Prevalence and antibiotic resistance of Campylobacter coli and Campylobacter jejuni in Greek swine farms


Prevalence and antibiotic resistance of Campylobacter coli and Campylobacter jejuni in Greek swine farms


Dimitrios Papadopoulos1, Evanthia Petridou1, (†) Georgios Filioussis1, Theofilos Papadopoulos1, Konstantinos Papageorgiou1, Maria Chatzistilianou2, Spyridon K. Kritas1

1Department of Microbiology and Infectious Diseases, Faculty of Veterinary Medicine, School of Health Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece; 2Clinic of  Pediatrics-Immunology and Infectious Disease, Faculty of Medicine, School of Health Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece


American-Journal-of-Microbiology-and-Immunology

Campylobacter species are one of four key global causes of human diarrheal diseases, according to W.H.O. It is considered to be the most common bacterial cause of human gastroenteritis in the world. The objective of this study was to estimate the prevalence of Campylobacter coli (C. coli) and Campylobacter jejuni (C. jejuni) in Greek commercial swine farms, and describe the antimicrobial resistance of the isolated strains. A total of 1,000 rectal swabs (50 per farm) were collected from twenty swine farms in Greece. Ten rectal samples had been randomly collected from each of five age-groups (suckling piglets, nursery pigs, grower pigs, finisher pigs, sows). Isolation of Campylobacter spp. was performed using the ISO 10272-1:2017. A PCR method, based on the amplification of mapAC.jejuni and ceuEC.coli specific genes, was used for identification of the isolated strains. All isolates were tested for their susceptibility against gentamycin, erythromycin, ciprofloxacin, tetracycline and meropenem; EUCAST guidelines were used for the interpretation. The results showed that 16 out of the 20 farms (80%) and 491 (49%) of the samples were positive for Campylobacter spp.  Prevalence of C.coli was 38% (95% CI 35.1-41.1) and of C.jejuni 10.9% (95% CI 9,1-13.0).  Sows were 1.4 times more likely to be colonized by Campylobacter spp than sucking piglets (p<0.05) while nursery and grower pigs were 2.14 and 2 times more likely to be colonized than sows p<0.001). However, colonization was not associated with farm size.  High rates of resistance were recorded for tetracycline (67,3%), while 18,1%, 7,3% and 3.9% of the isolates were resistant in ciprofloxacin, erythromycin and gentamycin respectively. Thirty-two of the isolates (6,52%) were classified as multidrug resistant; resistance to meropenem was not  found. Our findings indicate high prevalence of C.coli and C.jejuni in Greek pig farms with high resistant rates to tetracycline and ciprofloxacin; this constitutes a potential reservoir for resistance genes spread to the community.


Keywords: Campylobacter, Antimicrobial Resistance, Minimum Inhibitory Concentration (MIC), Antimicrobial Susceptibility Testing (AST), pigs, zoonosis

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How to cite this article:

Dimitrios Papadopoulos, Evanthia Petridou,Georgios Filioussis, Theofilos Papadopoulos, Konstantinos Papageorgiou, Maria Chatzistilianou, Spyridon K. Kritas.Prevalence and antibiotic resistance of Campylobacter coli and Campylobacter jejuni in Greek swine farms. American Journal of Microbiology and Immunology, 2020 5:6. DOI: 10.28933/ajmi-2020-02-2605


References:

1. Havelaar, A.H., Nauta, M.J., Mangen, M.J.J., de Koeijer, A.G., Bogaardt, M.J.,Evers, E.G., Jacobs-Reitsma, W.F., Pelt, W., van Wagenaar, J.A., de Wit, G.A.,van der Zee, H., 2005. Costs and benefits of controlling campylobacter in The Netherlands — integrating risk analysis, epidemiology and economics. RIVM Report 250911009/2005.
2. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017
3. Jackson BR, Zegarra JA, Lopez-Gatell H, Sejvar J, Arzate F, WatermanS, Nunez AS, Lopez B, Weiss J, Cruz RQ, Murrieta DY, Luna-GierkeR, Heiman K, Vieira AR, Fitzgerald C, Kwan P, Zarate-Bermudez M,Talkington D, Hill VR, Mahon B. 2014. Binational outbreak of Guillain-Barre syndrome associated with Campylobacter jejuni infection,Mexico and USA, 2011. Epidemiol Infect 142:1089–1099. dx.doi.org/10.1017/S0950268813001908
4. Koga M, Gilbert M, Li J, Koike S, Takahashi M, Furukawa K, Hirata K, Yuki N. (2005).Antecedent infections in Fisher syndrome: a common pathogenesis of molecular mimicry. Neurology 64:1605–1611.
dx.doi.org/10.1212/01.WNL.0000160399.08456.7C
5. Gradel KO, Nielsen HL, Schonheyder HC, Ejlertsen T, Kristensen B,Nielsen H. (2009). Increased short-and long-term risk of inflammatorybowel disease after Salmonella or Campylobactergastroenteritis.Gastroenterology137:495501.
dx.doi.org/10.1053/j.gastro.2009.04.001
6. Quintana-Hayashi, M. P., and Thakur, S. (2012). Longitudinal study of the persistence of antimicrobial-resistant Campylobacter strains in distinct swine production systems on farms, at slaughter, and in the environment. Appl. Environ. Microbiol. 78, 2698–2705. doi: 10.1128/AEM.07723-11
7. Avrain, L., Humbert, F., Sanders, P., Vernozy-Rozand, C., and Kempf, I. (2004). Antimicrobial resistance in Campylobacter from pigs in French slaughterhouses. Rev. Med. Vet. 155, 156–158
8. Sifre, E., Salha, B. A., Ducournau, A., Floch, P., Chardon, H., Megraud, F., et al. (2015). EUCAST recommendations for antimicrobial susceptibility testing applied to the three main Campylobacter species isolated in humans. J. Microbiol. Methods 119, 206–213. doi: 10.1016/j.mimet.2015.10.018
9. WHO Estimates of the Global Burden of Foodborne Diseases: Foodborne Disease Burden Epidemiology Reference Group 2007-2015, WHO, Geneva (2018)
10. Massipab C., Guet-Revilletab H., Grareab M. , Sommetcd A., Duboisab D. (2018). Enhanced culture recovery of Campylobacter with modified Cary-Blair medium: A practical field experienceJournal of Microbiological Methods149: 53-54 doi.org/10.1016/j.mimet.2018.05.001
11. ISO 10272-1:2017, Microbiology of the food chain- Horizontal method for detection and enumeration of Campylobacter spp. Part 1: Detection method. Geneva : ISO.
12. Protocol for PCR amplification of C.jejuni and C.coli, recommended by the EURL-AR, 2nd version, 2013.
13. M. Denis, C. Soumet, K. Rivoal, G. Ermel, D. Blivet, G. Salvat and P. Colin (1999).Development of a m-PCR assay for simultaneous identification of Campylobacter jejuniand C. coli. Letters in Applied Microbiology, 29, 406–410
14. European Committee on Antimicrobial Susceptibility Testing . Breakpoint tables for interpretation of MICs and zone diameters. Version 8.1, 2018.
15. Magiorakos A.-P., Srinivasan A., Carey R. B., et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection. 2012;18(3):268–281. doi: 10.1111/j.1469-0691.2011.03570.x.
16. Milnes, A. S., Stewart, I., Clifton-Hadley, F. A., Davies, R. H., Newell, D. G., Sayers, A. R., et al. (2008). Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica, in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol. Infect. 136, 739–751. doi: 10.1017/S0950268807009223
17. Tadesse, D. A., Bahnson, P. B., Funk, J. A., Thakur, S., Morrow, W. E., Wittum, T., et al. (2011). Prevalence and antimicrobial resistance profile of Campylobacter spp. isolated from conventional and antimicrobial-free swine production systems from differentU.S. regions. Foodborne Pathog. Dis. 8, 367–374. doi:10.1089/fpd.2010.0665
18. Haruna, M., Sasaki, Y., Murakami, M., Mori, T., Asai, T., Ito, K., et al. (2013). Prevalence and antimicrobial resistance of Campylobacter isolates from beef cattle and pigs in Japan. J. Vet. Med. Sci. 75, 625–628. doi: 10.1292/jvms.12-0432European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J. 2018, 16, 5500
19. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC).2017.The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016.EFSA Journal 2017;15(12):5077. doi: 10.2903/j.efsa.2017.5077
20. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC).2018.The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017.EFSA Journal EFSA Journal 2018;16(12):5500. doi: 10.2903/j.efsa.2018.5500
21. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC).2019.The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017.EFSA Journal 2019;17(2):5598. doi: 10.2903/j.efsa.2019.5598.