Isolation and characterization of thermophilic Campylobacter species from geese raised in Kars region (Turkey) using cultural, molecular and mass spectrometry methods

Document Type : Full paper (Original article)

Authors

1 Ph.D. Student in Microbiology, Department of Microbiology, Institute of Health Sciences, Kafkas University, Kars, 36100, Turkey

2 Department of Microbiology, Faculty of Veterinary Medicine, Kafkas University, Kars, 36100, Turkey

Abstract

Background: Thermophilic Campylobacters are found in the digestive tract of wild and domestic poultry and can be transmitted to humans following their fecal discharges. Aims: This study aimed to isolate thermophilic Campylobacter by culture from cloacal swabs of geese, commonly breeding in Kars region, and to identify the isolates by PCR and mass spectrometry. Antibiotics susceptibility and resistance genes of the isolates were also analysed. Methods: The study included 400 cloacal swab samples of clinically healthy geese. The samples were cultured on mCCDA medium following the pre-enrichment in Preston broth. Identification of the isolates was performed by phenotypic methods, PCR, and MALDI-TOF MS. Antibiotic susceptibility and resistance genes of the isolates were analysed with the disc diffusion method and PCR, respectively. Results: Thermophilic Campylobacter spp. were isolated from 157 (39.3%) samples. 151 (96.2%) isolates were identified Campylobacter jejuni and 6 (3.8%) Campylobacter coli by the phenotypic tests and PCR. Among 125 isolates analysed by MALDI-TOF MS, 119 (95.2%) were identified C. jejuni and 6 (4.8%) C. coli. The isolates’ resistance to ampicillin, tetracycline, ciprofloxacin, gentamicin, and azithromycin were found 33.8%, 41.4%, 75.2%, 12.1%, and 7.6%, respectively. The distributions of blaOXA61, tetO, gyrA, and aphA-3 genes were 3.2%, 90.8%, 50.8%, and 52.7%, respectively. Conclusion: Since geese are raised in pastures in the Kars region, protecting and not polluting the existing natural environment and preventing their contact with wild birds will prevent the spread of these microorganisms.

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References

Abdi-Hachesoo, B; Khoshbakht, R; Sharifiyazdi, H; Tabatabaei, M; Hosseinzadeh, S and Asasi, K (2014). Tetracycline resistance genes in Campylobacter jejuni and C. coli isolated from poultry carcasses. Jundishapur J. Microbiol., 7: e12129.
Allos, BM (2001). Campylobacter jejuni infections: update on emerging issues and trends. Clin. Infect. Dis., 32: 1201-1206.
Anonymous 1 (2020). www.mikrobiology.org/TR. (available at 12.08.2020).
Aydin, F; Atabay, HI and Akan, M (2001). The isolation and characterization of Campylobacter jejuni subsp. jejuni from domestic geese (Anser anser). J. Appl. Microbiol., 90: 637-642.
Bailey, MA; Taylor, RM; Brar, JS; Corkran, SC; Velásquez, C; Rama, EN; Oliver, HF and Singh, M (2019). Prevalence and antimicrobial resistance of Campylobacter from antibiotic-free broilers during organic and conventional processing. Poult. Sci., 98: 1447-1454.
Bakeli, G; Sato, K; Kumita, W; Saito, R; Ono, E; Chida, T and Okamura, N (2008). Antimicrobial susceptibility and mechanism of quinolone resistance in Campylobacter jejuni strains isolated from diarrheal patients in a hospital in Tokyo. J. Infect. Chemother., 14: 342-348.
Bardoň, J; Pudová, V; Koláčková, I; Karpíšková, R; Röderová, M and Kolář, M (2017). Virulence and antibiotic resistance genes in Campylobacter spp. in the Czech Republic. Epidemiol. Mikrobiol. Imunol., 66: 59-66.
Boyd, Y; Herbert, EG; Marston, KL; Jones, MA and Barrow, PA (2005). Host genes affect intestinal colonisation of newly hatched chickens by Campylobacter jejuni. Immunogenetics. 57: 248-253.
Chopra, IT and Roberts, M (2001). Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev., 65: 232-260.
Çokal, Y; Caner, V; Sen, A; Çetin, C and Karagenc, N (2009). Campylobacter spp. and their antimicrobial resistance patterns in poultry: An epidemiological survey study in Turkey. Zoonoses Public Health. 56: 105-110.
Coker, AO; Isokpehi, RD; Thomas, BN; Amisu, KO and Obi, CL (2002). Human Campylobacteriosis in developing countries. Emerg. Infect. Dis., 8: 237-244.
Colles, FM; Jones, TA; McCarthy, ND; Sheppard, SK; Cody, AJ; Dingle, KE; Dawkins, MS and Maiden, MCJ (2008). Campylobacter infection of broiler chickens in a free-range environment. Environ. Microbiol., 10: 2042-2050.
Elmalı, M; Yaman, H; Ulukanlı, Z and Genctav, K (2004). Isolation and identification of Campylobacter jejuni in goose carcass, goose c1oaka, goose bedding and goose, chicken and quail eggs. Vet. Bil. Derg., 20: 47-52 (in Turkish with an abst. in English).
Es-Soucratti, K; Hammoumi, A; Bouchrif, B; Asmai, R; En-Nassiri, H and Karraouan, B (2020). Occurrence and antimicrobial resistance of Campylobacter jejuni isolates from poultry in Casablanca-Settat, Morocco. Ital. J. Food Saf., 9: 54-59.
Evans, SJ (1997). Epidemiological studies of Salmonella and Campylobacter in poultry. Ph.D. Thesis, University of London, London, United Kingdom. PP: 1-331.
Evans, S and Sayers, AR (2000). A longitudinal study of Campylobacter infection of broiler flocks in Great Britain. Prev. Vet. Med., 46: 209-223.
Griggs, DJ; Peake, L; Johnson, MM; Ghori, S; Mott, A and Piddock, LJ (2009). Beta-lactamase-mediated beta-lactam resistance in Campylobacter species: prevalence of Cj0299 (blaOXA-61) and evidence for a novel beta-Lactamase in C. jejuni. Antimicrob. Agents Chemother., 53: 3357-3364.
Hasdemir, U (2007). The role of cell wall organization and active efflux pump systems in multidrug resistance of bacteria. Mikrobiyol. Bul., 41: 309-327 (in Turkish with an abst. in English).
Jamali, H; Ghaderpour, A; Radmehr, B; Wei, KSC; Chai, LC and Ismail, S (2013). Prevalence and antimicrobial resistance of Campylobacter species isolates in ducks and geese. Food Control. 50: 328-330.
Jones, K (2011). Campylobacters in water, sewage and the environment. J. Appl. Microbiol., 90: 68-79.
Jorgensen, F; Ellis-Iversen, J; Rushton, S; Bull, SA; Harris, SA; Bryan, SJ; Gonzalez, A and Humphrey, TJ (2011). Influence of season and geography on Campylobacter jejuni and C. coli subtypes in housed broiler flocks reared in Great Britain. Appl. Environ. Microbiol., 77: 3741-3748.
Kalupahana, RS; Mughini-Gras, L; Kottawatta, SA; Somarathne, S; Gamage, C and Wagenaar, JA (2018). Weather correlates of Campylobacter prevalence in broilers at slaughter under tropical conditions in Sri Lanka. Epidemiol. Infect., 146: 972-979.
Komba, EV; Mdegela, RH; Msoffe, PL; Nielsen, LN and Ingmer, H (2015). Prevalence, antimicrobial resistance and risk factors for thermophilic Campylobacter infections in symptomatic and asymptomatic humans in Tanzania. Zoonoses Public Health. 62: 557-568.
Lambert, T; Gerbaud, G; Trieu-Cuot, P and Courvalin, P (1985). Structural relationship between the genes encoding 3´-aminoglycoside phosphotransferases in Campylobacter and in Gram-positive cocci. Ann. Inst. Pasteur Microbiol., 136B: 135-150.
Leflon-Guibout, V and Munier, AL (2016). Campylobacter infections: Epidemiology, virulence factors, antibiotic resistance. J. Anti-Infect., 18: 160-168.
Luangtongkum, T; Jeon, B; Han, J; Plummer, P; Logue, CM and Zhang, Q (2009). Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol., 4: 189-200.
Mamur, J (1961). A procedure for the isolation of deoxyribonucleic acid from microorganisms. J. Mol. Biol., 3: 208-218.
Marotta, F; Janowicz, A; Marcantonio, LD; Ercole, C; Donato, GD; Garofolo, G and Giannatale, ED (2020). Molecular characterization and antimicrobial susceptibility of C. jejuni isolates from Italian wild bird populations. Pathogens. 9: 1-16.
Melo, RT; Grazziotin, AL; Valadares-Júnior, EC; Prado, RR; Mendonça, EP; Monteiro, GP; Peres, PABM and Rossi, DA (2019). Evolution of Campylobacter jejuni of poultry origin in Brazil. Food Microbiol., 82: 489-496.
Moriarty, EM; Karki, N; Mackenzie, M; Sinton, LW; Wood, DR and Gilpin, BJ (2011). Faecal indicators and pathogens in selected New Zealand waterfowl. N. Z. J. Mar. Fresh. Res., 45: 679-688.
Newell, DG (2001). Animal model of Campylobacter jejuni colonization and disease and the lessons to be learned from similar Helicobacter pylori models. J. Appl. Microbiol., 90: 57S-67S.
Newell, DG and Fearnley, C (2003). Sources of campylobacter colonization in broiler chickens. Appl. Environ. Microbiol., 69: 4343-4351.
Nowaczek, A; Urban-Chmiel, R; Dec, M; Puchalski, A; Stępień-Pyśniak, D; Marek, A and Pyzik, E (2019). Campylobacter spp. and bacteriophages from broiler chickens: Characterization of antibiotic susceptibility profiles and lytic bacteriophages. MicrobiologyOpen. 8: e784.
Proiettia, PC; Guelfia, G; Belluccia, S; De Lucab, S; Di Gregorioa, S; Pieramatia, C and Franciosini, MP (2020). Beta-lactam resistance in Campylobacter coli and Campylobacter jejuni chicken isolates and the association between blaOXA-61 gene expression and the action of β-lactamase inhibitors. Vet. Microbiol., 241: 108553.
Qin, S; Wang, Y; Zhang, Q; Zhang, M; Deng, F; Shen, Z; Wu, C; Wang, S; Zhang, J and Shen, J (2014). Report of ribosomal RNA methylase gene erm(B) in multidrug-resistant Campylobacter coli. J. Antimicrob. Chemother., 69: 964-968.
Refregier-Petton, J; Rose, N; Denis, M and Salvat, G (2001). Risk factors for Campylobacter spp. contamination in French broiler chicken flocks at the end of the rearing period. Prev. Vet. Med., 50: 89-100.
Ringoir, DD and Korolik, V (2002). Colonisation phenotype and colonization differences in Campylobacter jejuni strains in chickens before and after passage in vivo. Vet. Microbiol., 92: 225-235.
Sahin, O; Luo, N; Huang, S and Zhang, Q (2003). Effect of Campylobacter-specific maternal antibodies on Campylobacter jejuni colonization in young chickens. Appl. Environ. Microbiol., 69: 5372-5379.
Scerbova, J and Laukova, A (2016). Sensitivity to enterocins of thermophilic Campylobacter spp. from different poultry species. Foodborne Pathog. Dis., 13: 668-673.
Seng, P; Drancourt, M; Gouriet, F; La Scola, B; Fournier, PE; Rolain, JM and Raoult, D (2009). Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laserdesorption ionization time-of-flight mass spectrometry. Clin. Infect. Dis., 49: 543-551.
Shreeve, JE; Toszeghy, M; Pattison, M and Newell, DG (2000). Sequential spread of Campylobacter infection in a multi-pen broiler house. Avian Dis., 44: 983-988.
Silva, PR; Palma, JM; Souza, NR; de Moura, HM; Perecmanis, S and Patricia-Santana, A (2019). Isolation and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli found in chilled chicken carcasses in the Federal District Region and surrounding areas. Semin. Ciênc. Agrár., 40: 2247-2260.
Szczepanska, B; Andrzejewska, M; Spica, D and Klawe, J (2017). Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from children and environmental sources in urban and suburban areas. BMC Microbiol., 17: 1-9.
Szosland-Faltyn, A; Bartodziejska, B; Krolasik, J; Domanska, BP; Korsak, D and Chmiel, M (2008). The prevalence of Campylobacter spp. in Polish poultry meat. Pol. J. Microbiol., 67: 117-120.
Taremi, M; Soltan-Dalla, MM; Gachkar, L; Moez-Ardalan, S; Zolfagharian, K and Zali, MR (2006). Prevalence and antimicrobial resistance of Campylobacter isolated from retail raw chicken and beef meat, Tehran, Iran. Int. J. Food Microbiol., 108: 401-403.
The Clinical & Laboratory Standards Institute (CLSI) (2017). M 100: Performance Standarts for Antimicrobial Susceptibility Testing, 27th Edition, January 2017.
van der Wielen, PWJJ; Biesterveld, S; Notermans, S; Hofstra, H; Urlings, BAP and van Knapen, F (2000). Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Appl. Environ. Microbiol., 66: 2536-2540.
Wang, G; Clark, CG; Taylor, TM; Pucknell, C; Barton, C; Price, L; Woodward, DL and 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.
Wang, Y; Huang, WM and Taylor, DE (1993). Cloning and nucleotide sequence of the Campylobacter jejuni gyrA gene and characterization of quinolone resistance mutations. Antimicrob. Agents Chemother., 37: 457-463.
Wieczorek, K and Osek, J (2013). Antimicrobial resistance mechanisms among Campylobacter. Biomed. Res. Int., 2013: 340605.
Wysok, B; Wojtacka, J; Wiszniewska-Łaszczych, A and Szteyn, J (2020). Antimicrobial resistance and virulence properties of Campylobacter spp. originating from domestic geese in Poland. Animals. 10: 1-15.
Yakupoğulları, Y; Otlu, B; Çelik, B and Gözükara Bağ, HG (2019). Performance of MALDI-TOF MS for the identification of Gram-negative bacteria grown on Eosin Methylene Blue (EMB) agar: A simple method for improving the effectiveness of identification. Mikrobiyol. Bul., 53: 1-11 (in Turkish with an abstract in English).

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