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Antimicrobial Susceptibility Pattern of Flavobacterium Columnare Isolates Collected Worldwide from 17 Fish Species

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Antimicrobial Susceptibility Pattern of Flavobacterium Columnare Isolates Collected Worldwide from 17 Fish Species Journal of Fish Diseases2013, 36, 4 5-55 doi:10.1111/j.1365-2761.2012.01410.x Antimicrobial susceptibility pattern of Flavobacterium columnare isolates collected worldwide from 17 fish species A M Declercq1, F Boyen2, W Van den Broeck1, P Bossier3, A Karsi4, F Haesebrouck2 and A Decostere1 1 Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium 2 Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium 3 Laboratory of Aquaculture and Artemia Reference Center, Ghent University, Ghent, Belgium 4 Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi, USA isolates coming from wild channel catfish in A bstract which acquired resistance was encountered Flavobacterium columnare is the causative agent of towards Oxytetracycline only. Fifty per cent of the columnaris disease in diverse fish species resistant isolates from ornamental fish were shown worldwide. Although columnaris is an important to have acquired resistance against three classes of disease, the antimicrobial susceptibility pattern of antimicrobial agents, assigning these isolates as F. columnare is not well studied. Thus, the multiple resistant. These data might indicate less purpose of this study was to test the in vitro anti­ prudent use of antimicrobials especially in orna­ microbial susceptibility of 97F. columnare isolates mental fish species. collected worldwide between 1987 and 2011 from Keywords: antimicrobial susceptibility testing, 17 fish species. The broth microdilution technique broth microdilution, columnaris, Flavobacterium was utilized for reliable testing of these fastidious columnare, multiple resistance. organisms. None of the isolates displayed acquired resistance to florfenicol, gentamicin, ormetoprim- sulfadimethoxine and trimethoprim-sulfamethox- Introduction azole. Acquired resistance to chloramphenicol was Columnaris disease is a predominant bacterial dis­ detected in 1%, to nitrofuran in 5%, to Oxytetra­ ease o f both cultured and wild freshwater fish. cycline in 11% and to enrofloxacin, flumequine Many commercially important fish species are sus­ and oxolinic acid in 10%, 16% and 16% of the ceptible to columnaris disease, such as (but not isolates, respectively, as reflected by a bimodal or limited to) salmonids, eels, carp, goldfish, tilapia trimodal distribution of their minimum inhibitory and channel catfish (Rehulka & Minarik 2007; concentrations (MICs). One isolate showed Soto et al. 2008; Suomalainen, Bandilla & acquired resistance towards several antimicrobial Valtonen 2009). This disease also poses a problem agents including erythromycin. Another isolate for many freshwater tropical aquarium fish (Post revealed acquired resistance towards - amongst 1987; Decostere, Plaesebrouck & Devriese 1998). others - ampicillin. The isolates displaying F. columnare infections may result in skin lesions, acquired resistance originated from ornamental fin erosion and gili necrosis, with a high degree of fish species or Vietnamese catfish, except for two mortality, leading to severe economic losses Fish D iseases (Decostere et al. 1998). In the United States, Correspondence A M Declercq, Department of Morphology, F. columnare is the second most prevalent bacte­ Faculty of Veterinary Medicine, Ghent University Salisburylaan 133 9820 Merelbeke, Belgium rium, after Edwardsiella ictaluri, to cause disease cu (e-mail: [email protected] and mortality (Plawke & Thune 1992; Wagner E © 2012 Blackwell Publishing Ltd. 45 3 JournalO f Fish Diseases 2013, 36, 45—55 A M Declercq et al. Antimicrobial susceptibility pattern ^/"Flavobacterium columnare isolates et al. 2002), with yearly losses estimated at delayed growth (Flesami et al. 2010; Miller et al. 30 million dollars (Shoemaker et al. 2011). 2005). The Clinical and Laboratory Standards Up until now, only a limited number of Institute (CLSI) therefore proposed the use of the effective preventive measures against columnaris broth microdilution technique in 1:7 diluted disease are available, including an attenuated cation adjusted Mueller Flinton broth (CAMFIB) immersion vaccine registered for use in channel for fastidious growing organisms like F. columnare catfish in the United States only (Shoemaker et al. (CLSI 2006). Darwish, Farmer & flawke (2008) 2011). A F. columnare bacterin was also brought adopted much of the CLSI 2006 recommenda­ to market in the USA as an aid in the prevention tions but used 1:5 dilution o f CAMFIB as an of columnaris disease in healthy salmonids of over alternative method to the one proposed by 3 g (AFS-FCS 2011). Awaiting further research Clinical & Laboratory Standards Institute (CLSI) aimed at developing and validating more (2006), based on the work of Farmer (2004). precautionary measures, there is still an excessive They determined the minimum inhibitory con­ use of antimicrobial agents in the contemporary centration (MIC) of 23 F. columnare isolates to treatment of F. columnare (Shoemaker et al. eight antimicrobial agents. All isolates came from 2011). It should be noted that significant negative channel catfish except for three isolates originating attributes are associated with the use of antimicro­ from a common carp and two type strains isolated bials including the extensive expenditure on these from a Chinook salmon and a brown trout. All substances and possible allergic reactions elicited isolates were procured in the USA except for one in the user after food contact. Potential impacts (type strain) which was isolated in France. The on human health resulting from the emergence of authors underscored the noted resistance against drug-resistant bacteria and the associated risk of the combination of metoprim/sulfadimethoxine transfer of these resistant traits to the environment but did not interpret the other encountered MIC and human-associated bacteria are also a major values and acknowledged the relatively low num­ concern (Serrano 2005). ber o f tested isolates. To seize on the aforementioned risks associated The purpose of this study was to address the with antimicrobial use and to inform veterinary above described lack of information on the anti­ practitioners on the therapeutic value of antimi­ microbial susceptibility pattern of F. columnare. crobial agents, enabling them to make an Therefore, 97 isolates of F. columnare collected informed choice, antimicrobial susceptibility worldwide from 17 different fish species were monitoring is a necessary prerequisite. Flitherto, tested for their susceptibility to 12 antimicrobial only limited information is available on the anti­ agents by means of the broth microdilution microbial susceptibility pattern of F. columnare. technique. Antimicrobial susceptibility studies of Thomas- Jinu & Goodwin (2004) using agar disc diffusion revealed susceptibility of two of the four tested Materials and methods strains towards a combination of sulfadimethoxine Bacterial strains and ormetoprim and acquired resistance of two isolates towards Oxytetracycline. The same assay Ninety-seven F. columnare isolates originating was adopted to assess the antimicrobial suscepti­ from 17 fish species collected worldwide between bility of eight Finnish F. columnare strains by 1987 and 2011 from both cultured and wild fish Suomalainen et al. (2006). All strains were suscep­ populations were included in this study (Table 1). tible to ampicillin, erythromycin, gentamicin, The identity of F. columnare was confirmed by nitrofurantoin, streptomycin, tetracycline, trimeth- polymerase chain reaction (PCR). Briefly, genomic oprim-sulpha and florfenicol, but displayed DNA was extracted by suspending one colony of acquired resistance to neomycin and polymyxin B. a pure bacterial culture in 20 mL lysis buffer Flowever, agar disc diffusion tests are challenging (0.25% SDS, 0.05 N NaOH). This suspension because of the rhizoid growth of the organism, was heated at 95 °C for 5 min and centrifuged which tends to make the zones of inhibition ill for 10 s at 16.100 g for vapour deposition. One defined. Moreover, no specific breakpoints are hundred and eighty millilitres of sterile distilled available for F. columnare. Additionally, the appar­ water was added and centrifugation was carried ent zones of inhibition may be the result of out at 16.100 g for 5 min. Specific primers were © 2012 Blackwell Publishing Ltd 4 6 Jo u rn a l O f Fish Diseases 2013, 36, 45—55 A M D eclercq et al. Antimicrobial susceptibility pattern ^/"Flavobacterium columnare isolates T ab le 1 Flavobacterium columnare isolates included in the antimicrobial susceptibility testing Isolate of Flavobacterium columnare Fish host Origin Year of isolation Provided by JIP 44/87 Brown trout ( Salmo trutta) France 1987 Dr J.F. Bernardet (ATCC 49512) JIP 39/87 Black bullhead ( Ictalurus melas) France 1987 Dr J.F. Bernardet (ATCC 49513) LVDL 3414/89 European eel ( Anguila anguilla) France 1989 Dr J.F. Bernardet P06/90 Black bullhead Unknown 1990 Dr J.F. Bernardet 90-106 Channel catfish ( Ictalurus punctatus) USA 1990 Dr A. Karsi L90-629 Channel catfish USA 1990 Dr A. Karsi P 11/91 Rainbow trout ( Oncorhynchus mykiss) France 1991 Dr J.F. Bernardet C91-20 Channel catfish USA 1991 Dr A. Karsi LVDI 39/I Unknown France 1992 Dr J.F. Bernardet 92-002 Channel catfish USA 1992 Dr A. Karsi AI 94 Channel catfish USA 1994 Dr A.E. Goodwin LVDJ (D7461) Rainbow trout France 1994 Dr J.F. Bernardet 94-078 Channel catfish USA 1994 Dr A. Karsi BioMed Channel
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