Journal of Antimicrobial Chemotherapy (2000) 46, 223-228
© 2000 The British Society for Antimicrobial Chemotherapy
Increasing resistance to fluoroquinolones in Escherichia coli from urinary tract infections in The Netherlands
a National Institute of Public Health and the Environment, PO Box 1, 3720 BA Bilthoven and Public Health Laboratories at b Enschede, c Tilburg, d Rotterdam, e Goes and f Nijmegen, The Netherlands
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In continuous surveillance of routine samples from five Dutch laboratories, we studied resistance to the antibiotics most commonly prescribed for urinary tract infections (UTI) in The Netherlands, namely norfloxacin, amoxycillin, trimethoprim and nitrofurantoin, from 1989 to 1998 in >90000 Escherichia coli isolates. Resistance to norfloxacin increased from 1.3% in 1989 to 5.8% in 1998. Multiresistance, defined as resistance to norfloxacin and at least two of the other three antibiotics, increased from 0.5% in 1989 to 4.0% in 1998. Multivariate analysis of the norfloxacin resistance demonstrated that this yearly increase (the odds ratio was 1.0 in 1989, 1.6 in 1992, 2.9 in 1995 and 6.1 in 1998) was independent of other determinants of resistance to norfloxacin, such as age, gender and origin of the isolate. Analysis of strata, classified by year, age and gender, demonstrated an association between prescription of fluoroquinolones (defined daily doses per case of UTI) and resistance to norfloxacin in E. coli (P < 0.001). There was no significant association with the prescription of nitrofuran derivatives (nitrofurantoin) and trimethoprim with or without sulphamethoxazole. The yearly increase of resistance to fluoroquinolones in E. coli from UTI may stem from increased prescription of fluoroquinolones for UTI. Resistance of E. coli to these agents is likely to increase further as fluoroquinolone use increases in future.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Increasing resistance to amoxycillin and trimethoprim in Escherichia coli, the main causative pathogen of urinary tract infections (UTI), has been demonstrated in urinary tract isolates obtained from patients visiting their general practitioners (GPs).1–5 Additionally, findings from routine testing by medical microbiological laboratories indicate growing resistance to several antibiotics in E. coli from urinary tract isolates.3 In The Netherlands, the Dutch College of General Practitioners recommend a 3 day course of trimethoprim or nitrofurantoin for the treatment of UTI.4,6,7 However, in the past few years, fluoroquinolones have been prescribed more frequently for the treatment of such infections. This may have led to an increase in fluoroquinolone-resistant E. coli infections, which are difficult to treat.
In this article we report on the development of resistance to fluoroquinolones in E. coli isolates from UTI in The Netherlands. Data from a sentinel surveillance programme, which collected data on resistance from five laboratories from 1989 to 1998, were combined with data on prescription of fluoroquinolones in the community in order to investigate whether patterns of resistance correlate with trends in the prescription of these antibiotics.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Data sampling and processing
During the study period, 1989–98, five regional public health laboratories in The Netherlands (Rotterdam, Nijmegen, Goes, Tilburg and Enschede) forwarded all routine data on the occurrence of E. coli, including antibiotic susceptibility data, to the National Institute of Public Health and the Environment. These laboratories cover approximately 14% of the Dutch population (15.4 million inhabitants in 1994). They tested >75% of the E. coli isolates for resistance to amoxycillin, trimethoprim, nitrofurantoin and norfloxacin. Only E. coli isolates from urine were included. Repeat isolates of E. coli from the same patient taken within 2 months were ignored. Detailed information on the number of prescriptions and defined daily doses (DDDs) prescribed in the community (including nursing homes and outpatient clinics; excluding inpatient clinics) was obtained for fluoroquinolones, nitrofuran derivatives, trimethoprim and co-trimoxazole (sulphamethoxazole and trimethoprim) from the Drug Information Project of the Supervising Board for Health Care Insurance in The Netherlands, Amstelveen (1992–97). Information on the incidence of UTI was obtained from a sentinel GP surveillance system in the east of The Netherlands (Nijmegen and surroundings).
The incidence of UTI was used to investigate whether there was a link between the number of prescriptions and the incidence of resistance on the basis of groups stratified by age and gender. Data from a sentinel GP surveillance system indicated that the incidence of UTI was lower in younger age groups than in older age groups, resulting in a relatively low prescription rate of antibiotics for treatment of UTI. So, in order to link prescription to resistance directly, the number of prescriptions (DDD/1000 medically insured) was divided by the incidence (UTI/1000 person-years), giving the number of prescriptions per case of UTI (DDD/case UTI).
Laboratory methods
Susceptibility test results were interpreted with reference to breakpoints published by the Dutch Committee on Susceptibility Testing Guidelines.8 The breakpoints for resistance were: 
64 mg/L for amoxycillin and nitrofurantoin, and 16 mg/L for trimethoprim and norfloxacin. Sensitivity testing methods were not standardized.
Statistical methods
Analyses were performed with SAS software, version 6.12 (SAS Institute, Cary, NC, USA). The percentage of norfloxacin-resistant E. coli was univariately compared for independent variables, such as year of isolation, age of patient, source of isolate (laboratory), origin of the patient (general practice, nursing home, inpatient or outpatient clinic). Using multivariate, logistic regression, the relative risks for the dependent variable, resistance to norfloxacin, were estimated for the independent variables.
Because of cross-resistance between norfloxacin and other fluoroquinolones used for therapy of UTI, such as ciprofloxacin and ofloxacin, it is justifiable to compare norfloxacin resistance (as a marker for fluoroquinolone resistance) with the total prescription of fluoroquinolones. Separate strata for year of isolation, gender and age were used to study the associations between resistance to norfloxacin (excluding samples from inpatient clinics) and prescription of fluoroquinolones, nitrofuran derivatives and trimethoprim with or without sulphamethoxazole.
Linear regression curves were fitted using prescription rate as the independent variable and resistance as the dependent variable. The prescription rate, measured in DDD, was adjusted for the incidence of urinary tract infection in the different age groups (averaged for 6 years (1992–97) for every age group), resulting in DDD/case UTI.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Proportion of resistant E. coli strains
A total of 91 669 E. coli isolates were available for analysis; of these, 2232 were resistant to norfloxacin, 23 226 to trimethoprim, 4726 to nitrofurantoin and 31 903 to amoxycillin. Resistance to trimethoprim and norfloxacin had increased steadily over the study period, whereas resistance to amoxycillin and nitrofurantoin had remained constant (Table I
). The increase in norfloxacin resistance was associated with an increase in multiresistance, defined as resistance to norfloxacin and to at least two of the other three antibiotics (Table I).
|
The trend towards an increase in norfloxacin resistance was found in all five participating laboratories (Figure 1a
). The increase in norfloxacin resistance was most pronounced in E. coli isolates from general practice, outpatient clinics and nursing homes (Figure 1b). Resistance to norfloxacin increased in both males and females (Figure 1c). Age appeared to influence the development of resistance to norfloxacin over time: resistance remained low in the youngest age group (<15 years), but increased most steeply in the oldest age group (>74 years) (Figure 1d).
|
, general practice; •, nursing home; 
, outpatient clinic; 
, inpatient clinic), (c) gender (
, male) and (d) age group (for female patients only) (
, >74 years).Multivariate analysis of determinants of norfloxacin resistance
Multivariate analysis showed that the increase in norfloxacin resistance over time was independent of other risk factors, such as age, gender, laboratory and origin of the patient. The effects of age, gender and patient's origin on norfloxacin resistance were not influenced by the location of the laboratories (Table II). However, the effect of age on resistance was strongly determined by gender; in male patients, resistance to norfloxacin was already high in younger age groups, in contrast to the corresponding age groups in female patients (Table II).
|
Developments in the prescription of fluoroquinolones, nitrofurantoin and trimethoprim/co-trimoxazole in The Netherlands
Data from the Drug Information Project of the Supervising Board for Health Care Insurance in The Netherlands (GIP/CVZ), Amstelveen, indicated that the prescription of fluoroquinolones had doubled from 1990 onwards (Table III). In contrast, the prescription of nitrofuran derivatives (mainly nitrofurantoin), and trimethoprim with or without sulphamethoxazole had decreased in this period (Table III).
|
The use of fluoroquinolones/nitrofurantoin compared with developments in resistance
Linear regression of the association between prescription rate in DDD/case UTI for fluoroquinolones, nitrofuran derivatives and trimethoprim/co-trimoxazole and resistance to norfloxacin revealed a significant association only between norfloxacin resistance and the prescription of fluoroquinolones (P < 0.002). Prescription of nitrofuran derivatives (P > 0.1) and trimethoprim with or without sulphamethoxazole (P > 0.3) was not significantly associated with norfloxacin resistance. Figure 2 depicts the relationship between norfloxacin resistance and fluoroquinolone usage.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
This study indicates clearly that norfloxacin resistance in E. coli isolates is increasing. However, the absolute proportion of resistant strains must be interpreted with caution. Results from routine bacteriological testing from general practice tend to overestimate the resistance in this section of the patient population because the submission of specimens tends to be selective (possibly following the failure of empirical treatment). In a previous study from our centre, trimethoprim resistance in E. coli isolates routinely sent by GPs was more than twice that in isolates obtained from patients who had not been treated with antibiotics for at least 6 months.9 Comparison of our results with findings from previous studies on isolates of unselected patients2,3 shows a similar difference in the proportion of resistant strains. Nevertheless, an increase in resistance, as was demonstrated in our study, may be predictive of developments in the community, provided the results of the disc tests in local laboratories and MIC data show good agreement.10 In such a case, as was recently suggested for E. coli,10 small changes in resistance, which may be the first signs of emergence of an actual resistance problem, would be detected more easily when sample sizes are large. In studies with unselected samples from general practice, the sample size, typically <1000, may be too small to detect such changes.2,4
Univariate and multivariate analyses indicated a consistent increase in norfloxacin resistance over time; this increase was not associated with age, gender, laboratory or origin of the patient (see Table II
). Many of the norfloxacin-resistant strains were also resistant to two of the three other antibiotics tested (amoxycillin, trimethoprim and nitrofurantoin). We did not observe a significant increase in the strains resistant only to norfloxacin. This could indicate that, until now, norfloxacin has been prescribed only as a second-choice medication for patients in whom treatment with the antibiotics of first choice (trimethoprim or nitrofurantoin) has failed. However, we cannot exclude the possibility that this multiple resistance developed from selection of genetically linked resistance genes.
The incidence of resistance differed among laboratories, perhaps owing to different testing methods. However, the trend towards increasing resistance was demonstrated in every participating laboratory (Figure 1a). A multivariate logistic regression model did not reveal significant interaction between laboratory and year of sample collection (Table II), indicating that the trend to increased norfloxacin resistance was not a result of, for instance, changes in laboratory methods.
Data from the multivariate model (Table II) also indicated that gender strongly influenced the effect of age on fluoroquinolone resistance, probably on account of the different nature of UTI in males and females. In female patients uncomplicated cystitis is most common, wherease in male patients complicated UTIs are more common.11,12 Males with UTI may receive prolonged therapy with fluoroquinolones, which may explain the relatively high resistance to fluoroquinolones in isolates from young male patients. Our model did not demonstrate a strong interaction between effects of origin and age on resistance to norfloxacin. This may indicate that age and origin independently affect the risk of resistance to norfloxacin. It is, however, difficult to estimate the exact contributions of age, gender and origin on norfloxacin resistance, because the method by which isolates are selected differs between general practice, nursing homes and outpatient and inpatient clinics. The increased resistance in older age groups (mainly female) might result from increased cumulative lifetime exposure in the older patients,13 or to a more complicated nature of the UTI more obviously warranting prescription of fluoroquinolones, or to the recent increase in fluoroquinolone prescription, especially for older patients.
Currently there are no indications that fluoroquinolones are prescribed regularly for respiratory infections in The Netherlands. Thus, this group of antibiotics is still most often used for the therapy of UTI. Prescription of fluoroquinolones nearly doubled from 1990 to 1997. In contrast, prescription of nitrofuran derivatives (mainly nitrofurantoin) and trimethoprim/co-trimoxazole decreased over the study period. This indicates that not only GPs, but also physicians in nursing homes and outpatient clinics, are prescribing fluoroquinolones for UTI increasingly frequently. However, it is not clear whether they prescribe these antibiotics as first-, second- or third-choice for UTI.
A comparison of the trend in norfloxacin resistance and the rates of prescription for fluoroquinolones, nitrofuran derivatives and trimethoprim/co-trimoxazole indicated a significant relationship only between norfloxacin resistance and fluoroquinolone prescription. This suggests that increased prescription of fluoroquinolones may be the driving selection force leading to increased norfloxacin (fluoroquinolone) resistance in E. coli in the community. A recent case–control study showed that increased resistance to trimethoprim in Gram-negative bacteria isolated from urine samples14 is associated primarily with the increased use of this antibiotic and not with the use of other antibiotics. In two other hospital case–control studies, resistance to fluoroquinolones in Gram-negative bacteria from nosocomial infections15 or in E. coli isolated from bacteraemia16 was strongly associated with prescription of this group of antibiotics. In these studies, too, associations with the use of other antibiotics were not significant.14–16 Thus, our study indicates that resistance to norfloxacin in the community is only associated with the prescription of fluoroquinolones, and not with that of other antibiotics.
|
Acknowledgments |
|---|
The authors are obliged to J. F. Piepenbrink and R. J. van der Vaart from the Drug Information Project of the Supervising Board for Health Care Insurance in The Netherlands (GIP/CVZ), Amstelveen, for providing antibiotic prescription data for The Netherlands (1990–97), and to Dr E. H. van Lisdonk, from the department of Family Medicine, Academical Hospital Nijmegen, for providing data on the incidence of urinary tract infections from general practice.
|
Notes |
|---|
* Corresponding author. Tel: +31-30-2743865; Fax: +31-30-2744409; E-mail: wim.goettsch{at}rivm.nl
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
1 . Vromen, M., Van der Ven, A. J., Knols, A. & Stobberingh, E. E. (1999). Antimicrobial resistance patterns in urinary isolates from nursing home residents. Fifteen years of data reviewed. Journal of Antimicrobial Chemotherapy 44, 113–6.
2
.
Trienekens, T., Stobberingh, E. E., Beckers, F. & Knottnerus, A. (1994). The antibiotic susceptibility patterns of uropathogens isolated from general practice patients in Southern Netherlands. Journal of Antimicrobial Chemotherapy 33, 1064–6.
3 . Goettsch, W. G., Goossens, H., De Neeling, A. J. & Sprenger, M. J. (1999). Infections and bacterial resistance in the community. Nederlands Tijdschrift voor Geneeskunde 143, 1296–9.[Medline]
4 . Van der Does, M. C., Van Duijn, N. P., Timmerman, C. P. & Degener, J. E. (1998). Antibiotic resistance in uncomplicated urinary tract infections. Huisarts en Wetenschap 41, 421–3.
5 . Stobberingh, E. E. & Houben, A. W. (1988). Antibiotic resistance and antibiotic utilisation of urinary tract infection in 11 family practices in Maastricht. Nederlands Tijdschrift voor Geneeskunde 132, 1793–7.
6 . Sampers, G. H. & Petri, H. (1993). The duration of treatment of urinary tract infections before and after the release of the standard. Huisarts en Wetenschap 36, 137–9.
7 . Van Balen, F. A., Baselier, P. J., Van Pienbroek, E. & Winkens, R. A. (1989). Dutch College of General Practitioners standards for urinary tract infections. Huisarts en Wetenschap 32, 439–43.
8 . Van Klingeren, B. & Mouton, R. P. (Eds). (1990). Standardization of Susceptibility Testing Methods, 2nd edn, Supplement. RIVM, Bilthoven, The Netherlands.
9 . De Neeling, A. J., De Jong, J., Overbeek, B. P., De Bruin, R. W., Dessens-Kroon, M. & Van Klingeren, B. (1990). Quantitative Susceptibility Research on Intra- and Extramural Isolates of Escherichia coli. Report no. 359001002. National Institute of Public Health and the Environment, Bilthoven, The Netherlands.
10 . Livermore, D. M., Threlfall, E. J., Reacher, M. H., Johnson, A. P., James, D., Cheasty, T. et al. (2000). Are routine sensitivity test data suitable for the surveillance of resistance? Resistance rates amongst Escherichia coli from blood and CSF from 1991 to 1997, as assessed by routine and centralized testing. Journal of Antimicrobial Chemotherapy 45, 205–11.
11 . Warren, J. W. (1996). Clinical presentations and epidemiology of urinary tract infections. In Urinary Tract Infections, Molecular Pathogenesis and Clinical Management, (Mobley, H. L. & Warren, J. W., Eds), pp. 3–27. ASM Press, Washington, DC.
12 . Wolfhagen, M. J., Hoepelman, I. M., De Melker, R. A. & Verhoef, J. (1988). Diagnosis of uncomplicated urinary tract infections: complicated? Nederlands Tijdschrift voor Geneeskunde 132, 390–4.[Medline]
13 . Arstila, T., Huovinen, S., Lager, K., Lehtonen, A. & Huovinen, P. (1994). Positive correlation between the age of patients and the degree of antimicrobial resistance among urinary strains of Escherichia coli. Journal of Infection 29, 9–16.[Web of Science][Medline]
14
.
Steinke, D. T., Seaton, R. A., Philips, G., MacDonald, T. M. & Davey, P. G. (1999). Factors associated with trimethoprim-resistant bacteria isolated from urine samples. Journal of Antimicrobial Chemotherapy 43, 841–3.
15 . Richard, P., Delangle, M. H., Merrien, D., Barille, S., Reynaud, A., Minozzi, C. et al. (1994). Fluoroquinolone use and fluoroquinolone resistance: is there an association? Clinical Infectious Diseases 19, 54–9.[Web of Science][Medline]
16
.
Pena, C., Albareda, J. M., Pallares, R., Pujol, M., Tubau, F. & Ariza, J. (1995). Relationship between quinolone use and emergence of ciprofloxacin-resistant Escherichia coli in bloodstream infections. Antimicrobial Agents and Chemotherapy 39, 520–4.
Received 20 October 1999; returned 20 January 2000; revised 18 February 2000; accepted 27 March 2000
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  N. Allou, E. Cambau, L. Massias, F. Chau, and B. Fantin Impact of Low-Level Resistance to Fluoroquinolones Due to qnrA1 and qnrS1 Genes or a gyrA Mutation on Ciprofloxacin Bactericidal Activity in a Murine Model of Escherichia coli Urinary Tract Infection Antimicrob. Agents Chemother., October 1, 2009; 53(10): 4292 - 4297. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Bergman, S. T. Nyberg, P. Huovinen, P. Paakkari, A. J. Hakanen, and and the Finnish Study Group for Antimicrobial Resi Association between Antimicrobial Consumption and Resistance in Escherichia coli Antimicrob. Agents Chemother., March 1, 2009; 53(3): 912 - 917. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Yagci, F. Yoruk, A. Azap, and O. Memikoglu Prevalence and Risk Factors for Selection of Quinolone-Resistant Escherichia coli Strains in Fecal Flora of Patients Receiving Quinolone Therapy Antimicrob. Agents Chemother., March 1, 2009; 53(3): 1287 - 1289. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. De Backer, T. Christiaens, S. Heytens, A. De Sutter, E. E. Stobberingh, and G. Verschraegen Evolution of bacterial susceptibility pattern of Escherichia coli in uncomplicated urinary tract infections in a country with high antibiotic consumption: a comparison of two surveys with a 10 year interval J. Antimicrob. Chemother., August 1, 2008; 62(2): 364 - 368. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Gupta, T. M. Hooton, P. L. Roberts, and W. E. Stamm Short-Course Nitrofurantoin for the Treatment of Acute Uncomplicated Cystitis in Women Arch Intern Med, November 12, 2007; 167(20): 2207 - 2212. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. R. Lockhart, M. A. Abramson, S. E. Beekmann, G. Gallagher, S. Riedel, D. J. Diekema, J. P. Quinn, and G. V. Doern Antimicrobial Resistance among Gram-Negative Bacilli Causing Infections in Intensive Care Unit Patients in the United States between 1993 and 2004 J. Clin. Microbiol., October 1, 2007; 45(10): 3352 - 3359. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Uzunovic-Kamberovic Antibiotic resistance of coliform organisms from community-acquired urinary tract infections in Zenica-Doboj Canton, Bosnia and Herzegovina J. Antimicrob. Chemother., August 1, 2006; 58(2): 344 - 348. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Nys, T. van Merode, A. I. M. Bartelds, and E. E. Stobberingh Urinary tract infections in general practice patients: diagnostic tests versus bacteriological culture J. Antimicrob. Chemother., May 1, 2006; 57(5): 955 - 958. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. R. Johnson, B. Johnston, M. A. Kuskowski, R. Colodner, and R. Raz Spontaneous Conversion to Quinolone and Fluoroquinolone Resistance among Wild-Type Escherichia coli Isolates in Relation to Phylogenetic Background and Virulence Genotype Antimicrob. Agents Chemother., November 1, 2005; 49(11): 4739 - 4744. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Arslan, O. K. Azap, O. Ergonul, F. Timurkaynak, and on behalf of the Urinary Tract Infection Study Gro Risk factors for ciprofloxacin resistance among Escherichia coli strains isolated from community-acquired urinary tract infections in Turkey J. Antimicrob. Chemother., November 1, 2005; 56(5): 914 - 918. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Landgren, H. Oden, I. Kuhn, A. Osterlund, and G. Kahlmeter Diversity among 2481 Escherichia coli from women with community-acquired lower urinary tract infections in 17 countries J. Antimicrob. Chemother., June 1, 2005; 55(6): 928 - 937. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. R. Johnson, M. A. Kuskowski, T. T. O'Bryan, R. Colodner, and R. Raz Virulence Genotype and Phylogenetic Origin in Relation to Antibiotic Resistance Profile among Escherichia coli Urine Sample Isolates from Israeli Women with Acute Uncomplicated Cystitis Antimicrob. Agents Chemother., January 1, 2005; 49(1): 26 - 31. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Sommet, C. Sermet, P. Y. Boelle, M. Tafflet, C. Bernede, and D. Guillemot No significant decrease in antibiotic use from 1992 to 2000, in the French community J. Antimicrob. Chemother., August 1, 2004; 54(2): 524 - 528. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Kahlmeter, P. Menday, and O. Cars Non-hospital antimicrobial usage and resistance in community-acquired Escherichia coli urinary tract infection J. Antimicrob. Chemother., December 1, 2003; 52(6): 1005 - 1010. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Komp Lindgren, A. Karlsson, and D. Hughes Mutation Rate and Evolution of Fluoroquinolone Resistance in Escherichia coli Isolates from Patients with Urinary Tract Infections Antimicrob. Agents Chemother., October 1, 2003; 47(10): 3222 - 3232. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Kahlmeter and P. Menday Cross-resistance and associated resistance in 2478 Escherichia coli isolates from the Pan-European ECO{middle dot}SENS Project surveying the antimicrobial susceptibility of pathogens from uncomplicated urinary tract infections J. Antimicrob. Chemother., July 1, 2003; 52(1): 128 - 131. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. P. Metlay, B. L. Strom, and D. A. Asch Prior antimicrobial drug exposure: a risk factor for trimethoprim-sulfamethoxazole-resistant urinary tract infections J. Antimicrob. Chemother., April 1, 2003; 51(4): 963 - 970. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Kavatha, H. Giamarellou, Z. Alexiou, N. Vlachogiannis, S. Pentea, T. Gozadinos, G. Poulakou, A. Hatzipapas, and G. Koratzanis Cefpodoxime-Proxetil versus Trimethoprim-Sulfamethoxazole for Short-Term Therapy of Uncomplicated Acute Cystitis in Women Antimicrob. Agents Chemother., March 1, 2003; 47(3): 897 - 900. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Kahlmeter An international survey of the antimicrobial susceptibility of pathogens from uncomplicated urinary tract infections: the ECO{middle dot}SENS Project J. Antimicrob. Chemother., January 1, 2003; 51(1): 69 - 76. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Oteo, J. Campos, F. Baquero, and Spanish members of the European Antimicrobial Resi Antibiotic resistance in 1962 invasive isolates of Escherichia coli in 27 Spanish hospitals participating in the European Antimicrobial Resistance Surveillance System (2001) J. Antimicrob. Chemother., December 1, 2002; 50(6): 945 - 952. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Karlowsky, L. J. Kelly, C. Thornsberry, M. E. Jones, and D. F. Sahm Trends in Antimicrobial Resistance among Urinary Tract Infection Isolates of Escherichia coli from Female Outpatients in the United States Antimicrob. Agents Chemother., August 1, 2002; 46(8): 2540 - 2545. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Z. Qiang, T. Qin, W. Fu, W. P. Cheng, Y. S. Li, and G. Yi Use of a rapid mismatch PCR method to detect gyrA and parC mutations in ciprofloxacin-resistant clinical isolates of Escherichia coli J. Antimicrob. Chemother., March 1, 2002; 49(3): 549 - 552. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. C. McDonald, F.-J. Chen, H.-J. Lo, H.-C. Yin, P.-L. Lu, C.-H. Huang, P. Chen, T.-L. Lauderdale, and M. Ho Emergence of Reduced Susceptibility and Resistance to Fluoroquinolones in Escherichia coli in Taiwan and Contributions of Distinct Selective Pressures Antimicrob. Agents Chemother., November 1, 2001; 45(11): 3084 - 3091. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. de Neeling, B. P. Overbeek, A. M. Horrevorts, E. E. J. Ligtvoet, and W. G. Goettsch Antibiotic use and resistance of Streptococcus pneumoniae in The Netherlands during the period 1994-1999 J. Antimicrob. Chemother., September 1, 2001; 48(3): 441 - 444. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. E. van den Bogaard, N. London, C. Driessen, and E. E. Stobberingh Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers J. Antimicrob. Chemother., June 1, 2001; 47(6): 763 - 771. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Bertrand and D. Talon In vitro activity of co-amoxiclav acid against clinical isolates of Escherichia coli J. Antimicrob. Chemother., May 1, 2001; 47(5): 725 - 726. [Full Text] [PDF]
|
|
|
|
|
|
M. Cizman, A. Orazem, V. Krizan-Hergouth, and J. Kolman Correlation between increased consumption of fluoroquinolones in outpatients and resistance of Escherichia coli from urinary tract infections J. Antimicrob. Chemother., April 1, 2001; 47(4): 502 - 502. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||