Multidrug-resistant (MDR) Aeromonas recovered from the metropolitan area of Valencia (Spain): diseases spectrum and prevalence in the environment



Aeromonas infections are rare in Europe and often related to traveller’s diarrhoea. A total of 185 Aeromonas isolates from river water, fish and clinical sources, recovered during a 1-year period, were used to investigate the disease spectrum and impact of multidrug-resistant (MDR) strains. They were all identified by biochemical tests and 25 % of them were also identified by sequencing of the 16S rRNA gene. The minimum inhibitory concentrations (MICs) of 21 antimicrobials were determined for all isolates by broth microdilution/E-strips methods, and susceptibility was assessed according to the Clinical and Laboratory Standards Institute (CLSI). Strains pathogenicity was determined by using Swiss Webster mice as the animal model. Aeromonas diseases had an incidence of around 20 cases/million inhabitants in the metropolitan area of Valencia (Spain). Acute gastroenteritis in children with no history of travel abroad was the main pathology. These cases were related to A. caviae, A. veronii biovar sobria, A. hydrophila and A. dhakensis. A significant incidence of A. caviae in humans was found, while the other species were equally present in clinical and environmental origins. A. jandaei, A. bestiarum and A. media had mainly an environmental distribution. The prevalence of MDR Aeromonas was maximal in clinical samples, and resistance phenotypes were significantly related to this source. 7.2 % of environmental Aeromonas was resistant to at least five drugs; most of them were moderately virulent for mice and, in addition, belonged to clinically significant species. The present study demonstrates a diseases spectrum similar to that reported in tropical countries, and also that pathogenic and heavily MDR Aeromonas are present in environmental reservoirs. MDR Aeromonas from any source analysed were susceptible to aztreonam, netilmicin, cefotaxime, ceftazidime, cefepime and fluoroquinolones.

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  1. 1.
    Abbott SL, Cheung WKW, Janda JM (2003) The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J Clin Microbiol 41:2348–2357CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Alavandi SV, Ananthan S (2003) Biochemical characteristics, serogroups, and virulence factors of Aeromonas species isolated from cases of diarrhoea and domestic water samples in Chennai. Indian J Med Microbiol 21:233–238PubMedGoogle Scholar
  4. 4.
    Aravena-Román M, Inglis TJJ, Henderson B, Riley TV, Chang BJ (2012) Antimicrobial susceptibilities of Aeromonas strains isolated from clinical and environmental sources to 26 antimicrobial agents. Antimicrob Agents Chemother 56:1110–1112CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Blasco MD, Esteve C, Alcaide E (2008) Multiresistant waterborne pathogens isolated from water reservoirs and cooling systems. J Appl Microbiol 105:469–475CrossRefPubMedGoogle Scholar
  6. 6.
    Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P (2008) Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp. Emerg Infect Dis 14:231–237CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261CrossRefPubMedGoogle Scholar
  8. 8.
    Clinical and Laboratory Standards Institute (CLSI) (2006) Performance standards for antimicrobial susceptibility testing, 16th informational supplement document M2-A9 and M7-A7. CLSI, Wayne, PAGoogle Scholar
  9. 9.
    Das A, Saha D, Pal J (2009) Antimicrobial resistance and in vitro gene transfer in bacteria isolated from the ulcers of EUS-affected fish in India. Lett Appl Microbiol 49:497–502CrossRefPubMedGoogle Scholar
  10. 10.
    Davies J (2007) Microbes have the last word. A drastic re-evaluation of antimicrobial treatment is needed to overcome the threat of antibiotic-resistant bacteria. EMBO Rep 8:616–621CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Esteve C, Valera L, Gutiérrez C, Ventosa A (2003) Taxonomic study of sucrose-positive Aeromonas jandaei-like isolates from faeces, water and eels: emendation of A. jandaei Carnahan et al. 1992. Int J Syst Evol Microbiol 53:1411–1419CrossRefPubMedGoogle Scholar
  12. 12.
    Esteve C, Alcaide E (2009) Influence of diseases on the wild eel stock: the case of Albufera Lake. Aquaculture 289:143–149CrossRefGoogle Scholar
  13. 13.
    Esteve C, Alcaide E, Blasco MD (2012) Aeromonas hydrophila subsp. dhakensis isolated from feces, water and fish in Mediterranean Spain. Microbes Environ 27:367–373CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Filler G, Ehrich JHH, Strauch E, Beutin L (2000) Acute renal failure in an infant associated with cytotoxic Aeromonas sobria isolated from patient’s stool and from aquarium water as suspected source of infection. J Clin Microbiol 38:469–470PubMedPubMedCentralGoogle Scholar
  15. 15.
    González-Barca E, Ardanuy C, Carratalá J, Sanchez A, Fernández-Sevilla A, Grañena A (1997) Fatal myofascial necrosis due to imipenem-resistant Aeromonas hydrophila. Scand J Infect Dis 29:91–92CrossRefPubMedGoogle Scholar
  16. 16.
    Goñi-Urriza M, Capdepuy M, Arpin C, Raymond N, Caumette P, Quentin C (2000) Impact of an urban effluent on antibiotic resistance of riverine Enterobacteriaceae and Aeromonas spp. Appl Environ Microbiol 66:125–132CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Goñi-Urriza M, Pineau L, Capdepuy M, Roques C, Caumette P, Quentin C (2000) Antimicrobial resistance of mesophilic Aeromonas spp. isolated from two European rivers. J Antimicrob Chemother 46:297–301CrossRefPubMedGoogle Scholar
  18. 18.
    Gordon L, Giraud E, Ganière JP, Armand F, Bouju-Albert A, De la Cotte N, Mangion C, Le Bris H (2007) Antimicrobial resistance survey in a river receiving effluents from freshwater fish farms. J Appl Microbiol 102:1167–1175PubMedGoogle Scholar
  19. 19.
    Havelaar AH, Schets FM, van Silfhout A, Jansen WH, Wieten G, van der Kooij D (1992) Typing of Aeromonas strains from patients with diarrhoea and from drinking water. J Appl Bacteriol 72:435–444CrossRefPubMedGoogle Scholar
  20. 20.
    Huddleston JR, Zak JC, Jeter RM (2006) Antimicrobial susceptibilities of Aeromonas spp. isolated from environmental sources. Appl Environ Microbiol 72:7036–7042CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Janda JM, Kokka RP (1991) The pathogenicity of Aeromonas strains relative to genospecies and phenospecies identification. FEMS Microbiol Lett 90:29–33CrossRefGoogle Scholar
  22. 22.
    Khajanchi BK, Fadl AA, Borchardt MA, Berg RL, Horneman AJ, Stemper ME, Joseph SW, Moyer NP, Sha J, Chopra AK (2010) Distribution of virulence factors and molecular fingerprinting of Aeromonas species isolates from water and clinical samples: suggestive evidence of water-to-human transmission. Appl Environ Microbiol 76:2313–2325CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Lamy B, Kodjo A; colBVH Study Group, Laurent F (2009) Prospective nationwide study of Aeromonas infections in France. J Clin Microbiol 47:1234–1237CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Liu CY, Huang YT, Liao CH, Hsueh PR (2008) In vitro activities of tigecycline against clinical isolates of Aeromonas, Vibrio, and Salmonella species in Taiwan. Antimicrob Agents Chemother 52:2677–2679CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Long SS, Pickering LK, Prober CG (2012) Principles and practice of pediatric infectious diseases. Elsevier Saunders, St. LouisGoogle Scholar
  26. 26.
    Manjano-Mendoza A, Bravo-Fariñas L, Fernández-Abreu A, Martínez-Motas I, Núñez F, Mederos-Cuervo LM, Ramírez-Álvarez M, Castro-Escarpulli G (2009) Caracterización fenotípica de bacilos gramnegativos anaerobios facultativos oxidasa positiva, aislados de pacientes con enfermedad diarreica aguda en Cuba. Rev Biomed 20:25–32Google Scholar
  27. 27.
    Martínez-Murcía AJ, Benlloch S, Collins MD (1992) Phylogenetic interrelationships of members of the genera Aeromonas and Plesiomonas as determined by 16S ribosomal DNA sequencing: lack of congruence with results of DNA–DNA hybridizations. Int J Syst Bacteriol 42:412–421CrossRefPubMedGoogle Scholar
  28. 28.
    Martínez-Murcía AJ, Soler L, Saavedra MJ, Chacón MR, Guarro J, Stackebrandt E, Figueras MJ (2005) Phenotypic, genotypic, and phylogenetic discrepancies to differentiate Aeromonas salmonicida from Aeromonas bestiarum. Int Microbiol 8:259–269PubMedGoogle Scholar
  29. 29.
    Morita K, Watanabe N, Kurata S, Kanamori M (1994) β-lactam resistance of motile Aeromonas isolates from clinical and environmental sources. Antimicrob Agents Chemother 38:353–355CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Ørmen Ø, Granum PE, Lassen J, Figueras MJ (2005) Lack of agreement between biochemical and genetic identification of Aeromonas spp. APMIS 113:203–207CrossRefPubMedGoogle Scholar
  31. 31.
    Picão RC, Poirel L, Demarta A, Petrini O, Corvaglia AR, Nordmann P (2008) Expanded-spectrum beta-lactamase PER-1 in an environmental Aeromonas media isolate from Switzerland. Antimicrob Agents Chemother 52:3461–3462CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Puthucheary SD, Puah SM, Chua KH (2012) Molecular characterization of clinical isolates of Aeromonas species from Malaysia. PLoS One 7(2):e30205. doi:10.1371/journal.pone.0030205 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Quevauviller P, Barceló D, Beniston M, Djordjevic S, Harding RJ, Iglesias A, Ludwig R, Navarra A, Navarro Ortega A, Mark O, Roson R, Sempere D, Stoffel M, van Lanen HAJ, Werner M (2012) Integration of research advances in modelling and monitoring in support of WFD river basin management planning in the context of climate change. Sci Total Environ 440:167–177CrossRefPubMedGoogle Scholar
  34. 34.
    Reed LJ, Müench M (1938) A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493–497Google Scholar
  35. 35.
    Sánchez-Céspedes J, Figueras MJ, Aspiroz C, Aldea MJ, Toledo M, Alperí A, Marco F, Vila J (2009) Development of imipenem resistance in an Aeromonas veronii biovar sobria clinical isolate recovered from a patient with cholangitis. J Med Microbiol 58:451–455CrossRefPubMedGoogle Scholar
  36. 36.
    Sinha S, Shimada T, Ramamurthy T, Bhattacharya SK, Yamasaki S, Takeda Y, Nair GB (2004) Prevalence, serotype distribution, antibiotic susceptibility and genetic profiles of mesophilic Aeromonas species isolated from hospitalized diarrhoeal cases in Kolkata, India. J Med Microbiol 53:527–534CrossRefPubMedGoogle Scholar
  37. 37.
    Sugita H, Tanaka K, Yoshinami M, Deguchi Y (1995) Distribution of Aeromonas species in the intestinal tracts of river fish. Appl Environ Microbiol 61:4128–4130PubMedPubMedCentralGoogle Scholar
  38. 38.
    Thayumanavan T, Vivekanandhan G, Savithamani K, Subashkumar R, Lakshmanaperumalsamy P (2003) Incidence of haemolysin-positive and drug-resistant Aeromonas hydrophila in freshly caught finfish and prawn collected from major commercial fishes of coastal South India. FEMS Immun Med Microbiol 36:41–45CrossRefGoogle Scholar
  39. 39.
    Tomás JM (2012) The main Aeromonas pathogenic factors. ISRN Microbiology. Article ID 256261, 22 pages. doi:10.5402/2012/256261
  40. 40.
    Valera L, Esteve C (2002) Phenotypic study by numerical taxonomy of strains belonging to the genus Aeromonas. J Appl Microbiol 93:77–95CrossRefPubMedGoogle Scholar
  41. 41.
    van den Bogaard AE, Stobberingh EE (2000) Epidemiology of resistance to antibiotics. Links between animals and humans. Int J Antimicrob Agents 14:327–335CrossRefPubMedGoogle Scholar
  42. 42.
    Vila J, Marco F, Soler L, Chacón M, Figueras MJ (2002) In vitro antimicrobial susceptibility of clinical isolates of Aeromonas caviae, Aeromonas hydrophila and Aeromonas veronii biotype sobria. J Antimicrob Chemother 49:701–702CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Departamento de Microbiología y EcologíaUniversitat de ValènciaBurjassot, ValenciaIndia
  2. 2.Servicio de MicrobiologíaHospital Universitario la FeValenciaIndia

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