Skip to main content
SpringerLink
Log in

First study in the frequency of isolation and phenotypic antimicrobial resistance profiles of pig and cattle origin Campylobacter strains in Romania

  • Brief Report
  • Published:
Veterinary Research Communications Aims and scope Submit manuscript

Abstract

Campylobacter spp. is recognized as one of the most common pathogens involved in the development of gastrointestinal infections in humans. The current study aimed to enhance the knowledge on the occurrence and molecular characterization of Campylobacter spp. in pigs and cattle origin caecum samples (n = 56) collected in one year, from nine Romanian slaughterhouses, and to determine the antimicrobial resistance profile of the isolated strains. All Campylobacter spp. strains (n = 41) isolated from swine and cattle caecum samples were analyzed in terms of antimicrobial resistance, in accordance with the EURL protocol and with the Commission Implementing Decision No. 2020/1729. The prevalence rate for C. coli. in pig caecum samples was 92.3% (36/39), and the prevalence of C. jejuni, in cattle origin samples was 29.4% (5/17). C. coli strains isolated from pigs proved resistant to tetracycline 75% (27/36), ciprofloxacin 69.4% (25/36), erythromycin 8.3% (3/36), ertapenem 2.8% (1/36) and gentamicin 2.8% (1/36), but no resistance was observed towards chloramphenicol. C. jejuni strains originating from cattle expressed resistance to ciprofloxacin 60.0% (3/5) and tetracycline 20.0% (1/5), but they were susceptible to chloramphenicol, erythromycin, ertapenem and gentamicin. In the present study, 19.5% (7/36) C. coli strains isolated from pigs were identified as multidrug-resistant (MDR) bacteria. The obtained results demonstrated that pigs especially, but cattle to, can be considered important natural reservoirs for zoonotic multidrug-resistant Campylobacter strains, having a stimulating effect for further studies aiming at the molecular screening of the genotypic antimicrobial resistance processing of a higher number of samples.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data availability

No datasets were generated or analysed during the current study.

References

  • Abley MJ, Wittum TE, Moeller SJ, Zerby HN, Funk JA (2012) Quantification of Campylobacter in swine before, during, and after the slaughter process. J Food Prot 75:139–143

    Article  CAS  PubMed  Google Scholar 

  • Boes J, Nersting L, Nielsen EM, Kranker S, EnØe C, Wachmann HC, Baggesen L (2005) Prevalence and diversity of Campylobacter jejuni in pig herds on farms with and without cattle or poultry. J Food Prot 68:722–727

    Article  CAS  PubMed  Google Scholar 

  • Catalano A, Iacopetta D, Ceramella J, Scumaci D, Giuzio F, Saturnino C, Aquaro S, Rosano C, Sinicropi MS (2022) Multidrug resistance (MDR): a widespread phenomenon in pharmacological therapies. Molecules 27:616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chatre P, Haenni M, Meunier D, Botrel MA, Calavas D, Madec JY (2010) Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from cattle between 2002 and 2006 in France. J Food Prot 73:825–831

    Article  PubMed  Google Scholar 

  • Choi JH, Moon DC, Mechesso AF, Kang HY, Kim SJ, Song HJ, Yoon SS, Lim SK (2021) Antimicrobial Resistance profiles and Macrolide Resistance mechanisms of Campylobacter coli isolated from pigs and chickens. Microorganisms 9:1077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dotmatics® Available online at (2023) https://www.graphpad.com/quickcalcs/contingency1/ Accessed November 13

  • European Commission. Commission Implementing Decision (EU) (2020) /1729 of 17 November 2020 on the Monitoring and Reporting of Antimicrobial Resistance in Zoonotic and Commensal Bacteria and Repealing Implementing Decision 2013/652/EU; Official Journal of the European Union: Luxembourg, 2020; pp. 8–21. Available online: http://data.europa.eu/eli/dec_impl/2020/1729/oj. Accessed November 02, 2023

  • European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC) (2023) The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2020/2021. EFSA J 21:e07867

    PubMed  Google Scholar 

  • European Food Safety Authority; European Centre for Disease Prevention and Control (2022) The European Union One Health 2021 Zoonoses Report. EFSA J 20:e07666

    Google Scholar 

  • Eurostat Agricultural production – livestock and meat. Available online: https://ec.europa.eu/eurostat/statistics-explained/index.php?oldid=427096. Accessed December, 15

  • Fitzgerald C (2015) Campylobacter. Clin Lab Med 35:289–298

    Article  PubMed  Google Scholar 

  • Fonseca M, Heider LC, Stryhn H, McClure JT, Léger D, Rizzo D, Warder L, Dufour S, Roy JP, Kelton DF, Rnaud D, Barkema HW, Sanchez J (2023) Antimicrobial use and its association with the isolation of and antimicrobial resistance in Campylobacter spp. recovered from fecal samples from Canadian dairy herds: a cross-sectional study. Prev Vet Med 215:105925

    Article  PubMed  Google Scholar 

  • Gwimi PB, Faleke OO, Salihu MD, Magaji AA, Abubakar MB, Nwankwo IO, Ibitoye EB (2015) Prevalence of Campylobacter species in fecal samples of pigs and humans from Zuru Kebbi State, Nigeria. Int J One Health 1:1–5

    Article  Google Scholar 

  • Hailu W, Helmy YA, Carney-Knisely G, Kauffman M, Fraga D, Rajashekara G (2021) Prevalence and Antimicrobial Resistance profiles of Foodborne pathogens isolated from Dairy Cattle and Poultry Manure Amended Farms in Northeastern Ohio, the United States. Antibiotics 10:1450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hakkinen M, Heiska H, Hänninen ML (2007) Prevalence of Campylobacter spp. in cattle in Finland and antimicrobial susceptibilities of bovine Campylobacter jejuni strains. Appl Environ Microbiol 73:3232–3238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haruna M, Sasaki Y, Murakami M, Mori T, Asai T, Ito K, Yamada Y (2013) Prevalence and antimicrobial resistance of Campylobacter isolates from beef cattle and pigs in Japan. J Vet Med Sci 75:625–628

    Article  PubMed  Google Scholar 

  • Huang J, Zang X, Lei T, Ren F, Jiao X (2020) Prevalence of Campylobacter spp. in Pig Slaughtering line in Eastern China: analysis of Contamination sources. Foodborne Pathog Dis 17:712–719

    Article  CAS  PubMed  Google Scholar 

  • Hudson LK, Andershock WE, Yan R, Golwalkar M, M’ikanatha NM Nachamkin I, Thomas LS, Moore C, Qian X, Steece R et al (2021) Phylogenetic analysis reveals source attribution patterns for Campylobacter spp. in Tennessee and Pennsylvania. Microorganisms 9:2300

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishihara K, Yamamoto T, Satake S, Takayama S, Kubota S, Negishi H, Kojima A, Asai T, Sawada T, Takahashi T et al (2006) Comparison of Campylobacter isolated from humans and food-producing animals in Japan. J Appl Microbiol 100:153–160

    Article  CAS  PubMed  Google Scholar 

  • ISO 10272-1:2017 (2017) Microbiology of the Food Chain—Horizontal Method for detection and enumeration of Campylobacter spp.—Part 1: detection method. International Organization for Standardization, Geneva, Switzerland

    Google Scholar 

  • Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM (2015) Global Epidemiology of Campylobacter Infection. Clin Microbiol Rev 28:687–720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kempf I, Kerouanton A, Bougeard S, Nagard B, Rose V, Mourand G, Osterberg J, Denis M, Bengtsson BO (2017) Campylobacter coli in organic and conventional pig production in France and Sweden: prevalence and antimicrobial resistance. Front Microbiol 8:955

    Article  PubMed  PubMed Central  Google Scholar 

  • Linton D, Lawson AJ, Owen RJ, Stanley J (1997) PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. J Clin Microbiol 35:2568–2572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B et al (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–281

    Article  CAS  PubMed  Google Scholar 

  • Marin C, Lorenzo-Rebenaque L, Moreno-Moliner J, Sevilla-Navarro S, Montero E, Chinillac MC, Jordá J, Vega S (2021) Multidrug-resistant campylobacer jejuni on Swine Processing at a slaughterhouse in Eastern Spain. Animals 11:1339

    Article  PubMed  PubMed Central  Google Scholar 

  • Meistere I, Ķibilds J, Eglīte L, Alksne L, Avsejenko J, Cibrovska A, Makarova S, Streikiša M, Grantiņa-Ieviņa L, Bērziņ A (2019) Campylobacter species prevalence, characterisation of antimicrobial resistance and analysis of whole-genome sequence of isolates from livestock and humans, Latvia, 2008 to 2016. Eurosurveill 24:1800357

  • Munroe D, Prescott J, Penner J (1983) Campylobacter jejuni and Campylobacter coli serotypes isolated from chickens, cattle, and pigs. J Clin Microbiol 18:877–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popa SA, Morar A, Ban-Cucerzan A, Imre K (2022a) Last decade mini-review of the scientific progresses in the monitoring of the occurrence and antimicrobial susceptibility profile of poultry origin Campylobacter spp. within the European Union countries. Rev Rom Med Vet 32:75–82

  • Popa SA, Morar A, Ban-Cucerzan A, Tîrziu E, Herman V, Sallam KI, Morar D, Acaroz U, Imre M, Florea T et al (2022b) Occurrence of Campylobacter spp. and phenotypic antimicrobial resistance profiles of Campylobacter jejuni in slaughtered broiler chickens in North-Western Romania. Antibiotics 11:1713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Protocol for Isolation (Dec. 2020) Identification and storage of Campylobacter jejuni and/or C. Coli for the EU monitoring of antimicrobial resistance. EURL

  • Ramonaitė S, Rokaitytė A, Tamulevičienė E, Malakauskas A, Alter T, Malakauskas M (2013) Prevalence, quantitative load and genetic diversity of Campylobacter spp. in dairy cattle herds in Lithuania. Acta Vet Scand 55:87

    Article  PubMed  PubMed Central  Google Scholar 

  • Rukambile E, Sintchenko V, Muscatello G, Kock R, Alders R (2019) Infection, colonization and shedding of Campylobacter and Salmonella in animals and their contribution to human disease: a review. Zoonoses Public Health 66(6):562–578

    Article  PubMed  Google Scholar 

  • Sallam KI, Abd-Elghany SM, Hussein MA, Imre K, Morar A, Morshdy AE, Sayed-Ahmed MZ (2020) Microbial decontamination of beef carcass surfaces by lactic acid, acetic acid, and trisodium phosphate sprays. BioMed Res. Int 2020:2324358

  • Sato K, Bartlett P, Kaneene J, Downes F (2004) Comparison of prevalence and antimicrobial susceptibilities of Campylobacter spp. isolates from organic and conventional dairy herds in Wisconsin. Appl Environ Microbiol 70:1442–1447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheppard SK, Dallas JF, Strachan NJ, MacRae M, Mc Carthy ND, Wilson DJ, Gormley FJ, Falush D, Oqden ID, Maiden MC et al (2009) Campylobacter genotyping to determine the source of human infection. Clin Infect Dis 48:1072–1078

    Article  PubMed  Google Scholar 

  • Sithole V, Amoako DG, Abia ALK, Perrett K, Bester LA, Essack SY (2021) Occurrence, Antimicrobial Resistance, and molecular characterization of Campylobacter spp. in Intensive Pig Production in South Africa. Pathogens 10:439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanley K, Jones K (2003) Cattle and sheep farms as reservoirs of Campylobacter. J Appl Microbiol 94:104s–113s

    Article  PubMed  Google Scholar 

  • Tedersoo T, Roasto M, Mäesaar M, Fredriksson-Ahomaa M, Meremäe K (2023) Antimicrobial Resistance of Campylobacter coli isolated from Caecal Samples of fattening pigs at Slaughter. Microorganisms 11:1540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thépault A, Poezevara T, Quesne S, Rose V, Chemaly M, Rivoal K (2018) Prevalence of thermophilic Campylobacter in catle production at slaughterhouse level in France and link between C. Jejuni bovine strains and campylobacteriosis. Front Microbiol 9:471

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

This research is supported by the project “Increasing the impact of excellence research on the capacity for innovation and technology transfer within ULST Timișoara” code 6PFE, submitted in the competition Program 1—development of the national system of research—development, Subprogram 1.2—institutional performance, institutional development projects—development projects of excellence in RDI.

Author information

Authors and Affiliations

  1. Department of Animal Production and Veterinary Public Health, Faculty of Veterinary Medicine, University of Life Sciences “King Mihai I” from Timişoara, Calea Aradului No. 119, Timisoara, 300645, Romania

    Sebastian Alexandru Popa, Adriana Morar, Alexandra Ban-Cucerzan, Emil Tîrziu, Răzvan-Tudor Pătrînjan & Kálmán Imre

  2. Department of Infectious Diseases and Preventive Medicine, Faculty of Veterinary Medicine, University of Life Sciences “King Mihai I” from Timişoara, Timisoara, Romania

    Viorel Herman

  3. Department of Parasitology and Dermatology, Faculty of Veterinary Medicine, University of Life Sciences “King Michael I” from Timişoara, Timisoara, Romania

    Mirela Imre & Tiana Florea

  4. Department of Internal Medicine, Faculty of Veterinary Medicine, University of Life Sciences “King Mihai I” from Timişoara, Timisoara, Romania

    Doru Morar

Authors
  1. Sebastian Alexandru Popa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adriana Morar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexandra Ban-Cucerzan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emil Tîrziu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Viorel Herman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mirela Imre
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tiana Florea
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Doru Morar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Răzvan-Tudor Pătrînjan
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kálmán Imre
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: S.A.P and K.I; Methodology: A. B-C and R.T.P; Validation: A. B-C, E.T, V.H and M.I; Formal analysis: A.M, M.I, T.F; Investigation: S.A.P and K.I; Resources: E.T; Data curation: S.A.P and T.F; Writing—original draft preparation: S.A.P and K.I; Review and editing: A.M, A B-C, D.M, and K.I; Visualization: R.T.P; Supervision: A.M, E.T, and V.H; Funding acquisition: V.H.

Corresponding authors

Correspondence to Sebastian Alexandru Popa or Kálmán Imre.

Ethics declarations

Ethical approval

This study did not make use of live sentient animals. Ethics approval was not required as per the Animal Research Ethics Board – University of Life Sciences “King Mihai I” from Timișoara, Romania.

Competing interests

All authors have read and approved the final manuscript. Its contents are solely the responsibility of the authors. The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Popa, S.A., Morar, A., Ban-Cucerzan, A. et al. First study in the frequency of isolation and phenotypic antimicrobial resistance profiles of pig and cattle origin Campylobacter strains in Romania. Vet Res Commun (2024). https://doi.org/10.1007/s11259-024-10360-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11259-024-10360-w

Keywords

Search

Navigation