Skip to main content
SpringerLink
Log in

Prevalence of Arcobacter and Campylobacter in beef meat samples and characterization of the recovered isolates

  • Research Article
  • Published:
Journal of Consumer Protection and Food Safety Aims and scope Submit manuscript

Abstract

The present study aimed to isolate Arcobacter spp. and Campylobacter spp. from beef meat samples including cattle carcasses, cube meat and minced meat, and to determine the antibacterial susceptibility and genetic diversity of the recovered isolates. One hundred beef carcass surface samples from slaughterhouses and 100 beef meat samples (50 samples of cube meat and 50 minced meat) taken from different retail units were analysed. Of the examined samples, 17 (8.5%) and 43 (21.5%) were positive for Arcobacter spp. and Campylobacter spp. respectively. Twenty Arcobacter and 53 Campylobacter isolates were obtained from positive samples. Both Arcobacter and Campylobacter were concurrently isolated from 7 (3.5%) of the 17 positive samples. Arcobacter butzleri (18 isolates) and Campylobacter jejuni (37 isolates) were the most commonly isolated species. The results of Enterobacterial Repetitive Intergenic Consensus Polymerase Chain Reaction revealed extensive genetic heterogeneity among both Arcobacter and Campylobacter isolates. Seventeen and 30 different genotypes were identified in 18 A. butzleri and 37 C. jejuni isolates, respectively. Each of A. cryaerophilus, C. fetus and C. hyointestinalis isolates had two genotypes. Three and seven genotypes were identified in five C. lari and in seven C. coli isolates, respectively. While 5% of 20 Arcobacter isolates were resistant to amoxicillin-clavulanic acid, 5% of the isolates were resistant to neomycin. Of the 53 Campylobacter isolates, 9.43%, 22.64%, 7.54% and 3.77% were resistant to enrofloxacin, neomycin, tetracycline and streptomycin, respectively. Contaminated beef carcasses, cube meat and minced meat with various species and subspecies of arcobacters and campylobacters may pose a risk factor for human infections. Our study reveals the necessity of improving the hygiene quality in slaughterhouses and other meat processing units as there are different sources of contamination.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aarestrup FM, Nielsen EM, Madsen M, Engberg J (1997) Antimicrobial susceptibility patterns of thermophilic Campylobacter spp. from humans, pigs, cattle, and broilers in Denmark. Antimicrob Agents Chemother 41:2244–2250

    CAS  PubMed  PubMed Central  Google Scholar 

  • Abay S, Kayman T, Hizlisoy H, Aydin F (2012) In vitro antibacterial susceptibility of Arcobacter butzleri isolated from different sources. J Vet Med Sci 74:613–616

    CAS  PubMed  Google Scholar 

  • Abay S, Kayman T, Otlu B, Hizlisoy H, Aydin F, Ertas N (2014) Genetic diversity and antibiotic resistance profiles of Campylobacter jejuni isolates from poultry and humans in Turkey. Int J Food Microbiol 178:29–38

    CAS  PubMed  Google Scholar 

  • Aksu H, Bostan K, Aydın A (1997) İstanbul’da tüketime sunulan ham kıymalarda Campylobacter jejuni’nin mevcudiyeti üzerine bir araştırma. YYU Vet Fak Derg 8:102–104

    Google Scholar 

  • Aydin F, Gumuşsoy KS, Atabay HI, Iça T, Abay S (2007a) Prevalence and distribution of Arcobacter species in various sources in Turkey and molecular analysis of isolated strains by ERIC-PCR. J Appl Microbiol 103:27–35

    CAS  PubMed  Google Scholar 

  • Aydin F, Gumussoy KS, Ica T, Sumerkan B, Esel D, Akan M, Ozdemir A (2007b) The prevalence of Campylobacter jejuni in various sources in Kayseri, Turkey, and molecular analysis of isolated strains by PCR-RFLP. Turk J Vet Anim Sci 31:13–19

    CAS  Google Scholar 

  • Balamurugan S, Nattress FM, Baker LP, Dilts BD (2011) Survival of Campylobacter jejuni on beef and pork under vacuum packaged and retail storage conditions: examination of the role of natural meat microflora on C. jejuni survival. Food Microbiol 28:1003–1010

    PubMed  Google Scholar 

  • Bauer AW, Kirby WMM, Sherris JC, Turek M (1966) Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 45:493–496

    CAS  PubMed  Google Scholar 

  • Bostan K, Aksu H, Özgen O, Uğur M (2001) Effects of refrigerated and frozen storage on the survival of Campylobacter jejuni in ground and cubed beef. Pak J Biol Sci 4:888–890

    Google Scholar 

  • Bostan K, Aydın A, Ang MK (2009) Prevalence and antibiotic susceptibility of thermophilic Campylobacter species on beef, mutton, and chicken carcasses in Istanbul, Turkey. Microb Drug Resist 15:143–149

    CAS  PubMed  Google Scholar 

  • Cloak OM, Duffy G, Sheridan JJ, Blair IS, McDowell DA (2001) A survey on the incidence of Campylobacter spp. and the development of a surface adhesion polymerase chain reaction (SA-PCR) assay for the detection of Campylobacter jejuni in retail meat products. Food Microbiol 18:287–298

    CAS  Google Scholar 

  • CLSI (2008) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard-third edition M31-A3 vol. 28 no. 8 replaces M31-A2 vol. 22 no. 6. (Wayne, PA)

  • CLSI (2010) Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, twentieth informational supplement M100-S20. Vol. 30, no. 1 replaces M100-S19 vol. 29 no. 3. Wayne, Pennsylvania

  • Collado L, Figueras MJ (2011) Taxonomy, epidemiology, and clinical relevance of the Genus Arcobacter. Clin Microbiol Rev 24:174–192

    CAS  PubMed  PubMed Central  Google Scholar 

  • Córdoba-Calderón O, Redondo-Solano M, Castro-Arias E, Arias-EchandI ML (2017) Arcobacter isolation from minced beef samples in Costa Rica. J Food Protoc 80:775–778

    Google Scholar 

  • Diker KS (1985) Studies on the identification of Campylobacter species isolated from sheep and cattle. Doğa Bilim Dergisi 9:232–240

    Google Scholar 

  • Duffy LL, Fegan N (2012) Prevalence and concentration of Arcobacter spp. on Australian beef carcasses. J Food Protoc 75:1479–1482

    Google Scholar 

  • Elmalı M, Can HY (2017) Occurence and antimicrobial resistance of Arcobacter species in food and slaughterhouse samples. Food Sci Technol Camp 37(2):280–285

    Google Scholar 

  • Ferreira S, Queiroz JA, Oleastro M, Domingues FC (2016) Insights in the pathogenesis and resistance of Arcobacter: a review. Crit Rev Microbiol 42:364–383

    CAS  PubMed  Google Scholar 

  • González M, Mikkelä A, Tuominen P, Ranta J, Hakkinen M, Hänninen ML, Llarena AK (2016) Campylobacter spp. in the food chain and in the environment. Evira’s Res Rep 2:25–30

    Google Scholar 

  • Grau FH (1988) Campylobacter jejuni and Campylobacter hyointestinalis in the intestinal tract and on the carcasses of calves and cattle. J Food Protoc 51:857–861

    Google Scholar 

  • Gregory M, Klein B, Sahin O, Girgis G (2018) Isolation and characterization of Campylobacter hepaticus from layer chickens with spotty liver disease in the United States. Avian Dis 62(1):79–85

    PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hong J, Kim JM, Jung WK, Kim SH, Bae W, Koo HC, Gil J, Kim M, Ser J, Park YH (2007) Prevalence and antibiotic resistance of Campylobacter spp. isolated from chicken meat, pork, and beef in Korea, from 2001 to 2006. J Food Protoc 70:860–866

    CAS  Google Scholar 

  • Houf K, Tutenel A, De Zutter L, Van Hoof J, Vandamme P (2000) Development of a multiplex PCR assay for the simultaneous detection and identification of Arcobacter butzleri, Arcobacter cryaerophilus and Arcobacter skirrowii. FEMS Microbiol Lett 193:89–94

    CAS  PubMed  Google Scholar 

  • Houf K, de Zutter L, van Hoof J, Vandamme P (2002) Assessment of the genetic diversity among arcobacters isolated from poultry products by using two PCR-based typing methods. Appl Environ Microbiol 68:2172–2178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu TT, Lee J (2015) Global distribution and prevalence of Arcobacter in food and water. Zoonoses Public Health 62:579–589

    PubMed  Google Scholar 

  • ISO (2006) Horizontal method for detection and enumeration of Campylobacter spp.—part 1: detection method. ISO 10272- 1:2006, CH-1211 Geneve, Switzerland

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kabeya H, Maruyama S, Morita Y, Ohsuga T, Ozawa S, Kobayashi Y, Abe M, Katsube Y, Mikami T (2004) Prevalance of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. Int J Food Microbiol 90:303–308

    CAS  PubMed  Google Scholar 

  • Kaur T, Singh J, Huffman MA, Petrzelková KJ, Taylor NS, Xu S, Dewhirst FE, Paster BJ, Debruyne L, Vandamme P, Fox JG (2011) Campylobacter troglodytis sp. nov., isolated from feces of human-habituated wild chimpanzees (Pan troglodytes schweinfurthii) in Tanzania. Appl Environ Microbiol 77(7):2366–2373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kayman T, Abay S, Hızlısoy H (2013) Identification of Campylobacter spp. isolates with phenotypic methods and multiplex polymerase chain reaction and their antibiotic susceptibilities. Mikrobiyol Bul 47:230–239

    CAS  PubMed  Google Scholar 

  • Kramer JM, Frost JA, Bolton FJ, Wareing DRA (2000) Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. J Food Protoc 63:1654–1659

    CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA Sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  • Lee MH, Cheon DS, Choi S, Lee BH, Jung JY, Choi C (2010) Prevalence of Arcobacter species isolated from retail meats in Korea. J Food Protoc 73:1313–1316

    CAS  Google Scholar 

  • Little CL, Richardson JF, Owen RJ, de Pinna E, Threlfall EJ (2008) Campylobacter and Salmonella in raw red meats in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003–2005. Food Microbiol 25:538–543

    CAS  PubMed  Google Scholar 

  • Liu F, Ma R, Wang Y, Zhang L (2018) The clinical importance of Campylobacter concisus and other human hosted Campylobacter species. Front Cell Infect Microbiol 8:1–22

    Google Scholar 

  • Madden RH, Espie WE, Moran L, McBride J, Scates P (2001) Occurrence of Escherichia coli O157:H7, Listeria monocytogenes, Salmonella and Campylobacter spp. on beef carcasses in Northern Ireland. Meat Sci 58:343–346

    CAS  PubMed  Google Scholar 

  • Milesi S (2010) Università degli Studi di Milano graduate school of veterinary sciences for animal health and food safety Doctoral Program in Animal Nutrition and Food Safety Academic Year: 2009–2010, pp 50–51

  • Modirrousta S, Shapouri R, Rezasoltani S, Molaabaszadeh H (2016) Prevalence of Campylobacter spp. and their common serotypes in 330 cases of red-meat, chicken-meat and egg-shell in Zanjan City, Iran. Infect Epidemiol Med 2:8–10

    Google Scholar 

  • Nieva-Echevarria B, Martinez-Malaxetxebarria I, Girbau C, Alonso R, Fernández-Astorga A (2013) Prevalence and genetic diversity of Arcobacter in food products in the North of Spain. J Food Protoc 76:1447–1450

    Google Scholar 

  • Ongor H, Cetinkaya B, Acık MN, Atabay HI (2004) Investigation of arcobacters in meat and faecal samples of clinically healthy cattle in Turkey. Lett Appl Microbiol 38:339–344

    CAS  PubMed  Google Scholar 

  • Pérez-Cataluña A, Salas-Massó N, Diéguez AL, Balboa S, Lema A, Romalde JL, Figueras MJ (2018) Revisiting the taxonomy of the Genus Arcobacter: getting order from the Chaos. Front Microbiol 9:2077

    PubMed  PubMed Central  Google Scholar 

  • Rahimi E, Ameri M, Kazemeini HR (2010) Prevalence and antimicrobial resistance of Campylobacter species isolated from raw camel, beef, lamb and goat meat in Iran. Foodborne Pathog Dis 7:443–447

    CAS  PubMed  Google Scholar 

  • Rahimi E, Ameri M, Alimoradi M, Chakeri A, Bahrami AR (2013) Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from raw camel, beef, and water buffalo meat in Iran. Comp Clin Pathol 22:467–473

    CAS  Google Scholar 

  • Ramees TP, Dhama K, Karthik K, Rathore RS, Kumar A, Saminathan M, Tiwari R, Malik YS, Singh RK (2017) Arcobacter: an emerging food-borne zoonotic pathogen, its public health concerns and advances in diagnosis and control-a comprehensive review. Vet Q 37:136–161

    PubMed  Google Scholar 

  • 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 5:55–87

    Google Scholar 

  • Sammarco ML, Ripabelli G, Fanelli I, Grasso GM, Tamburro M (2010) Prevalence and biomolecular characterization of Campylobacter spp. isolated from retail meat. J Food Protoc 73:720–728

    CAS  Google Scholar 

  • Savasan S, Ciftci A, Diker S (2004) Emergence of quinolone resistance among chicken isolates of Campylobacter in Turkey. Turk J Vet Anim Sci 28:391–397

    Google Scholar 

  • Scullion R, Harrington CS, Madden RH (2006) Prevalence of Arcobacter spp. in raw milk and retail raw meats in northern Ireland. J Food Protoc 69:1986–1990

    Google Scholar 

  • Silva J, Leite D, Fernandes M, Mena C, Gibbs PA, Teixeira P (2011) Campylobacter spp. as a foodborne pathogen: a review. Front Microbiol 27:1–12

    Google Scholar 

  • Villarruel-López A, Márquez-González M, Garay-Martínez LE, Zepeda H, Castillo A, Mota de la Garza L, Murano EA, Torres-Vitela R (2003) Isolation of Arcobacter spp. from retail meats and cytotoxic effects of isolates against vero cells. J Food Protoc 66:1374–1378

    Google Scholar 

  • Vipham J, Brooks C, Miller M, Brashears M, Echeverry AA (2016) Survey of Campylobacter in beef cuts at retail. Beef research online. http://www.beefresearch.org/CMDocs/BeefResearch/Safety_Project_Summaries/FY09_A_survey_of_Campylobacter_in_beef_cuts.pdf. Accessed 12 Dec 2016

  • Wang G, Clark CG, Taylor TM, Pucknell C, Barton C, Price L, Woodward DL, Rodgers FG (2002) Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol 40:4744–4747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zacharow I, Bystron J, Wałecka-Zacharska E, Podkowik M, Bania J (2015) Prevalence and antimicrobial resistance of Arcobacter butzleri and Arcobacter cryaerophilus isolates from retail meat in Lower Silesia region, Poland. Pol J Vet Sci 18:63–69

    CAS  PubMed  Google Scholar 

Download references

Funding

Data relating to the isolation, identification and antibacterial susceptibility of the Campylobacter spp. in this study belongs to Aydın Yağiz’s MSc thesis. Aydın Yağiz’s MSc thesis was supported by the Scientific Research Council of Erciyes University, Kayseri, Turkey (Project no. TSY-11-3415). The authors would like to thank the Scientific Research Council of Erciyes University for the support.

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Veterinary Medicine, Erciyes University, Kayseri, Turkey

    Fuat Aydin & Seçil Abay

  2. Ministry of Agriculture and Forestry, General Directorate of Food and Control, Ankara, Turkey

    Aydın Yağiz

  3. Department of Microbiology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey

    Hamit Kaan Müştak

  4. Department of Microbiology, Faculty of Veterinary Medicine, Adnan Menderes University, Aydın, Turkey

    Kadir Serdar Diker

Authors
  1. Fuat Aydin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aydın Yağiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seçil Abay
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hamit Kaan Müştak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kadir Serdar Diker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seçil Abay.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aydin, F., Yağiz, A., Abay, S. et al. Prevalence of Arcobacter and Campylobacter in beef meat samples and characterization of the recovered isolates. J Consum Prot Food Saf 15, 15–25 (2020). https://doi.org/10.1007/s00003-019-01268-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00003-019-01268-8

Keywords

Search

Navigation