The evaluation of antibiotic resistance genes of Arcobacter butzleri isolated from animal products, and chicken slaughterhouse sewage in Mazandaran province, Northern Iran

Document Type : Full paper (Original article)

Authors

1 Ph.D. Student in Microbiology, Department of Microbiology, Faculty of Basic Sciences, Ayatollah Amoli Branch, Islamic Azad University, Amol, Iran

2 Department of Microbiology, Faculty of Basic Sciences, Ayatollah Amoli Branch, Islamic Azad University, Amol, Iran

3 Department of Microbiology, Faculty of Basic Sciences, Tonekabon Branch, Islamic Azad University, Tonekabon, Iran

4 Department of Pathobiology, Faculty of Veterinary Medicine, Amol University of Special Modern Technologies, Amol, Iran

5 Department of Microbiology, Faculty of Basic Sciences, Ahar Branch, Islamic Azad University, Ahar, Iran

Abstract

Background: Arcobacter butzleri, the most common genus of the Campylobacter family, is considered an emerging zoonotic pathogen. Aims: This study aimed to evaluate A. butzleri from diverse sources, in order to determine the antibiotic resistance pattern of isolates and the frequency of some genes responsible for their antibiotic resistance. Methods: In this study, 425 samples were collected from different sources (chicken slaughterhouse sewage, poultry meat, beef, sheep meat, dairy products) during different seasons of 2020-2021. Suspicious colonies were confirmed using biochemical tests. Furthermore, the polymerase chain reaction technique was used to confirm the phenotypic results using the 16S rRNA gene. The antibiotic resistance pattern of the isolates to 16 antibiotics were determined using the disk diffusion method. Also, the minimum inhibitory concentration (MIC) of their growth was detected using the tube dilution method in the presence of tetracycline, erythromycin, and gentamicin. Results: A total of 53 isolates of A. butzleri (12.5%) were isolated from (chicken slaughterhouse sewage=36, poultry meat=8, beef=4, sheep meat=5), which contain all three antibiotic resistance genes of abu_0814 (90.57%), OXA_464 (100%), and gyrA (83.02%). The findings of the present investigation showed the presence of A. butzleri in different sources and the high prevalence of antimicrobial resistance in the isolates. Nineteen isolates (36%) have extensive drug resistance and 34 isolates (64%) showed multi-drug resistance to the used antibiotics. Conclusion: The elevated level of antibiotic resistance observed in A. butzleri isolates originating from various samples suggests a significant use of antibiotics and a prevalent environmental contamination.

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References

Amare, L; Saleha, A; Zunita, Z; Jalila, A and Hassan, L (2011). Prevalence of Arcobacter spp. on chicken meat at retail markets and in farm chickens in Selangor, Malaysia. Food Control. 22: 732-736.
Arias, ML; Cid, A and Fernandéz, H (2011). Arcobacter butzleri: first isolation report from chicken carcasses in Costa Rica. Brazilian J. Microbiol., 42: 703-706.
Aski, HS; Tabatabaei, M; Khoshbakht, R and Raeisi, M (2016). Occurrence and antimicrobial resistance of emergent Arcobacter spp. isolated from cattle and sheep in Iran. Comp. Immunol. Microbiol. Infect. Dis., 44: 37-40.
Atabay, H and Corry, J (1997). The prevalence of Campylobacters and Arcobacters in broiler chickens. J. Applied Microbiol., 83: 619-626.
Atabay, HI; Unver, A; Sahin, M; Otlu, S; Elmali, M and Yaman, H (2008). Isolation of various Arcobacter species from domestic geese (Anser anser). Vet. Microbiol., 128: 400-405.
Bayles, KW (2000). The bactericidal action of penicillin: New clues to an unsolved mystery. Trends Microbiol., 8: 274-278. doi: 10.1016/S0966-842X(00)01762-5.
Brückner, V; Fiebiger, U; Ignatius, R; Friesen, J; Eisenblätter, M and Höck, M (2020). Prevalence and antimicrobial susceptibility of Arcobacter species in human stool samples derived from out- and inpatients: the prospective German Arcobacter prevalence study Arcopath. Gut Pathog., 12: 1-8. doi: 10.1186/s13099-020-00360-x.
Bucker, R; Troeger, H; Kleer, J; Fromm, M and Schulzke, JD (2009). Arcobacter butzleri induces barrier dysfunction in intestinal HT-29/B6 cells. J. Infect. Dis., 200: 756-764.
Çelik, E and Otlu, S (2020). Isolation of Arcobacter spp. and identification of isolates by multiplex PCR from various domestic poultry and wild avian species. Ann. Microbiol., 70: 1-7.
Chieffi, D; Fanelli, F and Fusco, V (2020). Arcobacter butzleri: Up-to-date taxonomy, ecology, and pathogenicity of an emerging pathogen. Compr. Rev. Food Sci. Food Saf., 19: 2071-2109.
Cho, S; Barrett, JB; Frye, JG and Jackson, CR (2020). Antimicrobial resistance gene detection and plasmid typing among multidrug resistant Enterococci isolated from freshwater. Microorganisms. 8: 1-15. doi: 10.3390/ microorganisms8091338.
Collado, L and Figueras, MJ (2011). Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin. Microbiol. Rev., 24: 174-192.
Di Noto, AM; Sciortino, S; Cardamone, C; Ciravolo, C; Napoli, C; Alio, V and Costa, A (2018). Detection of Arcobacter spp. in food products collected from Sicilia region: A preliminary study. Ital. J. Food Saf., 7: 2.
Fanelli, F; Di Pinto, A; Mottola, A; Mule, G; Chieffi, D; Baruzzi, F and Fusco, V (2019). Genomic characterization of Arcobacter butzleri isolated from shellfish: novel insight into antibiotic resistance and virulence determinants. Front. Microbiol, 10: 670-672.
Fera, MT; La camera, E; Carbone, M; Malara, D and Pennisi, MG (2009). Pet cats as carriers of Arcobacter spp. in Southern Italy. J. Appl. Microbiol., 106: 1661-1666.
Ferreira, S; Queiroz, JA; Oleastro, M and Domingues, F (2016). Insights in the pathogenesis and resistance of Arcobacter: A review. Crit. Rev. Microbiol., 42: 364-383.
González, A; Morejón, I and Ferrús, M (2017). Isolation, molecular identification and quinolone-susceptibility testing of Arcobacter spp. isolated from fresh vegetables in Spain. Food Microbiol., 65: 279-283.
Groicher, KH; Firek, BA; Fujimoto, DF and Bayles, K (2000). The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J. Bacteriol., 182: 1794-1801. doi: 10.1128/ JB.182.7.1794-1801.200.
Ho, TK; Lipman, LJ; van der Graaf-van Bloois, L; van Bergen, M and Gaastra, W (2006). Potential routes of acquisition of Arcobacter species by piglets. Vet. Microbiol., 114: 123-133.
Hodges, LM; Taboada, EN; Koziol, A; Mutschall, S; Blais, BW and Inglis, G (2021). Systematic evaluation of whole-genome sequencing based prediction of antimicrobial resistance in Campylobacter jejuni and C. coli. Front. Microbiol., 12: 776967. doi: 10.3389/fmicb.2021.776967.
Hormeño, L; Ugarte-Ruiz, M; Palomo, G; Borge, C; Florez-Cuadrado, D; Vadillo, S and Quesada, A (2018). ant (6)-I genes encoding aminoglycoside O-nucleotidyltransferases are widely spread among streptomycin resistant strains of Campylobacter jejuni and Campylobacter coli. Front. Microbiol., 23: 2515-2520.
Houf, K; Devriese, LA; Zutter, LD; Van Hoof, J and Vandamme, P (2001). Susceptibility of Arcobacter butzleri, Arcobacter cryaerophilus, and Arcobacter skirrowii to antimicrobial agents used in selective media. J. Clin. Microbiol., 39: 1654-1656.
Hudzicki, J (2009). Kirby-Bauer disk diffusion susceptibility test protocol. ASM., 15: 55-63.
Humphries, R; Bobenchik, AM; Hindler, JA and Schuetz, A (2021). Overview of changes to the Clinical and Laboratory Standards Institute performance standards for antimicrobial susceptibility testing, M100. J. Clin. Microbiol., 59: 10-1128.
International Commission on Microbiological Specifications for Foods (ICMSF) (2018). Micro-biological hazards and their control. Microorganisms in foods 7: Microbiological testing in food safety management. PP: 1-30.
Isidro, J; Ferreira, S; Pinto, M; Domingues, F; Oleastro, M; Gomes, JP and Borges, V (2020). Virulence and antibiotic resistance plasticity of Arcobacter butzleri: Insights on the genomic diversity of an emerging human pathogen. Infect. Genet. Evol., 80: 104213.
Kim, NH; Park, SM; Kim, HW; Cho, TJ; Kim, SH; Choi, C and Rhee, M (2019). Prevalence of pathogenic Arcobacter species in South Korea: Comparison of two protocols for isolating the bacteria from foods and examination of nine putative virulence genes. Food Microbiol., 78: 18-24.
Lehner, A; Tasara, T and Stephan, R (2005). Relevant aspects of Arcobacter spp. as potential foodborne pathogen. Int. J. Food Microbiol., 102: 127-135.
Miller, WG; Parker, CT; Rubenfield, M; Mendz, GL; Wosten, MM and Ussery, DW (2007). The complete genome sequence and analysis of the epsilonproteo-bacterium Arcobacter butzleri. PLoS One. 2: e1358. doi: 10.1371/journal.pone.0001358. doi: 10.3389/fmicb.2018. 02515.
Oren, A and Garrity, G (2020). List of new names and new combinations previously effectively, but not validly, published. Int. J. Syst. Evol. Microbiol., 70: 2960-2966.
Parisi, A; Capozzi, L; Bianco, A; Caruso, M; Latorre, L; Costa, A; Giannico, A; Ridolfi, D; Bulzacchelli, C and Santagada, G (2019). Identification of virulence and antibiotic resistance factors in Arcobacter butzleri isolated from bovine milk by whole genome sequencing. Ital. J. Food Saf., 8: 60-64.
 
Pérez-Cataluña, A; Salas-Masso, N; Dieguez, AL; Balboa, S; Lema, A; Romalde, JL and Figueras, M (2018). Revisiting the taxonomy of the genus Arcobacter: Getting order from the chaos. Food Microbiol., 4: 2077-2080.
Pérez-Cataluña, A; Salas-Masso, N; Dieguez, AL; Balboa, S; Lema, A; Romalde, JL and Figueras, M (2019a). Revisiting the taxonomy of the genus Arcobacter: Getting order from the chaos. Food Microbiol., 10: 2253-2261.
Pérez-Cataluña, A; Salas-Masso, N and Figueras, M (2019b). Arcobacter lacus sp. nov. and Arcobacter caeni sp. nov., two novel species isolated from reclaimed water. Int. J. Syst. Evol. Microbiol., 69: 3326-3331.
Ramees, TP; Dhama, K; Karthik, K; Rathore, RS; Kumar, A; Saminathan, M; Tiwari, R; Malik, YS and 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.
Scullion, R; Harrington, CS and Madden, RH (2006). Prevalence of Arcobacter spp. in raw milk and retail raw meats in Northern Ireland. J. Food Prot., 69: 1986-1990.
Shah, AH; Saleha, AA; Zunita, Z; Cheah, YK; Murugaiyah, M and Korejo, NA (2012). Genetic characterization of Arcobacter isolates from various sources. Vet. Microbiol., 160: 355-361.
Vandamme, P; Falsen, E; Rossau, R; Hoste, B; Segers, P; Tytgat, R and De Ley, J (1991). Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: Emendation of generic descriptionsand proposal of Arcobacter gen. nov. Int. J. Syst. Bacteriol., 41: 88-103.
Van den Abeele, AM; Vogelaers, D; Vanlaere, E and Houf, K (2016). Antimicrobial susceptibility testing of Arcobacter butzleri and Arcobacter cryaerophilus strains isolated from Belgian patients. J. Antimicrobial. Chem., 71: 1241-1244.
Vandenberg, O; Dediste, A; Houf, K; Ibekwem, S; Souayah, H; Cadranel, S; Douat, N; Zissis, G; Butzler, JP and Vandamme, P (2004). Arcobacter species in humans. Emerg. Infect. Dis., 10: 1863-1867.
Van Driessche, E; Houf, K; van Hoof, J; De Zutter, L and Vandamme, P (2003). Isolation of Arcobacter species from animal feces. FEMS Microbiol. Lett., 229: 243-248.
Webb, AL; Selinger, LB; Taboada, EN and Inglis, GD (2018). Subtype-Specific selection for resistance to fluoroquinolones but not to tetracyclines is evident in Campylobacter jejuni isolates from beef cattle in confined feeding operations in Southern Alberta, Canada. Appl. Environ. Microb., 84: 02713-02717. doi: 10.1128/AEM. 02713-17.
Yesilmen, S; Vural, A; Erkan, ME and Yildirim, IH (2014). Prevalence and antimicrobial susceptibility of Arcobacter species in cow milk, water buffalo milk and fresh village cheese. Int. J. Food Microbiol., 188: 11-14.
Zambri, M; Cloutier, M; Adam, Z; Lapen, DR; Wilkes, G and Sunohara, M (2019). Novel virulence, antibiotic resistance and toxin gene-specific PCR based assays for rapid pathogenicity assessment of Arcobacter faecis and Arcobacter lanthieri. BMC Microbiol., 19: 1-15. doi: 10.1186/s12866-018-1357-7.
Zhang, X; Alter, T and Gölz, G (2019). Characterization of Arcobacter spp. isolated from retail seafood in Germany. Food Microbiol., 82: 254-258. doi: 10.1016/j.fm.2019.02. 010.

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