Epidemiology and antimicrobial resistance of Enterobacteriaceae causing community-acquired urinary tract infections in Tétouan, Morocco (2022–2023)

Laila Farouk; Ayoub Ez-Zari; Lahcen Ouchari; Zine El Abidine Bzazou EL Ouazzani; Zakaria Mennane; Noureddine El Mtili

doi:10.1371/journal.pone.0347958

Abstract

Background

Urinary tract infections (UTIs) are among the most common community-acquired bacterial infections and Enterobacteriaceae are the leading etiological agents. Rising antimicrobial resistance (AMR) within this family poses major challenges for empirical treatment. This study aimed to describe the species distribution and antimicrobial resistance patterns of uropathogenic Enterobacteriaceae isolated from outpatients in Tétouan, Morocco.

Methods

A cross-sectional descriptive study was conducted between April 2022 and December 2023 in three medical laboratories. Enterobacteriaceae isolated from urine cultures with significant bacteriuria were identified using the VITEK®2 system. Antimicrobial susceptibility testing was performed according to EUCAST 2021 guidelines. Extended-spectrum β-lactamase (ESBL) production was assessed using the Modified Double Disc Synergy Test (MDDST). Statistical analyses were performed using SPSS version 26, with significance set at p < 0.05.

Results

A total of 422 Enterobacteriaceae isolates were obtained, predominantly from female patients (74.9%). Escherichia coli was the most frequent species (83.4%), followed by Klebsiella pneumoniae (9.2%). High resistance rates were observed for ampicillin (60.9%) and ticarcillin (56.2%), while resistance to imipenem (1.2%) and ertapenem (0.9%) remained low. ESBL production was detected in 20 isolates (4.7%), with E. coli being the predominant ESBL-producing species (16/20; 80.0%), while K. pneumoniae exhibited a higher species-specific prevalence (4/39; 10.3%). Male patients exhibited significantly higher resistance to several β-lactams, while pediatric patients showed higher resistance to cephalosporins and aminoglycosides.

Conclusion

Uropathogenic Enterobacteriaceae circulating in the community of Tétouan exhibit substantial resistance to commonly prescribed oral antibiotics, although carbapenems remain highly effective. The moderate prevalence of ESBL-producing strains highlights the need for reinforced antimicrobial stewardship and continuous regional surveillance to guide empirical treatment and limit the spread of resistant pathogens.

Citation: Farouk L, Ez-Zari A, Ouchari L, Bzazou EL Ouazzani ZEA, Mennane Z, El Mtili N (2026) Epidemiology and antimicrobial resistance of Enterobacteriaceae causing community-acquired urinary tract infections in Tétouan, Morocco (2022–2023). PLoS One 21(4): e0347958. https://doi.org/10.1371/journal.pone.0347958

Editor: Dwij Raj Bhatta, Tribhuvan University, NEPAL

Received: November 18, 2025; Accepted: April 9, 2026; Published: April 28, 2026

Copyright: © 2026 Farouk et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Urinary tract infections (UTIs) are among the most common bacterial infections globally, affecting both community and hospitalized populations and contributing to substantial morbidity and healthcare expenditure. Each year, an estimated 150 million individuals experience a UTI, underscoring the significant global burden of this condition [1–3]. UTIs occur when pathogenic microorganisms colonize and proliferate within the urinary tract, triggering an inflammatory response [2]. Clinically, UTIs are typically classified into uncomplicated infections—affecting otherwise healthy individuals with no urinary tract abnormalities—and complicated infections, which occur in the presence of structural or functional impairments, such as obstruction or renal dysfunction [4,5].

A wide range of microorganisms can cause UTIs, including Gram-negative and Gram-positive bacteria, fungi, and viruses. Nevertheless, members of the Enterobacteriaceae family—particularly Escherichia coli (E. coli), Klebsiella pneumonia (K. pneumonia), and Proteus mirabilis (P. mirabilis)—account for the majority of community- and hospital-acquired infections [6]. Effective management requires rapid identification of the causative pathogen and determination of its antimicrobial susceptibility profile. However, the inappropriate and excessive use of antibiotics has accelerated the emergence and dissemination of antimicrobial resistance (AMR), posing major challenges for empirical treatment and public health [7].

In response to the global rise in AMR, the World Health Organization (WHO) launched the Global Antimicrobial Resistance Surveillance System (GLASS) in 2015 to harmonize national reporting and enhance the comparability of resistance data across countries [8]. Morocco joined GLASS in 2018 and subsequently established a national coordination unit and technical committee to strengthen AMR surveillance [9]. Despite these national efforts, to our knowledge, published data on uropathogenic Enterobacteriaceae resistance in Morocco remain largely limited to a few urban centers, with northern regions, including Tétouan Province, particularly understudied. The lack of updated regional evidence limits the ability of clinicians to tailor empirical therapy and restricts the development of context-appropriate stewardship strategies.

To our knowledge, no published study has specifically characterized the epidemiology and antimicrobial resistance of community-acquired uropathogenic Enterobacteriaceae in Tétouan Province. Generating region-specific data is essential to support national surveillance initiatives, guide empirical treatment choices, and contribute to AMR containment strategies.

Therefore, the present study aimed to characterize the species distribution and antimicrobial resistance profiles of community-acquired uropathogenic Enterobacteriaceae in Tétouan, Morocco, in order to provide region-specific evidence to inform clinical practice and support national AMR surveillance efforts.

Materials and methods

Ethical approval and participant consent

This study was conducted in accordance with ethical standards for research involving human participants. The study protocol was reviewed and approved by the Institutional Review Board (IRB) of the Hospital–University Ethics Committee of Tangier (CEHUT) (IRB No.: AC111JV/2-025), issued on 23 January 2022. The IRB waived the requirement for informed consent because this was a study based on routinely collected diagnostic samples and medical records. No written or verbal informed consent was obtained, as the ethics committee determined that consent was not required. All patient data were fully anonymized prior to access by the investigators and were used exclusively for research purposes. The study did not involve direct contact with patients.

Study design and setting

A cross-sectional descriptive study was conducted between April 1, 2022, and December 31, 2023, in three clinical microbiology laboratories in Tétouan, Morocco, representing the three largest private medical laboratories located in the city center. Urine specimens were submitted for routine cyto-bacteriological examination of urine (ECBU) by attending physicians in outpatient settings, independently of this study. All consecutive positive cultures yielding Enterobacteriaceae from the three participating laboratories were eligible for inclusion, irrespective of patient demographics or clinical presentation. This study did not interfere with routine diagnostic procedures.

Significant bacteriuria was defined as ≥10⁵ colony-forming units (CFU)/mL, in accordance with established diagnostic guidelines [10]. Cultures were performed on chromogenic agar and blood agar plates. Positive cultures yielding Enterobacteriaceae were subcultured to ensure purity and preserved at −80 °C in glycerol broth until further identification and antimicrobial susceptibility testing.

Tétouan Province, located in Morocco’s northwestern Mediterranean zone, encompasses approximately 2,541 km² and had 573,784 inhabitants according to the 2019 provincial monograph [11].

Inclusion and exclusion criteria

All Enterobacteriaceae isolates obtained from positive community-acquired urine cultures were included in the study. Duplicate isolates from the same patient with the same bacterial species were excluded to ensure each patient contributed only one isolate per episode of bacteriuria. Polymicrobial urine cultures and positive cultures for unidentified germs were also excluded.

Identification and antimicrobial susceptibility testing

Identification of bacterial isolates was performed using the automated VITEK^® 2 microbiology system (Biomerieux, France), employing the Gram-negative (GN) colorimetric reagent cards.

Antimicrobial susceptibility testing (AST) was conducted using the VITEK^®2 GN AST-N233 card (Biomerieux, France). Results were interpreted according to the European Committee on Antimicrobial Susceptibility Testing (EUCAST) 2021 guidelines. Quality control was ensured using Escherichia coli ATCC 25922 as a reference strain. The VITEK^®2 system categorized isolates as susceptible, intermediate, or resistant; intermediate isolates were grouped with the resistant category for analytical purposes.

The antimicrobial agents tested against the Enterobacteriaceae isolates included (with tested concentrations in µg/mL): ampicillin (4, 8, 32), amoxicillin–clavulanic acid (4/2, 8/4, 16/8), ticarcillin (16, 32, 64), cefoxitin (8, 16, 32), cefotaxime (1, 4, 16, 32), ceftriaxone (1, 4, 16, 32), ceftazidime (1, 2, 8, 32), imipenem (1, 2, 6, 12), ertapenem (0.5, 2, 4), amikacin (8, 16, 64), gentamicin (4, 16, 32), tobramycin (8, 16, 64), ciprofloxacin (0.5, 2, 4), and trimethoprim-sulfamethoxazole (1/19, 4/76, 16/304). Isolates exhibiting resistance to at least three distinct classes of antibiotics were classified as multidrug-resistant (MDR) [12].

Detection of extended spectrum beta-lactamase production

Extended-spectrum β-lactamase (ESBL) production was detected using the Modified Double Disc Synergy Test (MDDST). A suspension of each test isolate, adjusted to 10⁵–10⁶ CFU/mL, was inoculated onto Mueller–Hinton agar (MHA). A disc of amoxicillin–clavulanic acid (30/10 µg) was placed at the center of the plate. Discs of third-generation cephalosporins—ceftazidime (30 µg), cefotaxime (30 µg), ceftriaxone (30 µg)—and aztreonam (30 µg) were placed 30 mm (center-to-center) from the amoxicillin–clavulanic acid disc. Plates were incubated at 37 °C for 24 hours. ESBL production was confirmed by the presence of an enhanced inhibition zone toward the clavulanic acid disc, forming the characteristic “champagne cork” appearance [13].

Data collection and statistical analysis

Data on patients’ age, sex, urine culture results, etiological agents, and antimicrobial susceptibility profiles were extracted from clinical laboratory databases. Detailed strain information, including demographic and resistance characteristics, is provided in S1 Supporting Data in S1 Table. Data were organized using Microsoft Excel to evaluate the distribution of patients across the variables studied.

Univariate logistic regression analysis was performed to assess gender-related differences in UTI occurrence across age groups, with male sex as the reference category. Chi-square (χ²) tests were used to compare categorical variables, including resistance rates by gender and age group. Statistical significance was defined as a p-value < 0.05. All analyses were performed using IBM SPSS Statistics version 26 (IBM Corp., Chicago, IL, USA).

Results

Socio-demographic patient’s characteristics

During the study period, a total of 422 clinical isolates of Enterobacteriaceae were collected. The majority were obtained from female patients (n = 316; 74.9%), resulting in a female-to-male ratio of 2.98. Participants’ ages ranged from 12 days to 97 years, with a mean age of 42.5 ± 30.20 years. The mean age was higher among males (50.8 years) compared to females (39.7 years). The highest incidence of UTIs was observed in patients aged ≤17 years (n = 114; 27.0%).

Univariate logistic regression analysis revealed significant gender disparities in UTI occurrence across several age groups. Females aged 18–24 years exhibited the highest odds of infection compared to males (OR = 13.94; 95% CI: 1.74–111.88; p = 0.013), followed by those aged 25–44 years (OR = 7.06; 95% CI: 2.56–19.49; p < 0.001) and 45–64 years (OR = 5.57; 95% CI: 1.88–16.56; p = 0.002). No statistically significant differences were observed in patients ≤17 years, 65–79 years, and ≥80 years (Table 1).

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Table 1. Sociodemographic characteristics and univariate logistic regression analysis of gender distribution across age groups among urinary tract infection patients in Tétouan, Morocco, 2022–2023 (N = 422).

https://doi.org/10.1371/journal.pone.0347958.t001

Enterobacteriaceae species distribution by age and gender

A total of 422 Enterobacteriaceae isolates were identified, with Escherichia coli being the predominant species (83.4%; n = 352), followed by K. pneumoniae (9.2%; n = 39) and P. mirabilis (3.1%; n = 13).

Gender distribution showed a predominance of female patients across most species, accounting for 77.3% (n = 272) of E. coli, 76.9% (n = 30) of K. pneumoniae, and 69.2% (n = 9) of P. mirabilis isolates. In contrast, Klebsiella oxytoca and other Enterobacteriaceae species were more frequently isolated from male patients, representing 75.0% (n = 6 out of 8) and 70.0% (n = 7 out of 10) of isolates, respectively.

Age distribution varied across species. Among E. coli isolates, the highest proportion was observed in patients aged ≤17 years (29.5%; n = 104), followed by those aged 65–79 years (22.4%; n = 79). K. pneumoniae was more frequently identified in older age groups, particularly among patients aged 65–79 years (28.2%; n = 11) and ≥80 years (17.9%; n = 7). Similarly, other Enterobacteriaceae species were predominantly observed in older patients, with 50.0% (n = 5) of isolates occurring in the 65–79 years group.

Overall, while E. coli predominated across all age groups, a relatively higher proportion of non-E. coli Enterobacteriaceae species was observed among older patients (Table 2).

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Table 2. Distribution of Enterobacteriaceae species according to gender and age groups among patients with urinary tract infections in Tétouan, Morocco, 2022–2023 (N = 422).

https://doi.org/10.1371/journal.pone.0347958.t002

Antibiotic resistance profiles

Among the 422 clinical isolates analyzed, ampicillin (AMP) showed the highest resistance rate (61.1%; n = 258), followed by ticarcillin (56.2%; n = 237). In contrast, resistance to ertapenem (0.9%; n = 4) and imipenem (1.1%; n = 5) remained very low. Additionally, 70 isolates (16.8%) were multidrug-resistance (MDR).

β-lactam resistance.

Among the penicillins, E. cloacae (n = 4) and K. pneumoniae (n = 39) exhibited the highest resistance to ampicillin (100% and 97.4%, respectively; n = 4/4 and n = 38/39) and amoxicillin–clavulanic acid (100% and 35.9%, respectively; n = 4/4 and n = 14/39). In contrast, E. coli (n = 352) and P. mirabilis (n = 13) showed lower resistance to ampicillin (55.1%; n = 194/352) and amoxicillin–clavulanic acid (15.4%; n = 2/13), respectively. For ticarcillin, K. pneumoniae (100%; n = 39/39) and K. oxytoca (100%; n = 4/4) were fully resistant, whereas E. cloacae displayed the lowest resistance (25%; n = 1/4).

Regarding cephalosporins, K. pneumoniae (n = 39) demonstrated the highest resistance to ceftriaxone (CRO), cefotaxime (CTX), and ceftazidime (CAZ), while E. cloacae (n = 4) showed the highest resistance to cefoxitin (FOX). K. oxytoca (n = 4) remained fully susceptible to all cephalosporins tested (0%; n = 0/4). Among carbapenems, the highest resistance was observed in P. mirabilis, with 4 of 13 isolates (30.8%) resistant to imipenem and 2 of 13 (15.4%) resistant to ertapenem. Given the small sample size of this species, these findings should be interpreted with caution. K. oxytoca (n = 4) and E. cloacae (n = 4) were fully susceptible to both agents (0%; n = 0/4).

Aminoglycoside resistance.

E. coli (n = 352) exhibited the highest resistance to tobramycin (21.3%; n = 75/352), while K. pneumoniae (n = 39) showed the highest resistance to gentamicin (20.5%; n = 8/39).

E. cloacae (n = 4) displayed the highest resistance to amikacin (25%; n = 1/4).

Quinolone and trimethoprim–sulfamethoxazole resistance.

E. cloacae (n = 4) exhibited the highest resistance to ciprofloxacin (25%; n = 1/4). E. coli (n = 352) demonstrated the highest resistance to trimethoprim–sulfamethoxazole (SXT) (36.6%; n = 129/352). K. oxytoca (n = 4) remained fully susceptible to both ciprofloxacin and SXT (0%; n = 0/4)

All antibiotic resistance profiles stratified by Enterobacteriaceae species and tested antimicrobial agents are summarized in Table 3.

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Table 3. Antibiotic resistance patterns of Enterobacteriaceae isolates among urinary tract infection patients in Tétouan, Morocco, 2022–2023 (N = 422).

https://doi.org/10.1371/journal.pone.0347958.t003

Prevalence, resistance profiles, and distribution of ESBL-producing isolates

Among the 422 Enterobacteriaceae isolates, 20 (4.7%) were confirmed as ESBL producers by MDDST. E. coli was the predominant ESBL-producing species, accounting for 16 of 20 ESBL isolates (80.0%), reflecting its overall abundance in the sample. When considering species-specific prevalence, 16 of 352 E. coli isolates were ESBL producers (4.6%), whereas 4 of 39 K. pneumoniae isolates were ESBL producers (10.3%), indicating a higher likelihood of ESBL production within K. pneumoniae.

ESBL-producing isolates showed complete resistance (100%) to tested penicillins (AMP, TIC) and third-generation cephalosporins (CRO, CAZ), while all remained susceptible to imipenem and ertapenem (Fig 1).

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Fig 1. Antibiotic resistance rate in uropathogenic extended-spectrum beta-lactamase producing isolates (n = 20) collected from outpatients in Tétouan, Morocco, 2022-2023.

The bar chart shows the percentage of resistance to tested antibiotics among extended-spectrum β-lactamase (ESBL)-producing uropathogenic Enterobacteriaceae isolates. Antibiotics tested include ampicillin (AMP), amoxicillin–clavulanic acid (AMC), ticarcillin (TIC), cefoxitin (FOX), ceftriaxone (CRO), cefotaxime (CTX), ceftazidime (CAZ), imipenem (IMP), ertapenem (ERT), amikacin (AK), gentamicin (GN), tobramycin (TOB), ciprofloxacin (CIP), and trimethoprim–sulfamethoxazole (SXT).

https://doi.org/10.1371/journal.pone.0347958.g001

Distribution of resistance patterns by gender and age

Male isolates exhibited significantly higher resistance rates to several β-lactam antibiotics compared with female isolates. Resistance to amoxicillin–clavulanic acid was observed in 37.7% of male isolates (n = 40/106) versus 24.4% of female isolates (n = 77/316; p = 0.009), while resistance to ampicillin was also more frequent among males (70.8%; n = 75/106 vs. 57.9%; n = 183/316; p = 0.026). Third-generation cephalosporin resistance, specifically to ceftriaxone and cefotaxime, was substantially greater in male isolates (13.2%; n = 14/106) than in female isolates (4.1%; n = 13/316; p = 0.002 for both). In contrast, resistance to imipenem and gentamicin did not differ significantly by gender.

Age-stratified analysis revealed differences in resistance patterns across pediatric, adult, and geriatric isolates. Cefoxitin resistance was highest among geriatric isolates (11.3%; n = 13/151, p = 0.034). Cefotaxime resistance was most prevalent in pediatric isolates (11.4%; n = 13/114; p = 0.033). Amikacin and gentamicin resistance were significantly higher in pediatric isolates (23.7%; n = 27/114, p = 0.018 and 25.4%; n = 29/114, p = 0.039, respectively). In contrast, ciprofloxacin resistance was highest in geriatric isolates (29.6%; n = 45/151) compared with adults (14.0%; n = 22/157) and pediatric isolates (21.1%; n = 24/114; p = 0.004).

For other antibiotics, although there were variations across age groups, these differences were not statistically significant (p > 0.05). Trimethoprim–sulfamethoxazole resistance remained consistently high across all age groups, while resistance to ticarcillin, tobramycin, and imipenem did not differ meaningfully by age.

ESBL prevalence was slightly higher among pediatric isolates (7.9%; n = 9/114) compared with adults (3.8%; n = 6/157) and geriatrics (3.3%; n = 5/151), but this difference was not statistically significant (p = 0.110). In contrast, ESBL occurrence was significantly greater in males (10.4%; n = 11/106) than in females (2.8%; n = 9/316; p = 0.001) (Table 4).

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Table 4. Gender- and age-associated patterns of antimicrobial resistance among clinical Enterobacteriaceae isolates in Tétouan, Morocco, 2022–2023 (N = 422).

https://doi.org/10.1371/journal.pone.0347958.t004

Discussion

Urinary tract infections (UTIs) remain among the most frequent bacterial infections worldwide, with Enterobacteriaceae as the leading etiological agents [14]. Their ability to colonize the gastrointestinal tract and subsequently invade the urinary system underlies their high prevalence [2]. This study, the first from Tétouan, Morocco, provides updated insight into the epidemiology and antimicrobial resistance (AMR) of community-acquired Enterobacteriaceae UTIs.

Among 422 isolates, women represented the majority of cases (F/M ratio 2.98), consistent with national findings (F/M 1.1–2.17) [15–19] and international reports showing that 57–89% of UTIs occur in women [20–26]. This distribution is largely attributed to anatomical and physiological characteristics, as well as exposure factors such as pregnancy and sexual activity [14]. UTIs occurred across all ages, with a mean patient age of 42.5 years, aligning with national reports (34–47 years) [15,17–19]. Pediatric (≤17 years) and elderly (≥65 years) patients represented 27.0% and 35.8% of cases, respectively, highlighting their well-established vulnerability to infection. In children, this susceptibility is mainly ascribed to immune immaturity and anatomical factors [27], whereas in older adults, it is driven by immunosenescence and a higher burden of age-related comorbidities [28,29].

Stratified analysis revealed a marked overrepresentation of women aged 18–64 years, similar to observations in Morocco and elsewhere [20,22,30]. In contrast, no significant sex differences were found among children or the elderly, corroborating reports that gender disparities are less pronounced in these age groups [29]. Together, these findings illustrate the distinct epidemiological profile of UTIs across demographic strata.

Escherichia coli dominated the isolates (83.4%), consistent with national [15–19,30–32] and global trends [20,24,28,33–35]. Its predominance reflects its commensal presence in the gut and its arsenal of virulence factors, including adhesins, toxins, and biofilm-forming capacity [36,37]. E. coli was particularly common among women, children, and older adults, as widely reported [20,22,28,38]. K. pneumoniae was the second most frequent species (9.2%), in agreement with national data (10–31%) [16–19,30–32] and international findings identifying it as the main alternative pathogen after E. coli [20,22,24,25,28]. Other species such as Enterobacter cloacae, Morganella morganii, and Citrobacter koseri were each present at proportions below 1.5%, whereas Klebsiella oxytoca accounted for 1.9% of isolates and Proteus mirabilis accounted for a slightly higher proportion (3.1%), a pattern consistent with their typical involvement in complicated or nosocomial infections rather than community-acquired UTIs [20,24,39]. The higher proportion of non-E. coli Enterobacteriaceae among older patients may reflect increased comorbidities and greater cumulative healthcare exposure in this group [30].

High resistance rates were observed for ampicillin (60.9%) and ticarcillin (56.2%), in line with Moroccan reports [15,31,32,40] and lower than in several African settings where resistance often exceeds 70% [23,34]. These findings confirm the limited usefulness of older β-lactams for community-acquired UTIs. Resistance to ciprofloxacin (21.3%) and trimethoprim–sulfamethoxazole (34.4%) was also considerable. Comparable or higher levels have been reported in Morocco [15–18,31] and across Africa [20,23,34], underscoring persistent challenges for empirical therapy. Amoxicillin–clavulanic acid resistance (27.5%) was lower than in many Moroccan studies [16,17,31,32] but higher than in some European cohorts [20], suggesting it may retain partial value locally but requires close monitoring. Third-generation cephalosporins exhibited relatively low resistance rates (6.2–7.8%), consistent with Moroccan [17–19,30–32] and European data [20,21]. Overall carbapenem resistance remained rare (<2%), confirming their ongoing effectiveness [25,28,34], although emerging resistance in parts of Africa and the Middle East [23,28] reinforces the need for sustained surveillance.

ESBL-producing isolates accounted for 4.7% of cases, a prevalence lower than that reported from several Moroccan cities (≈9–10.5%) [15,31,40] but similar to that observed in the nearby city of Tangier (4.3%) [32]. Internationally, this prevalence is substantially lower than in Senegal (62%) [41] and Djibouti (46%) [25]. ESBL isolates displayed extensive resistance to β-lactams and elevated resistance to aminoglycosides, ciprofloxacin, and SXT, in keeping with co-resistance patterns described nationally [15,17,18]. Carbapenems in ESBL-producing isolates remained fully effective, underscoring their critical role as last-line agents.

E. coli showed high resistance to ampicillin (55.1%), ticarcillin (51.7%), and SXT (36.6%), with ciprofloxacin resistance at 23.1%. These rates mirror national data [15–17,32] and fall within the higher range of European studies [20,42]. Amoxicillin–clavulanic acid resistance (25.9%) was moderate and lower than in many Moroccan reports, suggesting possible retained efficacy. Aminoglycoside resistance (17–20%) exceeded some national averages, potentially reflecting local prescribing patterns. Third-generation cephalosporin resistance remained below 8%, consistent with the relatively low ESBL prevalence. Carbapenem resistance was rare in E. coli (0.3%), although sporadic cases in neighboring regions [33,42] highlight the need for sustained monitoring. Third-generation cephalosporins remained largely effective against E. coli (<8% resistance), comparable to national (4–19%) [15,16,31,32,40] and European data (1.8–19.2%) [20,43]. These rates contrast sharply with high resistance reported in some African and Asian countries, where resistance may reach 100% [24,25,34,38,42]. This comparatively favorable profile supports their role as empirical options in Tétouan, in line with the relatively low ESBL prevalence [39,40].

K. pneumoniae exhibited near-universal resistance to ampicillin and ticarcillin, consistent with intrinsic penicillinase production [40]. Resistance to amoxicillin–clavulanic acid (35.9%) and aminoglycosides (12–20%) was moderate and aligned with national and international reports [15–18,28,32]. Third-generation cephalosporin resistance among K. pneumoniae (10.3%) remains concerning given this species’ well-documented capacity to acquire and disseminate ESBL determinants [44]. Other Enterobacteriaceae demonstrated varied resistance profiles, though low sample numbers limit interpretation.

Notably, P. mirabilis isolates demonstrated higher resistance to carbapenems (including ertapenem and imipenem), an unexpected finding that warrants cautious interpretation in community settings. However, this observation should be interpreted with caution given the small sample size (n = 13). The reduced susceptibility may partly reflect intrinsic characteristics of P. mirabilis, such as decreased permeability associated with the absence of the OmpF outer membrane porin and its naturally lower susceptibility to certain carbapenems [45,46]. Nevertheless, molecular characterization was beyond the scope of this study, and further investigations with larger cohorts and carbapenemase screening are needed to better elucidate these findings and assess their potential epidemiological implications, particularly given that carbapenemase-mediated resistance may exhibit low phenotypic expression [33].

Demographic characteristics were associated with distinct antimicrobial resistance patterns in this cohort. Male patients exhibited higher resistance rates to amoxicillin–clavulanic acid and third-generation cephalosporins, as well as a greater proportion of ESBL-producing isolates, a pattern previously reported in community-acquired urinary tract infections [20,26]. Pediatric isolates showed increased resistance to aminoglycosides and cefotaxime, whereas isolates from elderly patients demonstrated higher resistance to ciprofloxacin and cefoxitin, findings often linked in the literature to age-specific antibiotic exposure and patterns of healthcare utilization [20,27,28,30]. These variations underscore the importance of considering demographic characteristics when interpreting local resistance trends. Nevertheless, they should be interpreted cautiously, as age and sex were analyzed as descriptive epidemiological factors rather than causal determinants of antimicrobial resistance.

The overall findings indicate a continued need for strengthened antimicrobial stewardship in Tétouan. Although resistance levels were lower than those reported in several Moroccan cities, upward trends remain concerning. Sustained regional surveillance, integrated within national AMR monitoring efforts, will be essential to track resistance evolution and to inform empirical therapy. Expanding access to routine susceptibility testing and improving diagnostic capacity may help reduce reliance on purely empirical treatment and facilitate earlier detection of ESBL-producing and other resistant strains across population groups.

This study has several limitations. It was conducted in a single province and included only outpatients, which may limit generalizability. Data on comorbidities and prior antibiotic use were unavailable, and ESBL detection relied on phenotypic methods without molecular confirmation. Future research should address these gaps through multicenter surveys, molecular characterization of resistance mechanisms, and exploration of alternative therapeutic strategies, including non-traditional agents.

Conclusion

Community-acquired urinary tract infections in Tétouan were mainly caused by E. coli, with the highest burden observed among women and individuals at the extremes of age. The isolates showed substantial resistance to several first-line oral antibiotics, whereas the prevalence of ESBL-producing strains was moderate but clinically relevant. These findings provide locally generated evidence on pathogen distribution and antimicrobial resistance patterns and underscore the need for ongoing regional surveillance to support empirical treatment decisions. Continued monitoring will be essential to detect emerging resistance trends and to inform antimicrobial stewardship efforts within the national context.

Supporting information

S1 Table. Individual-level antimicrobial susceptibility profiles of Enterobacteriaceae isolates from community-acquired urinary tract infections in Tétouan (2022–2023).

The table presents isolate-level data including bacterial species, patient sex, age, and antimicrobial susceptibility results. Antimicrobial susceptibility testing results are reported as S (susceptible), I (intermediate), or R (resistant) according to EUCAST criteria. Antibiotics tested include ampicillin (AMP), amoxicillin–clavulanic acid (AMC), ticarcillin (TIC), cefoxitin (FOX), ceftriaxone (CRO), cefotaxime (CTX), ceftazidime (CAZ), imipenem (IMP), ertapenem (ETP), amikacin (AMK), gentamicin (GEN), tobramycin (TOB), ciprofloxacin (CIP), and trimethoprim–sulfamethoxazole (SXT). Ages are reported in years; values “<1” indicate patients younger than one year.

https://doi.org/10.1371/journal.pone.0347958.s001

(XLSX)

Acknowledgments

The authors express their sincere gratitude to the clinical private laboratories CHAMAL and ER-RAZI, located in Tétouan, for their valuable collaboration and support throughout this study.

References

1. Yang X, Chen H, Zheng Y, Qu S, Wang H, Yi F. Disease burden and long-term trends of urinary tract infections: A worldwide report. Front Public Health. 2022;10:888205. pmid:35968451
- View Article
- PubMed/NCBI
- Google Scholar
2. Dougnon V, Assogba P, Anago E, Déguénon E, Dapuliga C, Agbankpè J, et al. Enterobacteria responsible for urinary infections: a review about pathogenicity, virulence factors and epidemiology. J Appl Biol Biotechnol. 2020;8(1):117–24.
- View Article
- Google Scholar
3. Mancuso G, Midiri A, Gerace E, Marra M, Zummo S, Biondo C. Urinary Tract Infections: The Current Scenario and Future Prospects. Pathogens. 2023;12(4):623. pmid:37111509
- View Article
- PubMed/NCBI
- Google Scholar
4. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269–84. pmid:25853778
- View Article
- PubMed/NCBI
- Google Scholar
5. Nielubowicz GR, Mobley HLT. Host-pathogen interactions in urinary tract infection. Nat Rev Urol. 2010;7(8):430–41. pmid:20647992
- View Article
- PubMed/NCBI
- Google Scholar
6. Zhou Y, Zhou Z, Zheng L, Gong Z, Li Y, Jin Y, et al. Urinary Tract Infections Caused by Uropathogenic Escherichia coli: Mechanisms of Infection and Treatment Options. Int J Mol Sci. 2023;24(13):10537. pmid:37445714
- View Article
- PubMed/NCBI
- Google Scholar
7. Asadi Karam MR, Habibi M, Bouzari S. Urinary tract infection: Pathogenicity, antibiotic resistance and development of effective vaccines against Uropathogenic Escherichia coli. Mol Immunol. 2019;108:56–67. pmid:30784763
- View Article
- PubMed/NCBI
- Google Scholar
8. World Health Organization. Global antimicrobial resistance and use surveillance system (GLASS) report 2022. 2022 [cited 2025 Jan 3]. Available from: https://www.who.int/publications/i/item/9789240062702
- View Article
- Google Scholar
9. Nejjari C, El Achhab Y, Benaouda A, Abdelfattah C. Antimicrobial resistance among GLASS pathogens in Morocco: an epidemiological scoping review. BMC Infect Dis. 2022;22(1):438. pmid:35525923
- View Article
- PubMed/NCBI
- Google Scholar
10. Santos M, Mariz M, Tiago I, Martins J, Alarico S, Ferreira P. A review on urinary tract infections diagnostic methods: Laboratory-based and point-of-care approaches. J Pharm Biomed Anal. 2022;219:114889. pmid:35724611
- View Article
- PubMed/NCBI
- Google Scholar
11. High Commissariat for Planning, Kingdom of Morocco (HCP). Provincial Monograph of Tétouan. 2019 [cited 2025 Jan 3]. Available from: https://www.hcp.ma/region-tanger/attachment/1835579
- View Article
- Google Scholar
12. El Ouazzani ZEAB, Benaicha H, Reklaoui L, Alloudane R, Barrijal S. First detection of colistin resistance encoding gene mcr-1 in clinical Enterobacteriaceae isolates in Morocco. Iran J Med Microbiol. 2024;18(1):33–40.
- View Article
- Google Scholar
13. Mohammed AB, Anwar KA. Phenotypic and genotypic detection of extended spectrum beta lactamase enzyme in Klebsiella pneumoniae. PLoS One. 2022;17(9):e0267221. pmid:36173938
- View Article
- PubMed/NCBI
- Google Scholar
14. Timm MR, Russell SK, Hultgren SJ. Urinary tract infections: pathogenesis, host susceptibility and emerging therapeutics. Nat Rev Microbiol. 2025;23(2):72–86. pmid:39251839
- View Article
- PubMed/NCBI
- Google Scholar
15. Rafik A, Abouddihaj B, Asmaa D, Kaotar N, Mohammed T. Antibiotic resistance profiling of Uropathogenic Enterobacteriaceae, Casablanca, Morocco. E3S Web Conf. 2021;319:01002.
- View Article
- Google Scholar
16. Nakhli R, Rada R, Arsalane L, Zouhair S, Kamouni YE. Bacteriological Profile of Urinary Tract Infections at the Avicenne Military Hospital in Marrakech. Saudi J Pathol Microbiol. 2022;7(2):90–7.
- View Article
- Google Scholar
17. Benaissa E, Belouad E, Mechal Y, Benlahlou Y, Chadli M, Maleb A, et al. Multidrug-resistant community-acquired urinary tract infections in a northern region of Morocco: epidemiology and risk factors. Germs. 2021;11(4):562–9. pmid:35096673
- View Article
- PubMed/NCBI
- Google Scholar
18. Natoubi S, Barguigua A, Baghdad N, Nayme K, Timinouni M, Hilali A, et al. Occurrence of carbapenemases and extended-spectrum βeta-lactamases in uropathogenic enterobacteriaceae isolated from a community setting, Settat, Morocco. Asian J Pharm Clin Res. 2016;10(1):211.
- View Article
- Google Scholar
19. Ikhlas M, Hana H, Abdesalam H, Hajar EA, Wafaa F, Inass L. Urinary tract infections in patients admitted to the Nephrology Department. J Infect Dis Ther. 2018;3:34.
- View Article
- Google Scholar
20. Silva A, Costa E, Freitas A, Almeida A. Revisiting the Frequency and Antimicrobial Resistance Patterns of Bacteria Implicated in Community Urinary Tract Infections. Antibiotics (Basel). 2022;11(6):768. pmid:35740174
- View Article
- PubMed/NCBI
- Google Scholar
21. Suhartono S, Mahdani W, Hayati Z, Nurhalimah N. Species distribution of Enterobacteriaceae and non-Enterobacteriaceae responsible for urinary tract infections at Zainoel Abidin Hospital, Banda Aceh. Biodiversitas. 2021;22(8):826.
- View Article
- Google Scholar
22. Al-Mijalli SH. Bacterial uropathogens in urinary tract infection and antibiotic susceptibility pattern in Riyadh Hospital, Saudi Arabia. Cell Mol Med. 2017;3(1):1–6.
- View Article
- Google Scholar
23. Assouma FF, Sina H, Adjobimey T, Noumavo ADP, Socohou A, Boya B, et al. Susceptibility and Virulence of Enterobacteriaceae Isolated from Urinary Tract Infections in Benin. Microorganisms. 2023;11(1):213. pmid:36677505
- View Article
- PubMed/NCBI
- Google Scholar
24. Edin A, Tilahun D, Jara BA, Ayele A. Bacterial profile and antimicrobial susceptibility pattern of uropathogens at Bule Hora University Teaching Hospital, Ethiopia. Front Bacteriol. 2025;4:1439865.
- View Article
- Google Scholar
25. Mohamed HS, Houmed Aboubaker M, Dumont Y, Didelot M-N, Michon A-L, Galal L, et al. Multidrug-Resistant Enterobacterales in Community-Acquired Urinary Tract Infections in Djibouti, Republic of Djibouti. Antibiotics (Basel). 2022;11(12):1740. pmid:36551396
- View Article
- PubMed/NCBI
- Google Scholar
26. Patjas A, Martelius A, Ollgren J, Kantele A. International travel increases risk of UTI caused by ESBL-producing Enterobacterales. J Travel Med. 2024;31(1):taad155.
- View Article
- Google Scholar
27. Leung AKC, Wong AHC, Leung AAM, Hon KL. Urinary Tract Infection in Children. Recent Pat Inflamm Allergy Drug Discov. 2019;13(1):2–18. pmid:30592257
- View Article
- PubMed/NCBI
- Google Scholar
28. Taha AB. Bacterial etiology and antimicrobial resistance pattern of community-acquired urinary tract infection in older adults. Med Microecol. 2024;22:100114.
- View Article
- Google Scholar
29. Naghavi M, Vollset S, Ikuta K, Swetschinski LR, Gray A, Wool EE, et al. Global burden of bacterial antimicrobial resistance 1990–2021: a systematic analysis with forecasts to 2050. Lancet. 2024;404:1199–226.
- View Article
- Google Scholar
30. Saddari A, Benhamza N, Dalli M, Ezrari S, Benaissa E, Ben Lahlou Y, et al. Urinary tract infections older adults at Mohammed VI University Hospital of Oujda: case series. Ann Med Surg (Lond). 2023;85(5):1408–12. pmid:37229003
- View Article
- PubMed/NCBI
- Google Scholar
31. Mouline S, Jendouzi O, Assoufi N, Alayoud A, Azizi M. Epidemiology and antibiotic resistance of Enterobacteriaceae in UTIs at Oued Eddahab Military Hospital Agadir. SAS J Med. 2024;10(2):96–9.
- View Article
- Google Scholar
32. Mahrach Y, Arakrak A, Bakkali M, Laglaoui A. Resistance profile of Enterobacteriaceae in UTIs in Tangiers. Int J Adv Res. 2018.
- View Article
- Google Scholar
33. Tuhamize B, Tusubira D, Masembe C, Bessong P, Bazira J. Carbapenem resistance in Enterobacteriaceae among outpatients with UTI in Uganda. Cureus. 2024;16(10):e72387.
- View Article
- Google Scholar
34. Tansarli GS, Athanasiou S, Falagas ME. Antimicrobial susceptibility of Enterobacteriaceae causing UTIs in Africa. Antimicrob Agents Chemother. 2013;57(8):3628–39.
- View Article
- Google Scholar
35. Keser SK, Balihodzic AO. P01 Urinary tract infections caused by ESBL-producing Escherichia coli in outpatients from Sarajevo, Bosnia and Herzegovina. JAC Antimicrob Resist. 2022;4(Supplement_2).
- View Article
- Google Scholar
36. Kim B, Kim J-H, Lee Y. Virulence Factors Associated With Escherichia coli Bacteremia and Urinary Tract Infection. Ann Lab Med. 2022;42(2):203–12. pmid:34635614
- View Article
- PubMed/NCBI
- Google Scholar
37. Katongole P, Nalubega F, Florence NC, Asiimwe B, Andia I. Biofilm formation and virulence genes of uropathogenic E. coli in Uganda. BMC Infect Dis. 2020;20(1):453.
- View Article
- Google Scholar
38. Kitagawa K, Shigemura K, Yamamichi F, Alimsardjono L, Rahardjo D, Kuntaman K. International comparison of UTI pathogens and antimicrobial susceptibilities: Kobe vs Surabaya. Jpn J Infect Dis. 2018;71(1):8–13.
- View Article
- Google Scholar
39. Schito G, Naber K, Botto H, Palou J, Mazzei T, Gualco L, et al. The ARESC study: antimicrobial resistance survey of uncomplicated UTIs. Int J Antimicrob Agents. 2009;34(5):407–13.
- View Article
- Google Scholar
40. Hamamouchi J, Qasmaoui A, Halout K, Charof R, Ohmani F. Antibiotic resistance in uropathogenic enterobacteria. E3S Web Conf. 2021;319:01102.
- View Article
- Google Scholar
41. Sow SMM, DIOP A, NDIAYE B, Badiane F, Dieng D, DIALLO TA, et al. Epidemiology and Antibiotic Resistance of Uropathogenic Bacteria Isolated at Thierno Birahim Ndao Regional Hospital Center in Kaffrine (Senegal). Microbiol Infect Dis. 2024;8(3).
- View Article
- Google Scholar
42. McGuinness SL, Muhi S, Nadimpalli ML, Babiker A, Theunissen C, Stroffolini G, et al. Patient characteristics and antimicrobial susceptibility profiles of Escherichia coli and Klebsiella pneumoniae infections in international travellers: a GeoSentinel analysis. J Travel Med. 2025;32(1):taae090. pmid:38952011
- View Article
- PubMed/NCBI
- Google Scholar
43. Mortazavi-Tabatabaei SAR, Ghaderkhani J, Nazari A, Sayehmiri K, Sayehmiri F, Pakzad I. Antibacterial resistance patterns in UTIs: systematic review and meta-analysis. Int J Prev Med. 2019;10:169.
- View Article
- Google Scholar
44. Chong Y, Shimoda S, Shimono N. Current epidemiology, genetic evolution and clinical impact of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect Genet Evol. 2018;61:185–8. pmid:29626676
- View Article
- PubMed/NCBI
- Google Scholar
45. Mammeri H, Sereme Y, Toumi E, Faury H, Skurnik D. Interplay between porin deficiency, fitness, and virulence in carbapenem-non-susceptible Pseudomonas aeruginosa and Enterobacteriaceae. PLoS Pathog. 2025;21(2):e1012902. pmid:39919103
- View Article
- PubMed/NCBI
- Google Scholar
46. Lecuru M, Nicolas-Chanoine M-H, Tanaka S, Montravers P, Armand-Lefevre L, Denamur E, et al. Emergence of Imipenem Resistance in a CpxA-H208P-Variant-Producing Proteus mirabilis Clinical Isolate. Microb Drug Resist. 2021;27(6):747–51. pmid:33232636
- View Article
- PubMed/NCBI
- Google Scholar

[ref1] 1. Yang X, Chen H, Zheng Y, Qu S, Wang H, Yi F. Disease burden and long-term trends of urinary tract infections: A worldwide report. Front Public Health. 2022;10:888205. pmid:35968451
View Article
PubMed/NCBI
Google Scholar

[2] View Article

[3] PubMed/NCBI

[4] Google Scholar

[ref2] 2. Dougnon V, Assogba P, Anago E, Déguénon E, Dapuliga C, Agbankpè J, et al. Enterobacteria responsible for urinary infections: a review about pathogenicity, virulence factors and epidemiology. J Appl Biol Biotechnol. 2020;8(1):117–24.
View Article
Google Scholar

[6] View Article

[7] Google Scholar

[ref3] 3. Mancuso G, Midiri A, Gerace E, Marra M, Zummo S, Biondo C. Urinary Tract Infections: The Current Scenario and Future Prospects. Pathogens. 2023;12(4):623. pmid:37111509
View Article
PubMed/NCBI
Google Scholar

[9] View Article

[10] PubMed/NCBI

[11] Google Scholar

[ref4] 4. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269–84. pmid:25853778
View Article
PubMed/NCBI
Google Scholar

[13] View Article

[14] PubMed/NCBI

[15] Google Scholar

[ref5] 5. Nielubowicz GR, Mobley HLT. Host-pathogen interactions in urinary tract infection. Nat Rev Urol. 2010;7(8):430–41. pmid:20647992
View Article
PubMed/NCBI
Google Scholar

[17] View Article

[18] PubMed/NCBI

[19] Google Scholar

[ref6] 6. Zhou Y, Zhou Z, Zheng L, Gong Z, Li Y, Jin Y, et al. Urinary Tract Infections Caused by Uropathogenic Escherichia coli: Mechanisms of Infection and Treatment Options. Int J Mol Sci. 2023;24(13):10537. pmid:37445714
View Article
PubMed/NCBI
Google Scholar

[21] View Article

[22] PubMed/NCBI

[23] Google Scholar

[ref7] 7. Asadi Karam MR, Habibi M, Bouzari S. Urinary tract infection: Pathogenicity, antibiotic resistance and development of effective vaccines against Uropathogenic Escherichia coli. Mol Immunol. 2019;108:56–67. pmid:30784763
View Article
PubMed/NCBI
Google Scholar

[25] View Article

[26] PubMed/NCBI

[27] Google Scholar

[ref8] 8. World Health Organization. Global antimicrobial resistance and use surveillance system (GLASS) report 2022. 2022 [cited 2025 Jan 3]. Available from: https://www.who.int/publications/i/item/9789240062702
View Article
Google Scholar

[29] View Article

[30] Google Scholar

[ref9] 9. Nejjari C, El Achhab Y, Benaouda A, Abdelfattah C. Antimicrobial resistance among GLASS pathogens in Morocco: an epidemiological scoping review. BMC Infect Dis. 2022;22(1):438. pmid:35525923
View Article
PubMed/NCBI
Google Scholar

[32] View Article

[33] PubMed/NCBI

[34] Google Scholar

[ref10] 10. Santos M, Mariz M, Tiago I, Martins J, Alarico S, Ferreira P. A review on urinary tract infections diagnostic methods: Laboratory-based and point-of-care approaches. J Pharm Biomed Anal. 2022;219:114889. pmid:35724611
View Article
PubMed/NCBI
Google Scholar

[36] View Article

[37] PubMed/NCBI

[38] Google Scholar

[ref11] 11. High Commissariat for Planning, Kingdom of Morocco (HCP). Provincial Monograph of Tétouan. 2019 [cited 2025 Jan 3]. Available from: https://www.hcp.ma/region-tanger/attachment/1835579
View Article
Google Scholar

[40] View Article

[41] Google Scholar

[ref12] 12. El Ouazzani ZEAB, Benaicha H, Reklaoui L, Alloudane R, Barrijal S. First detection of colistin resistance encoding gene mcr-1 in clinical Enterobacteriaceae isolates in Morocco. Iran J Med Microbiol. 2024;18(1):33–40.
View Article
Google Scholar

[43] View Article

[44] Google Scholar

[ref13] 13. Mohammed AB, Anwar KA. Phenotypic and genotypic detection of extended spectrum beta lactamase enzyme in Klebsiella pneumoniae. PLoS One. 2022;17(9):e0267221. pmid:36173938
View Article
PubMed/NCBI
Google Scholar

[46] View Article

[47] PubMed/NCBI

[48] Google Scholar

[ref14] 14. Timm MR, Russell SK, Hultgren SJ. Urinary tract infections: pathogenesis, host susceptibility and emerging therapeutics. Nat Rev Microbiol. 2025;23(2):72–86. pmid:39251839
View Article
PubMed/NCBI
Google Scholar

[50] View Article

[51] PubMed/NCBI

[52] Google Scholar

[ref15] 15. Rafik A, Abouddihaj B, Asmaa D, Kaotar N, Mohammed T. Antibiotic resistance profiling of Uropathogenic Enterobacteriaceae, Casablanca, Morocco. E3S Web Conf. 2021;319:01002.
View Article
Google Scholar

[54] View Article

[55] Google Scholar

[ref16] 16. Nakhli R, Rada R, Arsalane L, Zouhair S, Kamouni YE. Bacteriological Profile of Urinary Tract Infections at the Avicenne Military Hospital in Marrakech. Saudi J Pathol Microbiol. 2022;7(2):90–7.
View Article
Google Scholar

[57] View Article

[58] Google Scholar

[ref17] 17. Benaissa E, Belouad E, Mechal Y, Benlahlou Y, Chadli M, Maleb A, et al. Multidrug-resistant community-acquired urinary tract infections in a northern region of Morocco: epidemiology and risk factors. Germs. 2021;11(4):562–9. pmid:35096673
View Article
PubMed/NCBI
Google Scholar

[60] View Article

[61] PubMed/NCBI

[62] Google Scholar

[ref18] 18. Natoubi S, Barguigua A, Baghdad N, Nayme K, Timinouni M, Hilali A, et al. Occurrence of carbapenemases and extended-spectrum βeta-lactamases in uropathogenic enterobacteriaceae isolated from a community setting, Settat, Morocco. Asian J Pharm Clin Res. 2016;10(1):211.
View Article
Google Scholar

[64] View Article

[65] Google Scholar

[ref19] 19. Ikhlas M, Hana H, Abdesalam H, Hajar EA, Wafaa F, Inass L. Urinary tract infections in patients admitted to the Nephrology Department. J Infect Dis Ther. 2018;3:34.
View Article
Google Scholar

[67] View Article

[68] Google Scholar

[ref20] 20. Silva A, Costa E, Freitas A, Almeida A. Revisiting the Frequency and Antimicrobial Resistance Patterns of Bacteria Implicated in Community Urinary Tract Infections. Antibiotics (Basel). 2022;11(6):768. pmid:35740174
View Article
PubMed/NCBI
Google Scholar

[70] View Article

[71] PubMed/NCBI

[72] Google Scholar

[ref21] 21. Suhartono S, Mahdani W, Hayati Z, Nurhalimah N. Species distribution of Enterobacteriaceae and non-Enterobacteriaceae responsible for urinary tract infections at Zainoel Abidin Hospital, Banda Aceh. Biodiversitas. 2021;22(8):826.
View Article
Google Scholar

[74] View Article

[75] Google Scholar

[ref22] 22. Al-Mijalli SH. Bacterial uropathogens in urinary tract infection and antibiotic susceptibility pattern in Riyadh Hospital, Saudi Arabia. Cell Mol Med. 2017;3(1):1–6.
View Article
Google Scholar

[77] View Article

[78] Google Scholar

[ref23] 23. Assouma FF, Sina H, Adjobimey T, Noumavo ADP, Socohou A, Boya B, et al. Susceptibility and Virulence of Enterobacteriaceae Isolated from Urinary Tract Infections in Benin. Microorganisms. 2023;11(1):213. pmid:36677505
View Article
PubMed/NCBI
Google Scholar

[80] View Article

[81] PubMed/NCBI

[82] Google Scholar

[ref24] 24. Edin A, Tilahun D, Jara BA, Ayele A. Bacterial profile and antimicrobial susceptibility pattern of uropathogens at Bule Hora University Teaching Hospital, Ethiopia. Front Bacteriol. 2025;4:1439865.
View Article
Google Scholar

[84] View Article

[85] Google Scholar

[ref25] 25. Mohamed HS, Houmed Aboubaker M, Dumont Y, Didelot M-N, Michon A-L, Galal L, et al. Multidrug-Resistant Enterobacterales in Community-Acquired Urinary Tract Infections in Djibouti, Republic of Djibouti. Antibiotics (Basel). 2022;11(12):1740. pmid:36551396
View Article
PubMed/NCBI
Google Scholar

[87] View Article

[88] PubMed/NCBI

[89] Google Scholar

[ref26] 26. Patjas A, Martelius A, Ollgren J, Kantele A. International travel increases risk of UTI caused by ESBL-producing Enterobacterales. J Travel Med. 2024;31(1):taad155.
View Article
Google Scholar

[91] View Article

[92] Google Scholar

[ref27] 27. Leung AKC, Wong AHC, Leung AAM, Hon KL. Urinary Tract Infection in Children. Recent Pat Inflamm Allergy Drug Discov. 2019;13(1):2–18. pmid:30592257
View Article
PubMed/NCBI
Google Scholar

[94] View Article

[95] PubMed/NCBI

[96] Google Scholar

[ref28] 28. Taha AB. Bacterial etiology and antimicrobial resistance pattern of community-acquired urinary tract infection in older adults. Med Microecol. 2024;22:100114.
View Article
Google Scholar

[98] View Article

[99] Google Scholar

[ref29] 29. Naghavi M, Vollset S, Ikuta K, Swetschinski LR, Gray A, Wool EE, et al. Global burden of bacterial antimicrobial resistance 1990–2021: a systematic analysis with forecasts to 2050. Lancet. 2024;404:1199–226.
View Article
Google Scholar

[101] View Article

[102] Google Scholar

[ref30] 30. Saddari A, Benhamza N, Dalli M, Ezrari S, Benaissa E, Ben Lahlou Y, et al. Urinary tract infections older adults at Mohammed VI University Hospital of Oujda: case series. Ann Med Surg (Lond). 2023;85(5):1408–12. pmid:37229003
View Article
PubMed/NCBI
Google Scholar

[104] View Article

[105] PubMed/NCBI

[106] Google Scholar

[ref31] 31. Mouline S, Jendouzi O, Assoufi N, Alayoud A, Azizi M. Epidemiology and antibiotic resistance of Enterobacteriaceae in UTIs at Oued Eddahab Military Hospital Agadir. SAS J Med. 2024;10(2):96–9.
View Article
Google Scholar

[108] View Article

[109] Google Scholar

[ref32] 32. Mahrach Y, Arakrak A, Bakkali M, Laglaoui A. Resistance profile of Enterobacteriaceae in UTIs in Tangiers. Int J Adv Res. 2018.
View Article
Google Scholar

[111] View Article

[112] Google Scholar

[ref33] 33. Tuhamize B, Tusubira D, Masembe C, Bessong P, Bazira J. Carbapenem resistance in Enterobacteriaceae among outpatients with UTI in Uganda. Cureus. 2024;16(10):e72387.
View Article
Google Scholar

[114] View Article

[115] Google Scholar

[ref34] 34. Tansarli GS, Athanasiou S, Falagas ME. Antimicrobial susceptibility of Enterobacteriaceae causing UTIs in Africa. Antimicrob Agents Chemother. 2013;57(8):3628–39.
View Article
Google Scholar

[117] View Article

[118] Google Scholar

[ref35] 35. Keser SK, Balihodzic AO. P01 Urinary tract infections caused by ESBL-producing Escherichia coli in outpatients from Sarajevo, Bosnia and Herzegovina. JAC Antimicrob Resist. 2022;4(Supplement_2).
View Article
Google Scholar

[120] View Article

[121] Google Scholar

[ref36] 36. Kim B, Kim J-H, Lee Y. Virulence Factors Associated With Escherichia coli Bacteremia and Urinary Tract Infection. Ann Lab Med. 2022;42(2):203–12. pmid:34635614
View Article
PubMed/NCBI
Google Scholar

[123] View Article

[124] PubMed/NCBI

[125] Google Scholar

[ref37] 37. Katongole P, Nalubega F, Florence NC, Asiimwe B, Andia I. Biofilm formation and virulence genes of uropathogenic E. coli in Uganda. BMC Infect Dis. 2020;20(1):453.
View Article
Google Scholar

[127] View Article

[128] Google Scholar

[ref38] 38. Kitagawa K, Shigemura K, Yamamichi F, Alimsardjono L, Rahardjo D, Kuntaman K. International comparison of UTI pathogens and antimicrobial susceptibilities: Kobe vs Surabaya. Jpn J Infect Dis. 2018;71(1):8–13.
View Article
Google Scholar

[130] View Article

[131] Google Scholar

[ref39] 39. Schito G, Naber K, Botto H, Palou J, Mazzei T, Gualco L, et al. The ARESC study: antimicrobial resistance survey of uncomplicated UTIs. Int J Antimicrob Agents. 2009;34(5):407–13.
View Article
Google Scholar

[133] View Article

[134] Google Scholar

[ref40] 40. Hamamouchi J, Qasmaoui A, Halout K, Charof R, Ohmani F. Antibiotic resistance in uropathogenic enterobacteria. E3S Web Conf. 2021;319:01102.
View Article
Google Scholar

[136] View Article

[137] Google Scholar

[ref41] 41. Sow SMM, DIOP A, NDIAYE B, Badiane F, Dieng D, DIALLO TA, et al. Epidemiology and Antibiotic Resistance of Uropathogenic Bacteria Isolated at Thierno Birahim Ndao Regional Hospital Center in Kaffrine (Senegal). Microbiol Infect Dis. 2024;8(3).
View Article
Google Scholar

[139] View Article

[140] Google Scholar

[ref42] 42. McGuinness SL, Muhi S, Nadimpalli ML, Babiker A, Theunissen C, Stroffolini G, et al. Patient characteristics and antimicrobial susceptibility profiles of Escherichia coli and Klebsiella pneumoniae infections in international travellers: a GeoSentinel analysis. J Travel Med. 2025;32(1):taae090. pmid:38952011
View Article
PubMed/NCBI
Google Scholar

[142] View Article

[143] PubMed/NCBI

[144] Google Scholar

[ref43] 43. Mortazavi-Tabatabaei SAR, Ghaderkhani J, Nazari A, Sayehmiri K, Sayehmiri F, Pakzad I. Antibacterial resistance patterns in UTIs: systematic review and meta-analysis. Int J Prev Med. 2019;10:169.
View Article
Google Scholar

[146] View Article

[147] Google Scholar

[ref44] 44. Chong Y, Shimoda S, Shimono N. Current epidemiology, genetic evolution and clinical impact of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect Genet Evol. 2018;61:185–8. pmid:29626676
View Article
PubMed/NCBI
Google Scholar

[149] View Article

[150] PubMed/NCBI

[151] Google Scholar

[ref45] 45. Mammeri H, Sereme Y, Toumi E, Faury H, Skurnik D. Interplay between porin deficiency, fitness, and virulence in carbapenem-non-susceptible Pseudomonas aeruginosa and Enterobacteriaceae. PLoS Pathog. 2025;21(2):e1012902. pmid:39919103
View Article
PubMed/NCBI
Google Scholar

[153] View Article

[154] PubMed/NCBI

[155] Google Scholar

[ref46] 46. Lecuru M, Nicolas-Chanoine M-H, Tanaka S, Montravers P, Armand-Lefevre L, Denamur E, et al. Emergence of Imipenem Resistance in a CpxA-H208P-Variant-Producing Proteus mirabilis Clinical Isolate. Microb Drug Resist. 2021;27(6):747–51. pmid:33232636
View Article
PubMed/NCBI
Google Scholar

[157] View Article

[158] PubMed/NCBI

[159] Google Scholar

Figures

Abstract

Background

Methods

Results

Conclusion

Introduction

Materials and methods

Ethical approval and participant consent

Study design and setting

Inclusion and exclusion criteria

Identification and antimicrobial susceptibility testing

Detection of extended spectrum beta-lactamase production

Data collection and statistical analysis

Results

Socio-demographic patient’s characteristics

Enterobacteriaceae species distribution by age and gender

Antibiotic resistance profiles

β-lactam resistance.

Aminoglycoside resistance.

Quinolone and trimethoprim–sulfamethoxazole resistance.

Prevalence, resistance profiles, and distribution of ESBL-producing isolates

Distribution of resistance patterns by gender and age

Discussion

Conclusion

Supporting information

S1 Table. Individual-level antimicrobial susceptibility profiles of Enterobacteriaceae isolates from community-acquired urinary tract infections in Tétouan (2022–2023).

Acknowledgments

References