The incidence and antimicrobial resistance of Arcobacter species in animal and poultry meat samples at slaughterhouses in Iran
,
Abstract
Background and Objectives: Arcobacter species are food-borne and zoonotic enteropathogens. Defined breakpoints for the investigation of antimicrobial resistance of Arcobacter are missing.
Materials and Methods: The study was performed to investigate the incidence and antimicrobial resistance of Arcobacter species in animals and poultry meat samples procured from slaughterhouses in Iran. To investigate the prevalence of antimicrobial resistance, samples were collected from cattle (n=100), sheep (n=100), goat (n=100), broiler chicken (n=100), turkey (n=100) and quail (n=100). Arcobacter isolates of meat samples were isolated, investigated by PCR method and antibiotic resistance was also investigated. The susceptibility was assessed by Kirby-Bauer disc diffusion.
Results: The results showed that 52 samples (8.66%) were positive for Arcobacter spp. The most prevalence were observed in broiler chickens (26%, n=26 samples), quail (13%, n=13 samples), turkey (8%, n=8), cattle (3%, n=3), sheep (1%, n=1) and goat (1%, n=1). Arcobacter butzleri had highest prevalence among Arcobacter species. All the isolates showed sensitivity to gentamicin, streptomycin and tetracycline.
Conclusion: Poultry meat is a potential source of infection with Arcobacter that must be considered in slaughterhouses in Iran. Arcobacter species showed sensitivity for a broad spectrum of antibiotics that can be used during infection with Arcobacter species.
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2. Aydin F, Yağiz A, Abay S. Prevalence of Arcobacter and Campylobacter in beef meat samples and characterization of the recovered isolates. J Consum Prot Food Saf 2020; 15:15-25.
3. Ferreira S, Queiroz JA, Oleastro M, Domingues F. Insights in the pathogenesis and resistance of Arcobacter: a review. Crit Rev Microbiol 2016; 42:364-383.
4. Fanelli F, Pinto AD, Mottola A, Mule G, Chieffi D, Baruzzi F, et al. Genomic characterization of Arcobacter butzleri isolated from shellfish: novel insight into antibiotic resistance and virulence determinants. Front Microbiol 2019; 10: 670.
5. Collado L, Figueras MJ. Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin Microbiol Rev 2011; 24:174-192.
6. Park S, Jung YT, Kim S, Yoon JH. Arcobacter acticola sp. Nov isolated from seawater on the east sea in south Korea. J Microbiol 2016; 54:655-659.
7. Chieffi D, Fanelli F, Fusco V. Arcobacter butzleri: Up-to-date taxonomy, ecology, and pathogenicity of an emerging pathogen. Compr Rev Food Sci Food Saf 2020; 19:2071-2109.
8. Collado L, Levican A, Perez J, Figueras MJ. Arcobacter defluvii sp. nov., isolated from sewage samples. Int J Syst Evol Microbiol 2011; 61:2155-2161.
9. Lee C, Agidi S, Marion JW, Lee J. Arcobacter in Lake Erie beach waters: an emerging gastrointestinal pathogen linked with human-associated fecal contamination. Appl Environ Microbiol 2012; 78:5511-5519.
10. De Smet S, De Zutter L, Van Hende J, Houf K. Arcobacter contamination on pre- and post-chilled bovine carcasses and in minced beef at retail. J Appl Microbiol 2010; 108:299-305.
11. Van Driessche E, Houf K, Van Hoof J, De Zutter L, Vandamme P. Isolation of Arcobacter species from animal feces. FEMS Microbiol Lett 2003; 229:243-248.
12. Dekker DD, Eibach KG, Boahen C, Wiafe Akenten Y, Pfeifer AE, Zautner E, et al. Fluoroquinolone-resistant Salmonella enterica, Campylobacter spp., and Arcobacter butzleri from local and imported poultry meat in Kumasi, Ghana. Foodborne Pathog Dis 2019; 16: 352-358.
13. Skirrow MB (2000). Clinical aspects of Campylobacter infection, in: I.Nachamkin, M.J. Blaser (Eds.), Campylobacter, second ed., ASM Press, Washington, DC. 69-88.
14. Kabeya H, Maruyama S, Morita Y, Ohsuga T, Ozawa S, Kobayashi Y, et al. Prevalence of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. Int J Food Microbiol 2004; 90:303-308.
15. Abay S, Kayman T, Hizlisoy H, Aydin F. In vitro antibacterial susceptibility of Arcobacter butzleri isolated from different sources. J Vet Med Sci 2012; 74:613-616.
16. Shirzad Aski H, Tabatabaei M, Khoshbakht R, Raeisi M. Occurrence and antimicrobial resistance of emergent Arcobacter spp. isolated from cattle and sheep in Iran. Comp Immunol Microbiol Infect Dis 2016; 44:37-40.
17. Kabeya H, Maruyama S, Morita Y, Ohsuga T, Ozawa S, Kobayashi Y, et al. Prevalence of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. Int J Food Microbiol 2004;90:303-308.
18. Son I, Englen MD, Berrang ME, Fedorka-Cray PJ, Harrison MA. Prevalence of Arcobacter and Campylobacter on broiler carcasses during processing. Int J Food Microbiol 2007; 113:16-22.
19. Rahimi E. Prevalence and antimicrobial resistance of Arcobacter species isolated from poultry meat in Iran. Br Poult Sci 2014; 55:174-180.
20. Atabay HI, Aydin F. Susceptibility of Arcobacter butzleri isolates to 23 antimicrobial agents. Lett Appl Microbiol 2001; 33:430-433.
21. Aydin F, Gümüşsoy KS, Atabay HI, Iça T, Abay S. Prevalence and distribution of Arcobacter species in various sources in Turkey and molecular analysis of isolated strains by ERIC-PCR. J Appl Microbiol 2007; 103:27-35.
22. Bogantes EV, Fallas-Padilla KL, Rodriguez-Rodriguez CE, Jaramillo HF, Echandi MLA. Zoonotic species of the genus Arcobacter in poultry from different regions of Costa Rica. J Food Prot 2015; 78:808-811.
23. Merga JY, Leatherbarrow A, Winstanley C, Bennett M, Hart CA, Miller WG, et al. Comparison of Arcobacter isolation methods, and diversity of Arcobacter spp. in Cheshire, United Kingdom. Appl Environ Microbiol 2011; 77:1646-1650.
24. Merga JY, Williams NJ, William G, Miller WG, Leatherbarrow AJH, Bennett M, et al. Exploring the diversity of Arcobacter butzleri from cattle in the UK using MLST and whole genome sequencing. PLoS One 2013; 8(2): e55240.
25. Levican A, Alkeskas A, G€unter C, Forsythe SJ, Figueras MJ. Adherence to and invasion of human intestinal cells by Arcobacter species and their virulence genotypes. Appl Environ Microbiol 2013; 79:4951-4957.
26. Yesilmen S, Vural A, Erkan ME, Yildirim IH. Prevalence and antimicrobial susceptibility of Arcobacter species in cow milk, water buffalo milk and fresh village cheese. Int J Food Microbiol 2014; 188:11-14.
27. Giacometti F, Lucchi A, Di Francesco A, Delogu M, Grilli E, Guarniero I, et al. Arcobacter butzleri, Arcobacter cryaerophilus and Arcobacter skirrowii circulation in a dairy farm and sources of milk contamination. Appl Environ Microbiol 2015; 81:5055-5063.
28. Badilla-Ramırez Y, Fallas-Padilla KL, Fernandez-Jaramillo H, Arias-Echandi ML. Survival capacity of Arcobacter butzleri inoculated in poultry meat at two different refrigeration temperatures. Rev Inst Med Trop Sao Paulo 2016; 58:22.
29. Ramees K, Kumaragurubaran K, Ramswaroop S, Ashok K, Mani Sa, Ruchi T, et al. Arcobacter: an emerging food-borne zoonotic pathogen, its public health concerns and advances in diagnosis and control-a comprehensive review. Vet Q 2017; 37:136-161.
30. Verma M, Joshi N, Rathore RS, Mohan HV. Detection of Arcobacter spp. in poultry, pigs, their meat and environmental samples by conventional and PCR assays. Indian J Anim Sci 2015; 85:954-957.
31. Vandenberg O, Houf K, Douat N, Vlaes L, Retore P, Butzler JP. Antimicrobial susceptibility of clinical isolates of non-jejuni/coli campylobacters and Arcobacters from Belgium. J Antimicrob Chemother 2006; 57:908-913.
32. Zacharow I, Bystron J, Waecka-Zacharska E, Podkowik M, Bania J. Prevalence and antimicrobial resistance of Arcobacter butzleri and Arcobacter cryaerophilus isolates from retail meat in Lower Silesia region. Pol J Vet Sci 2015; 18:63-69.
33. Shah AH, Saleha AA, Zunita Z, Murugaiyah M, Aliyu AB, Jafri N. Prevalence, distribution and antibiotic resistance of emergent Arcobacter spp. from clinically healthy cattle and goats. Transbound Emerg Dis 2013; 60:9-16.
34. Unver A, Atabay HI, Sahin M, Celebi €O. Antimicrobial susceptibilities of various Arcobacter species. Turk J Med Sci 2013; 43:548-552.
2. Aydin F, Yağiz A, Abay S. Prevalence of Arcobacter and Campylobacter in beef meat samples and characterization of the recovered isolates. J Consum Prot Food Saf 2020; 15:15-25.
3. Ferreira S, Queiroz JA, Oleastro M, Domingues F. Insights in the pathogenesis and resistance of Arcobacter: a review. Crit Rev Microbiol 2016; 42:364-383.
4. Fanelli F, Pinto AD, Mottola A, Mule G, Chieffi D, Baruzzi F, et al. Genomic characterization of Arcobacter butzleri isolated from shellfish: novel insight into antibiotic resistance and virulence determinants. Front Microbiol 2019; 10: 670.
5. Collado L, Figueras MJ. Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin Microbiol Rev 2011; 24:174-192.
6. Park S, Jung YT, Kim S, Yoon JH. Arcobacter acticola sp. Nov isolated from seawater on the east sea in south Korea. J Microbiol 2016; 54:655-659.
7. Chieffi D, Fanelli F, Fusco V. Arcobacter butzleri: Up-to-date taxonomy, ecology, and pathogenicity of an emerging pathogen. Compr Rev Food Sci Food Saf 2020; 19:2071-2109.
8. Collado L, Levican A, Perez J, Figueras MJ. Arcobacter defluvii sp. nov., isolated from sewage samples. Int J Syst Evol Microbiol 2011; 61:2155-2161.
9. Lee C, Agidi S, Marion JW, Lee J. Arcobacter in Lake Erie beach waters: an emerging gastrointestinal pathogen linked with human-associated fecal contamination. Appl Environ Microbiol 2012; 78:5511-5519.
10. De Smet S, De Zutter L, Van Hende J, Houf K. Arcobacter contamination on pre- and post-chilled bovine carcasses and in minced beef at retail. J Appl Microbiol 2010; 108:299-305.
11. Van Driessche E, Houf K, Van Hoof J, De Zutter L, Vandamme P. Isolation of Arcobacter species from animal feces. FEMS Microbiol Lett 2003; 229:243-248.
12. Dekker DD, Eibach KG, Boahen C, Wiafe Akenten Y, Pfeifer AE, Zautner E, et al. Fluoroquinolone-resistant Salmonella enterica, Campylobacter spp., and Arcobacter butzleri from local and imported poultry meat in Kumasi, Ghana. Foodborne Pathog Dis 2019; 16: 352-358.
13. Skirrow MB (2000). Clinical aspects of Campylobacter infection, in: I.Nachamkin, M.J. Blaser (Eds.), Campylobacter, second ed., ASM Press, Washington, DC. 69-88.
14. Kabeya H, Maruyama S, Morita Y, Ohsuga T, Ozawa S, Kobayashi Y, et al. Prevalence of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. Int J Food Microbiol 2004; 90:303-308.
15. Abay S, Kayman T, Hizlisoy H, Aydin F. In vitro antibacterial susceptibility of Arcobacter butzleri isolated from different sources. J Vet Med Sci 2012; 74:613-616.
16. Shirzad Aski H, Tabatabaei M, Khoshbakht R, Raeisi M. Occurrence and antimicrobial resistance of emergent Arcobacter spp. isolated from cattle and sheep in Iran. Comp Immunol Microbiol Infect Dis 2016; 44:37-40.
17. Kabeya H, Maruyama S, Morita Y, Ohsuga T, Ozawa S, Kobayashi Y, et al. Prevalence of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. Int J Food Microbiol 2004;90:303-308.
18. Son I, Englen MD, Berrang ME, Fedorka-Cray PJ, Harrison MA. Prevalence of Arcobacter and Campylobacter on broiler carcasses during processing. Int J Food Microbiol 2007; 113:16-22.
19. Rahimi E. Prevalence and antimicrobial resistance of Arcobacter species isolated from poultry meat in Iran. Br Poult Sci 2014; 55:174-180.
20. Atabay HI, Aydin F. Susceptibility of Arcobacter butzleri isolates to 23 antimicrobial agents. Lett Appl Microbiol 2001; 33:430-433.
21. Aydin F, Gümüşsoy KS, Atabay HI, Iça T, Abay S. Prevalence and distribution of Arcobacter species in various sources in Turkey and molecular analysis of isolated strains by ERIC-PCR. J Appl Microbiol 2007; 103:27-35.
22. Bogantes EV, Fallas-Padilla KL, Rodriguez-Rodriguez CE, Jaramillo HF, Echandi MLA. Zoonotic species of the genus Arcobacter in poultry from different regions of Costa Rica. J Food Prot 2015; 78:808-811.
23. Merga JY, Leatherbarrow A, Winstanley C, Bennett M, Hart CA, Miller WG, et al. Comparison of Arcobacter isolation methods, and diversity of Arcobacter spp. in Cheshire, United Kingdom. Appl Environ Microbiol 2011; 77:1646-1650.
24. Merga JY, Williams NJ, William G, Miller WG, Leatherbarrow AJH, Bennett M, et al. Exploring the diversity of Arcobacter butzleri from cattle in the UK using MLST and whole genome sequencing. PLoS One 2013; 8(2): e55240.
25. Levican A, Alkeskas A, G€unter C, Forsythe SJ, Figueras MJ. Adherence to and invasion of human intestinal cells by Arcobacter species and their virulence genotypes. Appl Environ Microbiol 2013; 79:4951-4957.
26. Yesilmen S, Vural A, Erkan ME, Yildirim IH. Prevalence and antimicrobial susceptibility of Arcobacter species in cow milk, water buffalo milk and fresh village cheese. Int J Food Microbiol 2014; 188:11-14.
27. Giacometti F, Lucchi A, Di Francesco A, Delogu M, Grilli E, Guarniero I, et al. Arcobacter butzleri, Arcobacter cryaerophilus and Arcobacter skirrowii circulation in a dairy farm and sources of milk contamination. Appl Environ Microbiol 2015; 81:5055-5063.
28. Badilla-Ramırez Y, Fallas-Padilla KL, Fernandez-Jaramillo H, Arias-Echandi ML. Survival capacity of Arcobacter butzleri inoculated in poultry meat at two different refrigeration temperatures. Rev Inst Med Trop Sao Paulo 2016; 58:22.
29. Ramees K, Kumaragurubaran K, Ramswaroop S, Ashok K, Mani Sa, Ruchi T, et al. Arcobacter: an emerging food-borne zoonotic pathogen, its public health concerns and advances in diagnosis and control-a comprehensive review. Vet Q 2017; 37:136-161.
30. Verma M, Joshi N, Rathore RS, Mohan HV. Detection of Arcobacter spp. in poultry, pigs, their meat and environmental samples by conventional and PCR assays. Indian J Anim Sci 2015; 85:954-957.
31. Vandenberg O, Houf K, Douat N, Vlaes L, Retore P, Butzler JP. Antimicrobial susceptibility of clinical isolates of non-jejuni/coli campylobacters and Arcobacters from Belgium. J Antimicrob Chemother 2006; 57:908-913.
32. Zacharow I, Bystron J, Waecka-Zacharska E, Podkowik M, Bania J. Prevalence and antimicrobial resistance of Arcobacter butzleri and Arcobacter cryaerophilus isolates from retail meat in Lower Silesia region. Pol J Vet Sci 2015; 18:63-69.
33. Shah AH, Saleha AA, Zunita Z, Murugaiyah M, Aliyu AB, Jafri N. Prevalence, distribution and antibiotic resistance of emergent Arcobacter spp. from clinically healthy cattle and goats. Transbound Emerg Dis 2013; 60:9-16.
34. Unver A, Atabay HI, Sahin M, Celebi €O. Antimicrobial susceptibilities of various Arcobacter species. Turk J Med Sci 2013; 43:548-552.
| Files | ||
| Issue | Vol 12 No 6 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i6.5027 | |
| Keywords | ||
| Arcobacter; Broiler chicks; Iran; Prevalence; Antimicrobial susceptibility | ||
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How to Cite
1.
Khodamoradi S, Abiri R. The incidence and antimicrobial resistance of Arcobacter species in animal and poultry meat samples at slaughterhouses in Iran. Iran J Microbiol. 2020;12(6):531-536.
