Prevalence and antimicrobial susceptibility of uropathogens isolated from ambulatorial and nosocomial infections at Nova Friburgo, Rio de Janeiro, Brazil

Prevalência e susceptibilidade antimicrobiana de uropatógenos isolados de infecções ambulatoriais e nosocomiais em Nova Friburgo, Rio de Janeiro, Brasil

Prevalencia y susceptibilidad antimicrobiana de uropatógenos aislados de infecciones ambulatorias y nosocomiales en Nova Friburgo, Rio de Janeiro, Brasil

This work is licensed under Creative Commons Attribution 4.0 International.

Urinary tract infection (UTI) is among the most common infectious diseases of humans and is the most common nosocomial infection in the developed world. The health care costs to treat UTI are approximately US$3.5 billion per year in the United States alone. Moreover, complications caused by frequent antimicrobial use, such as high-level antibiotic resistance, have brought worries.^1,2

UTIs are defined as the microbial colonization and tissue invasion of any part of the urinary tract, from the urethra to the kidneys.³ The frequency of the microorganisms involved in a UTI diagnosis depends on the place where the infection was acquired. For example, it will differ if the infections are intra or extra-nosocomial and it also differs for each hospital environment.⁴

The majority of these infections are caused by Enterobacteriaceae, mainly Escherichia coli which isolation rate varies from 70% to 90% from acute outpatient UTIs and 50% from hospital-acquired UTIs.⁵

The bacteria may infect the urethra and migrate to the kidney or prostate.⁶ Clinical conditions such as immunosuppression, surgical manipulations, urinary tract malformations, and catheters may predispose patients to nosocomial infection by microorganisms that, usually, are not uropathogenic.⁷

The global dissemination of drug-resistant organisms is troublesome for medical practitioners because it decreases the available options for appropriate treatment. This contributes to increased patient morbidity and mortality. The global spread of drug resistance was recently recognized as a major threat to human health.⁸For E. coli, the high reported resistance to fluoroquinolones means limitations to available oral treatment for conditions which are common in the community, such as urinary tract infections.⁹

Thus, this study aimed to investigate the prevalence and antimicrobial susceptibility of bacteria associated to UTI of out- and nosocominal patients examined and/or treated in a hospital at Nova Friburgo, Rio de Janeiro, Brazil.

This was a retrospective cross-sectional study conducted by collecting previously recorded data about UTIs microbiological cultures and antimicrobial susceptibility tests realized at the clinical laboratory of Casa de Saúde São Lucas, a private hospital in Nova Friburgo, Rio de Janeiro, Brazil.

The study and data access was authorized by the hospital Laboratory Technical Director, following the ethical principles described at Resolution No. 196/96 of the National Health Council/Ministry of Health of Brazil.

Outpatient urine cultures data were collected from November 2013 to May 2014 while hospitalized patients data were collected in two different periods, from July 2010 to November 2012 and July 2013 to June 2014.

All microorganisms were previously identified following techniques described by KONEMAN et al. (2008).¹⁰ Sensitivity testing was performed by disk diffusion method according to the CLSI (Clinical and Laboratory Standards Institute, 2010).¹¹ The data was analyzed and the results expressed as percentage.

A total of 2223 urine culture data were investigated. From the total, 1592 (71.61%) were from outpatients and 631 (28.39%) were from nosocomial patients.

From 1592 urine cultures from outpatients, 317 were positive (11.37%), while in the hospital setting, from the total of 613 urine samples, 136 (21.55%) were positive.

Females were more affected in both nosocomial (67.65%) and ambulatorial (89.50%) settings (Table 1).The age group of outpatients with positive cultures ranged from 0 to 92 years old. The overall prevalence was found in 13 to 40 year-olds, which comprised 45.86% of the cases (Table 1).

In the outpatient setting, the most prevalent bacteria was E. coli (76.50%), followed by Enterobacter sp. (12.02%) and Proteus sp. (5.46%). In nosocomial UTIs, the most prevalent microorganism was E. coli (65.96%), followed by Proteus sp. (7.80%) and Pseudomonas sp. (7.09%) (Table 2).

Table 1
Positivity of Urine Culture According to gender and age of outpatients.

Table 2
Microorganisms isolated from out- and nosocomial patients at Nova Friburgo, RJ, Brazil.

Antimicrobial susceptibility test results of the 3 most prevalent bacteria isolated from outpatients are shown at Table 3. E. coli isolates showed resistance to most of antibiotic tested, such as ampicillin (45.00%), nalidixic acid (37.14%), nitrofurantoin (35.71%), and pipemidic acid (32.86%). Enterobacter sp. isolates were resistant to ampicillin (95.45%), cephalexin and nitrofurantoin (77.27%). Proteus sp. showed resistance to nitrofurantoin (100%), ampicillin (90%) and trimethoprim/sulfamethoxazole (40%) (Table 3).

Table 3
Resistance profile of uropathogens isolated from outpatient samples in Nova Friburgo, from November 2013 to May 2014.

Antimicrobial susceptibility test results of the 3 most prevalent bacteria isolated from nosocomial patients are shown at Table 4. E. coli was again resistant to most of antibiotic tested, including ampicillin (56.69%), cephalothin, trimethoprim/sulfamethoxazole (43.01%), and ciprofloxacin (33.33%). Proteus sp. was resistant to ampicillin (72.73%), amoxicillin/clavulanic acid, cephalothin and trimethoprim/sulfamethoxazole (54.55%). Pseudomonas sp. showed resistance to trimethoprim/sulfamethoxazole (90%), cephalothin, nitrofurantoin (70%) and amoxicillin/clavulanic acid (60%) (Table 4).

Table 4
Resistance profile of uropathogens isolated in samples of hospitalized patients in Nova Friburgo, in the period of July 2010 to November 2012 and July 2013 to June 2014.

NT: not tested.

When the UTI is acquired in the hospital, the etiologic agents are quite diverse, composed predominantly Enterobacteriaceae, usually but not always E. coli, followed by Proteus sp., Pseudomonas sp., Klebsiella sp., Enterobacter sp., Enterococcus sp., and fungi, especially Candida sp.^12,13 In UTIs acquired in communities, Escherichia coli predominate, being isolated in 70% to 85% of cases. In our study, E. coli was the most prevalent microorganism isolated in both community and hospital UTIs, and showed considerable resistance against most of antibiotics used to treat UTIs.

Our results demonstrated that females (13-40 years old) are more susceptible to UTIs, corroborating with the literature. ^14,15E. coli from the outpatient samples were considerably resistant to nitrofurantoin. Recent international guidelines for the treatment of uncomplicated cystitis explicitly recognize the ecologic adverse effects of antimicrobial agents as an important factor for therapeutic choices.¹⁶ Although these guidelines recommend avoiding fluoroquinolones, such as ciprofloxacin, they remain indicating agents such as nitrofurantoin, which has shown resistance.¹⁷

Enterobacter sp. was resistant to most antimicrobial agents, and showed susceptibility only to gentamicin, quinolones, and ceftriaxone.

Proteus sp. showed resistance to ampicillin, cephalexin, trimethoprim - sulfamethoxazole and nalidixic acid, being susceptible to other antimicrobials.

All microorganisms isolated from outpatients in this work showed good sensitivity to antibiotics less frequently used in community UTI, such as second and third generation of cephalosporins (cefoxitin, ceftriaxone) and aminoglycosides (gentamicin).

At this work, bacteria isolated from nosocomial infections were more resistant to antimicrobials than microorganisms isolated from community infections. E. coli was 52.69% resistant to ampicillin and 43.01% to trimethoprim/sulfamethoxazole. More than 30% of E. coli isolates were resistant to ciprofloxacin, and even greater indices have been reported.¹⁸

These antimicrobials were widely used, and their indiscriminate use and self-medication can have caused the increase of resistance.¹⁹ The development of antimicrobial resistance among gram-negative pathogens has been progressive and is increasing in bacteria isolated from both nosocomial and community-acquired UTI.²⁰Contributing factors are the extensive use of antibiotics, both in human beings and animals, poor infection control, and the greatly increased global mobility of people, allowing the rapid spread of multidrug-resistant pathogens.²¹

Our data demonstrated that about a third of the strains isolated in the nosocomial environment were resistant to ciprofloxacin. Previous use of this antimicrobial can have induced resistance in these strains.

The use of ciprofloxacin as a first empirical treatment option for treatment of UTI is questionable, since this would select more resistant strains at the community setting and then, would be ineffective in the hospitals of the region where the our study was conducted.

Pathogens of particular concern include extended-spectrum β-lactamase–producing Enterobacteriaceae (ESBL), carbapenem-resistant Enterobacteriaceae (CRE), and multidrug-resistant Pseudomonas aeruginosa. Classic agents used to treat these pathogens have become outdated. Of the few new drugs available, many have already become targets for bacterial mechanisms of resistance.²²

Beta-lactamases are bacterial β-lactams enzymes that inactivate by hydrolysis, resulting in inefficiency of antibiotics. An ESBL group is able to hydrolyze and cause resistance for a large variety of new β-lactams, including third generation cephalosporins and monobactams, but not against cephamycins and carbapenems. ESBLs producing bacteria are common in hospitalized patients, but have also been reported in positive cases of community-acquired infections.²³

Treatment of these multiple drug resistant organisms is a deep scientific concern. At the level of a wider geographic scale, the incidence of ESBL-producing organisms is difficult to resolve due to various reasons, difficulty in detecting ESBL production and inconsistencies in reporting.²⁴

In our study, ceftriaxone and carbapenems offered the best antimicrobial activity for outpatient strains, and the associate antimicrobials piperacillin/tazobactam and ampicillin/sulbactam were most effective for nosocomial strains.

Until then, there are not regional studies published on the prevalence and antimicrobial susceptibility. These data are important for the surveillance of infections and to help in the clinical treatment.

Our data shows the importance of the study of prevalence and antimicrobial susceptible profiles of bacterial isolates at regional level. Thus, these results may contribute to better selection of antimicrobial for therapy of both hospital and ambulatorial-acquired UTIs in our community.

We offer our deepest thanks to Casa de Saúde São Lucas, especially to Dr. Glauber Cunha that provided support for the development of this study.