Survey on the presence of integrons in Edwardsiella ictaluri, the causative agent of bacillary necrosis on intensively farmed striped catfish (Pangasianodon hypophthalmus) in the Mekong Delta
Main Article Content
Abstract
The purpose of this research was to evaluate the presence of the integrons and characterise the gene cassette regions in E. ictaluri that causes bacillus necrosic of Pangasius on striped catfish (Pangasianodon hypophthalmus) in the Mekong Delta. By using PCR technique and gene sequencing, the finding identified 24/67 (35,82%) class 1 integron-positive E. ictaluri strains. Meanwhile, no class 2 and 3 integrons were detected in the study. Besides, our result also found many different gene cassette regions (0,65 kbp, 0,8 kbp, 0,95 kbp, 1,0 kbp, 1,2 kbp, 1,5 kbp and 2,5 kbp ) encoding to dihydrofolate reductase, aminoglycoside adenyltransferase, aminoglycoside N(6')-acetyltransferase and β-lactamase enzymes resistant to different antibiotics in E. ictaluri. The presence of the mobile genetic elements (class 1 integrons) in E. ictaluri in this research showed the ability that bacteria can transfer antimicrobial resistance genes to other bacteria in the aquatic environment. Therefore, using antibiotics for disease prevention in aquaculture should be managed more strictly
References
Arakawa, Y., M. Murakami, K. Suzuki, H. Ito, R. Wacharotayankun, S. Ohsuka, N. Kato and M. Ohta, 1995. A novel integron-like element carrying the metallo-beta-lactamase gene blaIMP. Antimicrobial Agents and Chemotherapy, 39: 1612-1615.
Bagré T.S., B. Sambe-Ba, H.B. Ibrahim, G.B. Tchamba, R. Dembélé, A.A. Wane, E. Bako, A.S. Traoré, N. Barro1 and A. Gassama-Sow, 2017. Isolation and characterization of enteropathogenic and enterotoxinogenic Escherichia coli from dairy products consumed in Burkina Faso. African Journal of Microbiology Research, 11: 537-545.
Barlow, R.S., J.M. Pemberton, P.M. Desmarchelier and K.S. Gobius, 2004. Isolation and characterization of integron-containing bacteria without antibiotic selection. Antimicrobial Agents and Chemotherapy, 48: 838-842.
Barraud O., M. Casellas, C. Dagot and M.C. Ploy, 2013. An antibiotic-resistant class 3 integron in an Enterobacter cloacae isolate from hospital effluent. Clinical Microbiology and Infection, 19: E306-E308.
Bauer, A.L., W.M.M. Kirby, J.C. Sherris and M. Turck, 1966. Antibiotic susceptibility testing by a standardized single disk method. American journal of clinical pathology, 45: 493-496.
Cambray, G., A.M. Guerout and D. Mazel, 2010. Integrons. Annual Review of Genetics, 44: 141-166.
Canal N., K.L. Meneghetti, C.P. de Almeida, M. da Rosa Bastos, L.M. Otton and G. Corcão, 2016. Characterization of the variable region in the class 1 integron of antimicrobial-resistant Escherichia coli isolated from surface water. Brazilian Journal of Microbiology, 47: 337-344.
Clinical and Laboratory Standards Institute, 2012. Performance standards for antimicrobial susceptibility testing; twenty-second information supplement, M100-S22, Vol. 32 No. 3, Replaces M100-S21, Vol. 31 No. 1. Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500, Wayne, PA 19087, 2012.
Correia M., F. Boavida, F. Grosso, M.J. Salgado, L.M. Lito, J.M. Cristino and A.M. Duarte, 2003. Molecular characterization of a new class 3 integron in Klebsiella pneumoniae. Antimicrobial Agents and Chemotherapy, 47: 2838-2843.
Davies, J. and D. Davies, 2010. Origins and Evolution of Antibiotic Resistance. Microbiology and Molecular Biology Reviews, 74: 417-433.
Dung, T.T., F. Haesebrouck, P. Sorgeloos, N.A Tuan and F. Pasmans, 2009. IncK plasmid-mediated tetracyclin resistance in Edwardsiella ictaluri isolates from diseased freshwater catfish in Vietnam. Aquaculture, 295: 157-159.
Dung, T.T., N.T.N. Ngoc, N.Q. Thinh, D.T.M. Thy, N.A. Tuan, A. Shinn and M. Crumlish, 2008. Common diseases of Pangasius Catfish farmed in Vietnam. Global Aquaculture Advocate, 11: 76-77.
Fluit, A.C. and F.J. Schmitz, 2004. Resistance integrons and super-integrons. Clinical Microbiology and Infection, 10: 272-288.
Fluit, A.C., and F.J. Schmitz, 1999. Class 1 integrons, gen cassettes, mobility, and epidemiology. European Journal of Clinical Microbiology and Infectious Diseases, 18: 761-770.
Frank T., V. Gautier, A. Talarmin, R. Bercion and G. Arlet, 2007. Characterization of sulfonamide resistance genes and class 1 integron gene cassettes in Enterobacteriaceae, Central African Republic (CAR). Journal of Antimicrobial Chemotherapy, 59: 742-745.
Goldstein, C., M.D. Lee, S. Sanchez, C. Hudson, B. Phillips, B. Register, M. Grady, C. Liebert, A.O. Summers, D.G. White, and J.J. Maurer, 2001. Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrobial Agents and Chemotherapy, 45: 723-726.
Infante B., M. Grape, M. Larsson, C. Kristiansson, L. Pallecchic, G.M. Rossolinic and G. Kronvalla, 2005. Acquired sulfonamide resistance genes in faecal Escherichia coli from healthy children in Bolivia and Peru. International Journal of Antimicrobial Agents, 25: 308-312.
Jacobs, L. and H.Y. Chenia, 2007. Characterization on integrons and tetrecycline resistance determinants in Aeromonas spp. isolated from South African aquaculture systems. International Journal of Food Microbiology, 114: 295-306.
Kadlec, K. and S. Schwarz. 2008. Analysis and distribution of class 1 and class 2 integrons and associated gen cassettes among Escherichia coli isolates from swine, horses, cats and dogs collected in the BfT-GermVet monitoring study. Journal of Antimicrobial Chemotherapy, 62: 469-473.
Karczmarczyk M., Y. Abbott, C. Walsh, N. Leonard and S. Fanning, 2011. Characterization of multidrug-resistant Escherichia coli isolates from animals presenting at a University Veterinary Hospital. Applied and Environmental Microbiology, 77: 7104-7112.
Kargar M., Z. Mohammadalipour, A. Doosti, S. Lorzadeh and A. Japoni-Nejad, 2014. High Frequency of Class 2 and 3 Integrons Related to Drug-Resistance in Clinical Isolates of Diarrheagenic E. coli in Iran. Osong Public Health and Research Perspective, 5: 193e198
Kim, S., S.H. Kim, J. Kim, J.H. Shin, B.K. Lee, and M.S. Park, 2010. Occurrence and distribution of various genetic structures of class 1 and class 2 integrons in Salmonella enterica isolates from foodborne disease patients in Korea for 16 years. Foodborne Pathogens and Disease, 8: 319-324.
Koczura R., A. Semkowska and J. Mokracka, 2014. Integron-bearing Gram-negative bacteria in lake waters. Letters in Applied Microbiology, 59: 514-519.
Koeleman, J.G.M., J. Stoof, M.W. Van Der Bijl, C.M.J.E. Vandenbroucke-Grauls and P.H.M. Savelkoul, 2001. Identification of epidemic strains of Acinetobacter baumannii by integrase gene PCR. Journal of Clinical Microbiology, 39: 8-13.
Kotlarska E., A. Łuczkiewicz, M. Pisowacka and A. Burzyński, 2015. Antibiotic resistance and prevalence of class 1 and 2 integrons in Escherichia coli isolated from two wastewater treatment plants, and their receiving waters (Gulf of Gdansk, Baltic Sea, Poland). Environmental Science and Pollut ion Research, 22: 2018-2030.
Lee M.F., C.F. Peng, Y.H. Lin, S.R. Lin and Y.H. Chen, 2008. Molecular diversity of class 1 integrons in human isolates of Aeromonas spp. from southern Taiwan. Japanese Journal of Infectious Diseases, 61: 343-349.
Levesque, C., L. Piche, C. Larose and P.H. Roy, 1995. PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrobial Agents and Chemotherapy, 39, 185-191.
Lin M., X. Wu, Q. Yan, Y. Ma, L. Huang, Y. Qin and X. Xu, 2016. Incidence of antimicrobial-resistance genes and integrons in antibiotic-resistant bacteria isolated from eels and aquaculture ponds. Diseases of Aquatic Organisms, 120: 115-123.
Lukkana, M., J. Wongtavatchai, and R. Chuanchuen, 2011. Class 1 Integrons in Aeromonas hydrophila isolates from farmed Nile Tilapia (Oreochromis nilotica). The Journal of Veterinary Medical Science, 4: 435-440.
Mandomando I., D. Jaintilal, M.J. Pons, X. Valles, M. Espasa, L. Mensa, B. Sigauque, S. Sanz, J. Sacarlal, E. Macete, F. Abacassamo, P.L. Alonso and J. Ruiz, 2009. Antimicrobial Susceptibility and Mechanisms of Resistance in Shigella and Salmonella Isolates from Children under Five Years of Age with Diarrhea in Rural Mozambique. Antimicrobial Agents and Chemotherapy, 53: 2450-2454.
Mazel, D., B. Dychinco, V.A. Webb and J. Davies, 2000. Antibiotic resistance in the ECOR collection: integrons and identification of a novel aad gene. Antimicrobial Agents and Chemotherapy, 44: 1568-1574.
Miko A., K. Pries, A. Schroeter and R. Helmuth, 2005. Molecular mechanisms of resistance in multidrug-resistant serovars of Salmonella enterica isolated from foods in Germany. Journal of Antimicrobial Chemotherapy, 56: 1025-1033.
Mokracka J., R. Koczura and A. Kaznowski, 2012. Multiresistant Enterobacteriaceae with class 1 and class 2 integrons in a municipal wastewater treatment plant. Water Research, 46: 3353-3363.
Navia M.M., J. Gascon and J. Vila, 2005. Analysis of the mechanisms of resistance to several antimicrobial agents in Shigella spp. causing travellers’ diarrhoea. Clinical Microbiology and Infectious Diseases, 11: 1035-1047.
Nawaz, M., A.A. Khan, S. Khan, K. Sung, K. Kerdahi and R. Steele, 2009. Molecular characterization of tetracycline resistant genes and integrons from avirulent strains of Escherichia coli isolated from catfish. Foodborne Pathogens and Disease, 5: 553-559.
Ndi, L.O. and M.D. Barton, 2012. Resistance Determinants of Pseudomonas species from Aquaculture in Australia. Journal of Aquaculture Research & Development, 3:1-6.
Ndi, O.L. and M.D. Barton, 2011. Incidence of class 1 integron and other antibiotic resistance determinants in Aeromonas spp. from rainbow trout farms in Australia. Journal of Fish Diseases, 34: 589-599.
Nguyen H.N.K., V.T.T. Hao, N.H. Thinh, P.M. Smooker, J. Shimeta and P.J. Coloe, 2014. Molecular characterization of antibiotic resistance in Pseudomonas and Aeromonas isolates from catfish of the Mekong Delta, Vietnam. Veterinary Microbiology, 171: 397-405.
Nguyễn Thiện Nam, Phạm Thanh Hương, Trần Duy Phương và Từ Thanh Dung, 2010. Nghiên cứu sự đa kháng thuốc của vi khuẩn Edwardsiella ictaluri gây bệnh trên cá tra (Pangasianodon hypophthalmus). Tạp chí Khoa học Trường Đại học Cần Thơ, số 14b: 200-210.
Peirano G., Y. Agersø, F.M. Aarestrup, E.M.F. dos Reis and D. dos Prazeres Rodrigues, 2006. Occurrence of integrons and antimicrobial resistance genes among Salmonella enterica from Brazil. Journal of Antimicrobial Chemotherapy, 58: 305-309.
Phu T.M., N.T. Phuong, T.T. Dung, D.M. Hai, V.N. Son, A. Rico, J.H. Clausen, H. Madsen, F. Murray and A. Dalsgaard, 2015. An evaluation of fish health-management practices and occupational health hazards associated with Pangasius catfish (Pangasianodon hypophthalmus) aquaculture in the Mekong Delta, Vietnam. Aquaculture Research, 47: 2778–2794.
Ploy M.C., D. Chainier, N.H. Tran Thi, I. Poilane, P. Cruaud, F. Denis, A. Collignon and T. Lambert, 2003. Integron-associated antibiotic resistance in Salmonella enterica serovar typhi from Asia. Antimicrobial Agents and Chemotherapy, 47: 1427-1429.
Rajpara N., B.M.R.N.S. Kutar, R. Sinha, D. Nag, H. Koley, T. Ramamurthy and A.K. Bhardwaj, 2015. Role of integrons, plasmids and SXT elements in multidrug resistance of Vibrio cholerae and Providencia vermicola obtained from a clinical isolate of diarrhea. Frontiers in Microbiology, 6: 1-11.
Roberts M.C., S. Schwarz and H.J.M. Aarts, 2012. Erratum: acquired antibiotic resistance genes: an overview. Frontiers in Microbiology, 3: 384.
Saenz Y., L. Brinas, E. Dominguez, J. Ruiz, M. Zarazaga, J. Vila and C. Torres, 2004. Mechanisms of Resistance in Multiple-Antibiotic-Resistant Escherichia coli Strains of Human, Animal, and Food Origins. Antimicrobial agents and Chemmotherapy, 48: 3996-4001.
Saenz Y., L. Vinue, E. Ruiz, S. Somalo, S. Martınez, B. Rojo-Bezares, M. Zarazaga and C. Torres, 2010. Class 1 integrons lacking qacEΔ1 and sul1 genes in Escherichia coli isolates of food, animal and human origins. Veterinary Microbiology, 144: 493-497.
Sakai, T., K. Yuasa, M. Sano and T. Iida, 2009. Identification of Edwardsiella ictaluri and E. tarda by Species-Specific Polymerase Chain Reaction Targeted to the Upstream Region of the Fimbrial Gene. Journal of Aquatic Animal Health, 21: 124-132.
Schmidt A.S., M.S. Bruuna, J.L. Larsena and I. Dalsgaard, 2001b. Characterization of class 1 integrons associated with R-plasmids in clinical Aeromonas salmonicida isolates from various geographical areas. Journal of Antimicrobial Chemotherapy, 47: 735-743.
Schmidt, A.S., M.S. Bruun, I. Dalsgaard and J.L. Larsen., 2001a. Incidence, distribution and spread of tetracycline resistance determinants and integron associated antibiotic resistance genes motile Aeromonads from a fish farming environment. Applied and Environmental Microbiology, 67: 5675-5682.
Shah S.Q.A., F.C. Cabello, T.M. L’Abée-Lund, A. Tomova, H.P. Godfrey, A.H. Buschmann and H. Sørum, 2014. Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites. Environmental Microbiology, 16: 1310-1320.
Shaheen B.W., O.A. Oyarzabal and D.M. Boothe, 2010. The role of class 1 and 2 integrons in mediating antimicrobial resistance among canine and feline clinical E. coli isolates from the US. Veterinary Microbiology, 144: 363-370.
Shin H.W., J. Lim, S. Kim, J. Kim, G.C. Kwon and S.H Koo, 2015. Characterization of Trimethoprim-Sulfamethoxazole Resistance Genes and Their Relatedness to Class 1 Integron and Insertion Sequence Common Region in Gram-Negative Bacilli. Journal of Microbiology and Biotechnology, 25: 137-142.
Sun J., M. Zhou, Q. Wu and Y. Ni, 2010. Characterization of two novel gene cassettes, dfrA27 and aadA16, in a non-O1, non-O139 Vibrio cholerae isolate from China. Clinical Microbiology and Infection, 16: 1125-1129.
Sunde M., 2005. Prevalence and characterization of class 1 and class 2 integrons in Escherichia coli isolated from meat and meat products of Norwegian origin. Journal of Antimicrobial Chemotherapy, 56: 1019-1024.
Tajbakhsh E., F. Khamesipour, R. Ranjbar and I.C. Ugwu, 2015. Prevalence of class 1 and 2 integrons in multi-drug resistant Escherichia coli isolated from aquaculture water in Chaharmahal Va Bakhtiari province, Iran. Annals of Clinical Microbiology and Antimicrobials, 14: 37.
Tchuinte S.P.L., T. Stalder, S. Venditti, A. Ngandjio, C. Dagot, M.C. Ploy and O. Barraud, 2016. Characterisation of class 3 integrons with oxacillinase gene cassettes in hospital sewage and sludge samples from France and Luxembourg. International Journal of Antimicrobial Agents, 48:431-434
van Essen-Zandbergen A., H. Smith, K. Veldman and D. Mevius, 2007. Occurrence and characteristics of class 1, 2 and 3 integrons in Escherichia coli, Salmonella and Campylobacter spp. in the Netherlands. Journal of Antimicrobial Chemotherapy, 59: 746-750.
Vega-Sanchez V., F. Latif-Eugenın, E. Soriano-Vargas, R. Beaz-Hidalgo, M.J. Figueras, Ma.G. Aguilera-Arreola and G. Castro-Escarpulli, 2014. Re-identification of Aeromonas isolates from rainbow trout and incidence of class 1 integron and b-lactamase genes. Veterinary Microbiology, 172: 528-533.
Vinué L., Y. Sáenz, B. Rojo-Bezares, I. Olarte, E. Undabeitia, S. Somaloa, M. Zarazaga and C. Torres, 2010. Genetic environment of sul genes and characterisation of integrons in Escherichia coli isolates of blood origin in a Spanish hospital. International Journal of Antimicrobial Agents, 35: 492-496.
Vinué, L., Y. Sáenz, S. Somalo, E. Escudero, M.A. Moreno, F. Ruiz-Larrea, and C. Torres, 2008. Prevalence and diversity of integrons and associated resistance genes in faecal Escherichia coli isolates of healthy humans in Spain. Journal of Antimicrobial Chemotherapy, 62: 934-937.
Wei Q., X. Jiang, Z. Yang, N. Chen, X. Chen, G. Li and Y. Lu, 2009. dfrA27, a new integron-associated trimethoprim resistance gene from Escherichia coli. Journal of Antimicrobial Chemotherapy, 63: 405-419.
White P.A., Christopher J. McIver, Yi-Mo Deng, William D. Rawlinson, 2000. Characterisation of two new gene cassettes, aadA5 and dfrA17. FEMS Microbiology Letters, 182: 265-269.
White, P.A., C.J. McIver and W.D. Rawlinson, 2001. Integrons and gen cassettes in the Enterobacteriaceae. Antimicrobial Agents and Chemotherapy, 45: 2658-2661.
Yan H., L. Li, M. Zong, M.J. Alam, S. Shinoda and L. Shi, 2010. Occurrence and characteristics of class 1 and 2 integrons in clinical bacteria isolates from patients in South China. Journal of Health Science, 56: 442-450.