The characterization and correlation between the phenotypic and genotypic resistance of Campylobacter spp. isolates from commercial broilers and native chickens in the south of Thailand

References

• Agyare, C., Etsiapa Boamah, V., Ngofi Zumbi, C. & Boateng Osei, F. (2019). Antibiotic use in poultry production and its effects on bacterial resistance. In Y. Kumar (Ed.), Antimicrobial Resistance—A Global Threat (pp. 34–51). London: IntechOpen.
   Google Scholar
• Aleksić, E., Miljković-Selimović, B., Tambur, Z., Aleksić, N., Biočanin, V. & Avramov, S. (2021). Resistance to antibiotics in thermophilic Campylobacters. Frontiers in Medicine, 8, 763434.
   Web of Science ®Google Scholar
• Alonso, R., Mateo, E., Churruca, E., Martinez, I., Girbau, C. & Fernández-Astorga, A. (2005). MAMA-PCR assay for the detection of point mutations associated with high-level erythromycin resistance in Campylobacter jejuni and Campylobacter coli strains. Journal of Microbiological Methods, 63, 99–103.
   PubMed Web of Science ®Google Scholar
• Anon. (2021a). Information on the number of farmers who raise animals and livestock in 2021. https://opendata.nesdc.go.th/dataset/d7681470-0120-47ab-8315-5cd28b9539c8/resource/1b116b37-ce19-415d-ae04-dd734add184f/download/-2564.pdf.
   Google Scholar
• Anon. (2021b). Climate and temperature development in Thailand. https://www.worlddata.info/asia/thailand/climate.php.
   Google Scholar
• Babacan, O., Harris, S.A., Pinho, R.M., Hedges, A., Jørgensen, F. & Corry, J.E.L. (2020). Factors affecting the species of Campylobacter colonizing chickens reared for meat. Journal of Applied Microbiology, 129, 1071–1078.
   PubMed Web of Science ®Google Scholar
• Batchelor, R.A., Pearson, B.M., Friis, L.M., Guerry, P. & Wells, J.M. (2004). Nucleotide sequences and comparison of two large conjugative plasmids from different Campylobacter species. Microbiology, 150, 3507–3517.
   PubMed Web of Science ®Google Scholar
• Blaser, M.J. & Engberg, J. (2014). Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In I. Nachamkin, C.M. Szymanski & M.J. Blaser (Eds.), Campylobacter (pp. 97–121). Washington, DC: ASM Press.
   Google Scholar
• Bolinger, H. & Kathariou, S. (2017). The current state of macrolide resistance in Campylobacter spp.: trends and impacts of resistance mechanisms. Applied and Environmental Microbiology, 83, e00416-17.
   PubMed Web of Science ®Google Scholar
• Boonmar, S., Morita, Y., Fujita, M., Sangsuk, L., Suthivarakom, K., Padungtod, P., Maruyama, S., Kabeya, H., Kato, M., Kozawa, K., Yamamoto, S. & Kimura, H. (2007). Serotypes, antimicrobial susceptibility, and gyr A gene mutation of Campylobacter jejuni isolates from humans and chickens in Thailand. Microbiology and Immunology, 51, 531–537.
   PubMed Web of Science ®Google Scholar
• Boonmar, S., Sangsuk, L., Suthivarakom, K., Padungtod, P. & Morita, Y. (2005). Serotypes and antimicrobial resistance of Campylobacter jejuni isolated from humans and animals in Thailand. Southeast Asian Journal of Tropical Medicine and Public Health, 36, 6.
   Google Scholar
• Borkakoty, B. (2020). Prevalence of Campylobacter enteritis in children under 5 years hospitalised for diarrhoea in two cities of Northeast India. Indian Journal of Medical Microbiology, 38, 32–36.
   PubMed Web of Science ®Google Scholar
• Cagliero, C., Mouline, C., Cloeckaert, A. & Payot, S. (2006). Synergy between efflux pump CmeABC and modifications in ribosomal proteins L4 and L22 in conferring macrolide resistance in Campylobacter jejuni and Campylobacter coli. Antimicrobial Agents and Chemotherapy, 50, 3893–3896.
   PubMed Web of Science ®Google Scholar
• Carrique-Mas, J.J., Bryant, J.E., Cuong, N.V., Hoang, N.V.M., Campbell, J., Hoang, N.V., Dung, T.T.N., Duy, D.T., Hoa, N.T., Thompson, C., Hien, V.V., Phat, V.V., Farrar, J. & Baker, S. (2014). An epidemiological investigation of Campylobacter in pig and poultry farms in the Mekong delta of Vietnam. Epidemiology and Infection, 142, 1425–1436.
   PubMed Web of Science ®Google Scholar
• CDC. (2013). Antibiotic resistance threats in the United States, 2013. https://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf.
   Google Scholar
• Charununtakorn, P., Prachantasena, S. & Luangtongkum, T. (2015). Antimicrobial resistance patterns and flaA genotypes of Campylobacter jejuni isolated from contracted broiler farms in Eastern Thailand. The Thai Journal of Veterinary Medicine, 45, 283–287.
   Web of Science ®Google Scholar
• Chokboonmongkol, C., Patchanee, P., Gölz, G., Zessin, K.-H. & Alter, T. (2013). Prevalence, quantitative load, and antimicrobial resistance of Campylobacter spp. from broiler ceca and broiler skin samples in Thailand. Poultry Science, 92, 462–467.
   PubMed Web of Science ®Google Scholar
• CLSI, VET01-A4. (2013). VET01-A4: performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard—fourth edition.
   Google Scholar
• CLSI, VET01S. (2015). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Wayne, PA: CLSI.
   Google Scholar
• Corcoran, D., Quinn, T., Cotter, L., O’Halloran, F. & Fanning, S. (2005). Characterization of a cmeABC operon in a quinolone-resistant Campylobacter coli isolate of Irish origin. Microbial Drug Resistance, 11, 303–308.
   PubMed Web of Science ®Google Scholar
• Corry, J.E.L. & Atabay, H.I. (2001). Poultry as a source of Campylobacter and related organisms. Journal of Applied Microbiology, 90, 96S–114S.
   PubMed Web of Science ®Google Scholar
• Dasti, J.I., Groß, U., Pohl, S., Lugert, R., Weig, M. & Schmidt-Ott, R. (2007). Role of the plasmid-encoded tet(O) gene in tetracycline-resistant clinical isolates of Campylobacter jejuni and Campylobacter coli. Journal of Medical Microbiology, 56, 833–837.
   PubMed Web of Science ®Google Scholar
• Dohoo, I. (Ed.). (2003). Veterinary Epidemiologic Research. Charlottetown: University of Prince Edward Island.
   Google Scholar
• Elhadidy, M., Miller, W.G., Arguello, H., Álvarez-Ordóñez, A., Duarte, A., Dierick, K. & Botteldoorn, N. (2018). Genetic basis and clonal population structure of antibiotic resistance in Campylobacter jejuni isolated from broiler carcasses in Belgium. Frontiers in Microbiology, 9, 1014.
   PubMed Web of Science ®Google Scholar
• Fravalo, P., Kooh, P., Mughini-Gras, L., David, J., Thébault, A., Cadavez, V. & Gonzales-Barron, U. (2021). Risk factors for sporadic campylobacteriosis: a systematic review and meta-analysis. Microbial Risk Analysis, 17, 100118.
   Web of Science ®Google Scholar
• Gibreel, A. (2006). Macrolide resistance in Campylobacter jejuni and Campylobacter coli. Journal of Antimicrobial Chemotherapy, 58, 243–255.
   PubMed Web of Science ®Google Scholar
• Gibreel, A., Tracz, D.M., Nonaka, L., Ngo, T.M., Connell, S.R. & Taylor, D.E. (2004). Incidence of antibiotic resistance in Campylobacter jejuni isolated in Alberta, Canada, from 1999 to 2002, with special reference to tet (O)-mediated tetracycline resistance. Antimicrobial Agents and Chemotherapy, 48, 3442–3450.
   PubMed Web of Science ®Google Scholar
• Guernier-Cambert, V., Trachsel, J., Maki, J., Qi, J., Sylte, M.J., Hanafy, Z., Kathariou, S. & Looft, T. (2021). Natural horizontal gene transfer of antimicrobial resistance genes in Campylobacter spp. from turkeys and swine. Frontiers in Microbiology, 12, 732969.
   PubMed Web of Science ®Google Scholar
• Hodges, L.M., Taboada, E.N., Koziol, A., Mutschall, S., Blais, B.W., Inglis, G.D., Leclair, D. & Carrillo, C.D. (2021). Systematic evaluation of whole-genome sequencing based prediction of antimicrobial resistance in Campylobacter jejuni and C. coli. Frontiers in Microbiology, 12, 776967.
   PubMed Web of Science ®Google Scholar
• Iovine, N.M. (2013). Resistance mechanisms in Campylobacter jejuni. Virulence, 4, 230–240.
   PubMed Web of Science ®Google Scholar
• Kalupahana, R.S., Mughini-Gras, L., Kottawatta, S.A., Somarathne, S., Gamage, C. & Wagenaar, J.A. (2018). Weather correlates of Campylobacter prevalence in broilers at slaughter under tropical conditions in Sri Lanka. Epidemiology and Infection, 146, 972–979.
   PubMed Web of Science ®Google Scholar
• Killip, S. (2004). What is an intracluster correlation coefficient? Crucial concepts for primary care researchers. The Annals of Family Medicine, 2, 204–208.
   PubMed Web of Science ®Google Scholar
• Magiorakos, A.-P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G., Harbarth, S., Hindler, J.F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D.L., Rice, L.B., Stelling, J., Struelens, M.J., Vatopoulos, A., Weber, J.T. & Monnet, D.L. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18, 268–281.
   PubMed Web of Science ®Google Scholar
• MOPH. (2020). Thailand’s One Health Report on Antimicrobial Consumption and Antimicrobial Resistance in 2018 (p. 168). http://ihppthaigov.net/DB/publication/attachresearch/432/chapter1.pdf.
   Google Scholar
• Mouftah, S.F., Cobo-Díaz, J.F., Álvarez-Ordóñez, A., Elserafy, M., Saif, N.A., Sadat, A., El-Shibiny, A. & Elhadidy, M. (2021). High-throughput sequencing reveals genetic determinants associated with antibiotic resistance in Campylobacter spp. from farm-to-fork. PLoS One, 16, e0253797.
   PubMed Web of Science ®Google Scholar
• Nigusu, Y., Abdissa, A. & Tesfaw, G. (2022). Campylobacter gastroenteritis among under-five children in Southwest Ethiopia. Infection and Drug Resistance, 15, 2969–2979.
   PubMed Web of Science ®Google Scholar
• OECD & Food and Agriculture Organization of the United Nations. (2017). OECD-FAO Agricultural outlook 2017-2026. Paris: OECD.
   Google Scholar
• Okada, K., Wongboot, W., Kamjumphol, W., Suebwongsa, N., Wangroongsarb, P., Kluabwang, P., Chuenchom, N., Swaddiwudhipong, W., Wongchai, T., Manosuthi, W., Assawapatchara, N., Khum-on, P., Udompat, P., Thanee, C., Kitsaran, S., Jirapong, L., Jaiwong, C., Nedsuwan, S., Siripipattanamongkol, C., Okada, P.A., Chantaroj, S., Komukai, S. & Hamada, S. (2020). Etiologic features of diarrheagenic microbes in stool specimens from patients with acute diarrhea in Thailand. Scientific Reports, 10, 4009.
   PubMed Web of Science ®Google Scholar
• Olah, P.A., Doetkott, C., Fakhr, M.K. & Logue, C.M. (2006). Prevalence of the Campylobacter multi-drug efflux pump (CmeABC) in Campylobacter spp. Isolated from freshly processed turkeys. Food Microbiology, 23, 453–460.
   PubMed Web of Science ®Google Scholar
• Padungtod, P., Kaneene, J.B., Hanson, R., Morita, Y. & Boonmar, S. (2006). Antimicrobial resistance in Campylobacter isolated from food animals and humans in northern Thailand. FEMS Immunology & Medical Microbiology, 47, 217–225.
   PubMed Web of Science ®Google Scholar
• Pavlova, M., Alexandrova, E., Donkov, G., Mitova-Mineva, Y., Kantardjiev, T. & Velev, V. (2020). Campylobacter infections among Bulgarian children: molecular characterization and antimicrobial susceptibility. Biotechnology & Biotechnological Equipment, 34, 1038–1042.
   Web of Science ®Google Scholar
• Payot, S., Bolla, J.-M., Corcoran, D., Fanning, S., Mégraud, F. & Zhang, Q. (2006). Mechanisms of fluoroquinolone and macrolide resistance in Campylobacter spp. Microbes and Infection, 8, 1967–1971.
   PubMed Web of Science ®Google Scholar
• Platts-Mills, J.A. & Kosek, M. (2014). Update on the burden of Campylobacter in developing countries. Current Opinion in Infectious Diseases, 27, 444–450.
   PubMed Web of Science ®Google Scholar
• Prachantasena, S., Charununtakorn, P., Muangnoicharoen, S., Hankla, L., Techawal, N., Chaveerach, P., Tuitemwong, P., Chokesajjawatee, N., Williams, N., Humphrey, T. & Luangtongkum, T. (2016). Distribution and genetic profiles of Campylobacter in commercial broiler production from breeder to slaughter in Thailand. PLoS One, 11, e0149585.
   PubMed Web of Science ®Google Scholar
• Prachantasena, S., Charununtakorn, P., Muangnoicharoen, S., Hankla, L., Techawal, N., Chaveerach, P., Tuitemwong, P., Chokesajjawatee, N., Williams, N., Humphrey, T. & Luangtongkum, T. (2017). Climatic factors and prevalence of Campylobacter in commercial broiler flocks in Thailand. Poultry Science, 96, 980–985.
   PubMed Web of Science ®Google Scholar
• Prachantasena, S., Ngasaman, R. & Wiriyaprom, R. (2022). Prevalence and risk factors of Campylobacter infection in goats in southern provinces of Thailand. Tropical Animal Health and Production, 54, 108.
   PubMed Web of Science ®Google Scholar
• Prim, R.C. (1957). Shortest connection networks and some generalizations. Bell System Technical Journal, 36, 1389–1401.
   Google Scholar
• Saengthongpinit, C., Viriyarampa, S. & Sakpuaram, T. (2005). Prevalence of Campylobacter spp. In Chicken from retail markets in Nakhon Pathom Province.
   Google Scholar
• Sibanda, N., McKenna, A., Richmond, A., Ricke, S.C., Callaway, T., Stratakos, A.C., Gundogdu, O. & Corcionivoschi, N. (2018). A review of the effect of management practices on Campylobacter prevalence in poultry farms. Frontiers in Microbiology, 9, 2002.
   PubMed Web of Science ®Google Scholar
• Sriviboone, S. & Komolsevin, R. (2018). Perception of Thai entrepreneurs toward halal certification. BU Academic Review, 17, 33–47.
   Google Scholar
• Statistical Year Book of Thailand. (2021). Statistical yearbook of Thailand. http://service.nso.go.th/nso/nsopublish/pubs/e-book/SYB-2021/index.html.
   Google Scholar
• Stintzi, A. (2003). Gene expression profile of Campylobacter jejuni in response to growth temperature variation. Journal of Bacteriology, 185, 2009–2016.
   PubMed Web of Science ®Google Scholar
• Tamhane, A.R., Westfall, A.O., Burkholder, G.A. & Cutter, G.R. (2016). Prevalence odds ratio versus prevalence ratio: choice comes with consequences. Statistics in Medicine, 35, 5730–5735.
   PubMed Web of Science ®Google Scholar
• Tang, Y., Jiang, Q., Tang, H., Wang, Z., Yin, Y., Ren, F., Kong, L., Jiao, X. & Huang, J. (2020). Characterization and prevalence of Campylobacter spp. from broiler chicken rearing period to the slaughtering process in Eastern China. Frontiers in Veterinary Science, 7, 227.
   PubMed Web of Science ®Google Scholar
• Thomrongsuwannakij, T., Blackall, P.J. & Chansiripornchai, N. (2017). A study on Campylobacter jejuni and Campylobacter coli through commercial broiler production chains in Thailand: antimicrobial resistance, the characterization of DNA gyrase subunit A mutation, and genetic diversity by flagellin A gene restriction fragment length polymorphism. Avian Diseases, 61, 186–197.
   PubMed Web of Science ®Google Scholar
• Truong, D.B., Van Cuong, N., Doan, P.H., Dung, N.T.T., Kiet, B.T., Rushton, J. & Carrique-Mas, J. (2021). Small-scale commercial chicken production: a risky business for farmers in the Mekong Delta of Vietnam. Preventive Veterinary Medicine, 195, 1–7.
   PubMed Web of Science ®Google Scholar
• Wang, G., Clark, C.G., Taylor, T.M., Pucknell, C., Barton, C., Price, L., Woodward, D.L. & Rodgers, F.G. (2002). Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. Journal of Clinical Microbiology, 40, 4744–4747.
   PubMed Web of Science ®Google Scholar
• Wangroongsarb, P., Cheunban, N., Jittaprasatsin, C., Kamthalang, T., Saipradit, N., Chaichana, P., Pulsrikarn, C., Parnmen, S. & Sripichai, O. (2021). Prevalence and antimicrobial susceptibility of Campylobacter isolated from retail chickens in Thailand. International Journal of Food Microbiology, 339, 109017.
   PubMed Web of Science ®Google Scholar
• Wong, J.T., de Bruyn, J., Bagnol, B., Grieve, H., Li, M., Pym, R. & Alders, R.G. (2017). Small-scale poultry and food security in resource-poor settings: a review. Global Food Security, 15, 43–52.
   Google Scholar
• Yao, H., Shen, Z., Wang, Y., Deng, F., Liu, D., Naren, G., Dai, L., Su, C.-C., Wang, B., Wang, S., Wu, C., Yu, E.W., Zhang, Q. & Shen, J. (2016). Emergence of a potent multidrug efflux pump variant that enhances Campylobacter resistance to multiple antibiotics. MBio, 7, e01543–16.
   PubMed Web of Science ®Google Scholar
• Zirnstein, G., Helsel, L., Li, Y., Swaminathan, B. & Besser, J. (2000). Characterization of gyrA mutations associated with fluoroquinolone resistance in Campylobacter coli by DNA sequence analysis and MAMA PCR. FEMS Microbiology Letters, 190, 1–7.
   PubMed Web of Science ®Google Scholar
• Zirnstein, G., Li, Y., Swaminathan, B. & Angulo, F. (1999). Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis. Journal of Clinical Microbiology, 37, 3276–3280.
   PubMed Web of Science ®Google Scholar