Determination of antibiotic resistance through three phenotypical methods in Campylobacter coli strains isolated from chicken meat marketed in Lima, Peru
DOI:
https://doi.org/10.17843/rpmesp.2025.422.14330Keywords:
Antibiotic Resistance, Campylobacter coli, chicken, meat, Minimum Inhibitory ConcentrationAbstract
Objectives. To determine the resistance and minimum inhibitory concentration (MIC) of erythromycin, azithromycin, ciprofloxacin, and tetracycline in Campylobacter coli strains isolated from chicken carcasses sold in Lima, Peru. Materials and methods. Cryopreserved strains of C. coli (n=106) were reactivated and then we evaluated concordance
(Kappa coefficient) of the resistance and MIC results between the disk diffusion (DD), E-test (ET), and microdilution plate (MDP) tests. Results. We reactivated 97 strains, of which 94 to 100% were resistant to ciprofloxacin, erythromycin, and tetracycline, while only 58% were resistant to azithromycin in the DD test. The ET and MDP tests showed 78 to 100% of resistant strains, with azithromycin having the lowest percentage of resistance. More than 70% of strains were resistant to at least three antibiotics in all three tests. In addition, 50%, 69%, and 100% of strains had a MIC ≥ 32 μg/mL for ciprofloxacin, azithromycin, and tetracycline/erythromycin, respectively. Conclusions. C. coli strains from chicken carcasses had a high percentage of multidrug resistance. The concordance between the three tests was almost perfect, but the ET strips showed maximum concentrations that are insufficient for MIC in these strains. We recommend resistance and MIC testing using MDP, as it allows for a wider range of antibiotic concentrations to be used.
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References
MIDAGRI. Panorama y perspectivas de la producción de pollo en el Perú, 2020 [Internet]. Lima: Dirección General De Políticas Agrarias, MIDAGRI; 2020. [citado el 10 de agosto de 2024]. Disponible en: https://cdn.www.gob.pe/uploads/document/file/696596/panorama-carne_de_pollo.pdf.
OMS. Resistencia a los antimicrobianos. 2020 [Internet]. Centro de Prensa, OMS; 2020 [citado el 15 de diciembre de 2023]. Disponible en: https://www.who.int/es/news-room/fact-sheets/detail/resistencia-a-los-antibióticos
Ardoino SM, Toso RE, Alvarez HL, Mariani EL, Cachau PD, Mancilla MV, et al. Antimicrobial as growth promoters (AGP) in poultry balanced feed: use, bacterial resistance, new alternatives and replacement
options. Cienc Vet. 2017;19(1):50–66. doi: 10.19137/cienvet-20171914
Quino W, Caro-Castro J, Hurtado V, Flores-León D, Gonzalez-Escalona N, Gavilan RG. Genomic Analysis and Antimicrobial Resistance of Campylobacter jejuni and Campylobacter coli in Peru. Front
Microbiol. 2022;12:802404. doi: 10.3389/fmicb.2021.802404.
Cooper KK, Mourkas E, Schiaffino F, Parker CT, Pinedo Vasquez TN, Garcia Bardales PF, et al. Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon. MBio. 2025;16(2):e0205424. doi:10.1128/mbio.02054-24.
CLSI. M07. Methods for Dilution Antimicrobial Susceptibility Test for Bacteria that grow Aerobically. 9th ed. Guidelines Clinical and Laboratory Standards Institute. 2012.
Syal K, Mo M, Yu H, Iriya R, Jing W, Guodong S, et al. Current and emerging techniques for antibiotic susceptibility tests. Theranostics. 2017;7(7):1795–805. doi: 10.7150/thno.19217.
CLSI. M45. Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. 3rd ed. Clinical and Laboratory Standards Institute. 2015.
Jiménez MA, Galas M, Corso A, Hormazábal JC, Duarte Valderrama C, Salgado Marcano N, et al. Consenso latinoamericano para definir, categorizar y notificar patógenos multirresistentes, con resistencia extendida o panresistentes. Rev Panam Salud Pública. 2019;1–8. doi: 10.26633/RPSP.2019.65.
Kouglenou SD, Agbankpe AJ, Dougnon V, Djeuda AD, Deguenon E, Hidjo M, et al. Prevalence and susceptibility to antibiotics from Campylobacter jejuni and Campylobacter coli isolated from chicken meat in southern Benin, West Africa. BMC Res Notes. 2020;13(1):1–6. doi: 10.1186/s13104-020-05150-x.
Hadi Ghaffoori Kanaan M, Jebur Obayes Al-Isawi A, Ahmad Mohamme F. Antimicrobial Resistance and Antibiogram of Thermotolerant Campylobacter Recovered from Poultry Meat in Baghdad Markets, Iraq. Arch Razi Inst. 2022;77(1):249–55. doi: 10.22092/ARI.2021.356362.1828.
Santos‐ferreira N, Ferreira V, Teixeira P. Occurrence and Multidrug Resistance of Campylobacter in Chicken Meat from Different Production Systems. Foods. 2022;11(13): 1827. doi: 10.3390/foods11131827.
Gimenez G, Weiler N, Nuñez L, Orrego MV, Cardozo L, Cantero G. Typification and evaluation of the antimicrobial sensitivity of Campylobacter jejuni and Campylobacter coli strains from chickens from Bajo Chaco - Paraguay, 2018 - 2020. Compend Ciencias Vet. 2022;12(1):14–9. doi: 10.18004/compend.cienc.vet.2022.12.01.14.
Gunasekaran K, Vellapandi S, Chitra AM, Kumaragurubaran K. Virulence, MLST analysis, and antimicrobial resistance of Campylobacter coli isolated from broiler chickens in Tamil Nadu, India. Iran
J Vet Res. 2022;23(2):128–36. doi: 10.22099/IJVR.2022.42199.6135.
Lee J, Jeong J, Lee H, Ha J, Kim S, Choi Y, et al. Antibiotic susceptibility, genetic diversity, and the presence of toxin producing genes in campylobacter isolates from poultry. Int J Environ Res Public Health. 2017;14(11). doi: 10.3390/ijerph14111400.
Lim SK, Moon DC, Chae MH, Kim HJ, Nam HM, Kim SR, et al. Macrolide resistance mechanisms and virulence factors in erythromycin-resistant campylobacter species isolated from chicken and swine feces and carcasses. J Vet Med Sci. 2016;78(12):1791–5. doi: 10.1292/jvms.16-0307.
Pergola S, Franciosini MP, Comitini F, Ciani M, De Luca S, Bellucci S, et al. Genetic diversity and antimicrobial resistance profiles of Campylobacter coli and Campylobacter jejuni isolated from broiler
chicken in farms and at time of slaughter in central Italy. J Appl Microbiol. 2017;122(5):1348–56. doi: 10.1111/jam.13419.
Wieczorek K, Wolkowicz T, Osek J. Antimicrobial resistance and virulence-associated traits of Campylobacter jejuni isolated from poultry food chain and humans with diarrhea. Front Microbiol. 2018;9. doi: 10.3389/fmicb.2018.01508.
Changkwanyeun R, Yamaguchi T, Kongsoi T, Changkaew K, Yokotama K, Kim H, Suthienkul O, et al. Impact of mutations in DNA gyrase genes on quinolone resistance in Campylobacter jejuni. Drug Test Anal. 2016;8(10):1071–1076. doi: 10.1002/dta.1937
Bolinger H, Kathariou S. The current state of macrolide resistance in Campylobacter spp.: Trends and impacts of resistance mechanisms. Applied and Environmental Microbiology. 2017;83(12):1–9. doi:
1128/AEM.00416-17.
Abdi-Hachesoo B, Khoshbakht R, Sharifiyazdi H, Tabatabaei M, Hosseinzadeh S, Asasi K. Tetracycline Resistance Genes in Campylobacter jejuni and C. coli Isolated From Poultry Carcasses.
Jundishapur J Microbiol. 2014;7(9):12129. doi: 10.5812/JJM.12129.
Sierra-Arguello YM, Quedi Furian T, Perdoncini G, Moraes HLS, Salle CTP, Rodrigues LB, et al. Fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli from poultry and human samples assessed by PCR-restriction fragment length polymorphism assay. PLoS One. 2018;13(7):1-9. doi: 10.1371/journal.pone.0199974.
Suman-Kumar M, Ramees TP, Dhanze H, Gupta S, Dubal ZB, Kumar A. Occurrence and antimicrobial resistance of Campylobacter isolates from broiler chicken and slaughter house environment in India. Anim Biotechnol. 2023;34(2):199–207. doi: 10.1080/10495398.2021.1953514.
Paravisi M, Laviniki V, Bassani J, Kunert Filho HC, Carvalho D, Wilsmann DE, et al. Antimicrobial resistance in campylobacter jejuni isolated from Brazilian poultry slaughterhouses. Braz J Poult Sci. 2020;22(2):1–10. doi: 10.1590/1806-9061-2020-1262.
Hull DM, Harrell E, van Vliet AHM, Correa M, Thakur S. Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019. PLoS One. 2021;16(2):e0246571. doi: 10.1371/journal.pone.0246571.
Sadeghi A, Ganji L, Fani F, Pouladfar G, Eslami P, Doregiraee F, et al. Prevalence, species diversity, and antimicrobial susceptibility of Campylobacter strains in patients with diarrhea and poultry meat samples: one-year prospective study. Iran J Microbiol. 2022;14(3):362–72. doi: 10.18502/ijm.v14i3.9775.
Avrain L, Humbert F, L’Hospitalier R, Sanders P, Vernozy-Rozand C, Kempf I. Antimicrobial resistance in Campylobacter from broilers: Association with production type and antimicrobial use. Vet Microbiol. 2003;96(3):267–76. doi: 10.1016/j.vetmic.2003.07.001.
Gatica-Eguiguren MA, Rojas H. Gestión sanitaria y resistencia a los antimicrobianos en animales de producción. Rev Peru Med Exp Salud Publica. 2018;35(1):118. doi: 10.17843/rpmesp.2018.351.3571.
Myintzaw P, Jaiswal AK, Jaiswal S, Myintzaw P. A Review on Campylobacteriosis Associated with Poultry Meat Consumption Food Rev Int. 2023;39(4):2107–2121. doi: 10.1080/87559129.2021.1942487.
Amjad M, Zia U-U-R. Poultry as A Source and Reservoir for Campylobacteriosis. Eur J Vet Med. 2023;3(1):11–17. doi: 10.24018/ejvetmed.2023.3.1.87.
Harvey SA, Winch PJ, Leontsini E, Torres Gayoso C, López Romero S, Gilman RH, et al. Domestic poultry-raising practices in a Peruvian shantytown: Implications for control of Campylobacter jejuni-associated diarrhea. Acta Trop. 2003;86(1):41–54. doi: 10.1016/S0001-706X(03)00006-8.
Pollet S, Rocha C, Zerpa R, Lilian P, Valencia A, Maximo C, et al. Campylobacterantimicrobial resistance in Peru: a ten-year observational study. BMC Infect Dis. 2012;12(193). doi: 10.1186/1471-2334-12-193.
Schiaffino F, Colston JM, Paredes-Olortegui M, François R, Pisanic N, Burga R, et al. Antibiotic resistance of Campylobacter species in a pediatric cohort study. Antimicrob Agents Chemother. 2019;63(2):1–10. doi: 10.1128/AAC.01911-18.
Al-Natour MQ, Alaboudi AR, Osaili TM, Obaidat MM. Resistance of Campylobacter jejuni Isolated from Layer Farms in Northern Jordan Using Microbroth Dilution and Disc Diffusion Techniques. J Food Sci. 2016;81(7):M1749–M1753. doi: 10.1111/1750-3841.13363.
Azrad M, Tkhawkho L, Isakovich N, Nitzan O, Peretz A. Antimicrobial susceptibility of Campylobacter jejuni and Campylobacter coli: Comparison between Etest and a broth dilution method. Ann Clin Microbiol Antimicrob. 2018;17(1):1–5. doi: 10.1186/s12941-018-0275-8.
Lazou TP, Chaintoutis SC. Comparison of disk diffusion and broth microdilution methods for antimicrobial susceptibility testing of Campylobacter isolates of meat origin. J Microbiol Methods. 2023;204:106649. doi: 10.1016/j.mimet.2022.106649.
Casagrande P, Pergola S, Bellucci S, Menchetti L, Miraglia D, Franciosini MP. Occurrence and antimicrobial susceptibility of Campylobacter spp. on fresh and refrigerated chicken meat products in
Central Italy. Poult Sci. 2018;97(8):2895–901. doi: 10.3382/ps/pey147.
Choi JH, Moon DC, Mechesso AF, Kang HY, Kim SJ, Song HJ, et al. Antimicrobial resistance profiles and macrolide resistance mechanisms of campylobacter coli isolated from pigs and chickens. Microorganisms. 2021;9(5). doi: 10.3390/microorganisms9051077.
Tedersoo T, Roasto M, Mäesaar M, Häkkinen L, Kisand V, Ivanova M, et al. Antibiotic Resistance in Campylobacter spp. Isolated from Broiler Chicken Meat and Human Patients in Estonia. Microorganisms. 2022;10(5):1–10. doi: 10.3390/microorganisms10051067.
Melo RT, Grazziotin AL, Júnior ECV, Prado RR, Mendonça EP, Monteiro GP, et al. Evolution of Campylobacter jejuni of poultry origin in Brazil. Food Microbiol. 2019;82:489–96. doi: 10.1016/j.fm.2019.03.009.
Zhang Q, Beyi AF, Yin Y. Zoonotic and antibiotic-resistant Campylobacter: a view through the One Health lens. One Heal Adv. 2023;1(1):1–9. doi: 10.1186/s44280-023-00003-1.
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Copyright (c) 2025 Kiara N. Cáceres-Bautista, Jorge L. Arroyo-Acevedo, Hugo J. Justil-Guerrero, Johnny A. Tinco-Jayo, Edwin C. Enciso-Roca, Enrique J. Aguilar-Felices, Miguel A. Rojas-Montes, Diego Diaz-Coahila, César A. Lázaro-de la Torre

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