Prevalence, antibiograms, antibiotic resistance genes, and virulence genes of Arcobacter butzleri isolated from healthy pigs in mid-northeastern Thailand

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Natthakorn Chaiyasaen
Kochakorn Direksin
Thitima Nutravong
Suttisak Nopwinyoowong


Pigs can have Arcobacter butzleri. However, information on A. butzleri in Thai pigs remains scarce. This work aimed to survey A. butzleri in healthy pigs and assess their antimicrobial susceptibility, potential transferrable antimicrobial resistance (AMR) genes, and virulence-associated genes (VAGs). Cross-sectional fecal samples of 203 pigs from 18 farms were cultured and molecularly identified. A. butzleri prevalence in all pigs was (31/203; 15.3%): nursery (0/8; 0%), finisher (27/144; 18.8%), and sow (4/51; 7.8%). The total farm A. butzleri prevalence was 50%: nursery (0/2: 0%), finisher (8/14: 57.1%), and sow (2/9: 22.2%) farms. From the 10 antibiotic disks evaluated, the isolates were mostly sensitive to imipenem (96.8%), tetracycline (83.9%), streptomycin (67.7%), and amoxycillin/clavulanic acid (54.8%); however, they were mostly resistant to cefotaxime (98.6%), sulbactam/cefoperazone (71%), ampicillin (67.7%), enrofloxacin (48.4%), and fosfomycin (42.9%) and were neither sensitive nor resistant to erythromycin. Most multidrug resistance patterns in this study were in four to six classes. Three isolates resisted all 10 antibiotics. However, only the TetO gene was detected in one isolate, whereas ESBLs (SHV, CTX-M, and TEM), PMQRs (qnrA, qnrS, qnrB, oqxAB, and aac(6’)-Ib-cr), ermB, and mefA genes were not found in any isolates. The rankings of VAGs presented in the isolates were ciaB (100%), mviN (97%), pldA (93%), tlyA (90%), cj1349 (90%), cadF (83%), hecB (10%), hecA (7%), and irgA (0%), and most isolates carried six VAGs (77%). A. butzleri is present in healthy pigs, and this database is the first to show A. butzleri VAG and AMR genes in Thai pigs

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Chaiyasaen, N. ., Direksin, K. ., Nutravong, T. ., & Nopwinyoowong, S. . (2023). Prevalence, antibiograms, antibiotic resistance genes, and virulence genes of Arcobacter butzleri isolated from healthy pigs in mid-northeastern Thailand: Veterinary Integrative Sciences, 21(2), 309–331. Retrieved from
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Aydin, F., Yağiz, A., Abay, S., Müştak, H.K., Diker, K.S., 2020. Prevalence of Arcobacter and Campylobacter in beef meat samples and characterization of the recovered isolates. J Verbrauch. Lebensm. 15(1), 15–25.

Bastyns, K., Cartuyvels, D., Chapelle, S., Vandamme, P., Goossens, H., De Wachter, R., 1995. A variable 23S rDNA region is a useful discriminating target for genus-specific and species-specific PCR amplification in arcobacter species. Syst. Appl. Microbiol.18(3), 353-356.

Bodhidatta, L., Srijan, A., Serichantalergs, O., Bangtrakulnonth, A., Wongstitwilairung, B.,McDaniel, P., Mason, C.J., 2013. Bacterial pathogens isolated from raw meat and poultry compared with pathogens isolated from children in the same area of rural Thailand. Southeast. Asian. J. Trop. Med. Public. Health. 44(2), 259-272.

Brückner, V., Fiebiger, U., Ignatius, R., Friesen, J., Eisenblätter, M., Höck, M., Alter, T.,Bereswill, S., Gölz, G., Heimesaat, M.M., 2020. Prevalence and antimicrobial susceptibility of Arcobacter species in human stool samples derived from out- And inpatients- And prospective German Arcobacter prevalence study Arcopath. Gut.Pathog. 12(21), 1-8.

Cattoir, V., Poirel, L., Rotimi, V., Soussy, C.J., Nordmann, P., 2007. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBLproducing enterobacterial isolates. J. Antimicrob. Chemother. 60(2), 394–397.

Cavaco, L. M., Hasman, H., Xia, S., Aarestrup, F.M., 2009. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother. 53(2),603–608.

Ciesielczuk, H., Hornsey, M., Choi, V., Woodford, N., Wareham, D.W., 2013. Development and evaluation of a multiplex PCR for eight plasmid-mediated quinolone-resistance determinants. J. Med. Microbiol. 62, 1823–1827.

Clinical and Laboratory Standards Institute, 2020. Performance standards for antimicrobial susceptibility testing (M100), 30th edition. CLSI, Wayne, USA.

de Oliveira, S.J., Bernardi, R.T., Vogt, F.I., Scartezzini, M., Hepp, D., Lunge, V.R., 2010. Gastric ulcers in fattening pigs: Isolation of Arcobacter spp. from stomachs with different severity of lesions. Acta. Sci. Vet. 38(4), 351-356.

Dermani, S.K., Akbari, M., Arjomandzadegan, M., 2017. Evaluation of detection methods for Arcobacter infections in diarrhea specimens among children under six years in Arak City. Infect. Epidemiol. Microbiol. 3(4), 127-131.

Douidah, L., de Zutter, L., Baré, J., De Vos, P., Vandamme, P., Vandenberg, O., Van den Abeele, A.M., Houf, K., 2012. Occurrence of putative virulence genes in Arcobacter species isolated from humans and animals. J. Clin. Microbiol. 50(3), 735-741.

Ellis, W.A., Neill, S.D., O’Brien, J.J., Ferguson, H.W., Hanna, J., 1977. Isolation of Spirillum/Vibrio-like organisms from bovine fetuses. Vet. Rec. 100(21), 451-452.

Ellis, W.A., Neill, S.D., O’Brien, J.J., Hanna, J., 1978. Isolation of spirillum-like organisms from pig fetuses. Vet. Rec. 102(5), 106.

Fanelli, F., Chieffi, D., Di Pinto, A., Mottola, A., Baruzzi, F., Fusco, V., 2020. Phenotype and genomic background of Arcobacter butzleri strains and taxogenomic assessment of the species. Food. Microbiol. 89, 1-16.

Fernandez, H., Villanueva, M.P., Mansilla, I., Gonzalez, M., Latif, F., 2015. Arcobacter butzleri and A. cryaerophilus in human, animals and food sources, in southern Chile.Braz. J. Microbiol. 46(1), 145-147.

Ferreira, S., Oleastro, M., Domingues, F., 2019. Current insights on Arcobacter butzleri in food chain. Curr. Opin. Food. Sci. 26, 9–17.

Gobbi, D.D.S., Spindola, M.G., Moreno, L.Z., Matajira, C.E.C., Oliveira, M.G.X., Paixão, R.,Ferreira, T.S.P., Moreno, A.M., 2018. Isolation and molecular characterization of Arcobacter butzleri and Arcobacter cryaerophilus from the pork production chain in Brazil. Pesq. Vet. Bras. 38(3), 393–399.

Hammerum, A.M., Larsen, J., Andersen, V.D., Lester, C.H., Skovgaard Skytte, T.S., Hansen, F., Olsen, S.S., Mordhorst, H., Skov, R.L., Aarestrup, F.M., Agersø, Y., 2014.Characterization of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli obtained from Danish pigs, pig farmers and their families from farms with high or no consumption of third- or fourth-generation cephalosporins. J.Antimicrob. Chemother. 69(10), 2650–2657.

Houf, K., Tutenel, A., Zutter, L., 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(1),89–94.

Ito, R., Mustapha, M.M., Tomich, A.D., Callaghan, J.D., McElheny, C.L., Mettus, R.T.,Shanks, R.M.Q., Sluis-Cremer, N., Doi, Y., 2017. Widespread fosfomycin resistance in Gram-negative bacteria attributable to the chromosomal fosA gene. mBio. 8(4),e00749-17.

Iwu, C.D., Ekundayo, T.C., Okoh, A.I., 2021. A systematic analysis of research on Arcobacter: public health implications from a food-environment interphase perspective. Foods.10(7), 1673.

Jasim, S.A., Al-abodi, H.R., Ali, W.S., 2021. Resistance rate and novel virulence factor determinants of Arcobacter spp., from cattle fresh meat products from Iraq. Microb. Pathog. 152, 104649.

Jiménez-Guerra, G., Moreno-Torres, I.C., Moldovan, T.D., Navarro-Marí, J.M., Gutiérrez-Fernández, J., 2020. Arcobacter butzleri and intestinal colonization. Rev. Esp.Quimioter. 33(1), 73–75.

Kietsiri, P., Muangnapoh, C., Lurchachaiwong, W., Lertsethtakarn, P., Bodhidatta, L.,Suthienkul, O., Waters, N.C., Demons, S.T., Vesely, B.A., Kietsiri Id, P.,Muangnapoh, C., Lurchachaiwong, W., Lertsethtakarn, P., Bodhidatta, L.,Suthienkul, O., Waters, N.C., Demons, S.T., Vesely, B.A., Kietsiri, P., … Vesely,B.A., 2021. Characterization of Arcobacter spp. isolated from human diarrheal,non-diarrheal and food samples in Thailand. PLoS ONE. 16(2), 1–13.

Kim, N.H., Park, S.M., Kim, H.W., Cho, T.J., Kim, S.H., Choi, C., Rhee, M.S., 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.

Lekagul, A., Tangcharoensathien, V., Mills, A., Rushton, J., Yeung, S., 2020. How antibiotics are used in pig farming: A mixed-methods study of pig farmers, feed mills and veterinarians in Thailand. BMJ Glob. Health. 5(2), 001918.

Mahmoud, N.E., Altayb, H.N., Gurashi, R.M., 2020. Detection of carbapenem-resistant genes in Escherichia Coli isolated from drinking water in Khartoum, Sudan. J. Environ.Public. Health. 2020, 2571293.

Mohan, H.V., Rathore, R.S., Dhama, K., Ramees, T.P., Patya, A., Bagalko, P.S., Wani, M.Y.,Bhilegaonk, K.N., Kumar, A., 2014. Prevalence of Arcobacter spp. in humans,animals and foods of animal origin in India Based on cultural isolation, Antibiogram, PCR and multiplex PCR detection. Asian. J. Anim. Vet. Adv. 9(8), 452–466.

Mollenkopf, D.F., Mathys, D.A., Feicht, S.M., Stull, J.W., Bowman, A.S., Daniels, J.B., Wittum, T.E., 2018. Maintenance of Carbapenemase-producing enterobacteriaceae in a farrow-to-finish swine production system.. Foodborne. Pathog. Dis. 15(6),372-376.

Monstein, H.J., Östholm-Balkhed, A., Nilsson, M.V., Nilsson, M., Dornbusch, K., Nilsson, L.E., 2007. Multiplex PCR amplification assay for the detection of blaSHV, blaTEM and blaCTX-M genes in Enterobacteriaceae. APMIS. 115(12), 1400–1408.

Nagai, K., Shibasaki, Y., Hasegawa, K., Davies, T.A., Jacobs, M.R., Ubukata, K., Appelbaum, P.C., 2001. Evaluation of PCR primers to screen for Streptococcus pneumoniae isolates and β-lactam resistance, and to detect common macrolide resistance determinants. J. Antimicrob. Chemother. 48(6), 915–918.

On, S.L.W., Jensen, T.K., Bille-Hansen, V., Jorsal, S.E., Vandamme, P., 2002. Prevalence and diversity of Arcobacter spp. isolated from the internal organs of spontaneous porcine abortions in Denmark. Vet. Microbiol. 85(2), 159–167.

Pérez-Cataluña, A., Salas-Massó, N., Diéguez, A.L., Balboa, S., Lema, A., Romalde, J.L., Figueras, M.J., 2018. Revisiting the taxonomy of the genus Arcobacter: getting order from the chaos. Front. Microbiol. 9, 2077.

Petrocchi-Rilo, M., Martínez-Martínez, S., Aguarón-Turrientes, Á., Roca-Martínez, E.,García-Iglesias, M.J., Pérez-Fernández, E., González-Fernández, A., Herencia-Lagunar, E., Gutiérrez-Martín, C.B., 2021. Anatomical site, typing, virulence gene profiling, antimicrobial susceptibility and resistance genes of streptococcus suis isolates recovered from pigs in Spain. Antibiotics. 10, 707.

Ramees, T.P., Dhama, K., Karthik, K., Rathore, R.S., Kumar, A., Saminathan, M., Tiwari, R.,Malik, Y.S., Singh, R.K., 2017. Arcobacter: An emerging food-borne zoonotic pathogen, its public health concerns and advances in diagnosis and control - A comprehensive review. Vet. Q. 37(1), 136–161.

Shrestha, R.G., Tandukar, S., Bhandari, D., Sherchan, S.P., Tanaka, Y., Sherchand, J.B.,Haramoto, E., 2019. Prevalence of Arcobacter and other pathogenic bacteria in river water in Nepal. Water. 11(7), 1416.

Soma Sekhar, M., Tumati, S.R., Chinnam, B.K., Kothapalli, V.S., Sharif, N.M., 2018. Occurrence of Arcobacter species in animal faeces, foods of animal origin and humans in Andhra Pradesh, India. Indian. J. Anim. Res. 52(11), 1649–1653.

Van den Abeele, A.M., Vogelaers, D., Vanlaere, E., Houf, K., 2016. Antimicrobial susceptibility testing of Arcobacter butzleri and Arcobacter cryaerophilus strains isolated from Belgian patients. J. Antimicrob. Chemother. 71(5), 1241-1244.

Vandamme, P., Falsen, E., Rossau, R., Hoste, B., Segers, P., Tytgat, R., De Ley, J., 1991. Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: Emendation of generic descriptions and proposal of Arcobacter gen. nov. Int. J. Syst. Bacteriol. 41(1), 88–103.

Verma, M.K., Ahmad, A.H., Pant, D., Rawat, P., Sharma, S., Arya, N., 2020. Screening of Enrofloxacin and Ciprofloxacin Residues in Chicken Meat by High-Performance Liquid Chromatography. J. Pharm. Res. Int. 32(21), 64-69.

Vicente-Martins, S., Oleastro, M., Domingues, F.C., Ferreira, S., 2018. Arcobacter spp. at retail food from Portugal: Prevalence, genotyping and antibiotics resistance. Food.Control. 85, 107–112.

Vlieghe, E.R., Huang, T.D., Phe, T., Bogaerts, P., Berhin, C., De Smet, B., Peetermans, W.E.,Jacobs, J.A., Glupczynski, Y., 2015. Prevalence and distribution of beta-lactamase coding genes in third-generation cephalosporin-resistant Enterobacteriaceae from bloodstream infections in Cambodia. Eur. J. Clin. Microbiol. Infect Dis. 34(6),1223–1229.

Wareham, D.W., Umoren, I., Khanna, P., Gordon, N.C., 2010. Allele-specific polymerase chain reaction (PCR) for rapid detection of the aac(6’)-Ib-cr quinolone resistance gene. Int. J. Antimicrob. Agents. 36(5), 476–477.

Whiteduck-Léveillée, K., Whiteduck-Léveillée, J., Cloutier, M., Tambong, J.T., Xu, R., Topp,E., Arts, M.T., Chao, J., Adam, Z., Lévesque, C.A., Lapen, D.R., Villemur, R.,Talbot, G., Khan, I.U.H., 2015. Arcobacter lanthieri sp. Nov., isolated from pig and dairy cattle manure. Int. J. Syst. Evol. Microbiol. 65(8), 2709–2716.

Yamauchi, Y., Uehara, Y., Boutin, S., Yamamoto, N., Kuwahara-Arai, K., Kirikae, T.,Hiramatsu, K., Zimmermann, S., 2020. Detection of Arcobacter species in human stool samples by culture and real-time PCR. Juntendo. Med. J. 66(5), 431–438.