DOI QR코드

DOI QR Code

Occurrence and antibiotic susceptibility of fish bacteria isolated from Oreochromis niloticus (Nile tilapia) and Clarias gariepinus (African catfish) in Uganda

  • Wamala, S.P. (Norwegian University of Life Sciences, Faculty of Veterinary Medicine) ;
  • Mugimba, K.K. (Norwegian University of Life Sciences, Faculty of Veterinary Medicine) ;
  • Mutoloki, S. (Norwegian University of Life Sciences, Faculty of Veterinary Medicine) ;
  • Evensen, O. (Norwegian University of Life Sciences, Faculty of Veterinary Medicine) ;
  • Mdegela, R. (Department of Veterinary Medicine and Public Health, College of Veterinary and Medical Sciences, Sokoine University of Agriculture) ;
  • Byarugaba, D.K. (College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University) ;
  • Sorum, H. (Norwegian University of Life Sciences, Faculty of Veterinary Medicine)
  • Received : 2017.10.25
  • Accepted : 2017.12.18
  • Published : 2018.02.28

Abstract

The intention of this study was to identify the bacterial pathogens infecting Oreochromis niloticus (Nile tilapia) and Clarias gariepinus (African catfish), and to establish the antibiotic susceptibility of fish bacteria in Uganda. A total of 288 fish samples from 40 fish farms (ponds, cages, and tanks) and 8 wild water sites were aseptically collected and bacteria isolated from the head kidney, liver, brain and spleen. The isolates were identified by their morphological characteristics, conventional biochemical tests and Analytical Profile Index test kits. Antibiotic susceptibility of selected bacteria was determined by the Kirby-Bauer disc diffusion method. The following well-known fish pathogens were identified at a farm prevalence of; Aeromonas hydrophila (43.8%), Aeromonas sobria (20.8%), Edwardsiella tarda (8.3%), Flavobacterium spp. (4.2%) and Streptococcus spp. (6.3%). Other bacteria with varying significance as fish pathogens were also identified including Plesiomonas shigelloides (25.0%), Chryseobacterium indoligenes (12.5%), Pseudomonas fluorescens (10.4%), Pseudomonas aeruginosa (4.2%), Pseudomonas stutzeri (2.1%), Vibrio cholerae (10.4%), Proteus spp. (6.3%), Citrobacter spp. (4.2%), Klebsiella spp. (4.2%) Serratia marcescens (4.2%), Burkholderia cepacia (2.1%), Comamonas testosteroni (8.3%) and Ralstonia picketti (2.1%). Aeromonas spp., Edwardsiella tarda and Streptococcus spp. were commonly isolated from diseased fish. Aeromonas spp. (n = 82) and Plesiomonas shigelloides (n = 73) were evaluated for antibiotic susceptibility. All isolates tested were susceptible to at-least ten (10) of the fourteen antibiotics evaluated. High levels of resistance were however expressed by all isolates to penicillin, oxacillin and ampicillin. This observed resistance is most probably intrinsic to those bacteria, suggesting minimal levels of acquired antibiotic resistance in fish bacteria from the study area. To our knowledge, this is the first study to establish the occurrence of several bacteria species infecting fish; and to determine antibiotic susceptibility of fish bacteria in Uganda. The current study provides baseline information for future reference and fish disease management in the country.

Keywords

References

  1. Abowei J, Briyai O. A review of some bacteria diseases in Africa culture fisheries. Asian Journal of Medical Sciences. 2011;3(5):206-17.
  2. Akinbowale OL, Peng H, Barton M. Antimicrobial resistance in bacteria isolated from aquaculture sources in Australia. J Appl Microbiol. 2006;100:1103-13. https://doi.org/10.1111/j.1365-2672.2006.02812.x
  3. Akoll P, Mwanja WW. Fish health status, research and management in East Africa: past and present. Afr J Aquat Sci. 2012;37(2):117-29. https://doi.org/10.2989/16085914.2012.694628
  4. Aravena-Roman M, et al. Antimicrobial susceptibilities of Aeromonas strains isolated from clinical and environmental sources to 26 antimicrobial agents. Antimicrob Agents Chemother. 2012;56(2):1110-2. https://doi.org/10.1128/AAC.05387-11
  5. Balsalobre L, et al. Detection of metallo-$\beta$-lactamases-encoding genes in environmental isolates of Aeromonas Hydrophila and Aeromonas jandaei. Lett Appl Microbiol. 2009;49(1):142-5. https://doi.org/10.1111/j.1472-765X.2009.02625.x
  6. Balsalobre L, et al. Presence of blaTEM-116 gene in environmental isolates of Aeromonas Hydrophila and Aeromonas jandaei from Brazil. Braz J Microbiol. 2010;41(3):718-9. https://doi.org/10.1590/S1517-83822010000300023
  7. Baron S, et al. Aeromonas diversity and antimicrobial susceptibility in freshwateran attempt to set generic epidemiological cut-off values. Front Microbiol. 2017;8:503.
  8. Barton BA. Stress in finfish: past present and future. A historical presentation. In: Iwama G, et al., editors. Fish stress and health in aquaculture, Society for Experimental Biology seminar series 62. Cambridge: Cambridge University Press; 1997. p. 1-33.
  9. Barton MD. Antibiotic use in animal feed and its impact on human health. Nutr Res Rev. 2000;13(2):279-99. https://doi.org/10.1079/095442200108729106
  10. Baya A, et al. Serratia Marcescens: a potential pathogen for fish. J Fish Dis. 1992; 15(1):15-26. https://doi.org/10.1111/j.1365-2761.1992.tb00632.x
  11. Bernardet JF, et al. Polyphasic study of Chryseobacterium strains isolated from diseased aquatic animals. Syst Appl Microbiol. 2005;28(7):640-60. https://doi.org/10.1016/j.syapm.2005.03.016
  12. Biyela PT, Lin J, Bezuidenhout CC. The role of aquatic ecosystems as reservoirs of antibiotic resistant bacteria and antibiotic resistance genes. Water Sci Technol. 2004;50(1):45-50.
  13. Bondad-Reantaso MG, et al. Disease and health management in Asian aquaculture. Vet Parasitol. 2005;132(3-4):249-72. https://doi.org/10.1016/j.vetpar.2005.07.005
  14. Brander KM. Global fish production and climate change. Proc Natl Acad Sci. 2007; 104(50):19709-14. https://doi.org/10.1073/pnas.0702059104
  15. Burkhardt-Holm P, Peter A, Segner H. Decline of fish catch in Switzerland. Aquat Sci. 2002;64(1):36-54. https://doi.org/10.1007/s00027-002-8053-1
  16. Byarugaba D. Antimicrobial resistance in developing countries and responsible risk factors. Int J Antimicrob Agents. 2004;24(2):105-10. https://doi.org/10.1016/j.ijantimicag.2004.02.015
  17. Byarugaba D, Kisame R, Olet S. Multi-drug resistance in commensal bacteria of food of animal origin in Uganda. Afr J Microbiol Res. 2011;5(12):1539-48. https://doi.org/10.5897/AJMR11.202
  18. Cabello FC. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol. 2006;8(7):1137-44. https://doi.org/10.1111/j.1462-2920.2006.01054.x
  19. Cantas L, et al. A brief multi-disciplinary review on antimicrobial resistance in medicine and its linkage to the global environmental microbiota. Front Microbiol. 2013;4:96.
  20. Castro-Escarpulli G, et al. Characterisation of Aeromonas spp. isolated from frozen fish intended for human consumption in Mexico. Int J Food Microbiol. 2003;84(1):41-9. https://doi.org/10.1016/S0168-1605(02)00393-8
  21. Chen HQ, Lu CP. Study on the pathogen of epidemic septicemia occurred in cultured cyprinoid fishes in southeastern China. Journal of Nanjing Agricultural University. 1991;14(4):87-91.
  22. Cipriano R. Aeromonas Hydrophila and motile Aereomonad septicemias of fish. Fish and disease leaflet 68. Washington: US Dept. of the Interior, Fish and Wildlife Service, Division of Fishery Research; 2001. p. 25.
  23. CLSI. Methods for dilution of antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard M7-A7. 7th ed. Wayne: Clinical and Laboratory Standards Institute; 2006.
  24. CLSI. Methods for antimicrobial dilution and disk susceptibility testing of iInfrequently isolated or fastidious bacteria, 3rd Edn CLSI guideline M45. Wayne: Clinical and Laboratory Standards Institute; 2015.
  25. Cruz JM, et al. An outbreak of Plesiomonas shigelloides in farmed rainbow trout, Salmo Gairdneri Richardson, in Portugal. Bulletin of the European Association of Fish Pathologists. 1986;6(1):20-22. https://eafp.org.
  26. Csaba G, et al. Septicaemia in silver carp (Hypophthalmichthys Molitrix Val.) and bighead carp (Aristichthys Nobilis rich.) caused by Pseudomonas Fluorescens. In: Symposia biologica Hungarica; 1984.
  27. Daskalov H, Stobie M, Austin B. Klebsiella Pneumoniae: a pathogen of rainbow trout (Oncorhynchus Mykiss, Walbaum)? Bull Eur Ass Fish Pathol. 1998;18(1):26.
  28. DePaola A, Peeler JT, Rodrick GE. Effect of oxytetracycline-medicated feed on antibiotic resistance of gram-negative bacteria in catfish ponds. Applied and Environmental Microbiology, 1995. 1995;61(6):2335-40.
  29. Douvoyiannis M, et al. Chryseobacterium indologenes bacteremia in an infant. Int J Infect Dis. 2010;14(6):e531-2. https://doi.org/10.1016/j.ijid.2009.06.015
  30. Fish U, W. Service. Suggested procedures for the detection and identification of certain finfish and shellfish pathogens. In: Standard procedures for aquatic animal health inspections. Bethesda: American Fisheries Society; 2010.
  31. Gonzalez-Rey C, et al. Serotypes and anti-microbial susceptibility of Plesiomonas shigelloides isolates from humans, animals and aquatic environments in different countries. Comparative Immunology, Microbiology & Infectious Diseases. 2004;27(2):129-39. https://doi.org/10.1016/j.cimid.2003.08.001
  32. Hemstreet B. An update on Aeromonas hydrophila from a fish health specialist for summer. Catfish Journal. 2010;24(4).
  33. Hudzicki J. Kirby-Bauer disk diffusion susceptibility test protocol. American Society for Microbiology. 2009. http://www.asmscience.org/content/education/ protocol/protocol.3189. Accessed 28 Dec 2017.
  34. Jalal K, et al. Antibiotic resistance microbes in tropical mangrove sediments in east coast peninsular, Malaysia. African Journal of Microbiology Research. 2010;4(8):640-5.
  35. Jeremic S, Jakic-Dimic D, Veljovic LJ. Citrobacter freundii as a cause of disease in fish. Acta Vet (Beograd). 2003;53(5-6):399-410. https://doi.org/10.2298/AVB0306399J
  36. Joh SJ, et al. Bacterial pathogens and flora isolated from farm-cultured eels (Anguilla Japonica) and their environmental waters in Korean eel farms. Vet Microbiol. 2013;163(1-2):190-5. https://doi.org/10.1016/j.vetmic.2012.11.004
  37. Jonsson I, Monsen T, Wistrom J. A case of Plesiomonas shigelloides Cellulitis and Bacteraemia from northern Europe. Scand J Infect Dis. 1997;29(6):631-2. https://doi.org/10.3109/00365549709035909
  38. Kalule J, Kaddu-Mulindwa D, Asiimwe B. Antimicrobial drug resistance and plasmid profiles of <i>salmonella</i> isolates from humans and foods of animal origin in Uganda. Advances in Infectious Diseases. 2012;02(04):151-5. https://doi.org/10.4236/aid.2012.24025
  39. Kummerer K. Antibiotics in the aquatic environment. Chemosphere. 2009;75(4):435-41. https://doi.org/10.1016/j.chemosphere.2008.12.006
  40. Li D, Yu T, Zhang Y, Yang M, Li Z, Liu M and Qi R. Antibiotic Resistance Characteristics of Environmental Bacteria from an Oxytetracycline Production Wastewater Treatment Plant and the Receiving River. Appl Environ Microbiol. 2010;76(11):3444-3451. https://doi.org/10.1128/AEM.02964-09
  41. Lio-Po G, Lim L. Infectious diseases of warmwater fish in fresh wate, in Diseases and disorders of finfish in cage culture. In: Woo P, Bruno D, editors. . Oxfordshire: CAB International; 2014. p. 193-253.
  42. MAAIF. Department of Fisheries Resources Annual Report 2010/2011. Ministry of Agriculture, Animal Industry and Fisheries (MAAIF) 2012. Entebbe, pp 13-19. http://aquaticcommons.org/id/eprint/20470. Accessed 28 Dec 2017.
  43. MacFaddin JF. Biochemical tests for identification of medical bacteria. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 2000.
  44. Makaritsis KP, et al. An immunocompetent patient presenting with severe septic arthritis due to Ralstonia pickettii identified by molecular-based assays: a case report. Cases Journal. 2009;2:8125. https://doi.org/10.4076/1757-1626-2-8125
  45. Maniati M, et al. Letters to the editor / international journal of antimicrobial agents, vol. 25; 2005. p. 345-53. https://doi.org/10.1016/j.ijantimicag.2005.01.009
  46. Meyer FP, Bullock GL. Edwardsiella Tarda, a new pathogen of channel catfish (Ictalurus Punctatus). Appl Microbiol. 1973;25(1):155-6.
  47. Mohanty BR, Sahoo PK. Edwardsiellosis in fish: a brief review. J Biosci. 2007;32(3): 1331-44. https://doi.org/10.1007/s12038-007-0143-8
  48. Mukonzo JK, et al. Over-the-counter suboptimal dispensing of antibiotics in Uganda. J Multidiscip Healthc. 2013;6:303-10.
  49. Newaj-Fyzul A, et al. Prevalence of bacterial pathogens and their anti-microbial resistance in tilapia and their pond water in Trinidad. Zoonoses Public Health. 2008;55(4):206-13. https://doi.org/10.1111/j.1863-2378.2007.01098.x
  50. Nielsen ME, et al. Is Aeromonas Hydrophila the dominant motile Aeromonas species that causes disease outbreaks in aquaculture production in the Zhejiang Province of China? Dis Aquat Org. 2001;46(1):23-9. https://doi.org/10.3354/dao046023
  51. Nisha RG, et al. Isolation of Plesiomonas shigelloides from infected cichlid fishes using 16S rRNA characterization and its control with probiotic pseudomonas sp. Acta Scientiae Veteriariae. 2014;42:1-7.
  52. Noakes DJ, Beamish RJ, Kent ML. On the decline of Pacific salmon and speculative links to salmon farming in British Columbia. Aquaculture. 2000; 183(3-4):363-86. https://doi.org/10.1016/S0044-8486(99)00294-X
  53. Noble RC, Overman SB. Pseudomonas stutzeri infection a review of hospital isolates and a review of the literature. Diagn Microbiol Infect Dis. 1994;19(1):51-6. https://doi.org/10.1016/0732-8893(94)90051-5
  54. Odeyemi OA, Ahmad A. Antibiotic resistance profiling and phenotyping of Aeromonas species isolated from aquatic sources. Saudi Journal of Biological Sciences. 2017;24(1):65-70. https://doi.org/10.1016/j.sjbs.2015.09.016
  55. Ogutu-Ohwayo R. The decline of the native fishes of lakes Victoria and Kyoga (East Africa) and the impact of introduced species, especially the Nile perch, Lates Niloticus, and the Nile tilapia, Oreochromis Niloticus. Environ Biol Fish. 1990;27(2):81-96. https://doi.org/10.1007/BF00001938
  56. Penders J, Stobberingh EE. Antibiotic resistance of motile aeromonads in indoor catfish and eel farms in the southern part of The Netherlands. Int J Antimicrob Agents. 2008;31(3):261-5. https://doi.org/10.1016/j.ijantimicag.2007.10.002
  57. Pridgeon JW, Klesius PH, Garcia JC. Identification and virulence of Chryseobacterium indologenes isolated from diseased yellow perch (Perca Flavescens). J Appl Microbiol. 2013;114(3):636-43. https://doi.org/10.1111/jam.12070
  58. Ramalivhana J, Obi C, Moyo S. Prevalence of extended-spectrum b-Lactamases producing Aeromonas Hydrophila isolated from stool samples collected in the Limpopo province, South Africa. Afr J Microbiol Res. 2010;4(12):1203-8.
  59. Ribeiro R, et al. Incidence and antimicrobial resistance of enteropathogens isolated from an integrated aquaculture system. Lett Appl Microbiol. 2010; 51(6):611-8. https://doi.org/10.1111/j.1472-765X.2010.02946.x
  60. Rutaisire J, et al. Aquaculture for increased fish production in East Africa. Afr J Trop Hydrobiol Fish. 2009;12(1):74-7.
  61. Sarter S, et al. Antibiotic resistance in gram-negative bacteria isolated from farmed catfish. Food Control. 2007;18(11):1391-6. https://doi.org/10.1016/j.foodcont.2006.10.003
  62. Shah SQA, et al. Prevalence of antibiotic resistance genes in the bacterial flora of integrated fish farming environments of Pakistan and Tanzania. Environmental Science & Technology. 2012;46(16):8672-9. https://doi.org/10.1021/es3018607
  63. Sorum H. Antimicrobial drug resistance in fish pathogens. In: Aarestrup FM, editor. Antimicrobial resistance in bacteria of animal origin, vol. 213-238. Washington: ASM Press; 2006.
  64. Sorum H, Sunde M. Resistance to antibiotics in the normal flora of animals. Vet Res. 2001;32(3-4):227-41. https://doi.org/10.1051/vetres:2001121
  65. Sreedharan K, Philip R, Singh I. Virulence potential and antibiotic susceptibility pattern of motile aeromonads associated with freshwater ornamental fish culture systems: a possible threat to public health. Braz J Microbiol. 2012;43:754-65. https://doi.org/10.1590/S1517-83822012000200040
  66. Subasinghe R, Bondad-Reantaso M, McGladdery S. Aquaculture development, health and wealth. In: Aquaculture in the third millennium. Bangkok and Rome: NACA and FAO; 2001.
  67. Tacon AGJ, Metian M. Fish matters: importance of aquatic foods in human nutrition and global food supply. Rev Fish Sci. 2013;21(1):22-38. https://doi.org/10.1080/10641262.2012.753405
  68. Tamale A, et al. Prevalence of Columnaris, ecto-parasite and fungal conditions in selected fish farms. In: International conference on agro-biotechnology, biosafety and seed Systems in Developing Countries; 2011.
  69. Thomas J, et al. Pathogenecity of Pseudomonas Aeruginosa in Oreochromis Mossambicus and treatment using lime oil nanoemulsion. Colloids Surf B Biointerfaces. 2014;116:372-7. https://doi.org/10.1016/j.colsurfb.2014.01.019
  70. Tidwell JH, Allan GL. Fish as food: aquaculture's contribution. Ecological and economic impacts and contributions of fish farming and capture fisheries. 2001;2(11):958-63.
  71. Tsui T-L, et al. Comamonas testosteroni infection in Taiwan: reported two cases and literature review. J Microbiol Immunol Infect. 2011;44(1):67-71. https://doi.org/10.1016/j.jmii.2011.01.013
  72. UNAS, et al., Antibiotic resistance in Uganda: situation analysis and recommendations. 2015.
  73. Usui M, et al. Use of Aeromonas spp. as general indicators of antimicrobial susceptibility among bacteria in aquatic environments in Thailand. Front Microbiol. 2016;7:710.
  74. Van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics: links between animals and humans. Int J Antimicrob Agents. 2000;14(4):327-35. https://doi.org/10.1016/S0924-8579(00)00145-X
  75. Wakabayashi H. Edwardsiella Tarda (Paracolobactrum anguillimortiferum) associated with pond-cultured eel diseases. Bulletin of the Japanese Society for the Science of Fish. 1973;39:931-9. https://doi.org/10.2331/suisan.39.931
  76. Walakira J, et al. Common fish diseases and parasites affecting wild and farmed tilapia and catfish in central and western Uganda. Uganda Journal of Agricultural Sciences. 2014;15(2):1-11.
  77. Walters GR, Plumb JA. Environmental stress and bacterial infection in channel catfish, Ictalurus Punctatus Rafinesque. J Fish Biol. 1980;17(2):177-85. https://doi.org/10.1111/j.1095-8649.1980.tb02751.x
  78. Xu J, et al. Pseudomonas Alcaligenes infection and mortality in cultured Chinese sturgeon, Acipenser sinensis. Aquaculture. 2015;446:37-41. https://doi.org/10.1016/j.aquaculture.2015.04.014

Cited by

  1. Antimicrobial activity of trans‐cinnamic acid and commonly used antibiotics against important fish pathogens and nonpathogenic isolates vol.125, pp.6, 2018, https://doi.org/10.1111/jam.14097
  2. Effect of dietary carob (Ceratonia siliqua) syrup on blood parameters, gene expression responses and ammonia resistance in tilapia (Oreochromis niloticus) vol.51, pp.5, 2018, https://doi.org/10.1111/are.14540
  3. Alternative Feed Raw Materials Modulate Intestinal Microbiota and Its Relationship with Digestibility in Yellowtail Kingfish Seriola lalandi vol.5, pp.2, 2018, https://doi.org/10.3390/fishes5020014
  4. Bacteriological Quality and Antibiotics' Susceptibility Profile of Small-medium Scale Commercial Fish farms in Nigeria vol.14, pp.1, 2018, https://doi.org/10.2174/1874331502014010198
  5. Effect of black cumin seed oil on growth, innate immunity and resistance against Pseudomonas fluorescens infection in Nile tilapia Oreochromis niloticus vol.28, pp.4, 2020, https://doi.org/10.1007/s10499-020-00539-8
  6. In Vitro Antibacterial Potential of Salix babylonica Extract against Bacteria that Affect Oncorhynchus mykiss and Oreochromis spp. vol.10, pp.8, 2020, https://doi.org/10.3390/ani10081340
  7. Protein-protein interaction network: an emerging tool for understanding fish disease in aquaculture vol.13, pp.1, 2021, https://doi.org/10.1111/raq.12468
  8. The Alteration of Intestinal Microbiota Profile and Immune Response in Epinephelus coioides during Pathogen Infection vol.11, pp.2, 2018, https://doi.org/10.3390/life11020099
  9. Polymer/inorganic hybrids containing silver nanoparticles and their activity in the disinfection of fish aquariums/ponds vol.60, pp.4, 2018, https://doi.org/10.1080/25740881.2020.1811318
  10. Experimental co‐infection by Aeromonas hydrophila and Aeromonas jandaei in pirarucu Arapaima gigas (Pisces: Arapaimidae) vol.52, pp.4, 2021, https://doi.org/10.1111/are.15021
  11. Prevalence and Antibiogram of Vibrio parahaemolyticus and Aeromonas hydrophila in the Flesh of Nile Tilapia, with Special Reference to Their Virulence Genes Detected Using Multiplex PCR Technique vol.10, pp.6, 2018, https://doi.org/10.3390/antibiotics10060654
  12. Prevalence of enterotoxin genes and antibacterial susceptibility pattern of pathogenic bacteria isolated from traditionally preserved fish products of Sikkim, India vol.125, pp.None, 2018, https://doi.org/10.1016/j.foodcont.2021.108009
  13. PACAP modulates the transcription of TLR-1/TLR-5/MyD88 pathway genes and boosts antimicrobial defenses in Clarias gariepinus vol.115, pp.None, 2021, https://doi.org/10.1016/j.fsi.2021.06.009
  14. Virulence and antimicrobial resistance potential of Aeromonas spp. associated with shellfish vol.73, pp.2, 2018, https://doi.org/10.1111/lam.13489
  15. Fatty Acids-Enriched Fractions of Hermetia illucens (Black Soldier Fly) Larvae Fat Can Combat MDR Pathogenic Fish Bacteria Aeromonas spp. vol.22, pp.16, 2021, https://doi.org/10.3390/ijms22168829
  16. Potential Influence of Regulation of the Food Value Chain on Prevalence and Patterns of Antimicrobial Resistance: the Case of Tilapia (Oreochromis niloticus) vol.87, pp.23, 2018, https://doi.org/10.1128/aem.00945-21
  17. The single or combined Silybum marianum and co-enzyme Q10 role in alleviating fluoride-induced impaired growth, immune suppression, oxidative stress, histological alterations, and reduced resistance t vol.548, pp.p2, 2022, https://doi.org/10.1016/j.aquaculture.2021.737693