Identification of antimicrobial resistance profiles and antimicrobial resistance genes of Campylobacter isolates from broiler farms in Sri Lanka

Authors

  • Jayasundara Liyanage Champika Sajeewa Perera Laboratory of Veterinary Public Health, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan. & Department of Livestock Production, Faculty of Agricultural Sciences, Sabaragamuwa University of Sri Lanka, P.O. Box 02, Belihuloya 70140, Sri Lanka.
  • Marakkale Manage Pathmalal Department of Zoology, University of Sri Jayewardenepura, Sri Soratha Mawatha, Nugegoda 10250, Sri Lanka.
  • Dehinga Prasadi Nayanashani De Silva Department of Chemistry, Faculty of Science, University of Colombo, Colombo 00700, Sri Lanka.
  • Kozue Miura Laboratory of Veterinary Public Health, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan.
  • Akio Yamada Laboratory of Veterinary Public Health, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan.
  • Kazuhiro Hirayama Laboratory of Veterinary Public Health, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan. & Research Center for Food Safety, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan.

DOI:

https://doi.org/10.55677/ijlsar/V03I1Y2024-03

Keywords:

Antimicrobial resistant genes, Antimicrobial resistant profile, Broiler, Campylobacter

Abstract

Antimicrobial resistant (AMR) bacteria including Campylobacter has become an emerging global concern in human and animal health. There are very few researches on AMR Campylobacter conducted in Sri Lanka and none of them studied about AMR genes to the best of our knowledge. The present study focused on the detection of AMR Campylobacter from broiler in Sri Lanka, resistant against frequently used antimicrobials. Further, presence of AMR genes or mutations in responsible genes were compared to the resistant phenotypes. Cloacal swabs were collected from 118 broilers in nine farms covering three provinces in Sri Lanka. One Campylobacter colony per sample was isolated and the antimicrobial susceptibility test of the isolates was performed by inoculating the isolates onto agar plates with threshold concentrations of eight antimicrobial agents which belong to six antimicrobial classes. Three genetic markers for antimicrobial resistance, point mutations in 23S rRNA gene and gyrA gene, and the presence of resistant gene, tet(O) were also investigated. Altogether, 73 samples were Campylobacter positive of which 59 were Campylobacter jejuni, 13 were Campylobacter coli and one was unidentified Campylobacter. All isolates were resistant to three or more antimicrobials tested. The isolates were frequently resistant to ciprofloxacin, nalidixic acid, trimethoprim-sulfamethoxazole, amoxicillin and tetracycline, and susceptible to gentamicin and streptomycin, while the resistance to erythromycin was different between the species. Genetic screening revealed that most of the isolates possessed one or more of these genetic markers. This study urges the need of continuous surveillance for AMR Campylobacter in Sri Lanka.

References

Alahakoon, A. U., Jo, C., & Jayasena, D. D. (2016). An Overview of Meat Industry in Sri Lanka: A Comprehensive Review. Korean Journal for Food Science of Animal Resources, 36(2), 137–144. https://doi.org/10.5851/kosfa.2016.36.2.137

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(1), 99–103. https://doi.org/10.1016/j.mimet.2005.03.013

De Silva, W. K. (2013). Country report: Sri Lanka. In Report of Thirty-seventh Session of the Animal Production and Health Commission for Asia and the Pacific (APHCA), pp. 128-130. (online) Available at: https://www.fao.org/3/i3485e/i3485e00.htm.

Deckert, A. E., Reid-Smith, R. J., Tamblyn, S., Morrell, L., Seliske, P., Jamieson, F. B., Irwin, R., Dewey, C. E., Boerlin, P., & Mcewen, S. A. (2013). Burden of illness and factors associated with duration of illness in clinical campylobacteriosis. Epidemiology and Infection, 141(12), 2536–2546. https://doi.org/10.1017/s0950268813000332

Ekkapobyotin, C., Padungtod, P., & Chuanchuen, R. (2008). Antimicrobial resistance of Campylobacter coli isolates from swine. International Journal of Food Microbiology, 128(2), 325–328. https://doi.org/10.1016/j.ijfoodmicro.2008.09.005

Elhadidy, M., Ali, M .M., El-Shibiny, A., Miller, W. G., Elkhatib, W. F., Botteldoorn, N., Dierick, K. (2020). Antimicrobial resistance patterns and molecular resistance markers of Campylobacter jejuni isolates from human diarrheal cases. PLoS ONE, 15(1): e0227833. https://doi.org/10.1371/journal.pone.0227833

European Food Safety Authority. (2010). Scientific Opinion on Quantification of the risk posed by broiler meat to human campylobacteriosis in the EU. (2010). EFSA Journal, 8(1), 1437. https://doi.org/10.2903/j.efsa.2010.1437

Fonseca, B. B., Fernandez, H., Rossi, D. A., (2016). Campylobacter spp. and Related Organisms in Poultry, Springer, Switzerland.

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(9), 3442–3450. https://doi.org/10.1128/aac.48.9.3442-3450.2004

Han, X., Zhu, D., Lai, H., Zeng, H., Zhou, K., Zou, L., Wu, C., Han, G., & Liu, S. (2016). Prevalence, antimicrobial resistance profiling and genetic diversity of Campylobacter jejuni and Campylobacter coli isolated from broilers at slaughter in China. Food Control, 69, 160–170. https://doi.org/10.1016/j.foodcont.2016.04.051

Holasova, M., Karpiskova, R., Karpiskova, S., Babak, V., & Schlegelova, J. (2007). Comparison of methods for the determination of antimicrobial resistance in Campylobacter spp. human and the food chain isolates. Veterinární Medicína, 52(4), 169–174. https://doi.org/10.17221/2030-vetmed

Iddamalgoda, A., Sugiyama, M., Oguri, K., Arahata, K., Premasiri, H. P. (1998). A study on development of Sri Lankan poultry industry-importance of rural poultry sector. Research Bulletin-Faculty of Agriculture Gifu University, 87-96. (online) Available at: http://repository.lib.gifu-u.ac.jp/bitstream/123456789/5544/1/KJ00000707791.pdf

Iovine, N. M. (2013). Resistance mechanisms in Campylobacter jejuni. Virulence, 4(3), 230–240. https://doi.org/10.4161/viru.23753

Khan, J. A., Rathore, R. S., Abulreesh, H. H., Qais, F. A., & Ahmad, I. (2018). Prevalence and Antibiotic Resistance Profiles of Campylobacter jejuni Isolated from Poultry Meat and Related Samples at Retail Shops in Northern India. Foodborne Pathogens and Disease, 15(4), 218–225. https://doi.org/10.1089/fpd.2017.2344

Kottawatta, K., Van Bergen, M., Abeynayake, P., Wagenaar, J., Veldman, K., & Kalupahana, R. (2017). Campylobacter in Broiler Chicken and Broiler Meat in Sri Lanka: Influence of Semi-Automated vs. Wet Market Processing on Campylobacter Contamination of Broiler Neck Skin Samples. Foods, 6(12), 105. https://doi.org/10.3390/foods6120105

Levy, S. B. (2002). Factors impacting on the problem of antibiotic resistance. Journal of Antimicrobial Chemotherapy, 49(1), 25–30. https://doi.org/10.1093/jac/49.1.25

Luangtongkum, T., Jeon, B., Han, J., Plummer, P., Logue, C. M., & Zhang, Q. (2009). Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiology, 4(2), 189–200. https://doi.org/10.2217/17460913.4.2.189

Nguyen, T. N. M., Hotzel, H., Njeru, J., Mwituria, J., El-Adawy, H., Tomaso, H., Neubauer, H., & Hafez, H. M. (2016). Antimicrobial resistance of Campylobacter isolates from small scale and backyard chicken in Kenya. Gut Pathogens, 8(1). https://doi.org/10.1186/s13099-016-0121-5

Nisar, M., Ahmad, M. U. D., Mushtaq, M. H., Shehzad, W., Hussain, A., Muhammad, J., Nagaraja, K. V., & Goyal, S. M. (2017). Prevalence and antimicrobial resistance patterns of Campylobacter spp. isolated from retail meat in Lahore, Pakistan. Food Control, 80, 327–332. https://doi.org/10.1016/j.foodcont.2017.03.048

Obeng, A., Rickard, H., Sexton, M., Pang, Y., Peng, H., & Barton, M. (2012). Antimicrobial susceptibilities and resistance genes in Campylobacter strains isolated from poultry and pigs in Australia. Journal of Applied Microbiology, 113(2), 294–307. https://doi.org/10.1111/j.1365-2672.2012.05354.x

Perera, J. L. C. S., De Silva, D. P. N., Hirayama, K. (2020). Impact of antibiotic resistant Campylobacter isolated from poultry: A concise review. Journal of Agriculture and Value Addition, 3(1), 60˗69.

Priyankarage, N. (2016). Use of antibiotics for non-therapeutic purpose in food animal production in Sri Lanka: current status, need for control, measures and initiatives. (online) Available at: https://cdn.cseindia.org/userfiles/Sri%20Lanka_NPriyankarage.pdf

Priyankarage, N. (2019). Current status of animal feed industry in Sri Lanka. (online) Available at: https://rr-asia.woah.org/wp-content/uploads/2020/01/2-4-current-status-of-animal-feed-industry-sri-lanka.pdf

Son, I., Englen, M. D., Berrang, M. E., Fedorka-Cray, P. J., & Harrison, M. A. (2007). Antimicrobial resistance of Arcobacter and Campylobacter from broiler carcasses. International Journal of Antimicrobial Agents, 29(4), 451–455. https://doi.org/10.1016/j.ijantimicag.2006.10.016

Tegner, C., Sunil-Chandra, N. P., Wijesooriya, W. R. P. L. I., Perera, B. V., Hansson, I., Fahlman, A. (2019). Detection, identification, and antimicrobial susceptibility of Campylobacter spp. and Salmonella spp. from free-ranging nonhuman primates in Sri Lanka. Journal of Wildlife Diseases, 55: 879-884.

Woźniak-Biel, A., Bugla-Płoskońska, G., Kielsznia, A., Korzekwa, K., Tobiasz, A., Korzeniowska-Kowal, A., & Wieliczko, A. (2018). High Prevalence of Resistance to Fluoroquinolones and Tetracycline Campylobacter Spp. Isolated from Poultry in Poland. Microbial Drug Resistance, 24(3), 314–322. https://doi.org/10.1089/mdr.2016.0249

Zhang, A., Song, L., Liang, H., Gu, Y., Zhang, C., Liu, X., Zhang, J., & Zhang, M. (2016). Molecular subtyping and erythromycin resistance of Campylobacter in China. Journal of Applied Microbiology, 121(1), 287–293. https://doi.org/10.1111/jam.13135

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. https://doi.org/10.1128/JCM.37.10.3276-80.1999

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Published

2024-01-04

How to Cite

Perera, J. L. C. S., Pathmalal, M. M., De Silva, D. P. N., Miura, K., Yamada, A., & Hirayama, K. (2024). Identification of antimicrobial resistance profiles and antimicrobial resistance genes of Campylobacter isolates from broiler farms in Sri Lanka. International Journal of Life Science and Agriculture Research, 3(1), 14–21. https://doi.org/10.55677/ijlsar/V03I1Y2024-03