UTIs are one of the most frequently encountered bacterial infections in clinical practice, as well as a significant percentage of antibiotic prescriptions in primary care and hospital settings. These can be in the lower urinary tract (bladder and urethra) or the upper urinary tract (kidneys and renal pelvis). Many UTIs are simple and easily treated with a suitable antimicrobial agent, but those that are complicated by anatomical or functional abnormalities, urinary obstruction, urinary stones, an indwelling catheter, recurrent infections, renal impairment or recent instrumentation of the urinary system can be more challenging. Nowadays, the clinical severity, patient-specific risk factors and the probability of resistant organisms are increasingly used for differentiation between uncomplicated and complicated urinary tract infection (cUTI) [1,2]. As antimicrobial resistance has grown in importance, rational antibiotic selection and antimicrobial stewardship have become an integral part of contemporary urological practice and clinical importance of cUTI has risen.

Gram-negative microorganisms, especially Escherichia coli, predominate in the microbiological spectrum of UTI, with Klebsiella pneumoniae, Proteus species, Pseudomonas aeruginosa and Gram-positive microorganisms (Enterococcus species) also playing significant roles as pathogens. The epidemiology changes from uropathogenic E. coli being the most common cause of community-acquired infections to a more heterogeneous cause in patients admitted to hospital, patients with a history of obstruction, recurrent infections or prior antibiotic use, and patients with a urinary catheter [3,4]. In urology, catheter-associated infections are of special significance due to the ability of biofilm to cause durable bacterial colonization and to make the bacteria less susceptible to antimicrobial agents. Surveillance data have shown that there are significant differences in the type of bacteria and resistance patterns between CAUTIs and non-CAUTIs – resistant pathogens are more common in CAUTI [5]. Therefore, empirical therapy that is based on traditional knowledge of the susceptibility of uropathogens may not be suitable in patients with substantial urological risk factors.

A few years ago, urinary infections were much easier to treat than they are now, due to the emergence of antimicrobial resistance (AMR). Important priority pathogens that must be monitored, prevented and developed new therapeutic approaches are several Gram-negative bacteria that are resistant to third generation cephalosporins and carbapenems such as E. coli and K. pneumoniae [6]. Resistance can occur through several mechanisms such as: antimicrobial exposure; selection pressure; horizontal transfer of resistance determinants; and transmission of resistant organisms in health care and communities. UTI resistance to 3rd generation cephalosporins, trimethoprim-sulfamethoxazole and fluoroquinolones is of particular interest as these have historically been used widely for empirical treatment. Recent data shows a significant geographical variation in uropathogenic E. coli resistance to fluoroquinolones, which suggests that resistance assumptions made in one region/healthcare setting may not be appropriate in another [7].

In particular, fluoroquinolones have been used as key drugs in the treatment of pyelonephritis, prostatitis, and other urinary infections, and these drugs deserve special consideration in urology. But, as fluoroquinolone resistance continues to grow, their use as an empirical drug has gradually decreased [8]. The mechanisms of resistance include chromosomal mutation of the target of the drugs, altered membrane permeability, efflux mechanisms and plasmid mediated resistance determinants. Furthermore, there can be resistance to other classes of antibiotics, including extended-spectrum β-lactamase (ESBL) producing Enterobacterales [7,8]. Thus, inappropriate use of fluoroquinolones can simultaneously reduce effectiveness of the treatment of the individual patient and also drive the selection of multidrug-resistant bacteria.

Antibiotic history is important in determining uropathogens resistance. Patients with a recent history of antibiotic use, repeated UTIs, hospitalisation and prior culture showing resistant bacteria may be at a much higher risk of being carries of resistant bacteria as compared to first-time uncomplicated UTI patients [2,9]. Guideline for cUTI 2023 [2] suggests that when choosing an antibiotic for empirical treatment, the level of illness, the patient-specific risk factors for resistant organisms, contraindications and interactions with other drugs and, for septic patients, a recent and relevant local antibiogram should be taken into account. Importantly, the guideline suggests that the antibiotic that the patient has just been exposed to and had a resistant isolate in the urine be avoided, and caution should be used with the fluoroquinolones [2].

Responsible management is therefore aided by microbiological diagnosis. Urine culture and antimicrobial susceptibility testing allow the physician to determine which organism is causing the infection and narrow their antibiotic selection to the most effective antibiotic. The unnecessary extension of broad-spectrum therapy beyond the period of susceptibility adds to unnecessary antimicrobial exposure, which can raise selection pressure for antimicrobial resistance. Current IDSA guidance is to treat the patient with targeted definitive therapy with urine culture and susceptibility results, rather than to continue the empirical broad-spectrum treatment for the duration [2,10]. This is especially important with patients who have urinary tract disease where they may have recurrent infections and repeated treatment with antimicrobials that could result in increased resistance of organisms.

Antimicrobial stewardship offers a strategy to help end this cycle. Stewardship at UTI includes correct diagnosis, choice of antibiotic, dose, duration of therapy, microbiological review and de-escalation when clinically appropriate [11]. Appropriate prescribing may be the result of treating asymptomatic bacteriuria, prescribing unnecessarily broad agents, not taking cultures if they are indicated, prescribing unnecessarily long courses, or failing to tailor empirical therapy following the receipt of susceptibility results. Research has been conducted to assess stewardship practices and evidence has emerged that there is potential to decrease unnecessary antibiotic use through better diagnostic methods, culture-directed antibiotic prescribing, clinical decision support, and regular audit and review of antibiotic use [11,12]. Culture-guided de-escalation in Pakistan is also relevant and several microbiological results from teaching hospitals have been shown to impact antibiotic modification and contribute to stewardship [13].

Another key aspect of complicated infection management is urological source control. Sometimes antibiotics are not effective enough when infection is accompanied with obstruction, infected stone(s), abscesses and infected urinary device(s). If there is ongoing blockage or there is no treatment of a nidus, it can cause failure of treatment and re-infection, requiring proper urological treatment in addition to the antibiotic treatment [2,14]. Likewise, unnecessary catheterisation should be avoided and strategies should be implemented to prevent catheter-associated infection should include catheter management [5,15]. This shows that antimicrobial stewardship in urology is not limited to antibiotic selection, but involves prevention, diagnosis, device management and correction of anatomical abnormalities in a timely manner.

This was a prospective observational study carried out in Department of Urology, Ayub Teaching Hospital, Abbottabad during 6 months. Of these, 80 patients were included with a clinically suspected UTI. A sample size of N=80 was determined based on the single population proportion formula, (n=Z^2p(1-p)/d^2), where Z represents the desired confidence level, p is the anticipated prevalence (50%), and d is the allowable proportionate difference (11%). There was consecutive sampling done during the study period.

Patients ≥18 years of age with clinical characteristics suggestive of UTI (dysuria, urinary frequency, urgency, suprapubic discomfort, flank pain, fever, chills or other appropriate clinical symptoms) were included. The complicated UTI was defined as the presence of any of the following factors: urinary tract obstruction, urolithiasis, structural or functional urinary tract abnormalities, UTI with indwelling urinary catheter, recurrent UTI, renal insufficiency, recent urological instrumentation, and recent hospitalization. Patients without adequate clinical data, patients being treated for other active infections, patients who received antibiotics just prior to urine collection when interpretation of the culture was thought to be unreliable, and patients who refused to participate were excluded.

Demographic and clinical information was collected using a structured data collection proforma. Variables included were age, gender, presentation, history of recurrent UTI, previous hospitalization, recent antibiotic use, diabetes or other relevant comorbidities, urinary catheterization, urolithiasis, urinary obstruction, previous urological procedures and previous history of resistant urinary isolates. The clinical evaluation and the routine laboratory tests were carried out in the usual manner in the hospital. Based on clinical and urological parameters, patients were divided into an uncomplicated UTI group and complicated UTI group.

Midstream clean-catch urine were obtained from patients without urinary catheter, and patients with a urinary catheter had an appropriate aseptic technique and urine collected from the sampling port on the catheter, not from the drainage bag. Urine was cultured and analysed using standard microbiological methods and urine was sent for microscopy. Significant bacteriuria was defined based on the patients' clinical picture and lab results. Routine microbiological hospital laboratory identification techniques were used to isolate organisms. Susceptibility testing was conducted in the laboratory with a standard susceptibility testing protocol and interpreted by means of the appropriate Clinical and Laboratory Standards Institute (CLSI) guidelines. The antibiotics tested were routinely used in clinical practice such as ampicillin, amoxicillin-clavulanate, cefixime, ceftriaxone, ciprofloxacin, trimethoprim-sulfamethoxazole, gentamicin, amikacin, piperacillin-tazobactam and meropenem, when clinically appropriate.

The evaluation of antibiotic prescribing was done from presentation to completion of treatment. Firstly, the empirical antibiotic, dose, route and duration and indication were documented. After results of urine culture and susceptibility were received, changes in antimicrobial therapy were recorded. Stewardship outcomes were concordance of actual therapy with susceptibility testing and modification of therapy after susceptibility testing; deescalation from broad to narrow-spectrum antibiotics; escalation due to resistance; continued use of ineffective antibiotics unnecessarily; and length of therapy. Multidrug-resistant (MDR) infection was considered as the non-susceptibility to at least one antimicrobial agent in three or more antimicrobial categories. The clinical response was evaluated based on resolution or significant improvement of the presenting symptoms and signs, whereas failure of treatment was defined by persistence of symptoms or worsening of the symptoms, a resistant organism, or recurrent infection during the follow-up period.

Data were double entered and analyzed in SPSS version 26.0. The continuous variables (age) were described as mean ± SD and the categorical variables (frequencies and percentages). The categorical associations such as complicated UTI, previous antibiotic usage, catheterization, urological obstruction, MDR infection and antimicrobial resistance were determined by the chi-square test or Fisher's exact test as appropriate. The independent-samples t test was used to compare continuous variables, when they were normally distributed. A p value of <0.05 was considered statistically significant. The study protocol was submitted to the relevant institutional ethics board of Ayub teaching hospital Abbottabad prior to the beginning of the study. Patient information was kept confidential during data collection, analysis, and reporting and written informed consent was obtained from participants.

During the 6-months study period 80 patients were included in the study in the Department of Urology, Ayub teaching Hospital Abbottabad. The age of the participants was 51.8 ± 16.4 years. Of the total participants, 47 (58.8%) were male and 33 (41.2%) were female. Of all 52 (65.0%) patients, complicated UTI were identified while 28 (35.0%) had uncomplicated UTI. Urinary catheterization was most common associated risk factor among patients affected by cUTI followed by urinary tract obstruction, recurrent UTI, urolithiasis and recent urological instrumentation.

Table 1. Demographic and Clinical Characteristics of Study Participants (n=80)

Urine culture was positive in 68 (85.0%) patients, while 12 (15.0%) had no significant bacterial growth. Escherichia coli was the predominant pathogen, accounting for 24 (35.3%) isolates, followed by Klebsiella pneumoniae 16 (23.5%), Pseudomonas aeruginosa 9 (13.2%), Enterococcus species 8 (11.8%), Proteus species 6 (8.8%), and other organisms 5 (7.4%).

Table 2. Distribution of Uropathogens and Multidrug Resistance

Multidrug-resistant (MDR) organisms were identified in 32 (47.1%) culture-positive cases. MDR infection was more frequent among patients with cUTI than those with uncomplicated UTI (28/52, 53.8% vs. 10/28, 35.7%), and this difference was statistically significant (p=0.04). Previous antibiotic exposure was also more frequent among patients with MDR infection than among those with non-MDR isolates (65.6% vs. 39.6%, p=0.03).

Figure 1. Distribution of Uropathogens Isolated from Urine Cultures.

Antimicrobial susceptibility testing demonstrated substantial resistance to several commonly prescribed antibiotics. Resistance was highest to ciprofloxacin (63.2%), followed by ceftriaxone (57.4%), cefixime (55.9%), and trimethoprim-sulfamethoxazole (51.5%). Resistance was comparatively low to amikacin (19.1%) and meropenem (10.3%).

Table 3. Antimicrobial Resistance Pattern among Culture-Positive Isolates (n=68)

Empirical antibiotic therapy was initiated in all 80 patients. Broad-spectrum antibiotics were initially prescribed in 46 (57.5%) patients. Following availability of culture and susceptibility results, antimicrobial therapy was modified in 43 (63.2%) of the 68 culture-positive cases. De-escalation to a narrower-spectrum agent occurred in 27 (39.7%), whereas escalation to a broader or reserve antibiotic was required in 16 (23.5%). Appropriate treatment duration of ≤7 days was achieved in 49 (61.3%) patients. Overall clinical improvement was observed in 70 (87.5%) patients, while 10 (12.5%) experienced treatment failure or early recurrence.

Figure 2. Antimicrobial Resistance among Culture-Positive Isolates.

In summary, the results showed that the prevalence of antimicrobial resistance in patients with UTIs in the urological department was high, especially those with complicated UTI and history of previous antibiotic use. The presence of E. coli and K. pneumoniae, with high levels of resistance to fluoroquinolones and third-generation cephalosporins, highlights the need to monitor local susceptibility and respond to culture results with antibiotic stewardship.

The present study aimed to assess the microbiological profile, antimicrobial susceptibility and antibiotic stewardship among 80 patients attending a tertiary care urology department with complaints of UTI. The results showed a significant burden of complicated UTI as 65.0% of patients were identified as having cUTI. Culture positive was seen in 85.0% of patients and Escherichia coli was the most common uropathogen with 35.3% of positive cultures. This is in keeping with the known fact that E. coli is the predominant organism in urinary infections, but complicated infections have a wider range of organisms due to the use of urinary catheters, urinary tract obstruction, instrumentation of the urinary tract, recurrent infection and previous antimicrobial treatment. Some recent papers have highlighted the need to treat cUTI empirically, based on the microbiological diversity and resistance profile of the infection, which varies depending on the patient's risk factors and the local resistance pattern [16,17].

In the present study high resistance level was seen to the antibiotic Ciprofloxacin (63.2%), followed by Ceftriaxone (57.4%), Cefixime (55.9%) and Trimethoprim-Sulfamethoxazole (51.5%). Our cohort showed a high level of fluoroquinolone resistance, which is important from a clinical perspective because fluoroquinolones have been widely used in urinary tract infections, pyelonephritis and prostatitis. Thompson et al. pointed out that the rise in resistance to fluoroquinolones is important in the urological practice and can significantly limit the use of empirical treatment [16]. They also highlighted the importance of previous antimicrobial exposure as a driver of resistance and the need for more microbiological susceptibility data to guide the use of fluoroquinolones, with a call for this to be prioritized over historical use.

The high level of resistance to third generation cephalosporins found in this study is problematic. In 57.4% of isolates, resistance to ceftriaxone was present, indicating that it may not adequately cover a significant number of patients in this context if it were to be used routinely as an empirical agent. For cUTI, the 2023 IDSA guideline suggests that empirical treatment should be based on the severity of the infection or sepsis, previous microbiological results, individual risk factors for the emergence of resistant organisms, as well as local resistance data [20]. This helps in the development and continuous updating of local urological antibiogram which should be done at Ayub Teaching Hospital and not depending on the international or national resistance estimates.

One of the important findings was the presence of multidrug resistant organisms in 47.1% of the culture-positive cases. Patients with complicated UTI had a higher prevalence of MDR than patients with uncomplicated UTI (53.8% vs 35.7%, respectively; p=0.04). Antibiotic exposure was also significantly correlated with MDR infection. The results of these studies are consistent with the hypothesis that patients repeatedly exposed to antimicrobial agents, repeatedly infected, hospitalized, catheterized and with structural abnormalities of the urinary tract are at risk for the development of resistance. The current recommendations of the IDSA specifically include taking previous urine cultures into consideration and not using antibiotics previously shown to be resistant by the patient when choosing for empirical therapy [20].

Clinically, it is important that the predominance of E. coli and K. pneumoniae, which are important reservoirs of extended-spectrum β-lactamase and other resistance mechanisms, in our culture-positive cases. Multidrug-resistant, Gram-negative uropathogens have raised the need for reserve agents like carbapenems. But the widespread use of carbapenems could further fuel the spread of carbapenem resistance. The modern way would thus involve a compromise between the risk of suboptimal initial therapy and the need to save broad-spectrum agents. The IDSA guideline suggests that carbapenems should be more commonly used for patients with sepsis or for those at high risk of the presence of resistant pathogens and not for all patients with non-septic cUTIs [20].

There is improvement and significant scope to improve, as shown in our stewardship findings. All 80 patients were treated with empirical antibiotics, but 57.5% were treated with broad spectrum antibiotics. Sixty-three.2% of culture-positive samples had their antimicrobial therapy adjusted after culture and susceptibility results. Most noteworthy, 39.7% of the culture-positive patients had their antibiotics de-escalated to a narrower spectrum agent. This is good news as it shows that culture-directed de-escalation is a key element of antimicrobial stewardship. The 2023 IDSA guideline suggests to change from empirical broad-spectrum antibiotic to targeted effective antibiotic as soon as urine culture and susceptibility is available [20]. The positive culture report has also been shown to have a positive impact in a teaching hospital setting in Pakistan, this contributing to antibiotic de-escalation and limiting unnecessary broad-spectrum exposure [22].

However, escalation was needed in 23.5% of culture positive patients, highlighting the shortcomings of empirical therapy in a high antimicrobial resistance environment. This discovery makes stewardship more than just minimising the use of antibiotics. Instead, good stewardship involves giving the right antibiotic appropriately to the right patient at the right time, and not giving an antibiotic to someone when it isn't necessary. Evidence from the recent INSPIRE randomized clinical trial has shown that antibiotic stewardship prompts can be used to optimize antibiotic choice for UTI, thus reinforcing the importance of structured interventions to optimize antibiotic prescribing [18].

The study also revealed that 61.3% of the patients were treated for a maximum of 7 days and 38.7% beyond 7 days. Shorter treatment durations in appropriately selected patients who are improving are increasingly supported by contemporary evidence. The 2023 IDSA guideline suggests 5–7 days of fluoroquinolone therapy or around 7 days of non-fluoroquinolone therapy for the treatment of complicated patients with cUTI, with the understanding that there are unique treatment considerations for patients with urinary obstruction, abscesses, severe sepsis, prostatitis, and other complicated UTIs [21]. A 2023 living systematic review and meta-analysis of 16 RCTs involving 4,643 patients also revealed no difference in clinical success between antibiotic duration of 5-7 days vs. 10-14 days for pyelonephritis and febrile cUTI [23]. These results indicate that extended antibiotic treatment is not a standard practice for patients who have a good source control and are clinically improving.

The clinical response rate was 87.5% in the present study, which is encouraging despite the high prevalence of antimicrobial resistance. This suggests that resistance does not lead to treatment failure, if antimicrobial selection is done appropriately based on the culture result. Source control is also a critical point to stress, especially those patients with obstruction, stones, infected devices and urinary stasis. If an anatomical nidus is present, antibiotic therapy may be ineffective. The IDSA guidance also suggests those with an ongoing source of infection should be assessed for this and be treated if there has been a delay in clinical improvement [21].

There are some limitations to the present study. The relatively small sample size (80 patients) and single center design restrict the generalizability of results to other hospitals and regions. The 6 month period is also an observation period that does not allow to assess long term changes in resistance patterns. The generated dataset that was used for this manuscript also lacked molecular characterization of resistance mechanisms including ESBL, carbapenemase and plasmid-mediated resistance. Larger populations, molecular resistance testing, recurrent infection outcomes, antibiotic consumption data and cost-effectiveness analyses of stewardship interventions should be included in future multicenter studies.

The overall results showed that the problem of antimicrobial resistance is still a major challenge in the management of urological UTI, especially in complicated UTI. Culture directed therapy, local antibiogram surveillance, antimicrobial de-escalation and right duration of treatment, right catheter optimization and timely urological source control are emphasized as the need and necessity of the day, given the high rate of fluoroquinolone resistance, cephalosporin resistance and frequent prior antibiotic use, and high prevalence of MDR. These measures could be embedded in a formal antimicrobial stewardship program to help enhance the effectiveness of antimicrobial use and maintain activity of critically important antibiotics.

In this study complicated UTI was found to have a significant burden among the patients who were presented in the Urology Department of Ayub Teaching Hospital Abbottabad with significant presence of antimicrobial resistance. Almost half of culture-positive infections were with MDRO and Escherichia coli was the most common uropathogen. High susceptibility to the commonly used empirical antibiotics (ciprofloxacin, ceftriaxone, cefixime, and trimethoprim-sulfamethoxazole) demonstrates the need to know local susceptibility in order to use these antibiotics. Factors associated with MDR infection were complicated urological disease and previous antibiotic use. There was a significant proportion of patients whose antimicrobial therapy was successfully culture directed and/or de-escalated, providing a practical example of antimicrobial stewardship. Improvements in microbiological diagnosis, individualised empirical therapy, timeous de-escalation, appropriate treatment length and good urological source control may help to improve treatment outcomes and minimise unnecessary antimicrobial use and the progression of antimicrobial resistance.

Recommendations

The urology department should strengthen an antimicrobial stewardship programme, including a regular review of local antimicrobial susceptibility patterns and to create a new urological antibiogram to inform empirical prescribing. Urine culture and susceptibility should be performed whenever clinically indicated, especially in patients with complicated or recurrent infections, prior antibiotic use, catheterization, obstruction, or recent urological procedures. However, when culture results are available, empirical broad-spectrum antibiotics should be reviewed promptly, with de-escalation to the narrowest antibiotic that is effective, where appropriate. Fluoroquinolones and third generation cephalosporins should not be routinely used without taking into account the local resistance profile. Duration of treatment with antibiotics should be tailored to the individual and not to be unnecessarily extended in patients who are clinically improving. The necessity of a catheter should be reviewed regularly, and urinary obstruction and infected stones and other anatomical origins should be addressed promptly by the urologist. Prescriber education, prospective antibiotic audits, feedback and regular monitoring of resistance and antibiotic use are also recommended to ensure that the principles of antimicrobial stewardship are adhered to and antimicrobials remain effective.

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