Mycobacterium chelonae associated with tumor-like skin and oral masses in farmed Russian sturgeons (Acipenser gueldenstaedtii)

BMC Veterinary Research

Marino Prearo³  Claudio Pedron²  Ilaria Giorgi³  Monica Caffara¹  Stefano Rocca⁴  Giovanni P Burrai⁴  Udo Hetzel⁵  Sara Nuvoli⁴  Antonio Pais⁶  Elisabetta Antuofermo⁴ 

[1] Department of Veterinary Medical Sciences, Alma Mater Studiorum, University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia (BO), Italy;DVM, 20090 Settala, Milano, Italy;State Veterinary Institute of Piedmont, Liguria and Aosta Valley, Fish Disease Laboratory, Via Bologna 148, 10154 Torino, Italy;Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Italy;Department of Veterinary Bioscience, Faculty of Veterinary Medicine, University of Helsinki, Agnes Sjöbergin katu 2, FI-00014 Helsinki, Finland;Section of Animal Science, Department of Agriculture, University of Sassari, Via Enrico de Nicola 1, 07100 Sassari, Italy

关键词: Mycobacteria;    Fish pathology;    Calcinosis circumscripta;    Aquaculture;    Acipenser gueldenstaedtii;   

Others  :  1119352
DOI  :  10.1186/1746-6148-10-18

 received in 2013-05-31, accepted in 2014-01-06,  发布年份 2014

【 摘 要 】

Background

Non-tuberculous mycobacteria responsible for piscine mycobacteriosis usually produce visceral granulomas in both freshwater and marine species. In this study, the first occurrence of Mycobacterium chelonae associated with tumor-like lesions in the Russian sturgeon (Acipenser gueldenstaedtii) is reported. Fifteen sturgeons from an Italian fish farm showing skin and oral cauliflower-like masses were investigated by histopathology, bacterial culture and molecular analyses.

Results

A total of 20 masses different in size located in the mouth and in pectoral and caudal fins (characterized by abundant calcium deposits and by mild to moderate granulomatous inflammation) were observed with a significant different degree of histological severity. All internal organs of the fish were negative for mycobacteria, Ziehl-Neelsen was positive in only one of the oral masses, whereas bacterial and PCR analyses detected the presence of M. chelonae for almost all the skin and oral masses. Based on these results, a calcinosis of dystrophic origin associated with a chronic granulomatous inflammation was considered as a primary diagnosis consequent to tissue injury in areas susceptible to trauma.

Conclusions

We hypothesized that the occurrence of M. chelonae in farmed sturgeons was only a secondary event related to its presence in a stressful rearing environment and subsequent to a dystrophic calcinosis occurred in previously damaged tissues.

【 授权许可】

   
2014 Antuofermo et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Sokolov LI, Berdicheskii LS: Acipenseridae. In The Freshwater Fishes of Europe. Vol. 1, Part II edition. Edited by Holcík J. Wiesbaden, Germany: AULA-Verlag; 1989:150-153.
• [2]Froese R, Pauly D: FishBase. 2012. http://www.fishbase.org webcite (version 02/2012)
• [3]Bronzi P, Rosenthal H, Arlati G, Williot P: A brief overview on the status and prospects of sturgeon farming in Western and Central Europe. J Appl Ichthyol 1999, 15:224-227.
• [4]Celikkale MS, Memis D, Ercan E, Cagiltay F: Growth performance of juvenile Russian sturgeon (Acipenser gueldenstaedtii Brandt & Ratzenburg, 1833) at two stocking densities in net cages. J Appl Ichthyol 2005, 21:14-18.
• [5]Kottelat M, Gesner J, Freyhof J: Acipenser gueldenstaedtii. IUCN Red List of Threatened Species. IUCN 2011. Version 2011.2 2010. http://www.iucnredlist.org webcite
• [6]Nathanailides C, Tsoumani M, Papazogloy A, Paschos I: Hatching time and post-hatch growth in Russian sturgeon Acipenser gueldenstaedtii. J Appl Ichthyol 2002, 18:651-654.
• [7]Bronzi P, Rosenthal H, Gessner J: Global sturgeon aquaculture production: an overview. J Appl Ichthyol 2011, 27:169-175.
• [8]Bauer ON, Pugachev ON, Voronin VN: Study of parasites and diseases of sturgeons in Russia: a review. J Appl Ichthyol 2002, 18(4–6):420-429.
• [9]Dottori M, Santi A, Ausini A, Carboni A: Isolation of Flexibacter columnaris from sturgeon (Acipenser transmontanus) with gill disease. Sel Vet 1990, 31:279-284.
• [10]Karatas S, Ercan D, Steinum TM, Turgay E, Memis D, Candan A: First isolation of a Flavobacterium johnsoniae like bacteria from cultured Russian sturgeon in Turkey. J Anim Vet Adv 2010, 9:1943-1946.
• [11]Wang L-F, Xie H-X, Zhang J, Li N, Yao W-J, Zhang L-Q, Xiong C-X, Nie P: Columnaris disease and genetic diversity of its bacterial pathogen Flavobacterium columnare in freshwater fish in China. Acta Hydrobiol Sin 2010, 34:367-377.
• [12]Cao HP, Yang XI, Gao P, Li Y, Zhang SJ, Deng L: Preliminary study of the pathogens isolates from bacterial septicaemia syndrome of sturgeons. Freshw Fisher 2007, 37:53-56.
• [13]Colussi S, Gasparri F, Brunetti R, Ferrari A, Marturano S, Prearo M: Aeromonas hydrophila infection in farmed Siberian sturgeon (Acipenser baeri). Ittiopatologia 2005, 2:105-110.
• [14]Quaglio F, Bocus R, Delgado ML, Gamberini L, Nobile L, Minelli C, Galuppi R, Restani R: Aeromonas hydrophila in sterlets (Acipenser ruthenus) in Padana plain. Boll Soc It Patol Ittica 2000, 28:17-32.
• [15]Vuillaume A, Brun R, Chene P, Sochon E, Lesel R: First isolation of Yersinia ruckeri from sturgeon, Acipenser baeri Brandt, in South West of France. Bull Eur Ass Fish Pathol 1987, 7:18-19.
• [16]Brunetti R, Gasparri F, Marturano S, Prearo M: Pseudomonas fluorescens infection in farmed Siberian sturgeon (Acipenser baeri). Ittiopatologia 2006, 3:221-226.
• [17]Groff JM, LaPatra SE, Munn RJ, Anderson ML, Osburn BI: Epitheliocystis infection in cultured white sturgeon (Acipenser transmontanus): antigenic and ultrastructural similarities of the causative agent to the chlamydiae. J Vet Diagn Invest 1996, 8:172-180.
• [18]Hedrick RP, Speas J, Kent ML, Mcdowell T: Adenovirus-Like particles associated with a disease of cultured white sturgeon, Acipenser-Transmontanus. Can J Fish Aquat Sci 1985, 42:1321-1325.
• [19]Kovacs GM, LaPatra SE, D'Halluin JC, Benko M: Phylogenetic analysis of the hexon and protease genes of a fish adenovirus isolated from white sturgeon (Acipenser transmontanus) supports the proposal for a new adenovirus genus. Virus Res 2003, 98:27-34.
• [20]Hedrick RP, Mcdowell TS, Groff JM, Yun S, Wingfield WH: Isolation of an epitheliotropic herpesvirus from white sturgeon Acipenser-Transmontanus. Dis Aquat Organ 1991, 11:49-56.
• [21]Watson LR, Yun SC, Groff JM, Hedrick RP: Characteristics and pathogenicity of a novel herpesvirus isolated from adult and subadult white sturgeon Acipenser-Transmontanus. Dis Aquat Organ 1995, 22:199-210.
• [22]Adkinson MA, Cambre M, Hedrick RP: Identification of an iridovirus in Russian sturgeon (Acipenser gueldenstaedtii) from Northern Europe. Bull Eur Ass 1998, 18:29-32.
• [23]Hedrick RP, Groff JM, Mcdowell T, Wingfield WH: An iridovirus infection of the integument of the white sturgeon Acipenser transmontanus. Dis Aquat Organ 1990, 8:39-44.
• [24]Lapatra SE, Groff JM, Jones GR, Munn B, Patterson TL, Holt RA, Hauck AK, Hedrick RP: Occurrence of white sturgeon iridovirus infections among cultured white sturgeon in the Pacific-Northwest. Aquaculture 1994, 126:201-210.
• [25]Raverty S, Hedrick R, Henry J, Saksida S: Diagnosis of sturgeon iridovirus infection in farmed white sturgeon in British Columbia. Can Vet J 2003, 44:327-328.
• [26]Manfrin A, Prearo M, Alborali L, Salogni C, Ghittino C, Fioravanti ML: Mycobacteriosis in sea bass, rainbow trout, striped bass and Siberian sturgeon in Italy. In Program, abstracts and report of EAFP Workshop “Zoonotic infections from fish and shellfish”: 14-19 September 2009. Prague, Czech Republic; 2009:5.
• [27]Ghaemi EO, Ghazesaeed K, Nasab FF, Hashemzade Z, Vatani S, Mohamedi M, Mansourian AR: Mycobacterium marinum infection in caviar fishes and fisherman’s in a Caspian Sea province in North of Iran. J Biol Sci 2006, 6:1150-1152.
• [28]Primm TP, Lucero CA, Falkinham JO: Health impacts of environmental mycobacteria. Clin Microbiol Rev 2004, 17:98-106.
• [29]Beran V, Matlova L, Dvorska L, Svastova P, Pavlik I: Distribution of mycobacteria in clinically healthy ornamental fish and their aquarium environment. J Fish Dis 2006, 29(7):383-393.
• [30]Chinabut S: Mycobacteriosis and nocardiosis. In Fish diseases and disorders. Edited by Woo PTK, Bruno DW. UK: CABI Publishing; 1999:319-340. 2nd Vol. 3: Viral, bacterial and fungal infections
• [31]Gauthier DT, Rhodes MW: Mycobacteriosis in fish: a review. Vet J 2009, 180:33-47.
• [32]Gauthier DT, Latour RJ, Heisey DM, Bonzek CF, Gartland J, Burge EJ, Vogelbein WK: Mycobacteriosis-associated mortality in wild striped bass (Morone saxatilis) from Chesapeake Bay. U.S.A. Ecol Appl 2008, 18:1718-1727.
• [33]Decostere A, Hermans K, Haesebrouck F: Piscine mycobacteriosis: a literature review covering the agent and the disease it causes in fish and humans. Vet Microbiol 2004, 99:159-166.
• [34]Jacobs JM, Stine CB, Baya AM, Kent ML: A review of mycobacteriosis in marine fish. J Fish Dis 2009, 32:119-130.
• [35]Brocklebank J, Raverty S, Robinson J: Mycobacteriosis in Atlantic salmon farmed in British Columbia. Can Vet J 2003, 44(6):486-489.
• [36]Whipps CM, Butler WR, Pourahmad F, Watral VG, Kent ML: Molecular systematics support the revival of Mycobacterium salmoniphilum (ex Ross 1960) sp nov., nom. rev., a species closely related to Mycobacterium chelonae. Int J Syst Evol Micr 2007, 57:2525-2531.
• [37]Ghittino P: Infezione da batteri acido resistenti. In Tecnologia e patologia in acquacoltura. Edited by Ghittino P. Tipografia Emilio Bono, Italy: Torino; 1985:111-112. Vol. 2: Patologia
• [38]Prearo M, Zanoni RG, Dall'Orto BC, Pavoletti E, Florio D, Penati V, Ghittino C: Mycobacterioses: emerging pathologies in aquarium fish. Vet Res Commun 2004, 28:315-317.
• [39]Zanoni RG, Florio D, Fioravanti ML, Rossi M, Prearo M: Occurrence of Mycobacterium spp. in ornamental fish in Italy. J Fish Dis 2008, 31:433-441.
• [40]Kent TP, Kubica PG: Public health mycobacteriology: a guide for the level III laboratory. Atlanta, Georgia: U.S. Department of Health and Human Services, Public Health Service, Centre for Diseases Control; 1985.
• [41]Telenti A, Marchesi F, Balz M, Bally F, Bottger EC, Bodmer T: Rapid identification of mycobacteria to the species level by polymerase chain-reaction and restriction enzyme analysis. J Clin Microbiol 1993, 31:175-178.
• [42]Zar JH: Biostatistical analysis. 5th edition. Upper Saddle River, New Jersey: Prentice-Hall; 2009.
• [43]Bruno DW, Griffiths J, Mitchell CG, Wood BP, Fletcher ZJ, Drobniewski FA, Hastings TS: Pathology attributed to Mycobacterium chelonae infection among farmed and laboratory-infected Atlantic salmon Salmo salar. Dis Aquat Organ 1998, 33:101-109.
• [44]Dos Santos NMS, do Vale A, Sousa MJ, Silva MT: Mycobacterial infection in farmed turbot Scophthalmus maximus. Dis Aquat Organ 2002, 52:87-91.
• [45]Daoust PY, Larson BE, Johnson GR: Mycobacteriosis in Yellow Perch (Perca-Flavescens) from 2 lakes in Alberta. J Wildlife Dis 1989, 25:31-37.
• [46]Bercovier H, Vincent V: Mycobacterial infections in domestic and wild animals due to Mycobacterium marinum, M-fortuitum, M-chelonae, M-porcinum, M-farcinogenes, M-smegmatis, M-scrofulaceum. M-xenopi, M-kansasii, M-simiae and M-genavense. Rev Sci Tech Oie 2001, 20(1):265-290.
• [47]Green SL, Lifland BD, Bouley DM, Brown BA, Wallace RJ, Ferrell JE: Disease attributed to Mycobacterium chelonae in South African clawed frogs (Xenopus laevis). Comparative Med 2000, 50:675-679.
• [48]Astrofsky KM, Schrenzel MD, Bullis RA, Smolowitz RM, Fox JG: Diagnosis and management of atypical Mycobacterium spp. infections in established laboratory zebrafish (Brachydanio rerio) facilities. Comparative Med 2000, 50:666-672.
• [49]Jubb KVF, Kennedy PC, Palmer’s NC: Pathology of domestic animals. 5th edition. Philadelphia: Saunders Elsevier; 2007.
• [50]Łojszczyk-Szczepaniak A, Orzelski M, Śmiech A: Canine calcinosis circumscripta retrospective studies. Medycyna Wet 2008, 64:1397-1400.
• [51]Reiter N, El-Shabrawi L, Leinweber B, Berghold A, Aberer E: Calcinosis cutis Part I. Diagnostic pathway. J Am Acad Dermatol 2011, 65:1-12.
• [52]Zerihun MA, Colquhoun DJ, Poppe TT: Experimental mycobacteriosis in Atlantic cod, Gadus morhua L. J Fish Dis 2012, 35:365-377.
• [53]Fuentes J, Haond C, Guerreiro PM, Silva N, Power DM, Canario AV: Regulation of calcium balance in the sturgeon Acipenser naccarii: a role for PTHrP. Am J Physiol Regul Integr Comp Physiol 2007, 293:R884-R893.
• [54]Viegas CSB, Cavaco S, Neves PL, Ferreira A, Joao A, Williamson MK, Price PA, Cancela ML, Simes DC: Gla-Rich protein is a novel vitamin k-dependent protein present in serum that accumulates at sites of pathological calcifications. Am J Pathol 2009, 175:2288-2298.
• [55]Viegas CSB, Simes DC, Laize V, Williamson MK, Price PA, Cancela ML: Gla-rich Protein (GRP), a new vitamin k-dependent protein identified from sturgeon cartilage and highly conserved in vertebrates. J Biol Chem 2008, 283:36655-36664.
• [56]Mrlik V, Slany M, Kubecka J, Seda J, Necas A, Babak V, Slana I, Kriz P, Pavlik I: A low prevalence of mycobacteria in freshwater fish from water reservoirs, ponds and farms. J Fish Dis 2012, 35:497-504.
• [57]Harriff MJ, Wu M, Kent ML, Bermudez LE: Species of environmental mycobacteria differ in their abilities to grow in human, mouse, and carp macrophages and with regard to the presence of mycobacterial virulence genes, as observed by DNA microarray hybridization. Appl Environ Microb 2008, 74(1):275-285.