Table 2 Summary of clinically relevant characteristics of the microorganisms covered in this work

Acinetobacter spp.

Originally presumed to be of little pathogenicity, Acinetobacter has emerged as a troublesome etiological agent of hospital-acquired infections worldwide. This strictly aerobic Gram-negative coccobacillus is able to accumulate diverse mechanisms of resistance leading to phenotypes resistant to most commercially available antibiotics. The mechanisms implicated in Acintetobacter spp. resistance include (1) decreased expression of bacterial porins, hindering the passage of beta-lactams into the periplasmic space (where they can attach to penicillin-binding proteins); (2) over-expression of bacterial efflux pumps, causing decreased concentration of beta-lactams (as well as quinolones and other antibiotics) in the periplasmic space; (3) mutations in gyrA and parC genes causing resistance to fluoroquinolones; (4) expression of aminoglycoside-modifying enzymes leading to resistance to this class of antibiotics; (5) chromosomally encoded inducible AmpC beta-lactamases conferring resistance to cephalosporins. Finally, Acinetobacter spp. acquired (plasmid-mediated) serine- and metallo-beta-lactamases confer resistance to carbapenems [23, 32].

Nosocomial UTIs are less frequent (most common Acinetobacter-related infection being ventilator-associated pneumonia) and are commonly diagnosed in elderly patients in ICU’s, mostly men with indwelling catheters [23]. Acinetobacter survives for long periods on wet and dry surfaces and several studies have documented extensive contamination of the environment in the vicinity of colonised patients: bed linen, bed curtains, sink traps and hospital floor [23].

Citrobacter spp.

Citrobacter, Enterobacter and Serratia are facultative anaerobic non-spore forming Gram-negative rods sometimes referred to as “CES” group and described together, due to the traits they share: (1) their biochemical characteristics; (2) prevalence and resistance patterns (observation corroborated by our data); (3) various intrinsic and acquired resistance mechanisms; and (4) the fact of being frequently associated with complicated UTIs, disease recurrence and prolonged treatment. Because of their AmpC beta-lactamase production, some authors group them with Pseudomonas spp. and indole-positive Proteus spp. to complete so-called “SPICE” group [33].

Citrobacter spp. is also one of the microorganisms implicated in the “purple urine bag syndrome”, a conspicuous phenomenon of dubious clinical significance [34].

Enterobacter spp.

The genus Enterobacter comprises of 22 species and is considered an opportunistic pathogen. While its pathogenicity and virulence remain rather unclear, its resistance mechanisms have been extensively studied. The production of beta-lactamase is a major mechanism of resistance to beta-lactams; E. aerogenes expresses AmpC beta-lactamase (cephalosporinase) that confers resistance to 1st generation cephalosporins but is inducible during treatment with a 3rd generation cephalosporin, leading again to resistance. Aminoglycoside-modifying enzymes are responsible for resistance to aminoglycosides and a mutation in one of their genetic determinants (aac-6′-Ib) leads to a fluoroquinolone-resistant phenotype. A change in porin expression in the presence of imipenem leads to a decreased penetration of beta-lactams into E. aerogenes and bacterial efflux pumps remove fluoroquinolones and tetracyclines from Enterobacter spp. isolates [35]. Enterobacter is an opportunistic nosocomial pathogen: in a report from Taiwan, E. cloacae hospital outbreak has been described, attributale to a contaminated ureteroscope [36].

Serratia spp.

Originally presumed a non-pathogenic microorganism and even used a tracer in medical experiments, Serratia has established itself as an accepted clinical pathogen with widely prevalent multi-antibiotic resistant strains [37]. In urology wards, nosocomial outbreaks of S. liquefaciens and S. marcescens have been described related to cystometry appliance and urine bottles, respectively [37, 38]. Indeed, urine-measurement containers, urinometers, urine-collecting basins and urinals as well as cystoscopy suite have been found to be reservoirs of S. marcescens [37].

Morganella spp. and Providencia spp.

Morganella and Providencia are sometimes (together with Proteus) grouped under the tribe Proteae. Originally not considered frank pathogens, they have emerged as importang causative agents of hospital-acquired infections in different organ systems [39]. Their common characteristics include (1) strong urease production; (2) frequent association with complicated UTIs, prolonged treatment and disease recurrence; (3) intrinsic resistance to nitrofurantoin and colistin (as confirmed by our data) and to tetracycline; (4) intrinsically decreased susceptibility to imipenem (not observed on our data); and (5) production of various beta-lactamases including AmpC [26].

Providencia frequently colonizes indwelling catheters; in a case-series (n = 14) of Providencia bacteraemia, UTI was identified as the source in 36% of cases and 71% of patients had an indwelling urinary catheter [40].

M. morganii, P. stuartii and P. rettgeri are among the causative microorganisms of the purple-urine bag syndrome (see above).

S. maltophilia

S. maltophilia intrinsic resistance mechanisms (low membrane permeability, chromosomally encoded multidrug resistance efflux pumps, beta-lactamases, antibiotic-modifying enzymes etc.) were suggested to have been acquired in non-human natural environments and not being due solely to clinical use of antibiotics. Its survival is facilitated by wet surfaces and aqueous solutions with minimal nutrients (e.g. drinking water, treated water, dialysate effluent) [24].