Antimicrobial susceptibility of Enterococcus spp. isolated from freshwater fish and personnel and equipment of fish markets in northern Greece

Published: Dec 20, 2017
antimicrobial susceptibility biogenic amines Enterococcus spp. freshwater fish

In total, 270 samples from freshwater fish and personnel and equipment from retail fish markets in three cities in northern Greece, were examined for presence of antimicrobial resistance and biogenic amine production of Enterococcus spp. strains. Enterococci were isolated from 9.6% of the samples; from 7.4% and 2.2%, respectively, Enterococcus faecium and Enterococcus casseliflavus were recovered. Isolates were tested for antibacterial susceptibility to 20 antibiotics used regularly in Greek hospitals. All isolates except one were multi drug resistant, to 7-15 antibiotics. Increased rates of resistance were recorded to penicillin, cephalosporins and erythromycin. Relatively increased rates were recoreded to quinupristin/casdalfopristin and linezolid, drugs commonly used as treatment options of infections by vancomycin-resistant enterococci. One E. faecium and one E. casseliflavus isolate showed intermediate resistance to vancomycin. Multiplex PCR assay for presence of van genes in E. faecium was negative. All E. faecium isolates and one third of E. casseliflavus isolates were able to decarboxylate tyrosine, but not histidine, ornithine or lysine. The results indicate that freshwater fish and fish markets are potential reservoirs of multi-drug resistant enterococci.

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Al Bulushi IM, Poole S, Deeth HC, Dykes GA (2009) Biogenic amines in fish: roles in intoxication, spoilage, and nitrosamine formation - A review. Crit Rev Food Sci Nutr 49:369-377.
Al Bulushi IM, Poole SE, Barlow R, Deeh HC, Dykes GA (2010) Speciation of Gram-positive bacteria in fresh and ambient-stored sub-tropical marine fish. Int J Food Microbiol 138:32-38.
Barros J, Igrejas G, Andrade M, Radhouani H, López M, Torres C, Poeta P (2011) Gilthead seabream (Sparus aurata) carrying antibiotic resistant enterococci. A potential bioindicator of marine contamination? Mar Pollut Bull 62:1245-1248.
Bover-Cid S, Holzapfel WH (1999) Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53:33-41.
Bover-Cid S, Hugas M, Izquierdo-Pulido M, Vidal-Carou MC (2001) Amino acid-decarboxylase activity of bacteria isolated from fermented pork sausages. Int J Food Microbiol 66:185-189.
Busani L, Del Grosso M, Paladini C, Graziani C, Pantosti A, Biavasco F, Caprioli A (2004) Antimicrobial susceptibility of vancomycinsusceptible and -resistant enterococci isolated in Italy from raw meat products, farm animals, and human infections. Int J Food Microbiol 97:17-22.
Chatterjee I, Iredell JR, Woods M, Lipman J (2007) The implications of enterococci for the intensive care unit. Critical care and resuscitation: J Australasian Academy of Critical Care Medicine 9:69-75.
Chingwaru W, Mpuchane SF, Gashe BA (2003) Enterococcus faecalis and Enterococcus faecium isolates from milk, beef, and chicken and their antibiotic resistance. J Food Prot 66:931-936.
Chong CY, Bakar FA, Russly AR, Jamilah B, Mahyudin NA (2011) The effects of food processing on biogenic amines formation. Int Food Research J 18:867-876.
Christidou A, Gikas A, Scoulica E, Pediaditis J, Roumbelaki M, Georgiladakis A, Tselentis Y (2004) Emergence of vancomycinresistant enterococci in a tertiary hospital in Crete, Greece: a cluster of cases and prevalence study on intestinal colonization. Clinical Microbiology and Infection 10:999-1005.
Çitak S, Yucel N, Orhan S (2004) Antibiotic resistance and incidence of Enterococcus species in Turkish white cheese. Int J Dairy Technol 57:27-31.
CLSI (2008)Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals Approved Standard CLSI Document M31-A3. Wayne, PA, USA.: Clinical and Laboratory Standards Institute.
Dalgaard P, Vancanneyt M, Euras Vilalta N, Swings J, Fruekilde P, Leisner JJ (2003) Identification of lactic acid bacteria from spoilage associations of cooked and brined shrimps stored under modified atmosphere between 0°C and 25°C. J Appl Microbiol 94:80-89.
David OM, Falegan CR, Ogunlade JT (2010) Levels of heavy and other metals in tilapia species raised in different ponds and resistant pattern of associated Enterococcus species. Advances in Environ Biology 4:47-52.
De Perio MA, Yarnold PR, Warren J, Noskin GA (2006) Risk Factors and Outcomes Associated with Non–Enterococcus faecalis, Non–Enterococcus faecium Enterococcal Bacteremia. Infect Control Hosp Epidemiol 27:28-33.
Domig KJ, Mayer HK, Kneifel W (2003) Methods used for the isolation, enumeration, characterisation and identification of Enterococcus spp.: 1. Media for isolation and enumeration. Int J Food Microbiol 88:147-164.
Eaton TJ, Gasson MJ (2001) Molecular Screening of Enterococcus Virulence Determinants and Potential for Genetic Exchange between Food and Medical Isolates. Appl Environ Microbiol 67:1628-1635.
Fernández M, Linares D, Rodríguez A, Alvarez M (2007) Factors affecting tyramine production in Enterococcus durans IPLA 655. Appl Microbiol Biotechnol 73:1400-1406.
Fisher K, Phillips C (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiol 155:1749-1757.
Franz CMAP, Holzapfel WH, Stiles ME (1999) Enterococci at the crossroads of food safety? Int J Food Microbiol 47:1-24.
Gardini F, Martuscelli M, Caruso MC, Galgano F, Crudele MA, Favati F, Guerzoni ME, Suzzi G (2001) Effects of pH, temperature and NaCl concentration on the growth kinetics, proteolytic activity and biogenic amine production of Enterococcus faecalis. Int J Food Microbiol 64:105-117.
Giraffa G (2003) Functionality of enterococci in dairy products. Int J Food Microbiol 88:215-222.
Giraffa G, Carminati D, Neviani E (1997) Enterococci Isolated from Dairy Products: A Review of Risks and Potential Technological Use. J Food Prot 60:732-737.
Giraffa G, Olivari AM, Neviani E (2000) Isolation of vancomycinresistant Enterococcus faecium from Italian cheeses. Food Microbiol 17:671-677.
Hayes JR, English LL, Carter PJ, Proescholdt T, Lee KY, Wagner DD, White DG (2003) Prevalence and Antimicrobial Resistance of Enterococcus Species Isolated from Retail Meats. Appl Environ Microbiol 69:7153-7160.
Hugas M, Garriga M, Aymerich MT (2003) Functionality of enterococci in meat products. Int J Food Microbiol 88:223-233.
Hummel A, Holzapfel WH, Franz CMAP (2007) Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Systematic Appl Microbiol 30:1-7.
Jaffrès E, Sohier D, Leroi F, Pilet MF, Prévost H, Joffraud JJ, Dousset X (2009) Study of the bacterial ecosystem in tropical cooked and peeled shrimps using a polyphasic approach. Int J Food Microbiol 131:20-29.
Karmakar MG, Gershon ES, Mehta PR (2004) Enterococcal infections with special reference to phenotypic characterization and drug resistance. Indian J Med Res119 (Suppl.):22-25.
Koluman A, Akan LS, Çakiroğlu FP (2009) Occurrence and antimicrobial resistance of enterococci in retail foods. Food Control 20:281-283.
Leclercq R, Courvalin P (1997) Resistance to glycopeptides in enterococci. Clin Infect Dis24:545-554.
Marine-Font A, Vidal-Carou C, Izquierdo-Pulido M, Veciana-Nogues T, Hernandez-Jover T (1995) Les amines biogenes dans les aliments: leur signification, leur analyse. Paris, France: Soci des experts-chimistes de France.
Masson F, Talon R, Montel MC (1996) Histamine and tyramine production by bacteria from meat products. Int J Food Microbiol 32:199-207.
Mejlholm O, Kjeldgaard J, Modberg A, Vest MB, Bøknæs N, Koort J, Björkroth J, Dalgaard P (2008) Microbial changes and growth of Listeria monocytogenes during chilled storage of brined shrimp (Pandalus borealis). Int J Food Microbiol 124:250-259.
National Nosocomial Infections Surveillance (2004) System Report, data summary from January 1992 through June 2004, issued October 2004. A report from the NNIS System. Am J Infect Control 32:470-485.
Omar NB, Castro A, Lucas R, Abriouel H, Yousif NMK, Franz CMAP, Holzapfel WH, Rubén PP, Martínez-Canãmero M, Gálvez A (2004) Functional and Safety Aspects of Enterococci Isolated from Different Spanish Foods. Systematic and Appl Microbiol 27:118-130.
Pavia M, Nobile CGA, Salpietro L, Angelillo IF (2000) Vancomycin Resistance and Antibiotic Susceptibility of Enterococci in Raw Meat. J Food Prot 63:912-915.
Peters J, Mac K, Wichmann-Schauer H, Klein G, Ellerbroek L (2003) Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany. Int J Food Microbiol88:311-314.
Petersen A, Dalsgaard A (2003) Antimicrobial resistance of intestinal Aeromonas spp. and Enterococcus spp. in fish cultured in integrated broiler-fish farms in Thailand. Aquaculture 219:71-82.
Poeta P, Costa D, Igrejas G, RodriguesJ, Torres C (2007) Phenotypic and genotypic characterization of antimicrobial resistance in faecal enterococci from wild boars (Sus scrofa). Veterinary Microbiol 125:368-374.
Poeta P, Costa D, Rodrigues J, Torres C (2006) Antimicrobial resistance and the mechanisms implicated in faecal enterococci from healthy humans, poultry and pets in Portugal. Int J Antimicrobial Agents 27:131-137.
Quigg A, Broach L, Denton W, Miranda R (2009) Water quality in the Dickinson Bayou watershed (Texas, Gulf of Mexico) and health issues. Marine Pollution Bulletin 58:896-904.
Reid K C, Cockerill III FR, Patel R (2001) Clinical and epidemiological features of Enterococcus casseliflavus/flavescens and Enterococcus gallinarum bacteremia: a report of 20 cases.Clin Infect Dis32:1540-1546.
Rice E, Messer J, Johnson C, Reasoner D (1995) Occurrence of highlevel aminoglycoside resistance in environmental isolates of enterococci. Appl Environ Microbiol 61:374-376.
Sarantinopoulos P, Andrighetto C, Georgalaki MD, Rea MC, Lombardi A, Cogan TM, Kalantzopoulos G, Tsakalidou E
(2001) Biochemical properties of enterococci relevant to their technological performance. Int Dairy J 11:621-647.
Sergelidis D, Abrahim A, Anagnostou V, Papa A, Papadopoulos T (2010) Prevalence and antimicrobial susceptibility of Enterococcus spp. in ready-to-eat salads (dips), the environment and the personnel of a salad processing plant in Northern Greece. J. Hellenic Vet Med Soc 61:308-315.
Silla Santos MH (1996) Biogenic amines: Their importance in foods. Int J Food Microbiol 29:213-231.
Tomé E, Pereira VL, Lopes CI, Gibbs PA, Teixeira PC (2008) In vitro tests of suitability of bacteriocin-producing lactic acid bacteria, as potential biopreservation cultures in vacuum-packaged coldsmoked salmon. Food Control 19:535-543.
Toye B, Shymanski J, Bobrowska M, Woods W, Ramotar K (1997) Clinical and epidemiological significance of enterococci intrinsically resistant to vancomycin (possessing the vanC genotype). J Clin Microbiol 35:3166-3170.
Tuncer Y (2009) Some technological properties of phenotypically identified enterococci strains isolated from Turkish tulum cheese. African J Biotechnol 8:7008-7016.
Valenzuela AS, Benomar N, Abriouel H, Cañamero MM, Gálvez A (2010) Isolation and identification of Enterococcus faecium from seafoods: Antimicrobial resistance and production of bacteriocin like substances. Food Microbiology 27:955-961.
Wilson IG, Mcafee GG (2002) Vancomycin-resistant enterococci in shellfish, unchlorinated waters, and chicken. Int J Food Microbiol 79:143-151.
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