Abstract
The aim of this study was to investigate the prevalence and genetic basis of multidrug resistance in Chryseobacterium indologenes from seawater and marine invertebrates used for human consumption, in Kaštela Bay, Adriatic Sea, Croatia. Out of 16 samples of seawater, Mediterranean mussel (Mytilus galloprovincialis Lam.), Rayed Mediterranean limpets (Patella caerulea L.) and Purple sea urchins (Paracentrotus lividus Lam.) collected, 15 were positive for C. indologenes. In total, 41 isolates were randomly selected and tested for antibiotic susceptibility by disc-diffusion and broth microdilution methods. PCR was used to detect alleles encoding extended-spectrum (ESBLs) and metallo-β-lactamases (MBLs). The clonality of β-lactamase-producing strains was evaluated by random amplified polymorphic DNA (RAPD) analysis. All C. indologenes isolates showed multiple resistance to at least 9 out of 16 antibiotics tested. Lowest resistance rates were found for piperacillin (9.7 %) and ciprofloxacin (24.4 %), whereas only piperacillin/tazobactam and trimethoprim/sulfamethoxazole showed 100 % activity. More than half of isolates carried bla IND-type gene, including 2 isolates carrying bla IND-2 and 21 carrying bla IND-7, that was identified as a major MBL genotype in isolates from Adriatic Sea. RAPD typing of IND-producing isolates revealed 6 major groups with no predominant clone in population. The presence of multidrug resistant and IND-producing C. indologenes in marine environment, including marine fauna, pose a risk for transmitting this opportunistic pathogen to humans through recreation or consummation of seafood. In addition, the antibiotic susceptibility test results have practical relevance for empirical treatment of C. indologenes infections.
Similar content being viewed by others
References
Bayraktar MR, Aktas E, Ersoy Y, Cicek A, Durmaz R (2007) Postoperative Chryseobacterium indologenes bloodstream infection caused by contamination of distillate water. Infect Control Hosp Epidemiol 28:368–369
Bellais S, Leotard S, Poirel L, Naas T, Nordmann P (1999) Molecular characterization of a carbapenem-hydrolyzing beta-lactamase from Chryseobacterium (Flavobacterium) indologenes. FEMS Microbiol Lett 171:127–132
Bellais S, Poirel L, Leotard S, Naas T, Nordmann P (2000) Genetic diversity of carbapenem-hydrolyzing metallo-beta-lactamases from Chryseobacterium (Flavobacterium) indologenes. Antimicrob Agents Chemother 44:3028–3034
Bernardet J-F, Vancanneyt M, Matte-Tailliez O, Grisez L, Tailliez P, Bizet C, Nowakowski M, Kerouault B, Swings J (2005) Polyphasic study of Chryseobacterium strains isolated from diseased aquatic animals. Syst Appl Microbiol 28:640–660
Bogomolni AL, Gast RJ, Ellis JC, Dennett M, Pugliares KR, Lentell BJ, Moore MJ (2008) Victims or vectors: a survey of marine vertebrate zoonoses from coastal waters of the Northwest Atlantic. Dis Aquat Org 81:13–38
Chen F-L, Wang G-C, Teng S-O, Ou T-Y, Yu F-L, Lee W-S (2012) Clinical and epidemiological features of Chryseobacterium indologenes infections: analysis of 215 cases. J Microbiol Immunol Infect. doi:10.1016/j.jmii.2012.08.007
Chou D-W, Wu S-L, Lee C-T, Tai F-T, Yu W-L (2011) Clinical characteristics, antimicrobial susceptibilities, and outcomes of patients with Chryseobacterium indologenes bacteremia in an intensive care unit. Jpn J Infect Dis 64:520–524
Clinical and Laboratory Standards Institute (2010) Performance standards for antimicrobial susceptibility testing. Approved standard M100-S20. CLSI, Wayne, PA, USA
DePaola A, Jones JL, Woods J, Burkhardt W 3rd, Calci KR, Krantz JA, Bowers JC, Kasturi K, Byars RH, Jacobs E, Williams-Hill D, Nabe K (2010) Bacterial and viral pathogens in live oysters: 2007 United States market survey. Appl Environ Microbiol 76:2754–2768
Du Moulin GC (1979) Airway colonization by Flavobacterium in an intensive care unit. J Clin Microbiol 10:155–160
Ellington MJ, Kistler J, Livermore DM, Woodford N (2007) Multiplex PCR for rapid detection of genes encoding acquired metallo-β-lactamases. J Antimicrob Chemother 59:321–322
Hsueh PR, Teng LJ, Yang PC, Ho SW, Hsieh WC, Luh KT (1997) Increased incidence of nosocomial Chryseobacterium indologenes infections in Taiwan. Eur J Clin Microbiol Infect Dis 16:568–574
Kirby JT, Sader HS, Walsh TR, Jones RN (2004) Antimicrobial susceptibility and epidemiology of a worldwide collection of Chryseobacterium spp report from the SENTRY Antimicrobial Surveillance Program (1997–2001). J Clin Microbiol 42:445–448
Lin X-H, Xu Y-H, Cheng J, Li T, Wang Z-X (2008) Heterogeneity of bla IND metallo-β-lactamase-producing Chryseobacterium indologenes isolates detected in Hefei, China. Int J Antimicrob Agents 32:398–400
Lin Y-T, Jeng Y-Y, Lin M-L, Yu K-W, Wang F-D, Liu C-Y (2010) Clinical and microbiological characteristics of Chryseobacterium indologenes bacteremia. J Microbiol Immunol Infect 43:498–505
Maravić A, Skočibušić M, Šamanić I, Puizina J (2012) Antibiotic susceptibility profiles and first report of TEM extended-spectrum β-lactamase in Pseudomonas fluorescens from coastal waters of the Kaštela Bay, Croatia. World J Microbiol Biotechnol 28:2039–2045
Matyar F, Kaya A, Dinçer S (2008) Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey. Sci Total Environ 407:279–285
Ottaviani D, Santarelli S, Bacchiocchi S, Masini L, Ghittino C, Bacchiocchi I (2005) Presence of pathogenic Vibrio parahaemolyticus strains in mussels from the Adriatic Sea, Italy. Food Microbiol 22:585–590
Perilli M, Caporale B, Celenza G, Pellegrini C, Docquier JD, Mezzatesta M, Rossolini GM, Stefani S, Amicosante G (2007) Identification and characterization of a new metallo-β-lactamase, IND-5, from a clinical isolate of Chryseobacterium indologenes. Antimicrob Agents Chemother 51:2988–2990
Pitout JDD, Gregson DB, Poirel L, McClure J-A, Le P, Church DL (2005) Detection of Pseudomonas aeruginosa producing metallo-β-lactamases in a large centralized laboratory. J Clin Microbiol 43:3129–3135
Reynaud I, Chanteperdrix V, Broux C, Pavese P, Croizé J, Maurin M, Stahl JP, Jacquot C (2007) A severe form of Chryseobacterium indologenes pneumonia in an immunocompetent patient. Med Mal Infect 37:762–764
Rose JM, Gast RJ, Bogomolni A, Ellis JC, Lentell BJ, Touhey K, Moore M (2009) Occurrence and patterns of antibiotic resistance in vertebrates off the Northeastern United States coast. FEMS Microbiol Ecol 67:421–431
Sader HS, Jones RN (2005) Antimicrobial susceptibility of uncommonly isolated non-enteric Gram-negative bacilli. Int J Antimicrob Agents 25:95–109
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Laboratory Press, New York
Smith J, Han R, Mailman T, MacDonald N (2012) Chryseobacterium indologenes: distinguishing pathogen from contaminant in a neonate. Pediatr Infect Dis J 7:31–35
Uyaguar M, Key P, Moore J, Jackson K, Scott G (2009) Acute effects of the antibiotic oxytetracycline on the bacterial community of the grass shrimp, Palaemonetes pugio. Environ Toxicol Chem 28:2715–2724
Yabuuchi E, Hashimoto Y, Ezaki T, Ido Y, Takeuchi N (1990) Genotypic and phenotypic differentiation of Flavobacterium indologenes Yabuuchi et al. 1983 from Flavobacterium gleum Holmes et al. 1984. Microbiol Immunol 34:73–76
Zamora L, Fernández-Garayzábal JF, Palacio MA, Sánchez-Porro C, Svensson-Stadler LA, Domínguez L, Moore ERB, Ventosa A, Vela AL (2012) Chryseobacterium oncorhynchi sp. nov., isolated from rainbow trout (Oncorhynchus mykiss). Syst Appl Microbiol 35:24–29
Zeba B, De Luca F, Dubus A, Delmarcelle M, Simporé J, Nacoulma OG, Rossolini GM, Frère J-M, Docquier J-D (2009) IND-6, a highly divergent IND-type metallo-beta-lactamase from Chryseobacterium indologenes strain 597 isolated in Burkina Faso. Antimicrob Agents Chemother 53:4320–4326
Acknowledgments
This work was supported by Ministry of Science, Education and Sports, Republic of Croatia, project “Faecal indicator and potential pathogens in coastal and marine waters“, Grant 177-0000000-3182 and project “Mechanisms of maintenance genome stability in higher plants”, Grant 177-1191196-0829.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Maravić, A., Skočibušić, M., Šamanić, I. et al. Profile and multidrug resistance determinants of Chryseobacterium indologenes from seawater and marine fauna. World J Microbiol Biotechnol 29, 515–522 (2013). https://doi.org/10.1007/s11274-012-1205-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-012-1205-0