Outbreaks of streptococcosis associated with Streptococcus agalactiae in farmed climbing perch (Anabas testudineus) in Vietnam https://doi.org/10.12982/VIS.2024.065
Article Sidebar
Main Article Content
Abstract
Streptococcus agalactiae causes serious economic damage to fish cultivation worldwide. The goal of this work was to isolate, identify, and evaluate the pathogenicity and susceptibility of the streptococci isolates to antibiotics recovered from climbing perch (A. testudineus) farmed in the southern part of Vietnam. Moribund and healthy fish were taken differently from intensive climbing perch farms. The diseased fish’s clinical signs were observed, including darkened body color, ascites, hepatomegaly, an enlarged kidney, and splenomegaly. Based on the conventional method, the API 20 Strep test, and 16S rRNA gene partial sequencing, S. agalactiae was associated with disease. They have non β-hemolytic activity, gram-positive cocci, catalase, and oxidase-negative enzymes. The LD50 trial performance of S. agalactiae showed the virulence of this bacteria in climbing perch and fulfilled Koch’s postulates with a value of 8.71 x 104 CFU/mL at day 7. Most of the challenged fish presented the same clinical signs as the natural infection. Hence, S. agalactiae were confirmed as the causative agents of the "dark body" disease. Antibiogram results demonstrated that S. agalactiae strains were completely susceptible to cefotaxime, doxycycline, and florfenicol. Interestingly, the results of this study found that S. agalactiae isolates are 100% resistant to sulfamethoxazole-trimethoprim. To the best of our knowledge, this is the first report of S. agalactiae as a pathogen of climbing perch.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Publishing an article with open access in Veterinary Integrative Sciences leaves the copyright with the author. The article is published under the Creative Commons Attribution License 4.0 (CC-BY 4.0), which allows users to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited.
References
Abuseliana, A. F., Daud, H. H. M., Aziz, S. A., Bejo, S. K. and Alsaid, M. 2011. Pathogenicity of Streptococcus agalactiae isolated from a fish farm in Selangor to juvenile Red tilapia (Oreochromis sp.). J. Anim. Vet. Adv. 10, 914-919.
Agnew, W. and Barnes, A. C., 2007. Streptococcus iniae: an aquatic pathogen of global veterinary significance and a challenging candidate for reliable vaccination. Vet. Microbiol. 122, 1-15.
Alam, M.K., Rahman, L., Khan, M.M.R. and Rahman, S.M.Z. 2006. Allozyme marker for the analysis of genetic variation of cross koi (♀ local ×♂ Thai) Anabas testudineus with their parents. Mole. Biol. Biotec. J. 4, 9-12.
Alazab, A., Sadat, A., and Younis, G., 2022. Prevalence, antimicrobial susceptibility, and genotyping of Streptococcus agalactiae in Tilapia fish (Oreochromis niloticus) in Egypt. J Adv Vet Anim Res. 9, 95-103.
Al-Harbi A. H., 2016 Phenotypic and genotypic characterization of Streptococcus agalactiae isolated from hybrid tilapia (Oreochromis niloticus × O. aureus). Aquac. 464, 515-520.
Amal, M. N. A., Zamri‐Saad, M., Iftikhar, A. R., Siti‐Zahrah, A., Aziel, S. and Fahmi, S. 2012. An outbreak of Streptococcus agalactiae infection in cage‐cultured golden pompano, Trachinotus blochii (Lacépède) in M alaysia. J. Fish Dis. 35, 849-852.
Bauer, A. W., Kirby, W. M. M., Sherris, J. C. and Turck, M. 1966. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol.45, 493-496.
Bondad‐Reantaso, M. G., MacKinnon, B., Karunasagar, I., Fridman, S., Alday‐Sanz, V., Brun, E. and Caputo, A. 2023. Review of alternatives to antibiotic use in aquaculture. Rev Aquac. 15:1421‐1451.
Buller, B. N., 2004. Bacteria from fish and other aquatic animals: a practical identification manual. AMA DataSet. UK, 390 pages.
Camus, A. C., Shewmaker, P. L., Mauel, M. J., and Wise, D. J. 2008. Streptococcus ictaluri arthritis, osteolysis, myositis, and spinal meningitis in channel catfish broodstock. J. Aquat. Anim. Health. 20, 54-62.
Chhanda, M. S., Parvez, I., Rumi, N. A., Hosen, M. H. A., and Islam, M. R. 2019. Identification of pathogenic bacteria from infected Thai koi (Anabas testudineus). Asian J. Med. Biol. Res. 5, 56-62.
CLSI. 2020. Performance standards for antimicrobial susceptibility testing for bacteria isolated from aquatic animals. In: CLSI supplement VET04 (Third Edition). Wayne, PA: Clinical and Laboratory Standards Institute.
Colussi, S., Pastorino, P., Mugetti, D., Antuofermo, E., Sciuto, S., Esposito, G., Polinas, M.,Tomasoni, M., Burrai, G. P. and Fernández-Garayzábal, J. F., 2022. Isolation and Genetic Characterization of Streptococcus iniae Virulence Factors in Adriatic
Sturgeon (Acipenser naccarii). Microorganisms. 10, 883.
Creeper, J. H. and Buller, N. B. 2006. An outbreak of Streptococcus iniae in barramundi (Lates calcarifera) in freshwater cage culture. Aust. Vet. J. 84, 408-411.
Deng, L., Li, Y., Geng, Y., Zheng, L., Rehman, T., Zhao, R. and Lai, W. 2019. Molecular serotyping and antimicrobial susceptibility of Streptococcus agalactiae isolated from fish in China. Aquac. 510, 84-89.
Deng, M. L., Geng, Y., Liu, D., Zhou, Y., Wang, K. Y., Huang, X. L. and Chen, C. 2015. Isolation identification and detection of virulence genes of Streptococcus iniae from Acipenser baerii. J Fish China. 39, 127-35.
Doménech, A., Fernández-Garayzábal, J. F., Pascual, C., Garcia, J. A., Cutuli, M. T., Moreno, M. A., Collins, M. D. and Dominiguez, L. 1996. Streptococcosis in cultured turbot, Scophthalmus maximus (L.), associated with Streptococcus parauberis. J. Fish Dis. 19, 33-38.
Dung, T. T., Thanh, H. T. N. T., Duy, N. K., 2013. Streptococcus iniae, causative agent of the disease "dark body" on climbing perch (Anabas testudineus). Can Tho University Journal of Science. 26, 101-102.
Duremdez, R., Al‐Marzouk, A., Qasem, J. A., Al‐Harbi, A. and Gharabally, H. 2004. Isolation of Streptococcus agalactiae from cultured silver pomfret, Pampus argenteus (Euphrasen), in Kuwait. J. Fish Dis. 27, 307-310.
Ehsan, R., Rahman, A., Paul, S. I., Ador, M. A. A., Haque, M. S., Akter, T. and Rahman, M. M., 2023 Aeromonas veronii isolated from climbing perch (Anabas testudineus) sufering from epizootic ulcerative syndrome (EUS). Aquacult Fish. 8, 288-295.
El Aamri, F., Padilla, D., Acosta, F., Caballero, M. J., Roo, J., Bravo, J., and Real, F. 2010. First report of Streptococcus iniae in red porgy (Pagrus pagrus, L.). J. Fish Dis. 33, 901-905.
Elliott, J. A., Facklam, R. R. and Richter, C. B. 1990. Whole-cell protein patterns of nonhemolytic group B, type Ib, streptococci isolated from humans, mice, cattle, frogs, and fish. J. Clin. Microbiol. 28, 628-630.
Evans, J. J., Klesius, P. H., Gilbert, P. M., Shoemaker, C. A., Al Sarawi, M. A., Landsberg, J., and Al Zenki, S. 2002. Characterization of β‐haemolytic Group B Streptococcus agalactiae in cultured seabream, Sparus auratus L., and wild mullet, Liza klunzingeri (Day), in Kuwait. J. Fish Dis. 25, 505-513.
Evans, J. J., Klesius, P. H., Pasnik, D. J., and Bohnsack, J. F. 2009. Human Streptococcus agalactiae isolate in Nile tilapia (Oreochromis niloticus). Emerging Infectious Diseases. 15, 774.
Fàbrega, A., Madurga, S., Giralt, E. and Vila, J. 2009. Mechanism of action of and resistance to quinolones. Microb. Biotechnol. 2, 40-61.
Facklam, R., Elliott, J., Shewmaker, L. and Reingold, A. 2005. Identification and characterization of sporadic isolates of Streptococcus iniae isolated from humans. J. Clin. Microbiol. 43, 933-937.
Frerichs, N. G. and Millar, S. D., 1993. Manual for the isolation and identification of fish bacterial pathogens. Pisces Press. U.K. 55pages.
Garcia, J. C., Klesius, P. H., Evans, J. J. and Shoemaker, C. A. 2008. Non-infectivity of cattle Streptococcus agalactiae in Nile tilapia, Oreochromis niloticus and channel catfish, Ictalurus punctatus. Aquaculture. 281, 151-154.
Geng, Y., Wang, K. Y., Huang, X. L., Chen, D. F., Li, C. W., Ren, S. Y. and Lai, W. M. 2012. Streptococcus agalactiae, an emerging pathogen for cultured yafish, Schizothorax prenanti, in China. Transbound. Emerg. Dis. 59, 369-375.
Haenen, O. L., Dong, H. T., Hoai, T. D., Crumlish, M., Karunasagar, I., Barkham, T., and Bondad‐Reantaso, M. G. 2023. Bacterial diseases of tilapia, their zoonotic potential and risk of antimicrobial resistance. Rev Aquac. 15, 154-185.
Hieu N. T., and Trang L. T. T., 2021. Current status of use and harmful effects of antibiotics in aquaculture. Vietnam Journal of Science and Technology. 12, 54-56.
Hoshina, T., Sano, T. and Morimoto, Y. 1958. A Streptococcus pathogenic to fish. J. Tokyo Univ. Fish. 44, 57-68.
Hossain, M. S., Hashem, S., Halim, M. A., Chowdhury, P., Sultana, S. and Khan, M. N., 2017. Bacterial community structure and infection in cultured Koi (Anabas testudineus) fish species. Int. j. fish. aquat. sci. 5, 520-524.
Klingklib, C., Suanyuk, N., 2017. Streptococcus agalactiae serotype Ib, an emerging pathogen affecting climbing perch (Anabas testudineus) and Günther’s walking catfish (Clarias macrocephalus) polycultured in southern Thailand. Thai J. Vet. Med. 47, 183-197.
Krause, K. M., Serio, A. W., Kane, T. R. and Connolly, L. E. 2016. Aminoglycosides: an overview. Cold Spring Harb Perspect Med. 6: a027029.
Lai, H. T. and Lin, J. J. 2009. Degradation of oxolinic acid and flumequine in aquaculture pond waters and sediments. Chemosphere. 75, 462-468.
Laith, A. A., Ambak, M. A., Hassan, M., Sheriff, S. M., Nadirah, M., Draman, A. S. and Najiah, M. 2017. Molecular identification and histopathological study of natural Streptococcus agalactiae infection in hybrid tilapia (Oreochromis niloticus). Veterinary world. 10, 101.
Lau, S. K., Woo, P. C., Tse, H., Leung, K. W., Wong, S. S. and Yuen, K. Y. 2003. Invasive Streptococcus iniae infections outside north America. Clin. Microbiol. 41, 1004-1009.
Legario, F. S., Choresca Jr, C. H., Turnbull, J. F., and Crumlish, M. 2020. Isolation and molecular characterization of streptococcal species recovered from clinical infections in farmed Nile tilapia (Oreochromis niloticus) in the Philippines. J. Fish Dis. 43, 1431-1442.
Liu, L., Li, Y. W., He, R. Z., Xiao, X. X., Zhang, X., Su, Y. L., and Li, A. X., 2014. Outbreak of Streptococcus agalactiae infection in barcoo grunter, Scortum barcoo (McCulloch & Waite), in an intensive fish farm in China. J. Fish Dis. 37, 1067-1072.
Martinez, G., Harel, J. and Gottschalk, M. 2001. Specific detection by PCR of Streptococcus agalactiae in milk. Can. J. Vet. Res. 65(1), 68.
Mazumder, A., Choudhury, H., Dey, A., and Sarma, D. 2021. Isolation and characterization of two virulent Aeromonads associated with haemorrhagic septicaemia and tail-rot disease in farmed climbing perch Anabas testudineus. Sci Rep. 11, 5826.
Mian, G. F., Godoy, D. T., Leal, C. A. G., Yuhara, T. Y., Costa, G. M., and Figueiredo, H. C. P. 2009. Aspects of the natural history and virulence of S. agalactiae infection in Nile tilapia. Vet. Microbiol. 136, 180-183.
Mohapatra, S. S., Dwibedy, S. K. and Padhy, I. 2021. Polymyxins, the last-resort antibiotics: Mode of action, resistance emergence, and potential solutions. J. Biosci. 46, 85.
Moore, E., Arnscheidt, A., Kruger A., Strompl, C., and Mau, M. 2004. Simplified protocols for the preparation of genomic DNA from bacterial cultures. Molecular Microbial Ecology Manual, Second Edition. 101, 3-18.
Mosaei, H. and Harbottle, J. 2019. Mechanisms of antibiotics inhibiting bacterial RNA polymerase. Biochem. Soc. Trans. 47, 339-350.
Musa, N., Wei, L. S., Musa, N., Hamdan, R. H., Leong, L. K., Wee, W. and Abdullah, S. Z. 2009. Streptococcosis in red hybrid tilapia (Oreochromis niloticus) commercial farms in Malaysia. Aquac. Res. 40, 630-632.
Ndashe, K., Hang’ombe, B. M., Changula, K., Yabe, J., Samutela, M. T., Songe, M. M., Kefi, A. S., Njobvu, C. L. and Sukkel, M. 2023. An Assessment of the Risk Factors Associated with Disease Outbreaks across Tilapia Farms in Central and Southern Zambia. Fishes. 8, 49.
Niu, G., Khattiya, R., Zhang, T., Boonyayatra, S. and Wongsathein, D. 2020. Phenotypic and genotypic characterization of Streptococcus spp. isolated from tilapia (Oreochromis spp.) cultured in river-based cage and earthen ponds in Northern Thailand. J Fish Dis. 43, 391-398.
Noga, J. E., (Editor), 2010. Fish disease-diagnosis and treatment (2nd Edition). John Wiley & Sons, 538.
Noinumsai, N., Thanakorn, S., and Waraporn, K. 2021. Growth and Survival of Thai Climbing Perch (Anabas testudineus) and Snake Skin Gourami (Trichogaster pectoralis) Reared in Brackish Water in Cement Pond in Salt-affected Soil. Journal of Food Health and Bioenvironmental Science. 14, 28-33.
Osman, K. M., Al-Maary, K. S., Mubarak, A. S., Dawoud, T. M., Moussa, I. M. I., Ibrahim, M. D. S., Hessain, A. M., Orabi, A. and Fawzy, N. M. 2017. Characterization and susceptibility of streptococci and enterococci isolated from Nile tilapia (Oreochromis niloticus) showing septicaemia in aquaculture and wild sites in Egypt. BMC Vet Res. Nov 25. 13, 357.
Ovung, A. and Bhattacharyya, J. 2021. Sulfonamide drugs: Structure, antibacterial property, toxicity, and biophysical interactions. Biophys. Rev. 13, 259-272.
Pandey, N., and Cascella, M., 2022. Beta lactam antibiotics. StatPearls [Internet].StatPearls Publishing.
Pasnik, D. J., Evans, J. J. and Klesius, P. H. 2009. Fecal strings associated with Streptococcus agalactiae infection in nile tilapia, Oreochromis niloticus. Open Vet. J. 3, 6-8.
Pereira, U. P., Mian, G. F., Oliveira, I. C. M., Benchetrit, L. C., Costa, G. M. and Figueiredo, H. C. P. 2010. Genotyping of Streptococcus agalactiae strains isolated from fish, human and cattle and their virulence potential in Nile tilapia. Vet. Microbiol. 140, 186-192.
Phu, T. M., Em, N. T., Thinh, N. Q., Ha, P. T. T., Nam, N. K., Huong, D. T. T., and Phuong, N. T. 2017. The use of drug, chemical, and probiotic in red tilapia (Oreochromis sp.) cage culture in Mekong Delta, Vietnam. Can Tho University Journal of Science. 51b, 80-87.
Pier, G. B. and Madin, S. H. 1976. Streptococcus iniae sp. nov., a beta-hemolytic streptococcus isolated from an Amazon freshwater dolphin, Inia geoffrensis. Int. J. Syst. Evol. Microbiol. 26, 545-553.
Pretto-Giordano, L. G., Müller, E. E., Freitas, J. C. D. and Silva, V. G. D., 2010. Evaluation on the Pathogenesis of Streptococcus agalactiae in Nile Tilapia (Oreochromis niloticus). Braz Arch Biol Technol. 53, 87-92.
Pulpipat, T., Boonyawiwat, V., Moonjit, P., Sanguankiat, A., Phatthanakunanan, S., Jala, S. and Surachetpong, W. 2023. Streptococcus agalactiae Serotype VII, an Emerging Pathogen Affecting Snakeskin Gourami (Trichogaster pectoralis) in Intensive Farming. Transbound Emerg Dis. 2023, 1-13.
Rahman, M. M., Rahman, M. A., Monir, M. S., Haque, M. E., Siddique, M. P., Khasruzzaman, A. K. M., Rahman, M. T., and Islam, M. A., 2021. Isolation and molecular detection of Streptococcus agalactiae from popped eye disease of cultured Tilapia and Vietnamese koi fishes in Bangladesh. J Adv Vet Anim Res. 8(1),14-23.
Reed, L. J. and Muench, H., 1938. A simple method of estimating fifty percent endpoints. Am. J. Epidemiol. 27, 493-497.
Romalde, J. L., Ravelo, C., Valdés, I., Magariños, B., de La Fuente, E., San Martín, C. and Toranzo, A. E., 2008. Streptococcus phocae, an emerging pathogen for salmonid culture. Vet. Microbiol. 130, 198-207.
Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-25.
Sherif, A. H., Abdellatif, J. I., Elsiefy, M. M., Gouda, M. Y. and Mahmoud, A. E. 2022. Occurrence of infectious Streptococcus agalactiae in the farmed Nile tilapia. Egypt. J. Aquat. Biol. Fish. 26, 403-432.
Shoemaker, C. A., Klesius, P. H. and Evans, J. J. 2001. Prevalence of Streptococcus iniae in tilapia, hybrid striped bass, and channel catfish on commercial fish farms in the United States. Am. J. Vet. Res. 62, 174-177.
Siti-Zahrah, A., B. Padilah, A. Azila, R. Rimatulhana, and H. Shahidan. 2008. Multiple streptococcal species infection in cage-cultured Red Tilapia but showing similar clinical signs. Pages 313–320 in M. G. Bondad-Reantaso, C. V. Mohan, M. Crumlish, and R. P. Subasinghe, editors. Diseases in Asian aquaculture VI. Asian Fisheries Society, Fish Health Section, Manila.
Suanyuk, N., Sukkasame, N., Tanmark, N., Yoshida, T., Itami, T., Thune, R. L. and Supamattaya, K. 2010. Streptococcus iniae infection in cultured Asian sea bass (Lates calcarifer) and red tilapia (Oreochromis sp.) in southern Thailand. Songklanakarin J Sci Technol. 32(4).
Sudpraseart, C., Wang, P. C., and Chen, S. C., 2021. Phenotype, genotype and pathogenicity of Streptococcus agalactiae isolated from cultured tilapia (Oreochromis spp.) in Taiwan. J Fish Dis. 44(6), 747-756.
Suhermanto A., Sukenda S., Zairin Jr. M., Lusiastuti A. M. and Nuryati S. 2019. Characterization of Streptococcus agalactiae bacterium isolated from tilapia (Oreochromis niloticus) culture in Indonesia. AACL Bioflux. 12, 756-766.
Suwannasang, A., Dangwetngam, M., Issaro, A., Phromkunthong, W. and Suanyuk, N. 2014. Pathological manifestations and immune responses of serotypes Ia and III Streptococcus agalactiae infections in Nile tilapia (Oreochromis niloticus). Songklanakarin J Sci Technol. 36, 499-506.
Syuhada, R., Zamri-Saad, M., Ina-Salwany, M. Y., Mustafa, M., Nasruddin, N. N., Desa, M. N. M., Nordin, S. A., Barkham, T., and Amal, M. N. A. 2020. Molecular characterization and pathogenicity of Streptococcus agalactiae serotypes Ia ST7 and III ST283 isolated from cultured red hybrid tilapia in Malaysia. Aquac. 515, 734-543.
Talwar, P. K., and Jhingran, A. G. 1991. Inland fishes of India and adjacent countries (Vol. 2). CRC press.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30, 2725-2729.
Tawab, A. A. E., Hofy, F. E., Ali, N., Saad, W., Mougy, E. E. and Mohammed, A. 2022 Antibiotic resistance genes in Streptococcus iniae isolated from diseased Oreochromis niloticus. Egypt. J. Aquat. Biol. Fish. 26, 413-428.
Thinh, N. H., Cuong, B. T. K., and Phuong, D. V. 2013. One case of severve infection of Trypanosoma sp. parasite in intensive culture climbing perch (Anabas testudineus). J. Mekong Fish. 1(7/2013), 62-72.
Trung, N. B., and Dung, T. T., 2018. Study of bacterial diseases on cage-cultured cobia (Rachycentron canadum) in Kien Giang province. Can Tho University Journal of Science. 2, 60-67.
Trung, N. B., Tinh, T. H., Hoa, T. T. T. and Dung, T. D. 2013. Isolation, identification, and antimicrobial susceptibility testing of Streptococcus iniae isolated from asian sea bass (Lates calcarifer). Proceedings of the IV National Fisheries Young Scientific Conference.
Wang, K., Chen, D., Huang, L., Lian, H., Wang, J., Xiao, D. and Lai, W. M. 2013. Isolation and characterization of Streptococcus agalactiae from Nile Tilapia Oreochromis niloticus in China. Afr. J. Microbiol. Res. 7, 317-323.
Yang, W. and Li, A. 2009. Isolation and characterization of Streptococcus dysgalactiae from diseased Acipenser schrenckii. Aquac. 294, 14-17.
Yanong, P. E. R. and Francis-Floyd, R. 2006. Streptococcal infections of Fish. Inst Food Agric Sci, Univ Florida Ext Circular No. 57.
Yuasa, K., Kitancharoen, N., Kataoka, Y. and Al-Murbaty, F. A. 1999. Streptococcus iniae, the causative agent of mass mortality in rabbitfish Siganus canaliculatus in Bahrain. J. Aquat. Anim. Health. 11, 87-93.
Zamri-Saad, M., Amal, M. N. A. and Siti-Zahrah, A. 2010. Pathological changes in red tilapias (Oreochromis spp.) naturally infected by Streptococcus agalactiae. J. Comp. Pathol. 143, 227-229.
Zappulli, V., Mazzariol, S., Cavicchioli, L., Petterino, C., Bargelloni, L. and Castagnaro, M. 2005. Fatal necrotizing fasciitis and myositis in a captive common bottlenose dolphin (Tursiops truncatus) associated with Streptococcus agalactiae. J. Vet. Diagn. Invest. 17, 617-622.