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Aeromonas veronii biovar veronii Infection in Cultured European Seabass (Dicentrarchus labrax) in Türkiye

Year 2023, Volume: 26 Issue: 6, 1397 - 1404, 31.12.2023

Süheyla Karataş Steınum , Emre Turgay , Remziye Eda Yardımcı , Terje Marken Steınum

https://doi.org/10.18016/ksutarimdoga.vi.1208007

Abstract

Fish in aquaculture systems are susceptible to infectious agents as they are kept in a densely populated and often physically restricted environment. Genus Aeromonas include well-known pathogens, and the member Aeromonas veronii has been reported to cause diseases in both humans and animals, either as primary infection or as mixed infection with other pathogens. This study describes a low mortality epizootic caused by Aeromonas veronii biovar veronii in European seabass (Dicentrarchus labrax) farmed in the Aegean Sea. The gills, kidneys and livers of moribund fish were pale. Erythema, haemorrhage and superficial ulcerative lesions were detected on the skin. In addition, petechial haemorrhage was observed on the tongue, maxilla, and operculum. The spleen was enlarged and multiple granulomas were detected in both the kidney and the spleen. Some fish had skin depigmentation, ecchymosis in the liver, and a bloody exudate in the abdominal cavity. The intestinal walls were lined with a clear yellowish fluid. Twenty-nine motile, Gram-negative bacterial isolates were obtained from the internal organs of diseased fish. According to morphology, biochemical properties and 16S rRNA gene sequencing results, all isolates were identified as Aeromonas veronii bv. veronii. All isolates were resistant to amoxicillin and ampicillin, and sensitive to oxytetracycline, enrofloxacin, ciprofloxacin, florfenicol, and flumequine.

Keywords

Aeromonas veronii biovar veronii Dicentrarchus labrax European seabass Histopathology

Supporting Institution

The Scientific Research Projects Coordination Unit of Istanbul University

Project Number

FYL-2018-30132

References

  • Abbott, S. L., Cheung, W. K., & Janda, J. M. (2003). The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. Journal of Clinical Microbiology, 41(6), 2348-2357.
  • Bauer, A. W., Kirby, W. M., Sherris, J. C. & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single diffusion method. American Journal of Clinical Pathology, 45, 493-496.
  • Brenner DJ, Boone DR, Garrity GM, Goodfellow M, Krieg NR, Rainey FA., Schleifer, K., Staley, J. T., & Vos, P. (2005). The Proteobacteria: Part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria. Bergey's Manual Trust. Springer, New York.
  • Cai, S. H., Wu, Z. H., Jian, J. C., Lu, Y. S., & Tang, J. F. (2012). Characterization of pathogenic Aeromonas veronii bv. veronii associated with ulcerative syndrome from Chinese longsnout catfish (Leiocassis longirostris Günther). Brazilian Journal of Microbiology, 43(1), 382-388.
  • Chen, F., Sun, J., Han, Z., Yang, X., Xian, J., Lv, A., Hu, X., & Shi, H. (2019). Isolation, identification and characteristics of Aeromonas veronii from diseased crucian carp (Carassius auratus gibelio). Frontiers in Microbiology, 10, 2742.
  • Culling, C. F. A. (1963). Handbook of Histopathological Techniques (including museum technique) 533 pp. London, Butterworths.
  • Dong, H. T., Techatanakitarnan C, Jindakittikul P, et al (2017). Aeromonas jandaei and Aeromonas veronii caused disease and mortality in Nile tilapia, Oreochromis niloticus (L.). Journal of Fish Diseases, 40(10), 1395-1403.
  • FAO (2021). FAO Yearbook. Fishery and Aquaculture Statistics 2019 Rome. ISBN: 978-92-5-135410-0 https://doi.org/10.4060/cb7874t
  • Fryer, J. L. & Rohovec, J. S. (2021). Bacterial diseases of fish. In Pathobiology of Marine and estuarine Organisms (pp. 53-83), CRC Press, Florida.
  • Gashgari, R. M. & Selim, S. A. (2015). Detection and characterization of antimicrobial resistance and putative virulence genes in Aeromonas veronii biovar Sobria Isolated from Gilthead sea bream (Sparus aurata L.). Foodborne Pathogens and Disease, 12(9), 806-811.
  • Hall, T. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. 95-98. In: Nucleic Acids Symposium Series.
  • Hickman-Brenner, F. W., Macdonald, K. L., Steigerwalt, A. G., Fanning, G. R., Brenner, D. J., & Farmer 3rd, J. J. (1987). Aeromonas veronii, a new ornithine decarboxylase-positive species that may cause diarrhea. Journal of Clinical Microbiology, 25(5), 900–906
  • Hoai, T. D., Trang, T. T., Van Tuyen, N., Giang, N. T. H., & Van Van, K. (2019). Aeromonas veronii caused disease and mortality in channel catfish in Vietnam. Aquaculture, 513, 734425.
  • Janda, J. M. & Abbott, S. L. (2010). The genus Aeromonas: taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews, 23(1), 35-73.
  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., & Lopez, R. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
  • Liu, D., Geng, Y., Wang, K., Chen, D., Huang, X. L., Ou, Y., He, C. L., Zhong, Z. J., & Lai, W. (2016). Aeromonas veronii infection in cultured channel catfish, Ictalurus punctatus, in Southwest China. The Israeli Journal of Aquaculture-Bamidgeh, 68, 1-8.
  • Nawaz, M., Khan, S. A., Khan, A. A., Sung, K., Tran, Q., Kerdahi, K., & Steele, R. (2010). Detection and characterization of virulence genes and integrons in Aeromonas veronii isolated from catfish. Food Microbiology, 27(3), 327-331.
  • Pei, C., Song, H., Zhu, L., Qiao, D., Yan, Y., Li, L., Zhao, X., Zhang, J., Jiang, X., & Kong, X. (2021). Identification of Aeromonas veronii isolated from largemouth bass Micropterus salmoides and histopathological analysis. Aquaculture, 540, 736707.
  • Rahman, M., Colque-Navarro, P., Kühn, I., Huys, G., Swings, J., & Möllby, R. (2002). Identification and characterization of pathogenic Aeromonas veronii biovar sobria associated with epizootic ulcerative syndrome in fish in Bangladesh. Applied and Environmental Microbiology, 68(2), 650-655.
  • Shameena, S. S., Kumar, K., Kumar, S., Kumar, S., & Rathore, G. (2020). Virulence characteristics of Aeromonas veronii biovars isolated from infected freshwater goldfish (Carassius auratus). Aquaculture, 518, 734819.
  • Smyrli, M., Prapas, A., Rigos, G., Kokkari, C., Pavlidis, M., & Katharios, P. (2017). Aeromonas veronii infection associated with high morbidity and mortality in farmed European seabass Dicentrarchus labrax in the Aegean Sea, Greece. Fish Pathology, 52(2), 68-81.
  • Smyrli, M., Triga, A., Dourala, N., Varvarigos, P., Pavlidis, M., Quoc, V. H., & Katharios, P. (2019). Comparative study on a novel pathogen of European seabass. Diversity of Aeromonas veronii in the Aegean Sea. Microorganisms, 7(11), 504.
  • Smyrli, M., Katharios, P. (2020). 12. Aeromonas spp. 107-116. In: Zrncic S (Ed), Diagnostic Manual for the main pathogens in European seabass and Gilthead seabream aquaculture. CIHEAM, Zaragoza.
  • Suau, A., Bonnet, R., Sutren, M., Godon, J. J., Gibson, G. R., Collins, M. D., & Doré, J. (1999). Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied and Environmental Microbiology, 65(11), 4799-4807.
  • Sun, J., Zhang, X., Gao, X., Jiang, Q., Wen, Y., & Lin, L. (2016). Characterization of virulence properties of Aeromonas veronii isolated from diseased Gibel Carp (Carassius gibelio). International Journal of Molecular Sciences, 17(4), 496.
  • Tanrıkul, T. & Dinçtürk, E. (2021). A New Outbreak in Sea Bass Farming in Turkey: Aeromonas veronii. Journal of the Hellenic Veterinary Medical Society, 72(3), 3051-3058.
  • Toranzo, A. E., Magariños, B., & Romalde, J. L. (2005). A review of the main bacterial fish diseases in mariculture systems. Aquaculture, 246(1-4), 37-61.
  • Uzun, E. & Ogut, H. (2015). The isolation frequency of bacterial pathogens from sea bass (Dicentrarchus labrax) in the Southeastern Black Sea. Aquaculture, 437, 30-37.
  • Vila, J., Marco, F., Soler, L., Chacon, M., & Figueras, M. J. (2002). In vitro antimicrobial susceptibility of clinical isolates of Aeromonas caviae, Aeromonas hydrophila and Aeromonas veronii biotype sobria. The Journal of Antimicrobial Chemotherapy, 49(4), 701-702.
  • Wayne, P. A. (2010). Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing: 20th informational supplement. CLSI document M100-S20.
  • Yu, J. H., Han, J. J., Kim, H. J., Kang, S. G., & Park, S. W. (2010). First report of Aeromonas veronii infection in farmed Israeli carp Cyprinus carpio in Korea. Journal of Fish Pathology, 23(2), 165-176.
  • Zhang, Z., Schwartz, S., Wagner, L., & Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 7(1-2), 203-214.
  • Zhu, M., Wang, X. R., Li, J., Li, G. Y., Liu, Z. P., & Mo, Z. L. (2016). Identification and virulence properties of Aeromonas veronii bv. sobria isolates causing an ulcerative syndrome of loach Misgurnus anguillicaudatus. Journal of Fish Diseases, 39(6), 777-781.

Türkiye'de Yetiştiriciliği Yapılan Levrek Balıklarında (Dicentrarchus labrax) Aeromonas veronii biovar veronii Enfeksiyonu

Year 2023, Volume: 26 Issue: 6, 1397 - 1404, 31.12.2023

Süheyla Karataş Steınum , Emre Turgay , Remziye Eda Yardımcı , Terje Marken Steınum

https://doi.org/10.18016/ksutarimdoga.vi.1208007

Abstract

Yetiştiricilik sistemlerindeki balıklar, stok yoğunluğu yüksek ve genellikle fiziksel olarak kısıtlı bir ortamda tutuldukları için enfeksiyöz ajanlara karşı hassastırlar. Aeromonas cinsinin içinde pek çok patojen tür içerdiği bilinmektedir ve bu cins üyelerinden Aeromonas veronii bakterisinin hem insanlarda hem de hayvanlarda birincil enfeksiyon şeklinde veya diğer patojenlerle karışık enfeksiyon olarak hastalıklara neden olduğu bildirilmiştir. Bu çalışma, Ege Denizi'nde yetiştirilen levrek balıklarında (Dicentrarchus labrax) Aeromonas veronii biovar veronii bakterisinin neden olduğu düşük ölüm oranına sahip bir epizootiği tanımlamaktadır. Hasta balıklarda solungaç, böbrek ve karaciğerin solgun olduğu tespit edilmiştir. Deride eritem, hemoraji ve yüzeyel ülseratif lezyonlar görülmüştür. Ayrıca dil, maksilla ve operkulumda peteşiyal hemoraji gözlenmiştir. Dalağın büyüdüğü ve hem böbrek hem de dalakta çoklu granülomalar tespit edilmiştir. Dalak ve böbrekte granülomlar gözlenmiştir. Bazı balıklarda deri depigmentasyonu, karaciğerde ekimoz ve karın boşluğunda kanlı eksüda görülmüştür. Bağırsak duvarları berrak ve sarımsı bir sıvıyla kaplı olarak bulunmuştur. Hasta balıkların iç organlarından 29 adet Gram negatif hareketli bakteri izolatı elde edilmiştir. Morfoloji, biyokimyasal özellikler ve 16S rRNA gen dizileme sonuçlarına göre tüm izolatlar Aeromonas veronii bv. veronii olarak tanımlanmıştır. Elde edilen izolatların amoksisilin ve ampisiline dirençli ve oksitetrasiklin, enrofloksasin, siprofloksasin, florfenikol ve flumekine duyarlı olduğu tespit edilmiştir.

Keywords

Aeromonas veronii biovar veronii Dicentrarchus labrax Levrek balığı Histopatoloji

Project Number

FYL-2018-30132

References

  • Abbott, S. L., Cheung, W. K., & Janda, J. M. (2003). The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. Journal of Clinical Microbiology, 41(6), 2348-2357.
  • Bauer, A. W., Kirby, W. M., Sherris, J. C. & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single diffusion method. American Journal of Clinical Pathology, 45, 493-496.
  • Brenner DJ, Boone DR, Garrity GM, Goodfellow M, Krieg NR, Rainey FA., Schleifer, K., Staley, J. T., & Vos, P. (2005). The Proteobacteria: Part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria. Bergey's Manual Trust. Springer, New York.
  • Cai, S. H., Wu, Z. H., Jian, J. C., Lu, Y. S., & Tang, J. F. (2012). Characterization of pathogenic Aeromonas veronii bv. veronii associated with ulcerative syndrome from Chinese longsnout catfish (Leiocassis longirostris Günther). Brazilian Journal of Microbiology, 43(1), 382-388.
  • Chen, F., Sun, J., Han, Z., Yang, X., Xian, J., Lv, A., Hu, X., & Shi, H. (2019). Isolation, identification and characteristics of Aeromonas veronii from diseased crucian carp (Carassius auratus gibelio). Frontiers in Microbiology, 10, 2742.
  • Culling, C. F. A. (1963). Handbook of Histopathological Techniques (including museum technique) 533 pp. London, Butterworths.
  • Dong, H. T., Techatanakitarnan C, Jindakittikul P, et al (2017). Aeromonas jandaei and Aeromonas veronii caused disease and mortality in Nile tilapia, Oreochromis niloticus (L.). Journal of Fish Diseases, 40(10), 1395-1403.
  • FAO (2021). FAO Yearbook. Fishery and Aquaculture Statistics 2019 Rome. ISBN: 978-92-5-135410-0 https://doi.org/10.4060/cb7874t
  • Fryer, J. L. & Rohovec, J. S. (2021). Bacterial diseases of fish. In Pathobiology of Marine and estuarine Organisms (pp. 53-83), CRC Press, Florida.
  • Gashgari, R. M. & Selim, S. A. (2015). Detection and characterization of antimicrobial resistance and putative virulence genes in Aeromonas veronii biovar Sobria Isolated from Gilthead sea bream (Sparus aurata L.). Foodborne Pathogens and Disease, 12(9), 806-811.
  • Hall, T. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. 95-98. In: Nucleic Acids Symposium Series.
  • Hickman-Brenner, F. W., Macdonald, K. L., Steigerwalt, A. G., Fanning, G. R., Brenner, D. J., & Farmer 3rd, J. J. (1987). Aeromonas veronii, a new ornithine decarboxylase-positive species that may cause diarrhea. Journal of Clinical Microbiology, 25(5), 900–906
  • Hoai, T. D., Trang, T. T., Van Tuyen, N., Giang, N. T. H., & Van Van, K. (2019). Aeromonas veronii caused disease and mortality in channel catfish in Vietnam. Aquaculture, 513, 734425.
  • Janda, J. M. & Abbott, S. L. (2010). The genus Aeromonas: taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews, 23(1), 35-73.
  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., & Lopez, R. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
  • Liu, D., Geng, Y., Wang, K., Chen, D., Huang, X. L., Ou, Y., He, C. L., Zhong, Z. J., & Lai, W. (2016). Aeromonas veronii infection in cultured channel catfish, Ictalurus punctatus, in Southwest China. The Israeli Journal of Aquaculture-Bamidgeh, 68, 1-8.
  • Nawaz, M., Khan, S. A., Khan, A. A., Sung, K., Tran, Q., Kerdahi, K., & Steele, R. (2010). Detection and characterization of virulence genes and integrons in Aeromonas veronii isolated from catfish. Food Microbiology, 27(3), 327-331.
  • Pei, C., Song, H., Zhu, L., Qiao, D., Yan, Y., Li, L., Zhao, X., Zhang, J., Jiang, X., & Kong, X. (2021). Identification of Aeromonas veronii isolated from largemouth bass Micropterus salmoides and histopathological analysis. Aquaculture, 540, 736707.
  • Rahman, M., Colque-Navarro, P., Kühn, I., Huys, G., Swings, J., & Möllby, R. (2002). Identification and characterization of pathogenic Aeromonas veronii biovar sobria associated with epizootic ulcerative syndrome in fish in Bangladesh. Applied and Environmental Microbiology, 68(2), 650-655.
  • Shameena, S. S., Kumar, K., Kumar, S., Kumar, S., & Rathore, G. (2020). Virulence characteristics of Aeromonas veronii biovars isolated from infected freshwater goldfish (Carassius auratus). Aquaculture, 518, 734819.
  • Smyrli, M., Prapas, A., Rigos, G., Kokkari, C., Pavlidis, M., & Katharios, P. (2017). Aeromonas veronii infection associated with high morbidity and mortality in farmed European seabass Dicentrarchus labrax in the Aegean Sea, Greece. Fish Pathology, 52(2), 68-81.
  • Smyrli, M., Triga, A., Dourala, N., Varvarigos, P., Pavlidis, M., Quoc, V. H., & Katharios, P. (2019). Comparative study on a novel pathogen of European seabass. Diversity of Aeromonas veronii in the Aegean Sea. Microorganisms, 7(11), 504.
  • Smyrli, M., Katharios, P. (2020). 12. Aeromonas spp. 107-116. In: Zrncic S (Ed), Diagnostic Manual for the main pathogens in European seabass and Gilthead seabream aquaculture. CIHEAM, Zaragoza.
  • Suau, A., Bonnet, R., Sutren, M., Godon, J. J., Gibson, G. R., Collins, M. D., & Doré, J. (1999). Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied and Environmental Microbiology, 65(11), 4799-4807.
  • Sun, J., Zhang, X., Gao, X., Jiang, Q., Wen, Y., & Lin, L. (2016). Characterization of virulence properties of Aeromonas veronii isolated from diseased Gibel Carp (Carassius gibelio). International Journal of Molecular Sciences, 17(4), 496.
  • Tanrıkul, T. & Dinçtürk, E. (2021). A New Outbreak in Sea Bass Farming in Turkey: Aeromonas veronii. Journal of the Hellenic Veterinary Medical Society, 72(3), 3051-3058.
  • Toranzo, A. E., Magariños, B., & Romalde, J. L. (2005). A review of the main bacterial fish diseases in mariculture systems. Aquaculture, 246(1-4), 37-61.
  • Uzun, E. & Ogut, H. (2015). The isolation frequency of bacterial pathogens from sea bass (Dicentrarchus labrax) in the Southeastern Black Sea. Aquaculture, 437, 30-37.
  • Vila, J., Marco, F., Soler, L., Chacon, M., & Figueras, M. J. (2002). In vitro antimicrobial susceptibility of clinical isolates of Aeromonas caviae, Aeromonas hydrophila and Aeromonas veronii biotype sobria. The Journal of Antimicrobial Chemotherapy, 49(4), 701-702.
  • Wayne, P. A. (2010). Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing: 20th informational supplement. CLSI document M100-S20.
  • Yu, J. H., Han, J. J., Kim, H. J., Kang, S. G., & Park, S. W. (2010). First report of Aeromonas veronii infection in farmed Israeli carp Cyprinus carpio in Korea. Journal of Fish Pathology, 23(2), 165-176.
  • Zhang, Z., Schwartz, S., Wagner, L., & Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 7(1-2), 203-214.
  • Zhu, M., Wang, X. R., Li, J., Li, G. Y., Liu, Z. P., & Mo, Z. L. (2016). Identification and virulence properties of Aeromonas veronii bv. sobria isolates causing an ulcerative syndrome of loach Misgurnus anguillicaudatus. Journal of Fish Diseases, 39(6), 777-781.
There are 33 citations in total.

Details

Primary Language English
Subjects Fish Biology
Journal Section RESEARCH ARTICLE
Authors

Süheyla Karataş Steınum 0000-0003-2006-7854

Emre Turgay 0000-0001-9964-3919

Remziye Eda Yardımcı 0000-0001-7737-8739

Terje Marken Steınum 0000-0001-5377-9765

Project Number FYL-2018-30132
Early Pub Date June 14, 2023
Publication Date December 31, 2023
Submission Date November 23, 2022
Acceptance Date April 13, 2023
Published in Issue Year 2023Volume: 26 Issue: 6

Cite

APA Karataş Steınum, S., Turgay, E., Yardımcı, R. E., Steınum, T. M. (2023). Aeromonas veronii biovar veronii Infection in Cultured European Seabass (Dicentrarchus labrax) in Türkiye. Kahramanmaraş Sütçü İmam Üniversitesi Tarım Ve Doğa Dergisi, 26(6), 1397-1404. https://doi.org/10.18016/ksutarimdoga.vi.1208007
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