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Vol. 26. Issue 3.
(May - June 2022)
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Vol. 26. Issue 3.
(May - June 2022)
Original Article
Open Access
Susceptibility to first choice antimicrobial treatment for urinary tract infections to Escherichia coli isolates from women urine samples in community South Brazil
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Zuleica Naomi Tanoa,
Corresponding author
zntanno@uel.br

Corresponding author.
, Renata K. Kobayashib, Evelyn Poliana Candidoc, Juliana Buck Diasc, Luis Felipe Peruginic, Eliana Carolina Vesperoc, Wander Rogerio Pavanellid
a Universidade Estadual de Londrina, Departamento de Medicina Interna, Londrina, PR, Brazil
b Universidade Estadual de Londrina, Departamento de Microbiologia, Londrina, PR, Brazil
c Universidade Estadual de Londrina, Departamento de Patologia, Análises Clínicas e Toxicológicas, Londrina, PR, Brazil
d Universidade Estadual de Londrina, Centro de Ciências Biológicas, Departamento de Ciências Biológicas, Laboratório de Imunoparasitologia de Doenças Negligenciadas e Câncer (LIDNC), Londrina, PR, Brazil
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Abstract

E. coli is the main pathogen of UTI. It is important to be aware the local epidemiological data for an appropriate initial treatment. Resistance to antimicrobial agents has increased, especially to first-choice antibiotics in the treatment of cystitis. There are few studies on the sensivity profile of community uropathogen in our region.

Objective

To characterize antimicrobials the sensitivity profile to E. coli isolated from urocultures of women treated at Basic Health Units and Emergency Care Units of Londrina- Paraná- Brazil during a period of 12 months (June 1, 2016 to June 1, 2017).

Methodology

A cross-sectional study was carried out from June 2016 to June 2017. All urine samples collected in the Basic Health Units and Emergency Departments in the city of Londrina (Paraná State, Brazil) were sent to a Central Laboratory where the identification and antimicrobial susceptibility testing were performed. Clinical Laboratory Standards Institute (CLSI) breakpoints were used for the interpretation of susceptibility testing results.

Results

56,555 urine cultures were performed in the period, of which 8,832 were positive, of which 5,377 were women. Of these samples, 4.7% were enterobacteria producing extended-spectrum beta-lactamases (ESBL) and 15.5% resistant to quinolones. TMP- SMX was resistant in more than 30% of the samples in all age groups. Among quinolone-resistant isolates, resistance to cephalothin, ampicillin and sulfamethoxazole-trimethoprim was greater than 60%. Nitrofurantoin was the only antimicrobial that showed 90% of sensitivity.

Conclusion

The antimicrobials sensitivity profile was similar to that reported in the literature, with TMP- SMX resistance greater than 30% in the studied samples. Nitrofurantoin maintains high sensitivity rates greater than 90%. Resistance to quinolones increases proportionally with age, as well ESBL.

Keywords:
Urinary tract infection
Bacteriuria
Drug resistance
Uropathogenic
Escherichia coli
Full Text
Background

Urinary Tract Infection (UTI) is the most common outpatient infection, and the second most frequent after respiratory tract infection.1 Women are more affected than men due to the shorter distance between the female urethra and bladder, which makes bacterial colonizers ascend to kidneys before they are removed by micturition.2 Symptomatic infection is more frequent in women aged 15-29 years (12.6%), whereas the incidence in men comprises 3% in USA.3

Among healthy women aged 18-39 years, 80% of UTIs are caused by E. coli, which is the target of empirical therapy. However, significant variations in antimicrobial susceptibility have been observed in several countries over the last years, with the progressive emergence of resistance to fluoroquinolones and other antibiotics commonly used for empirical treatment of community-acquired UTIs. Presence of extended spectrum beta-lactamases (ESBLs) in Latin America increased from 1.7% to 7.1 – 12.5%.4-6

Since 2011, the Infectious Diseases Society of America (IDSA) has recommended that trimethoprim-sulfamethoxazole (cotrimoxazole), nitrofurantoin, fosfomycin, or pivmecillinam, should be used whether local resistance rates of uropathogens causing acute uncomplicated UTIs do not exceed 20%, or whether the infecting strain is known to be susceptible to these drugs.7 Currently, guidelines recommend fosfomycin trometamol and nitrofurantoin as the first-choice treatment for patients with uncomplicated UTIs, for which cotrimoxazole is the third option.5 In Korea, nitrofurantoin, fosfomycin and pivmecillinam are the treatment of first choice for uncomplicated UTIs, whereas cotrimoxazole may be used only when antimicrobial susceptibility testing confirms drug sensitivity.8

The appropriate choice of antibiotics in patients with suspected uncomplicated UTI should be based on up-to-date surveillance data from patients in primary care settings. Thus, prospective surveillance of antibiotic resistance patterns in uropathogens from all patients attending these settings is crucial for guiding first- and second-line antibiotic selection.4

This study aimed to evaluate the antimicrobial susceptibility profile for first-line treatment for UTI caused by E.coli isolated in urine samples of women in the community and presence of extended-spectrum beta-lactamase (ESBL).

Material and methods

A cross-sectional study was carried out from June 2016 to June 2017. All urine samples collected at the Basic Health Units and Emergency Departments in the city of Londrina (Paraná State, Brazil) were sent to a Central Laboratory where the identification and antimicrobial susceptibility testing were performed. First-morning midstream urine samples were collected, of which 10 microliters were inoculated onto chromogenic media CPS ID 3 (BioMérieux, Marcy I’Étoile, France), and incubated overnight at 36°C. Urine culture was considered positive according to the following criteria: growth of a single bacterium (pure culture) and colony counts > 105 colony-forming units (CFU)/mL. Bacteria were identified according to phenotypic characteristics displayed on CPS ID 3 medium or by using the Vitek® 2 automated system (BioMérieux, Marcy I’Étoile, France). Urine culture of men and uropathogens other than E. coli were excluded. Data such as age and pregnancy status were analyzed through the WebSaúde system of Londrina city.

Antimicrobial susceptibility testing (AST)

AST was performed by using the AST-238 card, whose results were evaluated with the VITEK® 2 (BioMérieux, Marcy-I'Etoile, France) system. The following antibiotics were tested: amikacin (AST-N054 only), ampicillin, amoxicillin/clavulanic acid, aztreonam (AST-N054 only), cefalexin, cefepime, cefotaxime, ceftazidime, cefoxitin, cefuroxime, ciprofloxacin, norfloxacin, ertapenem, gentamicin, meropenem, nalidixic acid, nitrofurantoin, piperacillin, piperacillin/tazobactam, and trimethoprim. Clinical Laboratory Standards Institute (CLSI) breakpoints were used for the interpretation of susceptibility testing results. Isolates were classified as susceptible (S), intermediately resistant (I) or resistant (R) to the aforementioned antimicrobials, respectively, according to the following MIC breakpoints (µg/mL): ampicillin, ≤ 8, 16, ≥ 32; amoxicillin-clavulanate, ≤ 8/4, 16/8, ≥ 32/16; cefuroxime axetil, ≤ 4, 8-16, ≥ 32; norfloxacin, ≤ 4, 8, ≥ 16; ciprofloxacin, ≤ 1, 2, ≥ 4; cotrimoxazole, ≤ 2/38, ≥ 4/76; nitrofurantoin, ≤ 32, 64, ≥ 128; fosfomycin was evaluated by disk diffusion method (Oxoid, Cambridge, UK). The isolates were screened for ESBL production through chromID® ESBL agar plate test (BioMérieux, Marcy l’Étoile, France).

Statistical analysis

The results were stored and analyzed using SPSS 17. The participants were subdivided into four age groups (< 15, 15-45, 46- 59, and > 60 years), with their respective bacterial isolates. Two-sided chi-square test and Fisher's exact test were used to assess whether there were differences regarding the antimicrobial resistance profile of E. coli isolates across age groups. Significant differences in the prevalence of antimicrobial resistance between age groups were determined by odds ratio with 95% confidence intervals and p-value < 0.05. The study was approved by Ethics and Research Committee of the State University of Londrina (CAAE 56869816.0.0000.5231) and authorized by the Health Department of Londrina, Paraná.

Results

A total of 56,555 urine cultures were performed, of which 8,382 were positive, and out of these 5,794 (72.2%) were positive for E. coli. Women accounted for 92.8% (5,377/5,794) positive cultures. Moreover, 10% of these women were pregnant, as shown in Fig. 1. ESBL production was detected in 4.7% (n = 255) of the isolates.

Fig. 1.

Study population.

(0.19MB).

The average age of women was 47 years (ranging from 0 to 101 years). In this study, 1,777 (33%) women were aged 60 years and over had isolates presented with a higher frequency of ESBL production (8.3%) when compared to other age groups. Susceptibility rates to the quinolone nalidixic acid and the fluoroquinolones ciprofloxacin and norfloxacin were 73.3%, 85.7%, and 85.9%, respectively. For the isolates resistant to these three antimicrobials, susceptibility to fosfomycin was 98.3%.

The lowest susceptibility rate was observed for cephalothin (51.8%), followed by ampicillin (54%); while amikacin, ertapenem and meropenem presented the highest susceptibility rate (99.7%). Fig. 2 shows the sensitivity and resistance of all 4,377 samples.

Fig. 2.

Antimicrobial sensitivity/ resistance of all E. coli isolated (n = 5377).

(0.26MB).
Susceptibility to first-line UTI antimicrobials agents according to age

Cephalotin (48.1%) and ampicillin (52%) presented the lowest susceptibility patterns, regardless of age. Trimethoprim-sulfamethoxazole (TMP-SMX) displayed resistance rates greater than 30% in all age groups, whereas cefuroxime presented a susceptibility rate greater than 90%. Susceptibility to gentamicin, amoxicillin/clavulanic acid, piperacillin-tazobactan, cephalothin, cefepime, ceftriaxone, cefuroxime, nalidixic acid, norfloxacin, ciprofloxacin and TMP-SMX had a significant association with age. For the age group 15-45 years, quinolones maintained 90% of susceptibility, except for nalidixic acid, whose susceptibility rate was 78% (Table 1).

Table 1.

Antimicrobial susceptibility of E. coli isolated from women according to age range.

  < 1515-4546-59≥ 60p-value* 
  n   
Amikacin  347  100  2130  99.6  1113  99.9  1769  99.5  0.255 
Gentamicin  341  98.3  2037  95.2  1059  95.1  1629  91.7  <0.001 
Amoxicillin-clavulanic acid  305  87.9  1901  88.9  982  88.2  1518  85.4  0.011 
Ampicillin  190  54.8  1203  56.2  601  53.9  924  52.0  0.068 
Piperacillin-tazobactan  338  97.4  2091  97.8  1084  97.3  1703  95.8  0.005 
Cephalothin  186  53.6  1155  54.0  574  51.5  855  48.1  0.003 
Cefepime  339  97.2  2079  97.2  1064  95.5  1635  92  <0.001 
Ceftriaxone  341  98.3  2079  97.2  1062  95.3  1625  91.4  <0.001 
Cefuroxime  330  95.1  2009  93.9  1020  91.6  1500  84.4  <0.001 
Nalidixic acid  279  80.4  1684  78.7  810  72.7  1096  61.7  <0.001 
Norfloxacin  330  95.1  1941  90.7  941  84.5  1306  73.5  <0.001 
Ciprofloxacin  329  94.8  1938  90.6  940  84.4  1303  73.3  <0.001 
Ertapenem  347  100  2135  99.8  1106  99.3  1770  99.6  0.087 
Meropenem  347  100  2136  99.9  1108  99.5  1767  99.4  0.059 
Nitrofurantoin  334  96.3  2072  96.9  1082  97.1  1698  95.6  0.079 
SMX /TMP  255  73.5  1573  73.5  781  70.1  1200  67.5  <0.001 
ESBL  07  2.0  54  2.5  47  4.2  147  8.3  <0.001 
TOTAL  347  100  2139  100  1114  100  1777  100   

p valor qui square test or Exact Fisher Test.

Variables with significant association: gentamicin, amoxicillin-clavulanic, piperacillin tazobactan, cephalothin, cefepime, ceftriaxone, cefuroxime, nalidixic acid, norfloxacin, ciprofloxacin, SMX/TMP.

The level of antimicrobial resistance to the quinolones tested in this study (nalidixic acid, ciprofloxacin, and norfloxacin) was 15.5%. The susceptibility profile to other first-line antimicrobials used in the treatment of UTIs decreased dramatically, especially to cephalothin, ampicillin and TMP-SMX, which presented only 40% susceptibility in these isolates. The only first-line antimicrobial agent that maintained a rate of susceptibility greater than 90% for these isolates was nitrofurantoin, regardless of age. The presence of ESBL-producing isolates was not significantly associated with age when the isolate was resistant to the quinolones used in our study (Table 2).

Table 2.

Antimticrobial Susceptibility of samples resistant to three quinolones according to age range.

  < 1515-4546-59≥ 60Valor de p* 
  n   
Amikacin  17  100  146  99.5  166  100  338  99.6  <0.001 
Gentamicin  17  100  140  72.9  135  81.3  350  75.9  0.031 
Amoxicillin-clavulanic  15  88.2  146  76  130  78.3  338  73.3  0.339 
Ampicillin  02  11.8  32  16.7  46  27.7  89  19.3  0.041 
Piperacillin-tazobactan  15  88.2  178  92.7  158  95.2  417  90.5  0.246 
Cephalothin  05  29.4  62  32.3  58  34.9  127  27.5  0.294 
Cefepime  13  76.5  154  80.2  140  84.3  359  77.9  0.349 
Ceftriaxone  13  76.5  152  79.2  141  84.9  353  76.6  0.158 
Cefuroxime  12  70.6  140  72.9  122  73.5  291  63.1  0.024 
Ertapenem  17  100  192  100  161  97  456  98.9  0.076 
Meropenem  17  100  192  100  164  98.8  457  99.1  0.414 
Nitrofurantoin  16  94.1  184  95.8  159  95.8  426  92.4  0.254 
TMP/SMX  07  41.2  81  42.2  78  47  200  43.4  0.809 
ESBL  05  29.4  37  19.3  24  14.5  105  22.8  0.102 
TOTAL  17  100  192  100  166  100  461  100   

p-value chi-square and Fisher's Exact test.

Variables with significant association (p < 0.05): Amikacin, gentamicin, cefuroxime, ertapenem.

Discussion

Our cross-sectional study shows the antimicrobial susceptibility profile of uropathogens of urine cultures collected from women who attended the Basic Health and Emergency Units in Londrina, Southern Brazil. Londrina has 537,377 inhabitants, and is located at 23°18′36“S51°09′46”O.

E. coli was the most common pathogen isolated. Furthermore, women aged 15-45 years had the greatest number of positive urine cultures, as observed by other authors.2,9-11

In this study, men were excluded from analysis because they had complicated UTIs, which was not the scope of this work, as also performed by Dubbs et al.12 In a study carried out in Curitiba, Brazil, with outpatients who received care at the public health system, Reu et al.13 also reported that the lowest frequencies of E. coli, as causative agent of UTIs, were found between pregnant women, men, and boys. These data suggest that although E. coli was the most common uropathogen, its distribution may vary according to sex and patient physiological status, being less common in men.

Resistance to TMP-SMX was greater than 30% in this study, regardless of age. Specifically, 32.5% of isolates from patients aged 60 years and over showed resistance to this antimicrobial agent. According to Gupta et al.,7 TMP-SMX is recommended as the first-line treatment for uncomplicated UTIs, but only when resistance rates to this antibiotic do not exceed 20%.

It is known that antimicrobial resistance varies geographically, including within a country, as shown by Cunha et al.6 who reported a resistance rate of 50.6% to TMP-SMX in a Northeastern Brazilian city, while in India, in 2013, the resistance rate to this antibiotic was 52%, increasing up to 59.6% in 2017.14 However, in a study carried out in the USA, Yamaji et al.15 showed that frequencies of resistance to TMP-SMX in uropathogenic Escherichia coli (UPEC) isolates obtained from outpatients with UTI symptoms in 1999–2000 and in 2016–2017 had not increased significantly over the studied period (resistance increased slightly from 16.9% to 17.1%). Studies in which resistance to TMP-SMX is greater than 35% suggest the replacement and/or withdrawal of this antibiotic from first-line treatment of uncomplicated UTIs.16 Currently, guidelines have recommended the use of fosfomycin–trometamol and pivmecillinam as first- and second-line treatments for these infections, respectively.17

In this study, resistance to quinolones surpassed 10% in isolates from women aged ≥ 46 years, whereas the overall resistance level to quinolones was 15.5%. The association of quinolone resistance with older age had also been observed in the literature.

Quinolones are the most frequently selected antimicrobials for treating uncomplicated UTIs in many countries.18,19 Risk factors associated with resistance to this antimicrobial class include patients older than 60 years of age, presence of obstructive uropathy, recurrent UTI history, as well as the use of quinolones in the past three months.19,20,21

Despite FDA warnings about the use of quinolones in 2016,22 the rate of prescriptions of these antibiotics has not changed over years, and their inappropriate use was more frequent in the treatment of uncomplicated UTIs. Thus, the overuse and side-effects of quinolones must be incorporated into the clinical decision regarding antimicrobial treatment of all infections, such as upper respiratory tract infection, uncomplicated UTIs, and abdominal infections.23,24

Conversely, resistance to nitrofurantoin was very low in our study, less than 5% in all age groups, including the age group > 60 years, even among those isolates resistant to quinolones (7.6%). The same pattern was observed in a study conducted in Rio Grande do Norte, Brazil, in which 6.6% of E. coli was resistant to nitrofurantoin (n = 653).6 Likewise, a retrospective analysis performed by Sanchez et al.25 showed that, in the United States, nitrofurantoin retains a high level of antibiotic activity against urinary E. coli isolates. Nevertheless, the resistance levels to nitrofurantoin in India and Mexico are among the highest reported worldwide: 3% and 12.7%, respectively.14,26 These results show that nitrofurantoin remains the treatment of choice for uncomplicated UTIs, although it should not be used for the treatment of pyelonephritis, since its concentration in the renal parenchyma is too low.27

In this study, fosfomycin was tested for all quinolone-resistant isolates, showing high susceptibility. Similarly, in a study performed in India with 7,295 isolates obtained from patients with uncomplicated UTI, fosfomycin and nitrofurantoin displayed the greatest susceptibility levels.28 Other countries in Europe and in the USA also reported high rates of susceptibility to Fosfomycin.29,30 These results highlight the use of fosfomycin as the antibiotic of first choice in the treatment of UTIs.8 In Brazil, fosfomycin is an expensive antimicrobial agent, and unlike TPM-SMX, nitrofurantoin, norfloxacin, and ciprofloxacin, it is not available to patients in the public health system. In this scenario, exposure to fosfomycin is a fundamental risk factor which can lead to the selection of resistant E. coli isolates.

Among beta-lactams used for uncomplicated UTIs, amoxicillin/clavulanic acid displayed low levels of resistance regardless of age: 12.1%, 11.1%, 11.8% and 14.6%, for age groups < 15, 15-45, 46-59 and ≥ 60 years, respectively. While in Belgium, Germany, and Spain, levels of resistance to cefuroxime (second-generation cephalosporin) were 5.5%, 12.8%, and 16.6%, respectively (30), in this study cefuroxime showed a low resistance rate, similar to reports in the literature, and thus could be a treatment option for community-acquired UTIs in our region.

ESBL-positive isolates were more frequent the older the women, being more common in women over 60. The frequency of ESBL-producing isolates in the present study was 4.7%, which was lower than the 7.6% found by Abreu et al. in Northeast31 and 7.1% found by Gonçalves et al. in Central-Western Brazil.32 However, the rates were lower in the Southern (0.4%) and South 1.5% of the country.31-34

ESBL prevalence varies all over the world. A study carried out in Pakistan showed a prevalence of ESBL-production in 33% of E. coli isolated from community-acquired UTIs.35 Still, in Southern France, approximately 4% of E. coli isolates from community-acquired UTIs are ESBL producers.36 Prevalence of ESBL might change over time, as shown by Northwestern Memorial Hospital (Chicago, USA), where the percentage of ESBL-producing E. coli among community-onset urine isolates increased from 0.21% in 2003 to 2.99% in 2008, that is, a 14-fold increase within that period. Moreover, it was reported that CTX-M–producing E. coli accounted for the majority of ESBLs producers in that hospital.37

Our study has a few limitations. First, our data may not represent the real antimicrobial susceptibility profile of bacteria causing uncomplicated UTIs, because urine culture is not recommended at the first episode of uncomplicated UTI. Second, empirical treatment is based on a positive test strip (leukocytes+ or nitrites +) and clinical signs and symptoms. Information concerning patients’ clinical history, prior use of antimicrobials, recurrence of UTI and comorbidities was available. Third, fosfomycin was tested in isolates resistant to the three quinolones used in this study, but not in all isolates, since fosfomycin is expensive and unlike TMP-SMX, ciprofloxacin, norfloxacin, cephalothin, amoxicillin and nitrofurantoin, it is not offered free of charge by Public Health System.

In conclusion, our data show that TMP-SMX should not be considered as an option for first-line treatment of community-acquired UTIs in our region. Conversely, since nitrofurantoin and fosfomycin displayed the lowest resistance levels, they can be chosen as empirical antimicrobial treatment of uncomplicated UTIs. As antimicrobial resistance to quinolones increases with age, the treatment in older women should always be based on urine culture results. In addition, since resistance to the three quinolones tested in this work was 15.5%, empirical treatment for pyelonephritis should be avoided. Finally, stewardship is necessary for rational antimicrobial prescribing, in an attempt to decrease the selective pressure of resistance in our environment, as well as hospital costs related to hospitalization and patient deaths.

Acknowledgments

We thank Bill and Melinda Gates Foundation for the financial support. This Project is part of Grand Challenge Exploration – Brazil: New approaches to characterize the Global Burden of Antimicrobial Resistance.

References
[1]
SM Schappert, EA. Rechtsteiner.
Ambulatory medical care utilization estimates for 2007.
Vital Health Stat, 13 (2011), pp. 1-38
[2]
B. Foxman.
The epidemiology of urinary tract infection.
Nat Rev Urol, 7 (2010), pp. 653-660
[3]
CC. Johnson.
Definitions, classification, and clinical presentation of urinary tract infections.
Med Clin North Am, 75 (1991), pp. 241-252
[4]
G Córdoba, A Holm, F Hansen, AM Hammerum, L. Bjerrum.
Prevalence of antimicrobial resistant Escherichia coli from patients with suspected urinary tract infection in primary care, Denmark.
BMC Infect Dis, 17 (2017), pp. 670
[5]
DS Lee, S-J Lee, H-S. Choe.
Community-acquired urinary tract infection by Escherichia coli in the era of antibiotic resistance.
BioMed Res Int, 2018 (2018), pp. 1-14
[6]
MA Cunha, GL Assunção, IM Medeiros, MR. Freitas.
Antibiotic resistance patterns of urinary tract infections in a Northeastern Brazilian Capital.
Rev Inst Med Trop Sao Paulo, 58 (2016), pp. 2
[7]
K Gupta, TM Hooon, KG Naber, B Wullt, R Colgan, LG Miller, et al.
International Clinical Practice Guidelines for the Treatment of Acute Uncomplicated Cystitis and Pyelonephritis in Women: A 2010 Update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases.
Clin Infect Dis, 52 (2011), pp. e103-e120
[8]
C-I Kang, J Kim, DW Park, B-N Kim, U-S Ha, S-J Lee, et al.
Clinical practice guidelines for the antibiotic treatment of community-acquired urinary tract infections.
Infect Chemother, 50 (2018), pp. 67
[9]
C Aypak, A Altunsoy, N. Düzgün.
Empiric antibiotic therapy in acute uncomplicated urinary tract infections and fluoroquinolone resistance: a prospective observational study.
Ann Clin Microbiol Antimicrob, 8 (2009), pp. 27
[10]
CH Kung, WW Ku, CH Lee, CP Fung, SC Kuo, TL Chen, YT. Lee.
Epidemiology and risk factors of community-onset urinary tract infection caused by extended-spectrum β-lactamase-producing Enterobacteriaceae in a medical center in Taiwan: a prospective cohort study.
J Microbiol Immunol Infect, 48 (2015), pp. 168-174
[11]
JL Rocha, FF Tuon, JR. Johnson.
Sex, drugs, bugs, and age: rational selection of empirical therapy for outpatient urinary tract infection in an era of extensive antimicrobial resistance.
Braz J Infect Dis, 16 (2012), pp. 115-121
[12]
SB Dubbs, SK. Sommerkamp.
Evaluation and management of urinary tract infection in the emergency department.
Emerg Med Clin North Am, 37 (2019), pp. 707-723
[13]
CE Reu, W Volanski, KC Prediger, G Picheth.
Fadel-Picheth CMT. Epidemiology of pathogens causing urinary tract infections in an urban community in southern Brazil.
Braz J Infect Dis, 22 (2018), pp. 505-507
[14]
S Prasada, A Bhat, S Bhat, S Shenoy Mulki, S Tulasidas.
Changing antibiotic susceptibility pattern in uropathogenic Escherichia coli over a period of 5 years in a tertiary care center.
Infect Drug Resist, 12 (2019), pp. 1439-1443
[15]
R Yamaji, J Rubin, E Thys, CR Friedman, LW. Riley.
Persistent pandemic lineages of uropathogenic Escherichia coli in a College Community from 1999 to 2017.
J Clin Microbiol, 56 (2018),
[16]
O Guneysel, E Suman, TC. Ozturk.
Trimethoprim-sulfamethoxazole resistance and fosfomycin susceptibility rates in uncomplicated urinary tract infections: Time to change the antimicrobial preferences.
Acta Clin Croat, 55 (2016), pp. 49-57
[17]
F Caron, T Galperine, C Flateau, R Azria, S Bonacorsi, F Bruyère, et al.
Practice guidelines for the management of adult community-acquired urinary tract infections.
Med Mal Infect, 48 (2018), pp. 327-358
[18]
AK Stuck, MG Täuber, M Schabel, T Lehmann, H Suter, K. Mühlemann.
Determinants of quinolone versus trimethoprim-sulfamethoxazole use for outpatient urinary tract infection.
Antimicrob Agents Chemother, 56 (2012), pp. 1359-1363
[19]
R Benko, M Matuz, Z Juhasz, J Bognar, R Bordas, G Soos, et al.
Treatment of cystitis by hungarian general practitioners: a prospective observational study.
Front Pharmacol, 10 (2019), pp. 1498
[20]
V Seija, V Fratchez, V Ventura, M Pintos, M. González.
Factores asociados al desarrollo de infección urinaria de origen comunitario causada por Escherichia coli resistente a fluoroquinolonas. [Risk factors for community-acquired urinary tract infection caused by fluoroquinolone resistant E. coli].
Rev Chilena Infectol, 31 (2014), pp. 400-405
[21]
M Kobayashi, DJ Shapiro, AL Hersh, GV Sanchez, LA. Hicks.
Outpatient antibiotic prescribing practices for uncomplicated urinary tract infection in women in the United States, 2002-2011.
Open Forum Infect Dis, 3 (2016), pp. ofw159
[22]
FDA Drug Safety Communication. FDA advises restricting fluoroquinolone antibiotic use for certain uncomplicated infections; warns about disabling side effects that can occur together. 2016.
[23]
K Cowart, M Worley, NE Rouby, K. Sando.
Evaluation of FDA boxed warning on prescribing patterns of fluoroquinolones for uncomplicated urinary tract infections.
Ann Pharmacother, 53 (2019), pp. 1192-1199
[24]
A Bratsman, K Mathias, R Laubscher, L Grigoryan, S. Rose.
Outpatient fluoroquinolone prescribing patterns before and after US FDA boxed warning.
Pharmacoepidemiol Drug Saf, 29 (2020), pp. 701-707
[25]
GV Sanchez, A Babiker, RN Master, T Luu, A Mathur, J. Bordon.
Antibiotic resistance among urinary isolates from female outpatients in the United States in 2003 and 2012.
Antimicrob Agents Chemother, 60 (2016), pp. 2680-2683
[26]
FY Ramírez-Castillo, AC Moreno-Flores, FJ Avelar-González, F Márquez-Díaz, J Harel, AL. Guerrero-Barrera.
An evaluation of multidrug-resistant Escherichia coli isolates in urinary tract infections from Aguascalientes, Mexico: cross-sectional study.
Ann Clin Microbiol Antimicrob, 17 (2018), pp. 34
[27]
B. Kot.
Antibiotic resistance among uropathogenic Escherichia coli.
Pol J Microbiol, 68 (2019), pp. 403-415
[28]
P Batra, AK Abrol, S Gupta, P Pushpan, R. Kumar.
Susceptibility pattern of oral antimicrobials in uncomplicated UTI: Does fosfomycin still stand effective?.
J Family Med Prim Care, 9 (2020), pp. 850-853
[29]
EB Hirsch, BR Raux, PC Zucchi, Y Kim, C McCoy, JE Kirby, et al.
Activity of fosfomycin and comparison of several susceptibility testing methods against contemporary urine isolates.
Int J Antimicrob Agents, 46 (2015), pp. 642-647
[30]
M Kresken, B Körber-Irrgang, DJ Biedenbach, N Batista, V Besard, R Cantón, et al.
Comparative in vitro activity of oral antimicrobial agents against Enterobacteriaceae from patients with community-acquired urinary tract infections in three European countries.
Clin Microbiol Infect, 22 (2016),
[31]
AG Abreu, SG Marques, V Monteiro-Neto, AG. Gonçalves.
Extended-spectrum β-lactamase-producing enterobacteriaceae in community-acquired urinary tract infections in São Luís, Brazil.
Braz J Microbiol, 44 (2013), pp. 469-471
[32]
LF Gonçalves, P de Oliveira Martins-Júnior, ABF de Melo, RCRM da Silva, V de Paulo Martins, A Pitondo-Silva, et al.
Multidrug resistance dissemination by extended-spectrum β-lactamase-producing Escherichia coli causing community-acquired urinary tract infection in the Central-Western Region.
Brazil. J Glob Antimicrob Resist., 6 (2016), pp. 1-4
[33]
LA Minarini, AC Gales, IC Palazzo, AL. Darini.
Prevalence of community-occurring extended spectrum beta-lactamase-producing Enterobacteriaceae in Brazil.
Curr Microbiol, 54 (2007), pp. 335-341
[34]
C Wollheim, IM Guerra, VD Conte, SP Hoffman, FJ Schreiner, AP Delamare, AL Barth, S Echeverrigaray, SO. Costa.
Nosocomial and community infections due to class A extended-spectrum β-lactamase (ESBLA)-producing Escherichia coli and Klebsiella spp. in southern Brazil.
Braz J Infect Dis, 15 (2011), pp. 138-143
[35]
S Fatima, IN Muhammad, S Usman, S Jamil, MN Khan, SI. Khan.
Incidence of multidrug resistance and extended-spectrum beta-lactamase expression in community-acquired urinary tract infection among different age groups of patients.
Indian J Pharmacol, 50 (2018), pp. 69-74
[36]
A Zucconi, J Courjon, C Maruéjouls, F Saintpère, N Degand, L Pandiani, et al.
Managing ESBL-producing Enterobacteriaceae-related urinary tract infection in primary care: a tool kit for general practitioners.
Eur J Clin Microbiol Infect Dis, 37 (2018), pp. 983-986
[37]
C Qi, V Pilla, JH Yu, K. Reed.
Changing prevalence of Escherichia coli with CTX-M-type extended-spectrum beta-lactamases in outpatient urinary E. coli between 2003 and 2008.
Diagn Microbiol Infect Dis, 67 (2010), pp. 87-91
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