High antimicrobial resistance in Salmonella spp. and Escherichia coli isolates from swine fecal samples submitted to a veterinary diagnostic laboratory in Colombia
DOI:
https://doi.org/10.17533/udea.rccp.v35n1a03Keywords:
antibiotic, antimicrobial resistance, bacterial resistance, Escherichia coli, multi-resistance, multi-resistant bacteria, pigs, Salmonella spp., use of antimicrobialsAbstract
Background: Commensal microflora such as Escherichia coli and Enterococcus spp. are representative indicators of antimicrobial resistance (AMR) as they are part of the normal intestinal microflora and can acquire and disseminate AMR to pathogenic or zoonotic bacteria like Salmonella spp. Objective: To investigate the state of AMR among E. coli and Salmonella spp., potential pathogens in humans, isolated from cecal contents of pigs submitted to a veterinary diagnostic laboratory in Colombia from 2016 to 2019. Methods: Susceptibility testing was conducted using the Kirby-Bauer disk diffusion method according to the Clinical and Laboratory Standards Institute guidelines for antimicrobial zone diameter breakpoints. An E. coli strain (ATCC 25922) was used as the quality control organism. Isolates showing resistance to three or more antimicrobial classes were classified as multidrug-resistant (MDR) as defined by a joint group of the European Centre for Disease prevention and Control and the Center for Disease Control and Prevention of the USA. Results: A total of 112 E. coli and 192 Salmonella spp. colonies were isolated from 557 samples received between 2016 and 2019. In order of decreasing frequency, E. coli was resistant to tetracycline (100%), sulfamethoxazol-trimethoprim (97.5%), amoxicillin (86.4%), enrofloxacin (82.6%), tylosin (82.1%), doxycycline (59%), neomycin (50%), ciprofloxacin (45.5%), ceftiofur (35%), gentamicin (30%), tilmicosin (29%), and fosfomycin (12.5%). When compared with E. coli, Salmonella spp. was generally resistant to the same agents with slightly less resistance (between 10-30%) to eight of the antimicrobials tested. Salmonella spp. showed <20% resistance to three antimicrobials, as follows: neomycin (17%), gentamicin (16%), and fosfomycin (14%). Multi-resistance occurred in 68.7% (77/112) of E. coli and 70.3% (135/192) of Salmonella spp. isolates. Resistance of Salmonella spp. was alarming to all the critically important antimicrobials tested: fluoroquinolones (enrofloxacin, ciprofloxacin), ceftiofur (thirdgeneration cephalosporin), and macrolides (tylosin). Conclusions: According to our results, there is a high level of multidrug resistance (MDR) in E. coli and Salmonella spp. It is necessary to implement a nationwide antimicrobial resistance monitoring program in Colombia, together with proper antimicrobial prescribing guidelines for pigs. The indiscriminate use of antimicrobial growth promoters by the swine industry is generating widespread bacterial resistance and should be discontinued.
Downloads
References
Aidara-Kane A, Angulo FJ, Conly JM, Minato Y, Silbergeld EK, McEwen SA, Collignon PJ. World Health Organization (WHO) guidelines on use of medically important antimicrobials in food-producing animal. Antimicrob Resist Infect Control 2018; 7: 7. https://doi.org/10.1186/s13756-017-0294-9
Angulo FJ, Nunnery JA, Bair HD. Antimicrobial resistance in zoonotic enteric pathogens. Rev Sci Tech 2004; 23(2): 485-496. https://doi.org/10.20506/rst.23.2.1499
Arenas NE, Moreno-Melo V. Livestock production and emergency antibiotic resistance in Colombia: systematic review. Infectious 2018; 22(2): 110-119. https://doi.org/10.22354/in.v22i2.717
Ayala-Romero C, Ballen-Parada C, Rico-Gaitán M, Chamorro-Tobar I, Zambrano-Moreno D, Poutou-Piñales R, Carrascal-Camacho A. Prevalence of Salmonella spp. in mesenteric pig´s ganglia at Colombian slaughter houses. Rev MVZ Córdoba 2018; 23(1): 6474-6486. https://doi.org/10.21897/rmvz.1242
Belluco S, Barco L, Roccato A, Ricci A. Variability of Escherichia coli and Enterobacteriaceae counts on pig carcasses: A systematic review. Food Control 2005; 55: 115-126. https://doi.org/10.1016/j.foodcont.2015.02.042
Campos J, Mourão, Peixe L, Antunes P. Non-typhoidal Salmonella in the pig production chain: a comprehensive analysis of its impact on human health. Pathogens 2019; 8(1): 19. https://doi.org/10.3390/pathogens8010019
CLSI. Performance Standards for Antimicrobial Dick and Dilutions Susceptibility Test for Bacteria Isolated from Animals. 4th Edition. CLSI Supplement Vet08. Wayne, PA, 2018.
Cutler R, Gleeson B, Page S, Norris J, Browning G. Antimicrobial prescribing guidelines for pigs. Aust Vet J 2020; 98: 105-134. https://doi.org/10.1111/avj.12940
De Briyne N, Atkinson J, Pokludová L, Borriello SP. Antibiotics used most commonly to treat animals in Europe. Vet Rec 2014; 174(13): 325. https://doi.org/10.1136/vr.102462
European Food Safety Authority (EFSA). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J 2013; 11: 3129. https://doi.org/10.2903/j.efsa.2013.3129
European Food Safety Authority (EFSA). The European Union summary on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J 2019; 17(2): e05598. https://doi.org/10.2903/j.efsa.2018.5500
Giraldo-Cardona JP, Gualdrón-Ramírez D, Chamorro-Tobar I, Pulido-Villamarín A, Santamaría-Durán N, Castañeda-Salazar R, Zambrano-Moreno C, Carrascal-Camacho AK. Salmonella spp. prevalence, antimicrobial resistance and risk factor determination in Colombian swine farms. Pesq Vet Bras 2019; 39(10). https://doi.org/10.1590/1678-5150-pvb-6156
Haley CA, Dargatz DA, Bush EJ, Erdman MM, Ferdorka-Cray PJ. Salmonella prevalence and antimicrobial susceptibility from the National Animal Health Monitoring System Swine 2000 and 2006 Studies. J Food Prot 2012; 75(3): 428-436. https://doi.org/10.4315/0362-028X.JFP-11-363
Kadykalo S, Anderson MEC, Alsop JE. Passive surveillance of antimicrobial resistance in Salmonella and Escherichia coli isolates from Ontario livestock, 2007-2015. Can Vet J 2018; 59: 617-622. [access December 15th, 2020] URL: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5949941/pdf/cvj_06_617.pdf
Karp BE, Tate H, Plumblee JR, Dessai U, Whichard JM, Thacker EL, Hale KR, Wilson W, Friedman CR, Griffin PM, McDermott PF. 2017. National Antimicrobial Resistance Monitoring System: two decades of advancing public health through surveillance of antimicrobial resistance. Foodborne Pathog Dis 2017; 14(10): 545-557. https://doi.org/10.1089/fpd.2017.2283
Kidsley AK, Abraham S, Bell JM, O’Dea M, Laird TJ, Jordan D, Mitchell P, McDevitt CA, Trott DJ. Antimicrobial susceptibility of Escherichia coli and Salmonella spp. isolates from healthy pigs in Australia: results of a Pilot national survey. Front Microbial 2018; 9: 1207. https://doi.org/10.3389/fmicb.2018.01207
Lester SC, Pla MP, Wang F, Perez-Schael I, Jiang H, O´Brien TF. The carriage of Escherichia coli resistant to antimicrobial agents by healthy children in Boston, in Caracas, Venezuela, and in Qin Pu, China. N Engl J Med 1990; 323(5): 285-289. https://doi.org/10.1056/NEJM199008023230501
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect Dis 2012; 18: 268-281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Magnusson U, Sternberg S, Eklund G, Rozstalnyy A. Prudent and efficient use of antimicrobials in pigs and poultry. FAO Animal Production and Health Manual 23. Rome. FAO, 2019
Nijsten R, London N, Van den Bogaard A, Stobberingh E. In vitro transfers of antibiotic resistance between faecal Escherichia coli strains isolated from pig farmers and pigs. J Antimicrob Chemother 1996; 37(6): 1141-1154. https://doi.org/10.1093/jac/37.6.1141
Van den Bogaard AE, London N, Stobberingh EE. Antimicrobial in pig faecal samples from The Netherlands (five abattoirs) and Sweden. J Antimicrob Chemother 2000; 45: 663-671. https://doi.org/10.1093/jac/45.5.663
WHO Guidelines on Use of Medically Important Antimicrobials in Food-Producing Animals. 2017. Geneva: World Health Organization. [access December 15th, 2020] URL: https://www.ncbi.nlm.nih.gov/books/NBK487966/
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Revista Colombiana de Ciencias Pecuarias
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
The authors enable RCCP to reprint the material published in it.
The journal allows the author(s) to hold the copyright without restrictions, and will allow the author(s) to retain publishing rights without restrictions.