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Susceptibility testing of extended-spectrum-[beta]-lactamase (ESBL)-producing enterobacteriaceae against oral antimicrobials, including fosfomycin and mecillinam.

Introduction

New Zealand is a country with relatively low rates of resistant clinical pathogens (1,2). However over the last decade there has been a dramatic increase in the isolation rate of extended spectrum [beta]-lactamase (ESBL)-producing Enterobacteriaceae (3,4). At Canterbury Health Laboratories (CHL) in 2004 there were only 5 patients with ESBL-producing Enterobacteriaceae isolated, and all strains were E.coli. By 2012 the number of patients with ESBL-producing Enterobacteriaceae had climbed to nearly 200 patients, with eleven different species identified. This number had already been eclipsed in the first 8 months of 2013. Of most concern is the increasing prevalence of ESBL-producing Escherichia coli, causing urinary tract infections (UTIs) in community based patients: a trend which has been recognised globally (5-7).

ESBL-producing Enterobacteriaceae, particularly E.coli with CTX-M-15 type ESBLs, often associated with sequence type 131 (ST131), tend to be co-resistant to several antibiotic classes in addition to the expanded spectrum p-lactam antibiotics (8,9). The most recent study by the Institute of Environmental Science and Research showed a predominance of CTX-M-15 in New Zealand (10). Limited treatment options for these multi-resistant isolates have forced the use of carbapenems, particularly for serious infections, often resulting in the emergence of carbapenemase producing isolates--at an alarming rate in some countries (11). Patients in primary care, especially those with uncomplicated infections such as simple cystitis, could benefit from the availability of an effective oral agent, rather than costly and inconvenient IV administered antibiotics. In turn, the health system would benefit from reduced hospital admissions and other associated health costs.

Fosfomycin and mecillinam have been used extensively for the treatment of UTIs, mainly in Scandinavia and Europe, for decades while resistance rates remain low (12). Neither drug is currently licensed or funded in New Zealand. Fosfomycin tromethamine is the soluble salt form of fosfomycin, suitable for oral administration. High concentrations of fosfomycin are achieved in the urine as the drug is excreted unchanged. Bactericidal action is achieved by interference of peptidoglycan biosynthesis: an early stage of bacterial cell wall development (13). Fosfomycin has broad spectrum activity against a range of Gram positive and Gram negative organisms, although it not as useful against Pseudomonas aeruginosa and Acinetobacter baumanii (14). Although fosfomycin is only approved for the treatment of uncomplicated acute cystitis against susceptible strains of E.coli and Enterococcus faecalis, recent reviews have found it to be a viable option for the treatment of infections from a variety of body sites (15,16). Fosfomycin di-sodium salt is the parenteral version.

Pivmecillinam is the prodrug which releases the active agent mecillinam when absorbed. After oral administration mecillinam is rapidly absorbed, achieving peak plasma concentrations after 1 hour. In addition, much of the drug is excreted unchanged in the urine within the first 6 hours. Mecillinam is a [beta]-lactam which uniquely binds to Gram negative penicillin binding protein 2 (PBP-2), resulting in cell wall distortion, lysis and cell death (17). The main indication of use for mecillinam has also been for the treatment of acute uncomplicated cystitis.

The aim of this study was to gather local data on the in-vitro susceptibilities of ESBL-producing Enterobacteriaceae from our institution, against two potentially useful oral antibiotics: fosfomycin and mecillinam, and to compare the results with other routinely tested oral agents.

Methods and materials

Patient population

The Canterbury District Health Board (CDHB) oversees publicly funded health services to a wide geographical area, with a population in excess of 500,000. The largest of its fourteen hospitals is Christchurch Hospital, a 650 bed tertiary, teaching and research hospital. Canterbury Health Laboratories (CHL) provides laboratory testing services to the CDHB, private medical centres and national referring laboratories. During the study period the Bacteriology Department provided an integrated processing service for all community urine samples received by MedLab South Ltd (who were sharing CHL facilities following the destruction of their own laboratory in the 22 February 2011 earthquake).

Bacterial isolates

ESBL-producing Enterobacteriaceae isolates were collected at CHL from July to December 2011 and stored at -80[degrees]C in PROTECT cryopreservative fluid. Fosfomycin and mecillinam susceptibilities were retrospectively performed on non duplicate patient isolates. During the study period a total of 173 ESBL-producing isolates, from 112 patients, representing 3.45% of all Enterobacteriaceae tested, were processed for identification and susceptibility testing using BD Phoenix[TM] (Phoenix) Automated Microbiology System (Becton Dickinson Diagnostic Systems, Australia). Results were stored on BD EpiCenter software database V6.10A. Identification of isolates other than E.coli, Klebsiella oxytoca or Klebsiella pneumoniae was confirmed with Bruker MALDI-TOF, using Biotyper FlexControl 3.0 software (Science Directions Limited, New Zealand). A total of 109 non duplicate isolates, from 102 patients were available for inclusion in the study. The isolates consisted of E.coli 78 (71.6%), Klebsiella pneumoniae 21 (19.3%), Klebsiella oxytoca 2 (1.8%), Enterobacter cloacae 3 (1.8%), Citrobacter farmeri 2 (1.8%), Citrobacter brakaii 1 (0.9%), Rauoltella ornitholytica 1 (0.9%), and Serratia fonticola 1 (0.9%).

Antimicrobial susceptibility testing

Routine susceptibility testing was performed with BD Phoenix, using either NMIC/ID-75 (448087) or NMIC/ID-95 (448783) combo panels. Interpretation criteria for susceptibility results were applied using the Clinical and Laboratory Standards Institute (CLSI) guidelines and Phoenix BDXpert rules (18).

Phoenix panels were controlled with E.coli ATCC 25922, E.coli ATCC 35218 and Pseudomonas aeruginosa ATCC 27853. Susceptibility testing for fosfomycin and mecillinam was performed by disk diffusion using CLSI guidelines. Zone interpretations were expanded to include all bacterial species tested. Fosfomycin disks (200[micro]g) containing 50[micro]g of glucose-6-phosphate and mecillinam (10 [micro]g) were used (Oxoid, ThermoFisher NZ). Disks were controlled with E.coli ATCC 25922. For the purposes of this study, any intermediate susceptibility result was considered as resistant. ESBL production was confirmed by a modification of the double disk synergy test of Jarlier (1988), incorporating ceftriaxone, aztreonam, ceftazidime and cefepime around a central augmentin disk (19).

Results

A total of 109 non duplicate isolates, from 102 patients were included in this study. The patients consisted of 73 (71.6%) female and 29 (28.4%) male patients, and ranged in age from 6 weeks to 100 years old, with the median being 65.5 years. The majority of isolates were recovered from urine [88 (80.7%)], with a further 13 (11.9%) from wound swabs, 4 (3.7%) from blood culture and 4 (3.7%) from screening swabs. Two of the patients with septicaemia also had a concurrent UTI and a third patient was attending urology clinics. The differences in patient demographics most likely reflect the well recognised higher prevalence rates of UTIs in elderly women. Seventy four (72.5%) patients were community based with only 28 (27.5%) classified as hospitalised. Patients were considered to be community based if the sample was taken at a community health care service, from an outpatient clinic, from the emergency department, or the patient had been admitted for less than 48 hours. However, it was noted that many of the patients had previous hospital admissions in the preceding 3-6 months, so a hospital acquired infection could not be completely ruled out.

The percent susceptible results for all oral antimicrobials tested are summarised in Table 1. Parenteral antibiotics gentamicin and meropenem are also listed for comparison purposes. Fosfomycin and mecillinam were the most effective oral antimicrobials in-vitro, compared to other oral agents tested. The susceptibility of fosfomycin against all isolates tested was 96.3%, with E.coli showing the highest susceptibility rate of 98.7% and 19/21 (90.5%) K.pneumoniae isolates susceptible. Mecillinam also performed well, with 99/109 (90.8%) of all isolates classified as susceptible and it was particularly effective against 74/78 (94.9%) E.coli and 20/21 (95.2%) K.pneumoniae. Nitrofurantoin was active against 72/78 (92.3%) E.coli but had diminished susceptibility against the other isolates tested.

The remaining oral agents: augmentin, ciprofloxacin,

trimethoprim, and trimethoprim/sulphamethoxazole, performed poorly against the isolates tested, with overall susceptibilities ranging from as little as 22.9% for trimethoprim to 33.9% for ciprofloxacin. ESBL-carrying plasmids often contain other resistance mechanisms, making the isolates more likely to be multi-resistant, particularly to quinolones such as norfloxacin and ciprofloxacin. This co-resistance was demonstrated in our study by the low level of susceptibility to ciprofloxacin by both E.coli and K.pneumoniae (29.5% and 28.6% respectively). Furthermore, isolates that were resistant to ciprofloxacin were also more likely to be resistant to other antimicrobials including aminoglycosides. Results are summarised in Table 2.

Of the parenterally administered antimicrobials, gentamicin, a common empirical choice in a patient with suspected urosepsis, was only active in 50.5% of the isolates studied, but all isolates were susceptible to meropenem.

Discussion

Urinary tract infections are one of the most common bacterial infections in both hospital and community settings, with E.coli remaining the most predominant uropathogen. It is a concerning trend that ESBL-producing E.coli strains have gained such a foothold, especially in community acquired infections. Many UTIs can progress to serious illnesses including bacteraemia: in which there is a recognised higher mortality rate for patients who have multidrug resistant isolates coupled with a delay in receiving appropriate antibiotic therapy (20-22). In this study the predominant organism/source group was E.coli isolated from urine. While there were only four isolates recovered from blood culture during the study period, three of the four patients had either a concurrent UTI or urology comorbidity, and we have seen an increasing prevalence of patients infected with ESBL-producing E.coli septicaemia over the last 12 months at our institution (data not shown).

Enterobacteriaceae are spread by hand carriage, contaminated food and water. Risk factors for acquisition of ESBL-producing Enterobacteriaceae include previous exposure to antibiotics, previous health care intervention or resident of a long term care facility, or urinary catheter use (22,23). In New Zealand, Freeman et al. found that travel to the Indian subcontinent was a risk factor for community-onset UTI (24). A recent study in Sweden showed a high rate of faecal flora colonisation with ESBL-producing Enterobacteriaceae following international travel (25). Destinations of highest risk included the Indian subcontinent and Asia, with travellers being unlucky enough to suffer a gastrointestinal illness and those aged s65 years being the most vulnerable.

In this study we have found both fosfomycin and mecillinam to have a high in-vitro activity against a range of ESBL-producing Enterobacteriaceae, especially against E.coli. These results are similar to those found in other studies (13,26-28). A recent study in Turkey of 52 patients with UTI showed a successful clinical response at follow up in 49 patients, after 3 doses of fosfomycin (29). Notably many of these patients had complicated infections. Of some concern is the study by Oteo et al. that showed increasing fosfomycin resistance, possibly due to a resurgence of fosfomycin use in the community setting (30). It is also possible, however, that the spike in fosfomycin resistance was aligned with a local clonal spread of CTX-M-15-producing E.coli ST131. A multicenter evaluation in Japan of 192 CTX-M-producing E.coli found some transferable fosfomycin resistance enzymes co-existing on the CTX-M enzyme plasmid, indicating that dual transmission could occur. However, fosfomycin has been used for many years in Japan, and the overall activity of fosfomycin was 96.4% (26). Resistance to fosfomycin was recently extensively reviewed by Karageorgopoulos et al. (31). They concluded that fosfomycin appeared to be a reliable agent for the treatment of UTIs, due to high levels of drug excreted into urine, together with an acidic urine environment and low level of biological fitness of fosfomycin-resistant mutants. They cautioned against its use as a sole agent in serious infections and against organisms other than E.coli.

Although mecillinam has performed well in in-vitro studies against ESBL-producing Enterobacteriaceae, authors have warned against its use as mono therapy due to the apparent effect of high bacterial inoculum, and hence high concentrations of [beta]-lactamase production, which increases the MIC level of mecillinam (32,33). Thomas et al. and Brenwald et al. both suggest that mecillinam would be more effective if given in combination with a p-lactam inhibitor such as clavulanate. Similarly, in a more recent study from Greece, mecillinam was found to be highly active in-vitro against 47 of 48 (97.9%) ESBL -producing E.coli uropathogens, with the authors also suggesting the administration of a p-lactam inhibitor in combination with mecillinam for more effective treatment (34).

On a side note, we have also found fosfomycin to be a useful agent against Enterococcus faecalis and some E.faecium. In a separate in-house study, an evaluation of fosfomycin against 100 consecutive Enterococci isolated from urine (consisting of 91 E.faecalis and 9 E.faecium), showed excellent activity of fosfomycin against E.faecalis (97.8% susceptible), but less activity against E.faecium (63.6% susceptible). These organisms can cause UTI in elderly patients, many of whom can have limited treatment options due comorbidities such as renal insufficiency or penicillin allergy, perhaps ruling out the use of nitrofurantoin or ampicillin respectively.

The poor results of other antimicrobials in this study highlighted the limited oral treatment choices against ESBLs. Nitrofurantoin has been used for the treatment of simple cystitis and for prophylaxis for more than 50 years, and it did show high rates of susceptibility against E.coli. However, it was not as effective against K.pneumoniae and is not suitable for the treatment of members of the Proteus/Providencia/Morganella genera. Nitrofurantoin is contraindicated in patients with renal failure which can be common in elderly patients; and its longer dosing regimen may have implications for patient noncompliance. The poor performance of ciprofloxacin, trimethoprim and trimethoprim/sulphamethoxazole do not make these antibiotics a preferred choice, especially not for empirical treatment in patients with high risk factors of ESBL infections.

Although susceptibility against parenteral meropenem was 100%, it would seem prudent to conserve the use of carbapenems to selective cases only, or to limit their use to an initial 24 hour empirical treatment, changing to an oral agent once the results of laboratory susceptibility testing are known.

Further investigation on our study isolates could include the analysis of ESBL enzyme type, phylogenic group or sequence type, to determine any clonal relationship or association with multidrug resistance in our population.

Conclusions

With the prevalence rate of ESBL-producing

Enterobacteriaceae continuing to climb, there is a need to seek suitable alternative treatment options to carbapenems and other IV administered drugs. This need is especially acute for the treatment of community based patients and goes hand-in-hand with the desire to preserve the use of carbapenems where ever possible. The results of this study has shown that fosfomycin and mecillinam were highly active agents in-vitro against ESBL-producing Enterobacteriaceae in our population and may be considered as useful oral options, either for treatment or empirical use, particularly in high risk patients with community acquired UTIs. Laboratories need to be vigilant in their screening for ESBL-producing pathogens and could consider the addition of fosfomycin and mecillinam testing to their extended antibiotic panel.

Acknowledgments

Grateful thanks to Sandra Hainsworth and Mirjam Horsburgh (formerly MedLab South employees) for performing much of the disk diffusion testing on the study isolates.

References

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Author information

Julie Creighton, DipMLT, Senior Medical Laboratory Scientist [1] and Clinical Lecturer [2]

[1] Canterbury Health Laboratories, PO Box 151, Christchurch and

[2] University of Otago, Christchurch, New Zealand Email: julie.creighton@cdhb.health.nz
Table 1. Susceptibility results of ESBL-producing strains
to fosfomycin, mecillinam and other oral agents

Organism        No.        % susceptible
                isolates

                           FOS    MEC    AUG    NIT    CIP

E.coli          78         98.7   94.9   38.5   92.3   29.5
K. pneumoniae   21         90.5   95.2   19.1   14.3   28.6
Others (a)      10         90     50     10     50     80
TOTAL           109        96.3   90.8   32.1   73.4   33.9

Organism        No.
                isolates

                           TRM    SXT    GN     MER

E.coli          78         28.2   32.1   57.7   100
K. pneumoniae   21         14.3   14.3   33.3   100
Others (a)      10         40     40     30     100
TOTAL           109        22.9   29.4   50.5   100

(a) = K.oxytoca (2), E.cloacae (3), C.farmeri (2), C.
braakii (1), Raoultella ornithinotytica (1), and
Serratia fonticola (1)

FOS=fosfomycin, MEC=mecillinam, AUG=augmentin,
NIT=nitrofurantoin, CIP=ciprofloxacin, TRM=trimethoprim,
SXT=sulphamethoxazole/trimethoprim,
GN=gentamicin, MER=meropenem

Table 2. Percent of resistance to other antimicrobials as
determined by ciprofloxacin resistance

                            No.        % resistant
                            isolates

                                       GN     TOB    TRM    SXT

Ciprofloxacin resistant     72         59.5   64.3   78.3   81.1
Ciprofloxacin susceptible   37         40.5   40.0   65.2   56.8

GN=gentamicin, TOB=tobramycin,
TRM=trimethoprim, SXT=sulphamethoxazole/trimethoprim
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Date:Apr 1, 2014
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