Skip to main content
Download PDF

Temporal trends and risks factors for antimicrobial resistant Enterobacteriaceae urinary isolates from outpatients in Guadeloupe

BMC Microbiology volume 16, Article number: 121 (2016) Cite this article

Abstract

Background

Urinary tract infections are bacterial infections most commonly encountered in the community. The resistance rate of uropathogens to commonly prescribed antibiotics has increased worldwide but there are no published data concerning the resistance of strains isolated from community-acquired UTI in Guadeloupe. To assess the susceptibility patterns of Enterobacteriaceae strains isolated from outpatients in Guadeloupe we conducted a prospective study from December 2012 to May 2014 among outpatients consulting at private and public laboratories for urine analysis. Risk factors for E. coli resistance to amoxicillin, third-generation cephalosporin, and ciprofloxacin were also determined. To study the trends of E. coli resistance rates over the past 10 years, data on the susceptibility patterns of E. coli from 2003 to 2014 were also collected from three major laboratories for a retrospective study.

Results

During the prospective study, we isolated 1293 bacterial strains from the urine of outpatients presenting for urine analysis. The most commonly isolated bacteria were E. coli (57 %) and Klebsiella pneumoniae (15.5 %). Thirty seven per cent of the E. coli strains were resistant to amoxicillin. Resistance rates to third generation cephalosporin were low for E. coli and other Enterobacteriaceae (3.1 and 12.2 % respectively) and mostly due to the presence of an Extended Spectrum Beta-lactamase. Resistance to cotrimoxazole and ciprofloxacin was moderate (17.8 and 15.6 % respectively). However, the resistance rate of E. coli to ciprofloxacin has significantly increased during the last 10 years. Risk factors were consistent with previously reported data, especially for the increasing ciprofloxacin resistance with age.

Conclusion

General practitioners in Guadeloupe need to be better informed to favor the prescription of fosfomycin-trometamol to reduce the risk of resistance to fluoroquinolones.

Background

Urinary tract infections (UTI) are bacterial infections most commonly encountered in the community, regardless of age. UTIs are usually benign and the infection (cystitis, prostatitis, urethritis) is limited to the lower urinary tract requires a simple antibiotic treatment. However, recurrences are common and may evolve into an upper UTI (pyelonephritis) requiring a heavier antibiotic treatment and more extensive management [1].

Enterobacteriaceae, especially Escherichia coli, are the most prevalent uropathogens in patients with UTI, both in the community and hospitals [2]. In most cases, the treatment of uncomplicated UTIs is empirical. The French Language Infectious Disease Society (SPFIL) recommends using a single dose of fosfomycin-trometamol in combination for the first line treatment of UTI and pivmecillinam for second line therapy. Beta-lactams, quinolones or cotrimoxazole should be administered after susceptibility testing since strains resistant to these antibiotics are frequently isolated. Indeed, multi drug resistant strains are emerging, especially strains harboring Extended Spectrum Betalactamases (ESBL). ESBL enzymes can hydrolyze almost all beta-lactams (except for carbapenems and cephamycins) and their genes are often closely linked to other genes that confer resistance to several other classes of antibiotics. During the past decade, CTX-M enzymes have gradually replaced the classical TEM and SHV-type ESBLs in many countries. The rapid international spread of CTX-M-15 has been associated with the global dissemination of particular E. coli clones, such as sequence type 131 [3].

The resistance rate of uropathogens to commonly prescribed antibiotics has increased worldwide: resistance to quinolones and trimethoprim increased in Europe between the ECO-SENS I (1999–2000) and ECO-SENS II (2007–2008) studies and in Africa (Senegal, Central African Republic) between 2003 and 2006, reducing therapeutic options [4–7].

Guadeloupe, a French overseas territory located in the Caribbean, is a very high resource country according to the Human Development Index in 2013. There are no published data concerning the resistance of strains isolated from community-onset UTI in Guadeloupe and data from the Caribbean more generally are rare. We, therefore, conducted a prospective study, from December 2012 to May 2014, to assess the susceptibility patterns of Enterobacteriaceae strains isolated from outpatients and to determine the risk factors for UTIs due to Enterobacteriaceae resistant to commonly used antimicrobial agents. We also studied the genetic basis for the antibiotic resistance of ESBL-producing Enterobacteriaceae. Finally, to determine the recent trends of resistance to antibiotics, we conducted a retrospective study on the antibiotic resistance of E. coli isolated from outpatients during the last 10 years.

Methods

Patients

We collected 1293 bacterial strains isolated from the urine of outpatients presenting for a urine analysis from 13 of the 23 private Guadeloupian laboratories and the laboratory of the Hospital of Basse-Terre between December 2012 and May 2014. All strains responsible for lower and upper UTI and bacteriuria according to SPFIL criteria (pyuria ≥104 leucocyte/mL and bacteriuria ≥103 for E. coli or S. saprophyticus and ≥104 for other species) [8] were included in the study. Only one specimen was collected from each patient. The leucocyte count, isolation, identification and antibiotic susceptibility testing of bacteria were conducted by all laboratories according to their routine diagnostic procedures. All Enterobacteriaceae strains were sent to the Pasteur Institute of Guadeloupe for complete antibiotic susceptibility testing.

The study protocols were approved by the French Advisory Committee on Information Processing in Material Research in the Field of Health (CCTIRS 12–220). Written informed consent to participate in the study was obtained from all patients.

Antibiotic susceptibility testing of Enterobacteriaceae at the Pasteur Institute of Guadeloupe

We assessed the susceptibility to the following antibiotics by the disk diffusion technique on Mueller-Hinton agar (MH) as recommended by the Antibiogram Committee of the French Microbiology Society (ACFMS) [9]: amoxicillin (10 μg), amoxicillin-clavulanic acid (20 μg/10 μg), ticarcillin (75 μg), cephalothin (30 μg), cefotaxime (30 μg), ceftazidime (30 μg), cefoxitin (30 μg), aztreonam (30 μg), imipenem (10 μg) gentamicin (15 μg), amikacin (30 μg), trimethoprim/sulfamethoxazole (1,25/23,75 μg), nalidixic acid (30 μg), ciprofloxacin (5 μg), fosfomycin (50 μg), nitrofurantoin (300 μg) and tetracycline (30 UI).. Inhibition growth diameters were measured using the Adagio automated system (Bio-Rad, France). Intermediate and resistant strains were grouped together and classified as resistant strains. Extended spectrum beta-lactamases were detected for strains with reduced inhibition growth diameters around cefotaxime, ceftazidime or aztreonam by the combined disk method with the following combinations: cefotaxime (30 μg) and ceftazidime (30 μg); cefotaxime (30 μg) and clavulanate (10 μg); and ceftazidime (30 μg) and clavulanate (10 μg).

The minimum inhibitory concentration (MIC) for cefotaxime and ceftazidime were determined using the agar-dilution method as recommended by the ACFMS for ESBL-carrying strains [9]. The cut-off values used for classification were: susceptible strains were defined as those having a MIC <8 mg/L for cefotaxime, and a MIC ≤4 mg/L for ceftazidime; and resistant strains as those having a MIC ≥32 mg/L for cefotaxime and a MIC ≥8 mg/L for ceftazidime. E. coli ATCC 25922 was used as a control stain.

Molecular characterization of ESBL-producing strains

DNA was extracted using the Nucleospin tissue kit (Macherey Nagel, Hoerdt, France). Previously described polymerase chain reaction (PCR) methods were used to screen for plasmid-encoded bla CTX-M, bla tem and bla SHV genes [10–12]. Both bla CTX-M, bla SHV and bla TEM were then characterized by Direct DNA sequencing of the PCR products.

The nucleotide and deduced amino acid sequences were analyzed and compared with sequences available through the Internet on the National Center for Bio-technology Information web site (http://www.ncbi.nlm.nih.gov).

Epidemiological data

A standardized specific questionnaire was completed to collect demographic data. Risk factors for E. coli resistance to amoxicillin, third-generation cephalosporin (3GC) and ciprofloxacin were assessed from questions about: age, gender, chronic illness, hospitalization during the last year, UTI during the previous last 3 months, urinary catheterization during the previous year, antibiotic exposure during the last month, and hospital or family hospital occupation.

Evolution of antibiotic resistance in E. coli from 2003

To analyze the trends of resistance to antibiotics during the last 10 years, data were collected on the resistance of E. coli strains isolated from community-acquired UTIs in outpatients presenting at the emergency units of the hospitals of Basse-Terre and Pointe à Pitre and at the Pasteur Institute of Guadeloupe between 2003 and 2014. These data were added to that collected during the prospective study for 2013 and 2014.

Data analysis

Statistical analysis was performed using R software (reference: R Development Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2010. Available: http://www.R-project.org/).

We used logistic regression to estimate the relation between resistance to each antibiotic and the various covariates (age, gender, clinical symptoms). All covariates with a p value lower than 0.20 were included in the multivariable model. Multivariable, backward, step-by-step binomial negative regressions were used to take into account confounders, bias, and interactions linked to the dependent variable.

To compare annual resistance rates, we performed Poisson regression and chi2 tests. Statistical differences were considered significant for p-values <0.05.

Results

Patients

We collected a total of 1293 strains during the study period. Most (73.5 %) were isolated from women (sex ratio 0.34). The median age of patients was 57.4 years (range 0 to 95 years). Sixteen patients carried significant numbers of two different strains. We obtained epidemiological data for 340 patients; pregnant women accounted for 10.6 % of women interviewed, and 69 % of patients had UTI symptoms.

Bacterial strains and antibiotic susceptibility

More than 86 % of the isolates were Enterobacteriaceae: 736 E. coli (57.0 %), 202 Klebsiella pneumoniae (15.5 %), 56 Proteus mirabilis (4.3 %), 54 Enterobacter spp. (4.2 %), 38 Citrobacter koseri (2.9 %), and 35 other Enterobacteriaceae (2.7 %). Other Gram-negative bacteria (Pseudomonas spp. and Acinetobacter spp.) accounted for 0.6 % of the isolates. Among the isolates, 170 were Gram-positive bacteria (13.1 %): Streptococcus agalactiae (4.3 %), Enterococcus faecalis (4.2 %), and Staphylococcus saprophyticus (2.3 %).

Many of the E. coli isolates were susceptible to numerous drugs, but 42.1 % of the strains were resistant to amoxicillin and ticarcillin.

A small proportion of strains were not susceptible to 3GC (3.1 % E. coli and 12.2 % other Enterobacteriaceae; Table 1). Most 3GC-resistant strains had a MIC greater than 64 mg/L for cefotaxim and ceftazidime (85 and 67.5 %, respectively). This resistance was mostly due to the presence of an ESBL (n = 39, 85 %): 24 K. pneumoniae, 11 E. coli, 3 Enterobacter spp. and one M. morganii.

Table 1 Susceptibility of outpatients Enterobacteriaceae urinary isolates to various antimicrobial agents
Full size table

Resistance to cotrimoxazole and ciprofloxacin was 17.8 and 15.6 %, respectively.

Resistance rates to fosfomycin and nitrofurantoin were low among E. coli strains (1.6 and 1.2 % respectively). These rates were higher for other Enterobacteriaceae: 17.9 % for fosfomycin and 32.6 % for nitrofurantoin.

Only a small proportion of Enterobacteriaceae strains were resistant to gentamicin (6.4 %) and amikacin (0.5 %) (Table 1). Only one strain (Morganella morganii) was resistant to imipenem.

Most 3GC-resistant strains had at least one co-acquired resistance: 85 % were resistant to ciprofloxacin, 67.5 % to cotrimoxazole and 52.5 % to gentamicin (Table 2).

Table 2 Characteristics of the ESBLEa
Full size table

Determinants of antibiotic resistance in 3GC-R Enterobacteriaceae strains

The 39 ESBL producing strains are described in Table 2. Among them 38 expressed a CTX-M enzyme including 29 CTX-M15 and 7 CTX-M1. Additional β lactamases were found in most of strains (87.5 %).

Risk factors for E. coli resistance to amoxicillin, third-generation cephalosporin and ciprofloxacin

Strains isolated from male patients had a significantly higher amoxicillin resistance rate than those isolated from female patients (p = 0.04). The ciprofloxacin resistance rate tended to increase with increasing age (p < 0.01) (Table 3).

Table 3 Analysis of independent risk factors for E. coli resistance to amoxicillin, trimethoprim/sulfamethoxazole and ciprofloxacin
Full size table

Among 286 patients with an Enterobacteriaceae, 68 (23.7 %) declared to have received antibiotic treatment during the previous month and 72 (25.2 %) to have had a UTI during the three previous months. More Enterobacteriaceae strains isolated from patients who declared a UTI during the three previous months were resistant to amoxicillin (p = 0.02) and ciprofloxacin (p < 0.01) than those isolated from patients without a UTI during the three previous months. Moreover, urinary catheterization was associated with higher resistance rates for amoxicillin and cotrimoxazole (p < 0.01) (Table 3).

Evolution of antibiotic resistance in E. coli from 2003

Resistance rates for amoxicillin, cotrimoxazole and amikacin have been stable during the last 10 years. On the contrary, we found a significant (p < 0.01) increase in the reported resistance to nalidixic acid, ciprofloxacin, cefalotin, and gentamycin (Table 4). The increase in the 3GC resistance rate was not significant as assessed by the Poisson regression test but was significant as evaluated by the Chi2 test. Until 2008, fewer than 1.0 % of E. coli strains were resistant to 3GC, but this proportion increased significantly between 2008 and 2009 (p < 0.01) and has been stable during the last 5 years (Table 4).

Table 4 Trends of resistance rates to various antimicrobial agents of E. coli between 2003 and 2014
Full size table

Discussion

As expected, E. coli was the most frequent strain isolated from urines in Guadeloupe (57.0 % of isolates), but nevertheless less frequent than in Europe and Canada (range from 61.0 to 87.5 %) [13–18]. K. pneumoniae was the second most frequent pathogen (15.5 %), even in pre-menopausal women, with a rate similar to those reported in Africa and Asia (ranging from 13.8 to 25.5 %) [6, 19–22]. S. agalactiae was the most frequent Gram-positive bacteria (4.3 %), whereas generally reported rates are less than 3 %. The differences in relative prevalence may be due to environmental and/or host genetic factors, or the virulence of the bacterial pathogens. Of note, the prevalence of diabetes is high (8.2 %) in Guadeloupe [23] and UTIs due to K. pneumoniae and S. agalactiae have been reported to be two to three times more frequent among patients with diabetes than those without [24].

As previously described, S. saprophyticus was isolated more frequently from women under 35 years of age than men or older women [25].

Overall, resistance rates were similar to those observed in developed countries including mainland France. Indeed, we found an amoxicillin-resistance rate of 42.1 % for E. coli, similar to the rate of 43.4 % reported for North America [26] and slightly lower than the rate of 48.3 % reported for Europe [27] . This contrasts with the reported situation in African and developing Asian countries where resistance rates may be as high as 80 % [6, 7, 28, 29].

Moreover, resistance to 3GC was low, and although this rate increased significantly between 2008 and 2009, it remains below 4 % for E. coli strains and 7 % for all Enterobacteriaceae. Guadeloupe should be considered to be a low prevalence ESBL-producing Enterobacteriaceae territory as are the European and North American countries [5, 15, 27, 30]. In our study, bla CTX-M15 was detected in most of the ESBL-producing strains (74.3 %), highlighting the shift during the 2000s from ESBL bla TEM/bla SHV to ESBL group 1 bla CTX-M, and in particular to bla CTX-M15. This is in accordance with other epidemiological studies of ESBL-producing Enterobacteriaceae [31]. Most ESBL-producing strains (97.5 %) were resistant to other antibiotics in keeping with the ARESC and ECO-SENS II studies [5, 27]. Surprisingly, most ESBL-producing strains isolated in our study were K. pneumoniae, whereas in the community, E. coli strains with CTX-M enzymes usually predominate [32] because of the spread of clonal multidrug-resistant E. coli strains such as clone O25b-ST131 [33]. The prevalence of K. pneumoniae in our study can be explained not only by the high proportion of K. pneumoniae strains among uropathogens, but also by the spread of successful clones as described in Africa and Asia [34].

We did not isolate any carbapenemase-producing strains, although these strains have been observed in the community, even in low prevalence countries such as England [15] where their presence is often related to travel in Asia where these strains are endemic [35]. In Guadeloupe, Enterobacteriaceae carbapenemase-producing strains have just begun to emerge in hospital settings with the first description of an NDM-1-producing K. pneumoniae in 2014 [36], and more recently, of an OXA-48-producing E. coli [37].

Ciprofloxacin resistance remains moderate (15.6 %) compared to rates observed in Asia which can be as high as 75 % [19]. Nevertheless, we found that this rate has increased significantly during the last 10 years as described for other countries [6, 15, 26, 38]. Although we were not able to obtain retrospective data on fluoroquinolone consumption in Guadeloupe, increasing rates of ciprofloxacin-resistant strains suggest the inappropriate use of fluroquinolones in outpatients. Among the 48 patients reporting antibiotic consumption during the month prior to the infection, 15 had consumed a fluoroquinolone and among 24 patients that also reported a previous UTI, 12 received a fluoroquinolones whereas only one was given fosfomycin. Indeed, ciprofloxacin resistance in E. coli has been linked with ciprofloxacin consumption in the same month as the infection and the month before [39]. The rate of ciprofloxacin resistance tended to increase with age as has been described for mainland France and Canada [16, 40] Antimicrobial susceptibility testing of uropathogens is known to overestimate rates of resistance because antibiograms are performed mostly if empirical treatment fails, or if patients have underlying factors [41]. Nevertheless, the trends remain valid.

Consistent with previous reports [28, 42] we observed that prior UTI (likely to be associated with prior antibiotic treatment) was associated with higher amoxicillin and ciprofloxacin resistance rates. This suggests the abusive use of these antibiotics for the treatment of community acquired infections. Surprisingly, a previous antibiotic treatment was not associated with such a risk. Since the use of antibiotics for which the resistance rate exceeds 10–20 % is associated with an increased risk of treatment failure and the selection of resistant strains [43], ciprofloxacin should be administered only if compatible with the antimicrobial resistance pattern of the strain.

Conclusions

Although a few patients may have been infected by hospital-acquired strains, this is the first description of susceptibility patterns of urinary bacterial strains isolated from outpatients in Guadeloupe.

The antibiotic resistance rates among urinary bacteria isolates from outpatients in Guadeloupe are similar to those of North America and Europe. Nevertheless, this study highlights the need for general practitioners in Guadeloupe to be better informed so that they are encouraged to prescribe fosfomycin-trometamol for the treatment of UTI to reduce the risk of increasing resistance rates to fluoroquinolones.

Abbreviations

UTI, urinary tract infection; SPFIL, The French Language Infectious Disease Society; ESBL, Extended Spectrum beta lactamase; MIC, minimum inhibitory concentration; PCR, polymerase chain reaction; 3GC, third generation cephalosporin

References

  1. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13:269–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bishop MC. Uncomplicated Urinary Tract Infection. EAU Updat Ser. 2004;2:143–50.

    Article  Google Scholar 

  3. Rogers BA, Sidjabat HE, Paterson DL. Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother. 2011;66:1–14.

    Article  CAS  PubMed  Google Scholar 

  4. Kahlmeter G, Menday P. Cross-resistance and associated resistance in 2478 Escherichia coli isolates from the Pan-European ECO.SENS Project surveying the antimicrobial susceptibility of pathogens from uncomplicated urinary tract infections. J Antimicrob Chemother. 2003;52:128–31.

    Article  CAS  PubMed  Google Scholar 

  5. Kahlmeter G, Poulsen HO. Antimicrobial susceptibility of Escherichia coli from community-acquired urinary tract infections in Europe: The ECO SENS study revisited. Int J Antimicrob Agents. 2012;39:45–51.

    Article  CAS  PubMed  Google Scholar 

  6. Bercion R, Mossoro-Kpinde D, Manirakiza A, Le Faou A. Increasing prevalence of antimicrobial resistance among Enterobacteriaceae uropathogens in Bangui, Central African Republic. J Infect Dev Ctries. 2009;3:187–90.

    Article  PubMed  Google Scholar 

  7. Sire JM, et al. Antimicrobial resistance in outpatient Escherichia coli urinary isolates in Dakar, Senegal. J Infect Dev Ctries. 2007;1:263–8.

    CAS  PubMed  Google Scholar 

  8. SPILF 2014 Mise au point Diagnostic et Antibiothérapie des infections Urinaires Bactériennes Communautaires de l’Adulte. Splif. 2014. http://www.infectiologie.com/UserFiles/File/medias/Recos/2014-infections_urinaires-long.pdf.

  9. CA-SFM. Comite de l’Antibiogramme de la Societe Francaise de Microbiologie: Recommandations. 2013. Edition de janvier 2013.

    Google Scholar 

  10. Saladin M, et al. Diversity of CTX-M beta-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol Lett. 2002;209:161–8.

    CAS  PubMed  Google Scholar 

  11. Arlet G. Rouveau, M. & Philippon, a. Substitution of alanine for aspartate at position 179 in the SHV-6 extended-spectrum beta-lactamase. FEMS Microbiol Lett. 1997;152:163–7.

    Article  CAS  PubMed  Google Scholar 

  12. Eckert C, et al. Dissemination of CTX-M-Type β -Lactamases among Clinical Isolates of Enterobacteriaceae in Paris, France. Antimicrob Agents Chemother. 2004;48:1249–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hryniewicz K, et al. Antibiotic susceptibility of bacterial strains isolated from urinary tract infections in Poland. J Antimicrob Chemother. 2001;47:773–80.

    Article  CAS  PubMed  Google Scholar 

  14. Bruyère F, Vidoni M, Péan Y, Ruimy JA, Elfassi R. Analyse microbiologique de plus de 600 infections urinaires fébriles prises en charge dans un réseau de soin. Progrès en Urol. 2013;23:890–8.

    Article  Google Scholar 

  15. Ironmonger D, et al. Surveillance of antibiotic susceptibility of urinary tract pathogens for a population of 5.6 million over 4 years. J Antimicrob Chemother. 2015;70:1744–50.

    CAS  PubMed  Google Scholar 

  16. Laupland KB, Ross T, Pitout JDD, Church DL, Gregson DB. Community-onset urinary tract infections: A population-based assessment. Infection. 2007;35:150–3.

    Article  CAS  PubMed  Google Scholar 

  17. Magliano E, et al. Gender and age-dependent etiology of community-acquired urinary tract infections. ScientificWorldJournal. 2012;2012:349597.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Maraki S, Mantadakis E, Michailidis L, Samonis G. Changing antibiotic susceptibilities of community-acquired uropathogens in Greece, 2005–2010. J Microbiol Immunol Infect. 2013;46:202–9.

    Article  PubMed  Google Scholar 

  19. Lu PL, et al. Epidemiology and antimicrobial susceptibility profiles of Gram-negative bacteria causing urinary tract infections in the Asia-Pacific region: 2009–2010 results from the Study for Monitoring Antimicrobial Resistance Trends (SMART). Int J Antimicrob Agents. 2012;40:S37–43.

    Article  CAS  PubMed  Google Scholar 

  20. Hanley J, Branford I, Gugnan HC, Wilkinson C. U. T. urinary bacterial pathognes in St. Kitts.pdf. West Indies Med J. 2009;58:670.

    Google Scholar 

  21. Kothari A, Sagar V. Antibiotic resistance in pathogens causing community-acquired urinary tract infections in India: a multicenter study. J Infect Dev Ctries. 2008;2:354–8.

    Article  PubMed  Google Scholar 

  22. Akoachere J-FTK, Yvonne S, Akum NH, Seraphine EN. Etiologic profile and antimicrobial susceptibility of community-acquired urinary tract infection in two Cameroonian towns. BMC Res Notes. 2012;5:219.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Fosse-Edorh S. Journée modiale du diabète. Beh. 2014;30–31:491–529.

  24. Ronald A. The etiology of urinary tract infection: Traditional and emerging pathogens. Dis Mon. 2003;49:71–82.

    Article  PubMed  Google Scholar 

  25. Raz R, Colodner R, Kunin CM. Who are you - Staphylococcus saprophyticus? Clin Infect Dis. 2005;40:896–8.

    Article  PubMed  Google Scholar 

  26. Sanchez GV, Master RN, Karlowsky JA, Bordon JM. In vitro antimicrobial resistance of urinary Escherichia coli isolates among U.S. outpatients from 2000 to 2010. Antimicrob Agents Chemother. 2012;56:2181–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Schito GC, et al. The ARESC study: an international survey on the antimicrobial resistance of pathogens involved in uncomplicated urinary tract infections. Int J Antimicrob Agents. 2009;34:407–13.

    Article  CAS  PubMed  Google Scholar 

  28. Randrianirina F, et al. Antimicrobial resistance among uropathogens that cause community-acquired urinary tract infections in Antananarivo, Madagascar. J Antimicrob Chemother. 2007;59:309–12.

    Article  CAS  PubMed  Google Scholar 

  29. Ma KL, Wang CX. Analysis of the spectrum and antibiotic resistance of uropathogens in vitro: Results based on a retrospective study from a tertiary hospital. Am J Infect Control. 2013;41:601–6.

    Article  PubMed  Google Scholar 

  30. Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JDD. Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel. J Infect. 2008;57:441–8.

    Article  PubMed  Google Scholar 

  31. Arpin C, et al. Nationwide survey of extended-spectrum {beta}-lactamase-producing Enterobacteriaceae in the French community setting. J Antimicrob Chemother. 2009;63:1205–14.

    Article  CAS  PubMed  Google Scholar 

  32. Pitout JDD, Laupland KB. Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis. 2008;8:159–66.

    Article  CAS  PubMed  Google Scholar 

  33. Smith SP, Manges AR, Riley LW. Temporal changes in the prevalence of community-acquired antimicrobial-resistant urinary tract infection affected by Escherichia coli clonal group composition. Clin Infect Dis. 2008;46:689–95.

    Article  CAS  PubMed  Google Scholar 

  34. Breurec S, et al. Klebsiella pneumoniae resistant to third-generation cephalosporins in five African and two Vietnamese major towns: Multiclonal population structure with two major international clonal groups, CG15 and CG258. Clin Microbiol Infect. 2013;19:349–55.

    Article  CAS  PubMed  Google Scholar 

  35. Kumarasamy KK, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study. Lancet Infect Dis. 2010;10:597–602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bastian S, et al. First case of NDM-1 producing Klebsiella pneumoniae in Caribbean islands. Int J Infect Dis. 2015;34:e53–4.

    Article  Google Scholar 

  37. Breurec S, et al. Emergence of OXA-48-producing Escherichia coli in the Caribbean islands. J Glob Antimicrob Resist. 2015;3:217–8.

    Article  Google Scholar 

  38. Andrade SS, et al. Increased resistance to first-line agents among bacterial pathogens isolated from urinary tract infections in Latin America: Time for local guidelines? Mem Inst Oswaldo Cruz. 2006;101:741–8.

    CAS  PubMed  Google Scholar 

  39. Vernaz N, et al. Modelling the impact of antibiotic use on antibiotic-resistant Escherichia coli using population-based data from a large hospital and its surrounding community. J Antimicrob Chemother. 2011;66:928–35.

    Article  CAS  PubMed  Google Scholar 

  40. Grignon O, et al. Escherichia coli antibiotic resistance in emergency departments. Do local resistance rates matter? Eur J Clin Microbiol Infect Dis. 2014;34:571–7.

    Article  PubMed  Google Scholar 

  41. Heginbothom ML, et al. Laboratory testing policies and their effects on routine surveillance of community antimicrobial resistance. J Antimicrob Chemother. 2004;53:1010–7.

    Article  CAS  PubMed  Google Scholar 

  42. Dromigny JA, Nabeth P, Juergens-Behr A, Perrier-Gros-Claude JD. Risk factors for antibiotic-resistant Escherichia coli isolated from community-acquired urinary tract infections in Dakar, Senegal. J Antimicrob Chemother. 2005;56:236–9.

    Article  CAS  PubMed  Google Scholar 

  43. Dalhoff A. Global fluoroquinolone resistance epidemiology and implictions for clinical use. Interdiscip Perspect Infect Dis. 2012;2012:976273.

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all study participants.

The laboratory working group includes: Clément Bourgoin1, Farid Saheb1, Guy-Joseph Theodore1, Emmanuelle Bourgoin1, Frédéric Leroy1, William Laurent1, Arnaud Lethuillier1, Patricia Tamby1, Petra Kassab1, Anne-Christine Becker1, Pierre Marie1, Sandrine Hippomène2, Olivier Menuteau2, Marie-Line Péan2, Sylvaine Bastian3, Edith Malpote3, Didier Mattera4

1Laboratoire Biopole Antilles

2Laboratoire Synergibio

3Laboratoire de Microbiologie, Centre Hospitalo-Universitaire, Les Abymes

4Laboratoire de Biologie Clinique, Centre Hospitalier de Basse-Terre, Basse-Terre, Guadeloupe

Funding

This work was financed by grants from the Institut Pasteur International Network, ACIP A13_2011 and by grant FEDER FED-1-1.4 32932 from the European Union.

Availability of data and materials

Data supporting the findings is contained within the manuscript.

Author’s contributions

SG designed the study, analyzed data and wrote the manuscript, JM, CD and SS collected bacterial strains and epidemiological data, performed antimicrobial susceptibility testing and molecular characterization of ESBL-producing strains, MF performed molecular characterization of ESBL-producing strains, DH collected bacterial strains, epidemiological data and retrospective data on the resistance of E. coli strains and critically revised the manuscript, VR performed data analysis and critically revised the manuscript, ChD designed the study and critically revised the manuscript, SB collected retrospective data on the resistance of E. coli strains and critically revised the manuscript, AT designed the study and critically revised the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

The study protocols were approved by the French Advisory Committee on Information Processing in Material Research in the Field of Health (CCTIRS 12–220). Written informed consent to participate in the study was obtained from all patients.

Author information

Authors and Affiliations

  1. Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France

    Stéphanie Guyomard-Rabenirina, Joyce Malespine, Célia Ducat, Syndia Sadikalay, Mélanie Falord, Sébastien Breurec & Antoine Talarmin

  2. Laboratoire de Biologie Clinique, Centre Hospitalier de Basse-Terre, Basse-Terre, Guadeloupe, France

    Dorothée Harrois

  3. Faculté de Médecine, Université des Antilles, Pointe-à-Pitre, Guadeloupe, France

    Sébastien Breurec

  4. Laboratoire de Microbiologie Clinique et Environnementale, Centre Hospitalo-Universitaire de Pointe-à-Pitre/Abymes, Pointe-à-Pitre, Guadeloupe, France

    Sébastien Breurec

  5. Institut Pasteur de Nouvelle-Calédonie, Nouméa, Nouvelle-Calédonie, France

    Vincent Richard

  6. Institut Armand Frappier, Laval, Canada

    Charles Dozois

Authors
  1. Stéphanie Guyomard-Rabenirina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joyce Malespine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Célia Ducat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Syndia Sadikalay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mélanie Falord
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dorothée Harrois
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vincent Richard
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Charles Dozois
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sébastien Breurec
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Antoine Talarmin
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

The Laboratory working group

  • Clément Bourgoin
  • , Farid Saheb
  • , Guy-Joseph Theodore
  • , Emmanuelle Bourgoin
  • , Frédéric Leroy
  • , William Laurent
  • , Arnaud Lethuillier
  • , Patricia Tamby
  • , Petra Kassab
  • , Anne-Christine Becker
  • , Pierre Marie
  • , Sandrine Hippomène
  • , Olivier Menuteau
  • , Marie-Line Péan
  • , Sylvaine Bastian
  • , Edith Malpote
  •  & Didier Mattera

Corresponding author

Correspondence to Stéphanie Guyomard-Rabenirina.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guyomard-Rabenirina, S., Malespine, J., Ducat, C. et al. Temporal trends and risks factors for antimicrobial resistant Enterobacteriaceae urinary isolates from outpatients in Guadeloupe. BMC Microbiol 16, 121 (2016). https://doi.org/10.1186/s12866-016-0749-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12866-016-0749-9

Keywords

BMC Microbiology

ISSN: 1471-2180

Contact us