Motile aeromonads from farmed and wild freshwater fish in northern Italy: an evaluation of antimicrobial activity and multidrug resistance during 2013 and 2016

Abstract

Background: Antimicrobial resistant bacteria are emerging biological contaminants of the environment. In aquatic ecosystems, they originate mainly from hospitals, livestock manure and private households sewage water, which could contain antimicrobial agents and resistant microorganisms. Aeromonas spp. occur ubiquitously in aquatic environments and they cause disease in fish. Motile aeromonads are also associated with human gastrointestinal and wound infections and fish can act as a transmission route of antimicrobial resistance (AMR) aeromonads to humans. The environmental ubiquity, the natural susceptibility to antimicrobials and the zoonotic potential of Aeromonas spp. make them optimal candidates for studying the AMR in aquatic ecosystems. Results: The AMR patterns of 95 motile aeromonads isolated from freshwater fish during 2013 and 2016 were analyzed. All samples from fish came from farms and natural water bodies located in northern Italy, which is an area characterized by high anthropic impact on the environment. The isolates were biochemically identified as Aeromonas hydrophila, Aeromonas sobria or Aeromonas caviae and AMR was determined by the standard disk diffusion method. All isolates were resistant to cloxacillin, spiramycin and tilmicosin. High AMR frequencies (> 95%) were detected for tylosin, penicillin and sulfadiazine. AMR to danofloxacin, enrofloxacin, flumequine, ceftiofur, aminosidine, colistin, doxycycline, gentamicin, marbocyl and florfenicol was observed at low levels (< 10%). No AMR to cefquinome was found. Logistic regression showed several differences in antimicrobial activity between complexes. According to the source of aeromonads, only few differences in AMR between isolates from farmed and wild fish were observed. Conclusions: Our data revealed an increasing trend of AMR to neomycin and apramycin among Aeromonas isolates during the study period, while resistance to erythromycin, tetracycline and thiamphenicol decreased. All isolates were multidrug resistance (MDR), but A. caviae showed the highest number of MDR per isolate. In most isolates, various degrees of MDR were detected to macrolides, quinolones, fluoroquinolones, polymyxins and cephalosporins (third and fourth generations), which are listed, by the World Health Organisation, to be among the highest priority and critically important antimicrobials in human medicine. Our findings underlined that freshwater fish can act as potential source of MDR motile aeromonads. Due to their zoonotic potential, this can pose serious threat to human health.

The microbial safety of fish and fish products: Recent advances in understanding its significance, contamination sources, and control strategies

“…Aerom onas hydrophila strains are commonly resistant to ampicillin, tetracycline, and streptomycin. A 100% resistance rate to ampicillin in all A. hydrophila isolates has been reported repeatedly (Borella et al., 2020; Castro‐Escarpulli et al., 2003; Dahdouh et al., 2016; Guz & Kozinska, 2004; Radu et al., 2003; Wang & Silva, 1999; Wu et al., 2019). In addition, multidrug‐resistant strains were also detected at high rates in A. hydrophila isolates from fish and fish products.…”

“…In addition, multidrug‐resistant strains were also detected at high rates in A. hydrophila isolates from fish and fish products. In particular, all A. hydrophila isolates recovered from retail fish in Malaysia (Radu et al., 2003), retail frozen fish fillets or farmed fish in Egypt (Dahdouh et al., 2016; Hafez et al., 2018), and farmed and wild freshwater fish in Italy (Borella et al., 2020) were resistant to at least three antibiotics. Multidrug‐resistant A. hydrophila against ampicillin, bacitracin, and tetracycline (tetracycline, oxytetracycline, or chlortetracycline) has also been detected in U.S. domestic catfish fillets (Wang & Silva, 1999).…”

The Role of Aquatic Ecosystems (River Tua, Portugal) as Reservoirs of Multidrug-Resistant Aeromonas spp.

“…To further gain knowledge on the MDR in the aquatic environmental bacteria, 25 out of 30 Aeromonas isolates showed an MDR profile to 19 antibiotics, where 83.33% of the strains were resistant to more than three antibiotic classes, indicating a high level of multi-resistance in the Tua River basin ( Figure 5). Previous studies [18,[60][61][62][63][64] reported β-lactams and quinolone-resistant isolates of Aeromonas spp. recovered from freshwater, fishes, and humans.…”

“…isolated from the Tua River, representing a potential risk to the population since an appreciable part of the population residing in the Tua River Basin still uses fish and river mussels in their daily diet. Foodborne diseases (FD) are a priority in public health issues around the world due to their incidence and mortality [64]. The genus Aeromonas is regarded not only as an important disease-causing pathogen of cold-blooded species but also as the etiologic agent responsible for a variety of infectious complications in both immunocompetent and immunocompromised persons [23].…”

The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA2B2 efflux pump-mediated macrolide resistance

“…However, the widespread use of antibiotics has led to the emergence of antimicrobial resistance in A. hydrophila and bioaccumulation in host tissues, which seriously threatened human and public health. Some strains of A. hydrophila have been found to be resistant to macrolides, tetracyclines, sulfonamides, and quinolones [ 11 , 12 ]. In response to this phenomenon, understanding of resistance mechanisms has become an urgent necessity for development of an effective therapeutic strategy against this pathogen.…”