/statistics/food-statistics-pocketbook/food-statistics-in-your-pocket-global-and-uk-supply
Doi, Y., & Paterson, D. L. (2015). Carbapenemase-producing Enterobacteriaceae. Seminars in Respiratory and Critical Care Medicine, 36(1), 74-84. https://doi.org/10.1055/s-0035-1544208
Doualla-Bell, F., Boyd, D. A., Savard, P., Yousfi, K., Bernaquez, I., Wong, S., & Bekal, S. (2021). Analysis of an IncR plasmid carrying blaNDM-1 linked to an azithromycin resistance region in Enterobacter hormaechei involved in an outbreak in Quebec. Microbiology Spectrum, 9(3), e0199821. https://doi.org/10.1128/spectrum.01998-21
Duggett, N. A., Sayers, E., AbuOun, M., Ellis, R. J., Nunez-Garcia, J., Randall, L., & Anjum, M. F. (2017). Occurrence and characterization of mcr-1-harbouring Escherichia coli isolated from pigs in Great Britain from 2013 to 2015. The Journal of Antimicrobial Chemotherapy, 72(3), 691-695. https://doi.org/10.1093/jac/dkw477
Durso, L. M., & Cook, K. L. (2014). Impacts of antibiotic use in agriculture: What are the benefits and risks? Current Opinion in Microbiology, 19, 37-44. https://doi.org/10.1016/j.mib.2014.05.019
European Centre for Disease Prevention and Control (ECDC). (2019). Carbapenem-resistant Enterobacteriaceae, second update. https://www.ecdc.europa.eu/en/publications-data/carbapenem-resistant-enterobacteriaceae-second-update#no-link
European Food Safety Authority (EFSA). (2011). Scientific Opinion on Campylobacter in broiler meat production: Control options and performance objectives and/or targets at different stages of the food chain. EFSA Journal, 9(4), 2105. https://doi.org/10.2903/j.efsa.2011.2105
European Food Safety Authority (EFSA). (2013). Scientific Opinion on Carbapenem resistance in food animal ecosystems. EFSA Journal, 11(12), 3501. https://doi.org/10.2903/j.efsa.2013.3501
European Food Safety Authority (EFSA). (2018). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal, 16(12), e05500. https://doi.org/10.2903/j.efsa.2018.5500
Faldynova, M., Videnska, P., Havlickova, H., Sisak, F., Juricova, H., Babak, V., & Rychlik, I. (2013). Prevalence of antibiotic resistance genes in faecal samples from cattle, pigs and poultry. Veterinarni Medicina, 58, 298-304. https://doi.org/10.17221/6865-VETMED
Falgenhauer, L., Ghosh, H., Guerra, B., Yao, Y., Fritzenwanker, M., Fischer, J., & Chakraborty, T. (2017). Comparative genome analysis of IncHI2 VIM-1 carbapenemase-encoding plasmids of Escherichia coli and Salmonella enterica isolated from a livestock farm in Germany. Veterinary Microbiology, 200, 114-117. https://doi.org/10.1016/j.vetmic.2015.09.001
Farkas, A., Tarco, E., & Butiuc-Keul, A. (2019). Antibiotic resistance profiling of pathogenic Enterobacteriaceae from Cluj-Napoca, Romania. Germs, 9(1), 17-27. https://doi.org/10.18683/germs.2019.1153
Food and Agriculture Organization (FAO). (2021). FAO in China. http://www.fao.org/china/fao-in-china/china-at-a-glance/en/
Food and Drug Administration (FDA). (2016a). 2015 summary report on antimicrobials sold or distributed for use in food-producing animals. https://www.fda.gov/media/102160/download
Food and Drug Administration (FDA). (2016b). NARMS integrated report: 2012-2013. The National Antimicrobial Resistance Monitoring System: Enteric bacteria. https://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth%20/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoring%20System/UCM453398.pdf
Food and Drug Administration (FDA). (2021). 2020 summary report on antimicrobials sold or distributed for use in food-producing animals. https://www.fda.gov/media/154820/download
Fernández, J., Guerra, B., & Rodicio, M. R. (2018). Resistance to carbapenems in non-typhoidal Salmonella enterica serovars from humans, animals and food. Veterinary Sciences, 5(2), 40. https://doi.org/10.3390/vetsci5020040
Fischer, J., Hille, K., Ruddat, I., Mellmann, A., Köck, R., & Kreienbrock, L. (2017). Simultaneous occurrence of MRSA and ESBL-producing Enterobacteriaceae on pig farms and in nasal and stool samples from farmers. Veterinary Microbiology, 200, 107-113. https://doi.org/10.1016/j.vetmic.2016.05.021
Fischer, J., Rodríguez, I., Schmoger, S., Friese, A., Roesler, U., Helmuth, R., & Guerra, B. (2012a). Escherichia coli producing VIM-1 carbapenemase isolated on a pig farm. Journal of Antimicrobial Chemotherapy, 67(7), 1793-1795. https://doi.org/10.1093/jac/dks108
Fischer, J., Rodríguez, I., Schmoger, S., Friese, A., Roesler, U., Helmuth, R., & Guerra, B. (2012b). Salmonella enterica subsp. enterica producing VIM-1 carbapenemase isolated from livestock farms. Journal of Antimicrobial Chemotherapy, 68(2), 478-480. https://doi.org/10.1093/jac/dks393
Fischer, J., San José, M., Roschanski, N., Schmoger, S., Baumann, B., Irrgang, A., & Guerra, B. (2017). Spread and persistence of VIM-1 carbapenemase-producing Enterobacteriaceae in three German swine farms in 2011 and 2012. Veterinary Microbiology, 200, 118-123. https://doi.org/10.1016/j.vetmic.2016.04.026
Food Standards Agency (FSA). (2020). EU Harmonised Survey of Antimicrobial Resistance (AMR) on retail meats (pork and beef/chicken). Author.
Food Standards Agency (FSA). (2021a). A survey of AMR E. coli on beef and pork on retail sale in the UK (2021). Author.
Food Standards Agency (FSA). (2021b). EU Harmonised Surveillance of Antimicrobial Resistance (AMR) in E. coli from retail meats in the UK (2020-year 6, chicken). https://www.food.gov.uk/research/antimicrobial-resistance/eu-harmonised-surveillance-of-antimicrobial-resistance-amr-in-e-coli-from-retail-meats-in-uk-2020-year-6-chicken
Food Standards Agency (FSA). (2022a). Modelling framework to quantify the risk of AMR exposure via food products - Example of chicken and lettuce. https://www.food.gov.uk/research/antimicrobial-resistance/modelling-framework-to-quantify-the-risk-of-amr-exposure-via-food-products-example-of-chicken-and-lettuce
Food Standards Agency (FSA). (2022b). Survey of Antimicrobial Resistance (AMR) bacteria in lamb and turkey meat on retail sale in the UK. https://www.food.gov.uk/research/antimicrobial-resistance/survey-of-antimicrobial-resistance-amr-bacteria-in-lamb-and-turkey-meat-on-retail-sale-in-the-uk
Gabida, M., Gombe, N. T., Chemhuru, M., Takundwa, L., Bangure, D., & Tshimanga, M. (2015). Foodborne illness among factory workers, Gweru, Zimbabwe, 2012: A retrospective cohort study. BMC Research Notes, 8, 493-493. https://doi.org/10.1186/s13104-015-1512-2
Ghaith, D. M., Zafer, M. M., Ismail, D. K., Al-Agamy, M. H., Bohol, M. F. F., Al-Qahtani, A., & Mostafa, I. Y. (2018). First reported nosocomial outbreak of Serratia marcescens harboring blaIMP-4 and blaVIM-2 in a neonatal intensive care unit in Cairo, Egypt. Infection and Drug Resistance, 11, 2211-2217. https://doi.org/10.2147/IDR.S174869
Grundmann, H., Glasner, C., Albiger, B., Aanensen, D. M., Tomlinson, C. T., Andrasević, A. T., & Brown, D. J. (2017). Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): A prospective, multinational study. The Lancet Infectious Diseases, 17(2), 153-163. https://doi.org/10.1016/S1473-3099(16)30257-2
Guerra, B., Fischer, J., & Helmuth, R. (2014). An emerging public health problem: Acquired carbapenemase-producing microorganisms are present in food-producing animals, their environment, companion animals and wild birds. Veterinary Microbiology, 171(3), 290-297. https://doi.org/10.1016/j.vetmic.2014.02.001
Gullberg, E., Albrecht, L. M., Karlsson, C., Sandegren, L., & Andersson, D. I. (2014). Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. mBio, 5(5), e01918-14. https://doi.org/10.1128/mBio.01918-14
Hartantyo, S. H. P., Chau, M. L., Koh, T. H., Yap, M., Yi, T., Cao, D. Y. H., & Ng, L. C. (2020). Foodborne Klebsiella pneumoniae: Virulence potential, antibiotic resistance and risks to food safety. Journal of Food Protection, 83(7), 1096-1103. https://doi.org/10.4315/jfp-19-520
He, T., Wang, Y., Sun, L., Pang, M., Zhang, L., & Wang, R. (2016). Occurrence and characterization of blaNDM-5-positive Klebsiella pneumoniae isolates from dairy cows in Jiangsu, China. Journal of Antimicrobial Chemotherapy, 72(1), 90-94. https://doi.org/10.1093/jac/dkw357
He, T., Wei, R., Zhang, L., Sun, L., Pang, M., Wang, R., & Wang, Y. (2017). Characterization of NDM-5-positive extensively resistant Escherichia coli isolates from dairy cows. Veterinary Microbiology, 207, 153-158. https://doi.org/10.1016/j.vetmic.2017.06.010
Ho, P.-L., Wang, Y., Liu, M. C.-J., Lai, E. L.-Y., Law, P. Y.-T., Cao, H., & Chow, K.-H. (2018). IncX3 epidemic plasmid carrying blaNDM-5 in Escherichia coli from swine in multiple geographic areas in China. Antimicrobial Agents and Chemotherapy, 62(3), e02295-02217. https://doi.org/10.1128/aac.02295-17
Hopkins, K. L., Findlay, J., Meunier, D., Cummins, M., Curtis, S., Kustos, I., & Woodford, N. (2017). Serratia marcescens producing SME carbapenemases: An emerging resistance problem in the UK? Journal of Antimicrobial Chemotherapy, 72(5), 1535-1537. https://doi.org/10.1093/jac/dkw567
Horton, R. A., Duncan, D., Randall, L. P., Chappell, S., Brunton, L. A., Warner, R., & Teale, C. J. (2016). Longitudinal study of CTX-M ESBL-producing E. coli strains on a UK dairy farm. Research in Veterinary Science, 109, 107-113. https://doi.org/10.1016/j.rvsc.2016.09.018
Huijbers, P. M. C., Blaak, H., de Jong, M. C. M., Graat, E. A. M., Vandenbroucke-Grauls, C. M. J. E., & de Roda Husman, A. M. (2015). Role of the environment in the transmission of antimicrobial resistance to humans: A review. Environmental Science & Technology, 49(20), 11993-12004. https://doi.org/10.1021/acs.est.5b02566
Ibrahim, D. R., Dodd, C. E. R., Stekel, D. J., Ramsden, S. J., & Hobman, J. L. (2016). Multidrug resistant, extended spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from a dairy farm. FEMS Microbiology Ecology, 92(4), fiw013. https://doi.org/10.1093/femsec/fiw013
Iovleva, A., & Doi, Y. (2017). Carbapenem-resistant Enterobacteriaceae. Clinics in Laboratory Medicine, 37(2), 303-315. https://doi.org/10.1016/j.cll.2017.01.005
Irrgang, A., Pauly, N., Tenhagen, B.-A., Grobbel, M., Kaesbohrer, A., & Hammerl, J. A. (2020). Spill-over from public health? First detection of an OXA-48-producing Escherichia coli in a German pig farm. Microorganisms, 8(6), 855.
Janda, J. M., & Abbott, S. L. (2021). The changing face of the family Enterobacteriaceae (order: “Enterobacterales”): New members, taxonomic issues, geographic expansion, and new diseases and disease syndromes. Clinical Microbiology Reviews, 34(2), e00174-00120. https://doi.org/10.1128/CMR.00174-20
Johnson, T. J. (2017). Carbapenemase-producing enterobacteriaceae in swine production in the United States: Impact and opportunities. Antimicrobial Agents and Chemotherapy, 61(2), e02348-02316. https://doi.org/10.1128/AAC.02348-16
Khanna, A., Khanna, M., & Aggarwal, A. (2013). Serratia marcescens - A rare opportunistic nosocomial pathogen and measures to limit its spread in hospitalized patients. Journal of Clinical and Diagnostic Research, 7(2), 243-246. https://doi.org/10.7860/JCDR/2013/5010.2737
Kim, S.-H., Wei, C.-I., Tzou, Y.-M., & An, H. (2005). Multidrug-resistant Klebsiella pneumoniae isolated from farm environments and retail products in Oklahoma. Journal of Food Protection, 68(10), 2022-2029. https://doi.org/10.4315/0362-028x-68.10.2022
Krishnaraju, M., Kamatchi, C., Jha, A., Devasena, N., Vennila, R., Sumathi, G., & Vaidyanathan, R. (2015). Complete sequencing of an IncX3 plasmid carrying blaNDM-5 allele reveals an early stage in the dissemination of the blaNDM gene. Indian Journal of Medical Microbiology, 33(1), 30-38. https://doi.org/10.4103/0255-0857.148373
Li, X., Fu, Y., Shen, M., Huang, D., Du, X., Hu, Q., & Yu, Y. (2018). Dissemination of blaNDM-5 gene via an IncX3-type plasmid among non-clonal Escherichia coli in China. Antimicrobial Resistance and Infection Control, 7, 59-59. https://doi.org/10.1186/s13756-018-0349-6
Liebana, E., Carattoli, A., Coque, T. M., Hasman, H., Magiorakos, A.-P., Mevius, D., & Threlfall, J. (2012). Public health risks of enterobacterial isolates producing extended-spectrum β-lactamases or AmpC β-lactamases in food and food-producing animals: An EU perspective of epidemiology, analytical methods, risk factors, and control options. Clinical Infectious Diseases, 56(7), 1030-1037. https://doi.org/10.1093/cid/cis1043
Liu, B.-T., Zhang, X.-Y., Wan, S.-W., Hao, J.-J., Jiang, R.-D., & Song, F.-J. (2018). Characteristics of carbapenem-resistant Enterobacteriaceae in ready-to-eat vegetables in China. Frontiers in Microbiology, 9, 1147. https://doi.org/10.3389/fmicb.2018.01147
Liu, Z., Xiao, X., Li, Y., Liu, Y., Li, R., & Wang, Z. (2019). Emergence of IncX3 plasmid-harboring blaNDM-5 dominated by Escherichia coli ST48 in a goose farm in Jiangsu, China. Frontiers in Microbiology, 10, 2002. https://doi.org/10.3389/fmicb.2019.02002
López-Rojas, R., Domínguez-Herrera, J., McConnell, M. J., Docobo-Peréz, F., Smani, Y., Fernández-Reyes, M., & Pachón, J. (2011). Impaired virulence and in vivo fitness of colistin-resistant Acinetobacter baumannii. Journal of Infectious Diseases, 203(4), 545-548. https://doi.org/10.1093/infdis/jiq086
Lowrance, T. C., Loneragan, G. H., Kunze, D. J., Platt, T. M., Ives, S. E., Scott, H. M., & Brashears, M. M. (2007). Changes in antimicrobial susceptibility in a population of Escherichia coli isolated from feedlot cattle administered ceftiofur crystalline-free acid. American Journal of Veterinary Research, 68(5), 501-507. https://doi.org/10.2460/ajvr.68.5.501
Magiorakos, A. P., Burns, K., Rodríguez Baño, J., Borg, M., Daikos, G., Dumpis, U., & Weber, J. T. (2017). Infection prevention and control measures and tools for the prevention of entry of carbapenem-resistant Enterobacteriaceae into healthcare settings: Guidance from the European Centre for Disease Prevention and Control. Antimicrobial Resistance and Infection Control, 6, 113-113. https://doi.org/10.1186/s13756-017-0259-z
Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., & Monnet, D. L. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18(3), 268-281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Maron, D. F., Smith, T. J. S., & Nachman, K. E. (2013). Restrictions on antimicrobial use in food animal production: An international regulatory and economic survey. Globalization and Health, 9(1), 48. https://doi.org/10.1186/1744-8603-9-48
McEwen, S. A., & Collignon, P. J. (2018). Antimicrobial resistance: A One Health perspective. Microbiology Spectrum, 6(2). https://doi.org/10.1128/microbiolspec.ARBA-0009-2017
Melander, R. J., Mattingly, A. E., Nemeth, A. M., & Melander, C. (2023). Overcoming intrinsic resistance in gram-negative bacteria using small molecule adjuvants. Bioorganic & Medicinal Chemistry Letters, 80, 129113. https://doi.org/10.1016/j.bmcl.2022.129113
Mills, M. C., & Lee, J. (2019). The threat of carbapenem-resistant bacteria in the environment: Evidence of widespread contamination of reservoirs at a global scale. Environmental Pollution, 255, 113143. https://doi.org/10.1016/j.envpol.2019.113143
Mollenkopf, D. F., Stull, J. W., Mathys, D. A., Bowman, A. S., Feicht, S. M., Grooters, S. V., & Wittum, T. E. (2017). Carbapenemase-producing Enterobacteriaceae recovered from the environment of a swine farrow-to-finish operation in the United States. Antimicrobial Agents and Chemotherapy, 61(2), e01298-16. https://doi.org/10.1128/AAC.01298-16
Morrison, B. J., & Rubin, J. E. (2015). Carbapenemase producing bacteria in the food supply escaping detection. PLoS ONE, 10(5), e0126717. https://doi.org/10.1371/journal.pone.0126717
Mutuku, C., Gazdag, Z., & Melegh, S. (2022). Occurrence of antibiotics and bacterial resistance genes in wastewater: Resistance mechanisms and antimicrobial resistance control approaches. World Journal of Microbiology and Biotechnology, 38(9), 152. https://doi.org/10.1007/s11274-022-03334-0
Navarro-Garcia, F. (2014). Escherichia coli O104:H4 pathogenesis: An enteroaggregative E. coli/Shiga toxin-producing E. coli explosive cocktail of high virulence. Microbiology Spectrum, 2(6). https://doi.org/10.1128/microbiolspec.EHEC-0008-2013
Nordmann, P., Gniadkowski, M., Giske, C. G., Poirel, L., Woodford, N., & Miriagou, V. (2012). Identification and screening of carbapenemase-producing Enterobacteriaceae. Clinical Microbiology and Infection, 18(5), 432-438. https://doi.org/10.1111/j.1469-0691.2012.03815.x
Nordmann, P., Poirel, L., & Dortet, L. (2012). Rapid detection of carbapenemase-producing Enterobacteriaceae. Emerging Infectious Diseases, 18(9), 1503-1507. https://doi.org/10.3201/eid1809.120355
Noster, J., Thelen, P., & Hamprecht, A. (2021). Detection of multidrug-resistant Enterobacterales-From ESBLs to carbapenemases. Antibiotics, 10(9), 1140. https://doi.org/10.3390/antibiotics10091140
Odenthal, S., Akineden, Ö., & Usleber, E. (2016). Extended-spectrum β-lactamase producing Enterobacteriaceae in bulk tank milk from German dairy farms. International Journal of Food Microbiology, 238, 72-78. https://doi.org/10.1016/j.ijfoodmicro.2016.08.036
Office International des Epizooties (OIE). (2018). OIE annual report on antimicrobial agents intended for use in animals. https://www.oie.int/app/uploads/2021/03/annual-report-amr-3.pdf
Office International des Epizooties (OIE). (2019). Survey on monitoring the quantities of antimicrobial agents used in animals in OIE member countries. https://www.woah.org/fileadmin/Home/eng/Our_scientific_expertise/docs/pdf/AMR/Annual_Report_AMR_3.pdf
Özcan, N., Atmaca, S., & Özbek, E. (2022). P11 The ratio and antibiotic resistance profiles of Serratia species among other causative bacteria isolated from blood cultures between 2015 and 2020. JAC-Antimicrobial Resistance, 4(1), dlac004.010. https://doi.org/10.1093/jacamr/dlac004.010
Parkins, M. D., & Gregson, D. B. (2008). Community-acquired Serratia marcescens spinal epidural abscess in a patient without risk factors: Case report and review. The Canadian Journal of Infectious Diseases & Medical Microbiology, 19(3), 250-252. https://doi.org/10.1155/2008/210951
Patel, G., & Bonomo, R. A. (2013). “Stormy waters ahead”: Global emergence of carbapenemases. Frontiers in Microbiology, 4, 48-48. https://doi.org/10.3389/fmicb.2013.00048
Peirano, G., Ahmed-Bentley, J., Fuller, J., Rubin, J. E., & Pitout, J. D. D. (2014). Travel-related carbapenemase-producing Gram-negative bacteria in Alberta, Canada: The first 3 years. Journal of Clinical Microbiology, 52(5), 1575-1581. https://doi.org/10.1128/JCM.00162-14
Peirano, G., Matsumura, Y., Adams, M., Bradford, P., Motyl, M., Chen, L., & Pitout, J. D. D. (2018). Genomic epidemiology of global carbapenemase-producing Enterobacter spp., 2008-2014. Emerging Infectious Disease Journal, 24(6), 1010. https://doi.org/10.3201/eid2406.171648
Peng, Z., Li, X., Hu, Z., Li, Z., Lv, Y., Lei, M., & Wang, X. (2019). Characteristics of carbapenem-resistant and colistin-resistant Escherichia coli co-producing NDM-1 and MCR-1 from pig farms in China. Microorganisms, 7(11), 482.
Pitout, J. D. D., Nordmann, P., & Poirel, L. (2015). Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrobial Agents and Chemotherapy, 59(10), 5873-5884. https://doi.org/10.1128/AAC.01019-15
Podschun, R., & Ullmann, U. (1998). Klebsiella spp. as nosocomial pathogens: Epidemiology, taxonomy, typing methods, and pathogenicity factors. Clinical Microbiology Reviews, 11(4), 589-603.
Poirel, L., Berçot, B., Millemann, Y., Bonnin, R. A., Pannaux, G., & Nordmann, P. (2012a). Carbapenemase-producing Acinetobacter spp. in Cattle, France. Emerging Infectious Diseases, 18(3), 523-525. https://doi.org/10.3201/eid1803.111330
Poirel, L., Bonnin, R. A., & Nordmann, P. (2012b). Genetic features of the widespread plasmid coding for the carbapenemase OXA-48. Antimicrobial Agents and Chemotherapy, 56(1), 559-562. https://doi.org/10.1128/AAC.05289-11
Poirel, L., Carbonnelle, E., Bernabeu, S., Gutmann, L., Rotimi, V., & Nordmann, P. (2012c). Importation of OXA-48-producing Klebsiella pneumoniae from Kuwait. Journal of Antimicrobial Chemotherapy, 67(8), 2051-2052. https://doi.org/10.1093/jac/dks167
Poirel, L., Madec, J.-Y., Lupo, A., Schink, A.-K., Kieffer, N., Nordmann, P., & Schwarz, S. (2018). Antimicrobial resistance in Escherichia coli. Microbiology Spectrum, 6(4). https://doi.org/10.1128/microbiolspec.ARBA-0026-2017
Poletto, R., & Hötzel, M. J. (2012). The Five Freedoms in the global animal agriculture market: Challenges and achievements as opportunities. Animal Frontiers, 2(3), 22-30. https://doi.org/10.2527/af.2012-0045
Potter, R. F., D'Souza, A. W., & Dantas, G. (2016). The rapid spread of carbapenem-resistant Enterobacteriaceae. Drug Resistance Updates, 29, 30-46. https://doi.org/10.1016/j.drup.2016.09.002
Qin, J., Zhao, Y., Wang, A., Chi, X., Wen, P., Li, S., & Xu, H. (2021). Comparative genomic characterization of multidrug-resistant Citrobacter spp. strains in Fennec fox imported to China. Gut Pathogens, 13(1), 59. https://doi.org/10.1186/s13099-021-00458-w
Queenan, A. M., & Bush, K. (2007). Carbapenemases: The versatile β-lactamases. Clinical Microbiology Reviews, 20(3), 440-458. https://doi.org/10.1128/cmr.00001-07
Randall, L., Heinrich, K., Horton, R., Brunton, L., Sharman, M., Bailey-Horne, V., & Jones, J. (2014). Detection of antibiotic residues and association of cefquinome residues with the occurrence of Extended-Spectrum β-Lactamase (ESBL)-producing bacteria in waste milk samples from dairy farms in England and Wales in 2011. Research in Veterinary Science, 96(1), 15-24.
Rayamajhi, N., Kang, S. G., Lee, D. Y., Kang, M. L., Lee, S. I., Park, K. Y., & Yoo, H. S. (2008). Characterization of TEM-, SHV- and AmpC-type β-lactamases from cephalosporin-resistant Enterobacteriaceae isolated from swine. International Journal of Food Microbiology, 124(2), 183-187. https://doi.org/10.1016/j.ijfoodmicro.2008.03.009
Roschanski, N., Fischer, J., Falgenhauer, L., Pietsch, M., Guenther, S., Kreienbrock, L., & Roesler, U. H. (2018). Retrospective analysis of bacterial cultures sampled in German chicken-fattening farms during the years 2011-2012 revealed additional VIM-1 carbapenemase-producing Escherichia coli and a serologically rough Salmonella enterica serovar Infantis. Frontiers in Microbiology, 9, 538. https://doi.org/10.3389/fmicb.2018.00538
Roschanski, N., Friese, A., von Salviati- Claudius, C., Hering, J., Kaesbohrer, A., Kreienbrock, L., & Roesler, U. (2017). Prevalence of carbapenemase producing Enterobacteriaceae isolated from German pig-fattening farms during the years 2011-2013. Veterinary Microbiology, 200, 124-129. https://doi.org/10.1016/j.vetmic.2015.11.030
Rozwandowicz, M., Brouwer, M. S. M., Fischer, J., Wagenaar, J. A., Gonzalez-Zorn, B., Guerra, B., & Hordijk, J. (2018). Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy, 73(5), 1121-1137. https://doi.org/10.1093/jac/dkx488
Schrader, S. M., Botella, H., & Vaubourgeix, J. (2023). Reframing antimicrobial resistance as a continuous spectrum of manifestations. Current Opinion in Microbiology, 72, 102259. https://doi.org/10.1016/j.mib.2022.102259
Seiffert, S. N., Perreten, V., Johannes, S., Droz, S., Bodmer, T., & Endimiani, A. (2014). OXA-48 carbapenemase-producing Salmonella enterica serovar Kentucky isolate of sequence type 198 in a patient transferred from Libya to Switzerland. Antimicrobial Agents and Chemotherapy, 58(4), 2446-2449. https://doi.org/10.1128/AAC.02417-13
Shon, A. S., Bajwa, R. P. S., & Russo, T. A. (2013). Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: A new and dangerous breed. Virulence, 4(2), 107-118. https://doi.org/10.4161/viru.22718
Silva, C., Currie, S., & Igrejas, P. (2019). Extended-spectrum-β-lactamase and carbapenemase-producing Enterobacteriaceae in food-producing animals in Europe. In J. L. Capelo-Martínez & G. Igrejas (Eds.), Antibiotic drug resistance (pp. 261-273). John Wiley & Sons, Inc. https://doi.org/10.1002/9781119282549.ch12
Singh, S. B., Young, K., & Silver, L. L. (2017). What is an “ideal” antibiotic? Discovery challenges and path forward. Biochemical Pharmacology, 133, 63-73. https://doi.org/10.1016/j.bcp.2017.01.003
Suay-García, B., & Pérez-Gracia, M. T. (2019). Present and future of carbapenem-resistant Enterobacteriaceae (CRE) infections. Antibiotics, 8(3), 122.
Temkin, E., Adler, A., Lerner, A., & Carmeli, Y. (2014). Carbapenem-resistant Enterobacteriaceae: Biology, epidemiology, and management. Annals of the New York Academy of Sciences, 1323, 22-42.
U.S. Department of Agriculture (USDA). (2021). Ag and food statistics: Charting the essentials. Author.
Van Boeckel, T. P., Brower, C., Gilbert, M., Grenfell, B. T., Levin, S. A., Robinson, T. P., & Laxminarayan, R. (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences of the United States of America, 112(18), 5649-5654. https://doi.org/10.1073/pnas.1503141112
Vancov, T., & Highway, B. (2010). Antibiotic resistance dissemination and sewage treatment plants.
Velasova, M., Smith, R. P., Lemma, F., Horton, R. A., Duggett, N. A., Evans, J., & Randall, L. P. (2019). Detection of extended-spectrum β-lactam, AmpC and carbapenem resistance in Enterobacteriaceae in beef cattle in Great Britain in 2015. Journal of Applied Microbiology, 126(4), 1081-1095. https://doi.org/10.1111/jam.14211
Wailan, A. M., Paterson, D. L., Caffery, M., Sowden, D., & Sidjabat, H. E. (2015). Draft genome sequence of NDM-5-producing Escherichia coli sequence type 648 and genetic context of blaNDM-5 in Australia. Genome Announcements, 3(2), e00194-00115. https://doi.org/10.1128/genomeA.00194-15
Wallinga, D., & Avinash, K. (2020). New data: Animal vs. human antibiotic use remains lopsided. https://www.nrdc.org/experts/david-wallinga-md/most-human-antibiotics-still-going-us-meat-production
Wang, R., Liu, Y., Zhang, Q., Jin, L., Wang, Q., Zhang, Y., & Wang, H. (2018). The prevalence of colistin resistance in Escherichia coli and Klebsiella pneumoniae isolated from food animals in China: Coexistence of mcr-1 and blaNDM with low fitness cost. International Journal of Antimicrobial Agents, 51(5), 739-744. https://doi.org/10.1016/j.ijantimicag.2018.01.023
Wang, X., Wang, Y., Wang, Y., Zhang, S., Shen, Z., & Wang, S. (2018). Emergence of the colistin resistance gene mcr-1 and its variant in several uncommon species of Enterobacteriaceae from commercial poultry farm surrounding environments. Veterinary Microbiology, 219, 161-164. https://doi.org/10.1016/j.vetmic.2018.04.002
Wang, Y., Zhang, R., Li, J., Wu, Z., Yin, W., Schwarz, S., & Shen, J. (2017). Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production. Nature Microbiology, 2(4), 16260. https://doi.org/10.1038/nmicrobiol.2016.260
Webb, H. E., Bugarel, M., den Bakker, H. C., Nightingale, K. K., Granier, S. A., Scott, H. M., & Loneragan, G. H. (2016). Carbapenem-resistant bacteria recovered from faeces of dairy cattle in the high plains region of the USA. PLoS ONE, 11(1), e0147363. https://doi.org/10.1371/journal.pone.0147363
Widmann, M., Pleiss, J., & Oelschlaeger, P. (2012). Systematic analysis of metallo-β-lactamases using an automated database. Antimicrobial Agents and Chemotherapy, 56(7), 3481-3491. https://doi.org/10.1128/AAC.00255-12
Winokur, P. L., Vonstein, D. L., Hoffman, L. J., Uhlenhopp, E. K., & Doern, G. V. (2001). Evidence for transfer of CMY-2 AmpC β-lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. Antimicrobial Agents and Chemotherapy, 45(10), 2716-2722. https://doi.org/10.1128/aac.45.10.2716-2722.2001
Woodford, N., Wareham, D. W., Guerra, B., & Teale, C. (2013). Carbapenemase-producing Enterobacteriaceae and non-Enterobacteriaceae from animals and the environment: An emerging public health risk of our own making? Journal of Antimicrobial Chemotherapy, 69(2), 287-291. https://doi.org/10.1093/jac/dkt392
World Health Organization (WHO). (2017). Antimicrobial resistance in the food chain. https://www.who.int/foodsafety/areas_work/antimicrobial-resistance/amrfoodchain/en/
World Integrated Trade Solution (WITS). (2021). Food products exports by country in US$ thousand 2019. https://wits.worldbank.org/CountryProfile/en/Country/WLD/Year/2018/TradeFlow/Export/Partner/by-country/Product/16-24_FoodProd
Wu, Z. (2019). Antibiotic use and antibiotic resistance in food-producing animals in China. OECD Publishing. https://doi.org/10.1787/4adba8c1-en
Xiang, R., Zhang, A.-Y., Ye, X.-L., Kang, Z.-Z., Lei, C.-W., & Wang, H.-N. (2018). Various sequence types of Enterobacteriaceae isolated from commercial chicken farms in China and carrying the blaNDM-5 gene. Antimicrobial Agents and Chemotherapy, 62(10), e00779-18. https://doi.org/10.1128/aac.00779-18
Xiao, R., Huang, D., Du, L., Song, B., Yin, L., Chen, Y., & Zeng, G. (2023). Antibiotic resistance in soil-plant systems: A review of the source, dissemination, influence factors, and potential exposure risks. Science of the Total Environment, 869, 161855. https://doi.org/10.1016/j.scitotenv.2023.161855
Xu, Q., Fu, Y., Zhao, F., Jiang, Y., & Yu, Y. (2020). Molecular characterization of carbapenem-resistant Serratia marcescens clinical isolates in a tertiary hospital in Hangzhou, China. Infection and Drug Resistance, 13, 999-1008. https://doi.org/10.2147/IDR.S243197
Yaici, L., Haenni, M., Saras, E., Boudehouche, W., Touati, A., & Madec, J.-Y. (2016). blaNDM-5-carrying IncX3 plasmid in Escherichia coli ST1284 isolated from raw milk collected in a dairy farm in Algeria. Journal of Antimicrobial Chemotherapy, 71(9), 2671-2672. https://doi.org/10.1093/jac/dkw160
Yao, Y., Falgenhauer, L., Falgenhauer, J., Hauri, A. M., Heinmüller, P., Domann, E., & Imirzalioglu, C. (2021). Carbapenem-resistant Citrobacter spp. as an emerging concern in the hospital-setting: Results from a genome-based regional surveillance study. Frontiers in Cellular and Infection Microbiology, 11, 744431. https://doi.org/10.3389/fcimb.2021.744431
Yong, D., Toleman, M. A., Giske, C. G., Cho, H. S., Sundman, K., Lee, K., & Walsh, T. R. (2009). Characterization of a new metallo-beta-lactamase gene, blaNDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrobial Agents and Chemotherapy, 53(12), 5046-5054. https://doi.org/10.1128/AAC.00774-09
Zhang, F., Xie, L., Wang, X., Han, L., Guo, X., Ni, Y., & Sun, J. (2016). Further spread of blaNDM-5 in Enterobacteriaceae via IncX3 plasmids in Shanghai, China. Frontiers in Microbiology, 7, 424. https://doi.org/10.3389/fmicb.2016.00424
Zhang, R., Li, J., Wang, Y., Shen, J., Shen, Z., & Wang, S. (2019). Presence of NDM in non-E. coli Enterobacteriaceae in the poultry production environment. Journal of Antimicrobial Chemotherapy, 74(8), 2209-2213. https://doi.org/10.1093/jac/dkz193
Zhang, R., Liu, L., Zhou, H., Chan, E. W., Li, J., Fang, Y., & Chen, S. (2017). Nationwide surveillance of clinical carbapenem-resistant Enterobacteriaceae (CRE) strains in China. EBioMedicine, 19, 98-106. https://doi.org/10.1016/j.ebiom.2017.04.032
Zhang, W. X., Chen, H. Y., Chen, C., Chen, J. H., Wan, F. S., Li, L. X., & Zhang, J. (2021). Resistance phenotype and molecular epidemiology of carbapenem-resistant Klebsiella pneumoniae isolates in Shanghai. Microbial Drug Resistance, 27(10), 1312-1318. https://doi.org/10.1089/mdr.2020.0390
Zinsstag, J., Meisser, A., Schelling, E., Bonfoh, B., & Tanner, M. (2012). From ‘two medicines’ to ‘One Health’ and beyond. Onderstepoort Journal of Veterinary Research, 79(2), 2012. https://doi.org/10.4102/ojvr.v79i2.492