Abstract
This study assessed the prevalence of bacterial uropathogens, antibiotic resistance, associated factors, and extended-spectrum β-lactamases ( ESBL)-producing Enterobacteriaceae uropathogens in diabetes mellitus (DM) patients at Debre Markos Comprehensive Specialized Hospital, Ethiopia. A cross-sectional study was conducted from April to July 2023 among 189 DM patients. Urine samples were processed using standard urine culture techniques. Bacterial identification was performed based on colony morphology on culture media, Gram staining, microscopic examination, and biochemical tests. Antimicrobial susceptibility testing was performed using the Kirby–Bauer disc diffusion method, and ESBL production was confirmed by the combination disc method according to CLSI guidelines for Enterobacteriaceae. Significant bacteriuria was found in 17.5% (33/189), higher in females (27.6%) than males (8.8%). Identified risk factors included female sex, age 25–34, prior UTI, and recent hospitalization. Escherichia coli (45.5%) was the predominant isolate. Multidrug resistance (MDR) was observed in 42.4% of isolates, and 57.9% of Gram-negative bacteria were ESBL producers.These findings highlight the clinical significance of high MDR and ESBL prevalence, emphasizing challenges in empiric therapy and the importance of routine susceptibility testing among diabetic patients.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12879-026-12633-y.
Keywords: Diabetes mellitus, Urinary tract infection, Antimicrobial resistance, Extended-spectrum β- lactamase, Ethiopia
Introduction
Non-communicable diseases are becoming a global threat that lead to a high rate of morbidity and mortality. Diabetes mellitus(DM) is one of the most prevalent long-lasting, non-communicable, and endocrine system disorder [1]. The 2017 International Diabetics Federation estimated that 451 million (8.4%) people between the ages of 18 and 99 had DM globally, and 5 million individuals between the ages of 20 and 79 years of age died due to this disease [2]. By 2045, it is anticipated that there will be 693 million (9.9%) people worldwide with DM. The number of deaths and disability-adjusted life years (DALYs) associated with DM will all continue to rise in the near future [3]. Ethiopia had the largest number of diabetics (2.6 million) in the African region in 2017 with a national prevalence of 5.2% [4].
In recent years, the high prevalence of DM all over the world together with increased risk of urinary tract infections (UTIs) has becoming a significant financial burden on healthcare systems [5]. Studies indicated that individuals with DM are more likely to suffer from severe form of UTI with life threating complications [5–7].Which may be due to abnormalities in the host immune system and a high urine glucose level of those patients [8]. High urine glucose levels encourage the growth and colonization of bacteria in the urinary tract which causes problems with renal function and ultimately leads to renal failure in these patients [9]. Patients with diabetes have been found to have higher rates of asymptomatic bacteruria and symptomatic UTIs than people without the disease [10]. Factors such as incomplete bladder emptying due to autonomic neuropathy and older age further enhance the risk of UTIs in diabetic patients [11]. Additionally, due to anatomical and physiological differences, UTIs are more common in women than in men, as women have shorter urethras that are closer to the rectum, as well as a moist environment around the urethra and insufficient prostatic fluid [12].
Microorganisms like bacteria, fungi, and viruses colonize and grow in the urinary system (Urinary Tract), resulting in UTIs (the presence of significant bacteria in urine specimens). Perhaps the incidence of UTIs due to viruses and fungi is low [13]. Uropathogens can be isolated from urine cultures in a variety of locations with varying prevalence [6, 14]. The principal causative agents of UTIs are Gram-negative bacteria; however, Gram-positive bacteria can also cause UTIs. The most common uropathogens are E.coli, Klebsiella species, Proteus species, Citrobacter species, Staphylococcus aureus, Coagulase negative Staphylococcus, Enterococcus faecalis, and Pseudomonas aeruginosa [6, 15]. E. coli is the most frequent cause of UTIs in both men and women with and without DM.
The bacterial agents and rates of resistance to the most commonly prescribed medications for treating UTIs may have changed over time. Furthermore, the rapid spread of MDR bacteria has recently become a major public health concern, particularly due to β-lactamase-producing MDR strains. The production of extended-spectrum β-lactamases (ESBLs) has helped bacteria to expand their activity even against the newly developed B-lactam antibiotics. ESBL producing microorganisms pose tremendous therapeutic consequences and significant clinical challenges when they remain undetected and making the treatment of UTI more difficult [11, 16]. These strains are more drug-resistant and carry a higher morbidity and mortality index, especially for multidrug-resistant Gram-negative bacteria [16]. They show reduced susceptibility to both narrow- and extended-spectrum cephalosporins and monobactams, but their effectiveness is not impacted by cephamycins and carbapenems. Typically, they exhibit resistance to fluoroquinolones, aminoglycosides, and co-trimoxazole [11].
Comprehensive data on ESBL-producing Enterobacteriaceae causing urinary tract infections are generally scarce in African countries compared to the developed world. In Ethiopia, assessing the spread and burden of these organisms is challenging due to the limited number of studies and the absence of coordinated epidemiological surveillance [17]. Thus, monitoring the local prevalence of uropathogens and their resistance pattern regularly and continuously is vital for public health in order to encourage appropriate use of the currently available antibiotic drugs.There is a lack of published data from Debre Markos on the distribution of uropathogens, antimicrobial resistance patterns, and ESBL production among diabetic patients. Understanding these local patterns is crucial because MDR and ESBL-producing organisms limit treatment options, increase healthcare costs, and may worsen patient outcomes, especially in resource-limited settings like Ethiopia. To address this evidence gap, this study was conducted to assess the bacterial profile, antimicrobial resistance patterns, associated factors, and ESBL-producing Enterobacteriaceae uropathogens among diabetic patients at Debre Markos Comprehensive Specialized Hospital, Ethiopia.
Materials and methods
Study design, duration, site, and study participant details
In this cross-sectional study, a total of 189 diabetes mellitus (DM) patients were enrolled from April to July 2023 at the diabetic clinic of Debre Markos Comprehensive Specialized Hospital, located 299 km northwest of Addis Ababa and 264 km southeast of Bahir Dar, Ethiopia. Participants were recruited during routine clinic visits, irrespective of urinary symptoms, and both symptomatic urinary tract infections (UTIs) and asymptomatic bacteriuria (ASB) were included according to operational definitions described below. Patients who had taken antibiotics within two weeks prior to sample collection were excluded to avoid bias in culture results. Participation was voluntary, and written informed consent was obtained from adult participants, while assent was obtained from guardians of minors. Ethical approval was secured from the Ethical Review Committee of the College of Medicine and Health Sciences, Debre Markos University (No: HSC/RCS/135/11/12; Date: 04/04/2023).
Operational definitions
Symptomatic urinary tract infection (UTI)
Symptomatic UTI was defined as the presence of at least one urinary tract–related symptom, including dysuria, urinary frequency, urgency, suprapubic pain, flank pain, or fever [18], in combination with significant bacteriuria (≥ 10⁵ colony-forming units [CFU]/mL) on urine culture [19].
Asymptomatic bacteriuria (ASB)
Asymptomatic bacteriuria was defined as the presence of significant bacteriuria (≥ 10⁵ CFU/mL) in a urine specimen obtained from a patient without any urinary tract–related symptoms at the time of sample collection.
Significant bacteriuria
was defined as the growth of ≥ 10⁵ colony-forming units (CFU)/mL of a single bacterial species from a midstream urine sample [19]. This threshold was selected to maintain consistency with previous Ethiopian studies and is considered appropriate for a study population in which the majority of participants were asymptomatic and screened routinely at a diabetic clinic.
Data collection
Clinical and socio-demographic information—including age, sex, marital status, residence, education, occupation, body mass index, type of DM, blood glucose level, previous history of UTIs, catheterization, hospitalization, water intake (defined as consuming less than 14.5 cups (3 L) per day for men, and less than 11 cups (2.7 L) per day for women) [20], and smoking habits—was collected through a structured questionnaire adapted from relevant literature and patient medical records. The questionnaire was initially prepared in English, translated into Amharic, and back-translated to ensure consistency. It was pretested on 5% of the study population at a nearby health facility, and necessary modifications were made prior to actual data collection. Data were collected by trained nurses under close supervision. Urine samples were collected and processed following standard microbiological procedures within a few hours of collection. This study focused exclusively on DM patients; therefore, the findings may not be generalizable to non-diabetic populations or other patient groups.
Sample collection and transportation
Each diabetic patient was instructed on how to collect a ‘clean-catch’ mid-stream urine specimen. Accordingly, about 5 to 10 ml of urine specimens were collected in a sterile screw-capped container from each diabetic patient and was delivered to the microbiology laboratory of Debre Markos Comprehensive Specialized Hospital for analysis within 2 h of collection. Specimens that are not processed within 2 h were kept refrigerated at 4 °C until analyzed.
Isolation and identification of bacterial uropathogens
Urine samples were inoculated onto the following agar plates using a sterile calibrated wire loop measuring 0.001 mL [21]: cysteine-lactose electrolyte deficient (CLED) medium plates (Oxoid Ltd, UK), MacConkey agar (Oxoid Ltd), blood agar plates (Oxoid Ltd), and mannitol salt agar (Biomark Labs). The plates were then incubated aerobically at 37 °C for 16–18 h. The inoculated plates were inspected for significant growth; with a pure colony count yielding bacterial growth of 105 colony-forming units (CFU) or more per ml of urine, and was further processed [19]. Bacterial identification was done presumptively based on the appearance of bacteria on culture media, microscopic examination, and the gram-reaction. Gram-negative bacteria were further identified using indole production, citrate utilization, H2S formation, gas formation, urea hydrolysis, lysine decarboxylation, lactose fermentation, and motility. The mannitol fermentation test, catalase, and coagulase tests were utilized to identify gram-positive bacteria using the standard procedure [19].
Antimicrobial susceptibility test
Antimicrobial susceptibility testing (AST) of all identified bacterial isolates from significant bacteriuria specimens was done on Mueller-Hinton agar (MHA) (Oxoid, UK) using the Kirby–Bauer disk diffusion method based on Clinical and Laboratory Standard Institute (CLSI) guideline [22]. Three to five pure colonies were taken from the culture growth, transferred, and mixed in 5 mL of sterile physiological saline (0.85%) until a homogeneous suspension was formed. The turbidity of the suspension was adjusted to the McFarland 0.5 standard. Sterile cotton swabs were used to inoculate the organism from the bacterial suspension onto the MHA plates. The inoculated plates were left at room temperature to dry for 3 to 5 min. Antibiotic disks were then placed on the plates, which were incubated in aerobic atmosphere at 37 °C for 16–18 h.The diameters of the zones of inhibition around the disks were measured using a caliper. The interpretation of the results of the AST was categorized as susceptible, intermediate, or resistant based on the CLSI guideline [22].
The following antimicrobials were selected to determine antibiotic susceptibilities based on CLSI recommendations and common local prescriptions for treating UTIs. Accordingly; Norfloxacin (NOR, 10 µg), Ceftriaxone (CRO,30 µg), Cefotaxime (CTX, 30 µg), Ciprofloxacin (CIP, 5 µg), Ceftazidime (CAZ, 30 µg), Nitrofurantoin (F, 30 µg), Trimethoprim-Sulfamethoxazol (SXT, 25 µg), Ampicillin (AMP, 10 µg), Nalidixic acid (NAL, 30 µg), Meropenem (MEM, 30 µg), Tetracycline (TTC, 30 µg), Piperacilline( PIP,10 µg) and Gentamycin (GN, 10 µg) (all from Oxoid, UK) were used for gram-negative bacteria. Furthermore, Ciprofloxacin (CIP, 5 µg), Norfloxacin (NOR, 10 µg), Nitrofurantoin (F, 30 µg), Cefoxitine (FOX, 30 µg), Tetracycline (TTC, 30 µg), Trimethoprim-sulfamethoxazole(SXT, 25 µg), Gentamicin (GN, 10 µg), and Penicillin (PEN, 10 µg)(all from Oxoid, UK) for gram-positive bacteria.
Detection of extended spectrum beta-lactamase
ESBL screening and confirmatory testing were performed only on Enterobacteriaceae isolates, in accordance with CLSI guidelines [22]. Initial screening for ESBL was conducted by measuring the diameters of the zones of inhibition produced by Ceftriaxone (30 µg), Ceftazidime (30 µg), or Cefotaxime (30 µg) in antimicrobial susceptibility tests on MHA (Oxoid, UK) according to the CLSI 2022 screening criteria. These breakpoints indicative of suspicion for ESBL production were zone of inhibition for Ceftazidime (30 µg), ≤ 22 mm, Ceftriaxone ≤ 25 mm, and Cefotaxime ≤ 27 mm [22].
After the initial screening, phenotypic detection of ESBL production was confirmed by a combined disk synergy test according to CLSI guidelines [22]. The organism to be tested was spread onto a MHA plate using similar procedures as for AST. Ceftazidime (CAZ), Ceftazidime-Clavulanic Acid (CAC), Cefotaxime (CTX), Cefotaxime-Clavulanic Acid (CEC) were used for the phenotypic presence of ESBL confirmatory test. After incubation at 37 °C for 16–18 h, an increase in the inhibition zone diameter of > 5 mm for a combination disc versus Ceftazidime or Cefotaxime disc alone was confirmed as ESBL production and the isolate was interpreted as ESBL producer [22].
Quality control
Quality control measures included using Escherichia coli ATCC® 25922 and Klebsiella pneumoniae ATCC® 700603 to validate culture media and antibiotic disk performance. Media sterility was checked routinely, and all AST procedures were conducted following CLSI guidelines to ensure accuracy and reproducibility. Identification of bacterial uropathogens was carried out using standard microbiological techniques, including culture on selective media, Gram staining, and a series of biochemical tests such as indole production, citrate utilization, urea hydrolysis, motility, catalase, and coagulase tests [19]. Extended-spectrum beta-lactamase (ESBL) detection was confirmed using the combined disk synergy test according to CLSI guidelines [22].
Statistical analysis
The data were entered into Epidata Version 4.6 and transferred to and analyzed using Statistical Package for the Social Sciences (SPSS) version 27.0 for analysis. Descriptive statistics were calculated for demographic and health characteristics. Logistic regression was employed to asses associations between variables. All significant variables in bivariate analysis with a p-value < 0.25 were entered into a multivariate logistic regression model to avoid possible confounders. The strength of associations was expressed using adjusted odds ratios (AORs) with 95% confidence intervals (CIs). A p-value < 0.05 was considered statistically significant. Model fitness was assessed using the Hosmer–Lemeshow goodness-of-fit test.
Result
Participant characteristics
A total of 189 diabetic patients were included in the study, of which 163 (86.2%) had no symptoms of UTI and 26 (13.8%) had symptoms. Of these, 102 (54.1%) of the study participants were male. The age range of the participants was from 15 to 80 years, with a mean age of 43.7 (± 16.75) years. Furthermore, 107 (56.6%) of the participants were categorized as having type II DM, and 107 (56.7%) had lived with DM for a duration of ≥ 5 years. A prior history of urinary tract infection and catheterization was found in 34 (18%) and 4(2.1%) of the study participants, respectively. The detailed sociodemographic, behavioral, and clinical characteristics of the patients are listed in Table 1.
Table 1.
Socio-demographic, clinical and behavioral characteristics of the study participants (n = 189) at Debre Markos comprehensive specialized Hospital, Ethiopia, 2023
| Variable | Category | Frequency | Percentage (%) |
|---|---|---|---|
| Sex | Male | 102 | 54.1 |
| Female | 87 | 46.0 | |
| Age (year) | 15–24 | 22 | 11.6 |
| 25–34 | 45 | 23.8 | |
| 35–44 | 29 | 15.3 | |
| 45–54 | 50 | 26.5 | |
| ≥ 55 | 43 | 22.8 | |
| Marital status | Single | 49 | 25.9 |
| Married | 126 | 66.7 | |
| Divorce | 1 | 0.5 | |
| Windowed | 13 | 6.9 | |
| Residence | Urban | 142 | 75.1 |
| Rural | 47 | 24.9 | |
| Educational status | Unable to read and write | 56 | 29.6 |
| Read and write | 44 | 23.3 | |
| Primary school | 24 | 12.7 | |
| Secondary school | 30 | 15.9 | |
| College and above | 35 | 18.5 | |
| Occupation | Student | 13 | 6.9 |
| Farmer | 49 | 25.9 | |
| Merchant | 13 | 6.9 | |
| Government worker | 35 | 18.5 | |
| Daily laborer | 19 | 10.1 | |
| Housewife | 41 | 21.7 | |
| Other | 19 | 10.1 | |
| Type of DM | Type I | 49 | 25.9 |
| Type II | 140 | 74.1 | |
| Fasting blood glucose level(mg/dl) | < 126 | 73 | 38.6 |
| ≥ 126 | 116 | 61.4 | |
| Previous UTI history | Yes | 34 | 18.0 |
| No | 155 | 82.0 | |
| Current symptoms of UTI | Yes | 26 | 13.8 |
| No | 163 | 86.2 | |
| History of hospitalization | Yes | 9 | 4.8 |
| No | 180 | 95.2 | |
| History of catheterization | Yes | 4 | 2.1 |
| No | 185 | 97.9 | |
| Smoking status | Yes | 6 | 3.2 |
| No | 183 | 96.8 | |
| Water Drinking habits | Yes | 50 | 26.5 |
| No | 139 | 73.5 |
Prevalence of urinary tract infection and isolated bacterial uropathogens
Out of the 189 participants, significant bacteriuria was detected in 33 (17.5%) (95%, CI: 12.7, 22.9) diabetic patients. Most of the significant bacteriuria findings were among females 24(27.6%), while males accounted for 9(8.8%). A high prevalence of significant bacteriuria 16(35.6%) was observed in the age range of 25–34 years. The prevalence of significant bacteriuria among symptomatic and asymptomatic diabetic patients was 3 (11.5%) and 30(18.4%), respectively (Table 3).
Table 3.
Bivariate and multivariate logistic regression analysis for associated factors with urinary tract infection among diabetic patients at Debre Markos comprehensive specialized Hospital, Ethiopia, 2023
| Variables | Cultures | COR (95% CI) | P-value | AOR (95% CI) | P-value | ||
|---|---|---|---|---|---|---|---|
| Sg positive | Sg negative | ||||||
| Sex | Male | 9(8.8) | 93(91.2) | 1 | 1 | ||
| Female | 24(27.6) | 63(72.4) | 3.937(1.716–9.029) | 0.004 | 3.89 (1.527–9.95) | 0.004* | |
| Age | 15–24 | 3(13.6) | 19(86.4) | 1.539(0.313–7.581) | 0.596 | 0.905(0.140–5.84) | 0.916 |
| 25–34 | 16(35.6) | 29(64.4) | 5.379(1.626–17.79) | 0.006 | 5.39(1.442–21.278) | 0.013* | |
| 35–44 | 2(6.9) | 27(93.1) | 0.722(0.123–4.227) | 0.718 | 0.823(0.124–5.48) | 0.841 | |
| 45–54 | 8(16.0) | 42(84.0) | 1.857(0.518–6.659) | 0.342 | 1.566(0.380–6.447) | 0.534 | |
| ⩾55 | 4(9.3) | 39(90.7) | 1 | 1 | |||
| Residence | Urban | 25(75.8) | 117(75.4) | 1.042(434-2.498) | 0.927 | ||
| Rural | 8(24.2) | 39(2.0) | 1 | ||||
| Marital status | Single | 9(18.8) | 39(81.3) | 0.769(0.175–3.379) | 0.728 | ||
| Married | 21(16.8) | 104(83.2) | 0.673(0.171–2.656) | 0.572 | |||
| Windowed | 3(9.1) | 10(8.3) | 1 | ||||
| Educational status | Unable to read and write | 6(10.7) | 50(89.3) | 1 | |||
| Read and write | 8(18.2) | 36(818) | 1.389(0.390–4.497) | 0.612 | |||
| Primary school | 8(33.3) | 16(66.7) | 4.167(1.256–13.82) | 0.250 | |||
| Secondary school | 6(20) | 24(80) | 2.083(0.608–7.141) | 0.243 | |||
| College and above | 5(14.3) | 30(80.7) | 1.389(0.390–4.947) | 0.612 | |||
| Occupation | Student | 1(7.7) | 12(92.3) | 1 | |||
| Farmer | 11(22.4) | 38(77.6) | 3.474(0.406–29.748) | 0.256 | |||
| Merchant | 2(15.4) | 11(84.6) | 2.182(0.173–27.556) | 0.574 | |||
| Gov, t worker | 5(14.3) | 30(85.6) | 2.000(0.211–18.956) | 0.546 | |||
| Housewife | 5(12.3) | 36(86.8) | 3.200(0.315–32.532) | 0.326 | |||
| Daily laborer | 4(21.3) | 15(79.7) | 1.667(0.177–15.722) | 0.656 | |||
| Retirement | 5(26.3) | 14(73.7) | 4.286(0.438–41.951) | 0.211 | |||
| Previous history of UTI | No | 19(12.3) | 136(87.7) | 1 | 1 | ||
| Yes | 14(41.2) | 20 (58.8) | 5.011(2.174–11.546) | 0.000 | 4.97 (1.82 -13.559) | 0.002* | |
| Type of DM | Type I | 6(12.2) | 43(87.8) | 1 | |||
| Type II | 27(19.3) | 113(80.7) | 1.712(0.661–4.436) | 0.268 | |||
| Fasting blood glucose level | < 126 mg/dl | 11(15.10 | 62(84.9) | 1 | |||
| ≥ 126 mg/dl | 22(19.0) | 94(81.0) | 1.319(0.598–2.911) | 0.493 | |||
| Current symptoms of UTI | No | 30(18.4) | 133(81.6) | 1 | |||
| Yes | 3(11.5) | 23(88.5) | 0.578(0.13–2.052) | 0.397 | |||
| History of hospitalization | No | 28(15.6) | 152(84.4) | 1 | 1 | ||
| Yes | 5(55.6) | 4(44.4) | 6.786(1.715–26.84) | 0.006 | 5.97(1.14-31.297) | 0.034* | |
| History of catheterization | No | 32(17.2) | 153(82.7) | 1 | |||
| Yes | 1(25.0) | 3(75.0) | 1.594(0.161–15.817) | 0.691 | |||
| Water drinking habit | Yes | 7(14.0) | 43(86.0) | 1.41(0.572-3. 495) | 0.787 | ||
| No | 26(18.7) | 113(81.3) | 1 | ||||
| Smoking status | Yes | 1(16.7) | 5(83.3) | 0.944(0.107–8.354) | 0.959 | ||
| No | 32(17,5) | 151(82.5) | 1 | ||||
Among the 33(17.5%) cases of significant bacteriuria, 21(63.6%) and 12(36.4%) were Gram-negative and gram- positive bacteria isolates, respectively (Table 2).
Table 2.
Uropathogenic bacteria (n = 33) isolated from urine specimen taken from the study participants at Debre Markos comprehensive specialized Hospital, Ethiopia, 2023
| Bacterial isolates | Frequency (N) | Percentage (%) |
|---|---|---|
| Gram-negative | 21 | 63.6 |
| E. coli | 15 | 45.5 |
| K. pneumoniae | 2 | 6.1 |
| P. aeruginosa | 2 | 6.1 |
| K. oxytoca | 1 | 3 |
| Citrobacter spp | 1 | 3 |
| Gram-positive | 12 | 36.4 |
| S. aureus | 5 | 15.1 |
| CONS | 7 | 21.2 |
| Total | 33 | 100 |
Among the total study participants, seven distinct bacterial species were isolated. However, double or multiple bacterial findings were not identified. The predominant bacterial isolates were E. coli 15(45.5%) followed by Coagulase-negative staphylococci 7(21.2%), and S. aureus 5(15.2%) (Table 2).
Factors associated with urinary tract infections among diabetic patients
In the bivariate logistic regression analysis, sex, age, previous history of UTI, and hospitalization were associated with UTI at a significance level of P < 0.25 and were therefore included in the multivariate logistic regression model (Table 3).
In the multivariate analysis, females had significantly higher odds of UTI compared with males (AOR = 3.9; 95% CI: 1.5–9.95; P = 0.004). Participants aged 25–34 years had higher odds of UTI than those aged ≥ 55 years (AOR = 5.4; 95% CI: 1.6–17.8; P = 0.013). Patients with a history of hospitalization were more likely to have UTI than those without such a history (AOR = 5.97; 95% CI: 1.1–31.3; P = 0.034). Similarly, patients with a previous history of UTI had increased odds of developing UTI (AOR = 4.97; 95% CI: 1.8–13.6; P = 0.002) (Table 3).
Antimicrobial resistance profile of bacterial uropathogens
The antimicrobial resistance pattern of uropathogenic Gram-negative and Gram-positive bacteria are appended in Table 4. The antimicrobial resistance levels of gram-negative uropathogenic bacteria indicated a high resistance rate to ampicillin (73.7%) and tetracycline (57.9%), while the lowest resistance was observed for Nalidixic acid (47.4%), Ciprofloxacin (38.1%), and Trimethoprim-sulfamethoxazole (31.6%). Whereas all gram-negative bacteria showed the highest level of sensitivity to Gentamycin (100%) followed by Nitrofurantoin (90.5%)(Table 4).
Table 4.
Antimicrobial susceptibility pattern of gram-negative (n = 21) and gram-positive bacteria (n = 12) among diabetic patients at Debre Markos comprehensive specialized Hospital, Ethiopia, 2023
| Bacteria isolate | Pattern | AMP | MEM | CIP | SXT | NOR | GN | TE | NAL | F | PIP | CAZ | CRO | CTX | PEN |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Gram Negative Isolates | |||||||||||||||
| E.coli (n = 15) | S | 1(6.7) | 12(80.0) | 7(46.7) | 9(60.0) | 9(60.00) | 15(100) | 3(20.0) | 5(33.) | 13(86.7) | NA | 7(46.5) | 8(35.3) | 7(46.7) | NA |
| I | 3(20.0) | 1(6.7) | 3(20.0) | 0(0.0) | 2(13.3) | 0(0.0) | 3(20.0) | 3(20.0) | 0(0.0) | NA | 3(20) | 3(20) | 4(26.7) | NA | |
| R | 11(73.3) | 2(13.3) | 5(33.3) | 6(40.0) | 4(26.7) | 0(0.0) | 9(60.0) | 7(46.7) | 2(13.3) | NA | 5(33.3) | 4(26.7) | 4(26.7) | NA | |
| K. pneumoniae (n = 2) | S | 0(0.0) | 1(50.) | 0(0.0) | 2(100.0) | 0(0.0) | 2(100) | 1(50.0) | 1(50.0) | 2(100) | NA | 0(0.0) | 0(0.0) | 0(0.0) | NA |
| I | 0(0.0) | 1(50.0) | 0(0.0) | 0(0.0) | 1(50.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.00 | NA | 0(0.0) | 0(0.0) | 0(0.0) | NA | |
| R | 2(100.0) | 0(0.0) | 2(100.0) | 0(0.00 | 1(50.0) | 0(0.0) | 1(50.0) | 1(50.0) | 0(0.0) | NA | 2(100) | 2(100) | 2(100) | NA | |
| Citrobacter SPP (n = 1) | S | 0(0.0) | 0(0.0) | 1(100.0) | 1(100.0) | 1(100) | 1(100) | 1(100) | 0(0.0) | 1(100) | NA | 0(0.0) | 1(100) | 0(0.0) | NA |
| I | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 1(100) | 0(0.0) | NA | 1(100) | 0(0.0) | 0(0.0) | NA | |
| R | 1(100.0) | 1(100.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | NA | 0(0.0) | 0(0.0) | 1(100) | NA | |
| K. oxytoca (n = 1) | S | 1(100.0) | 0(0.0) | 0(0.0) | 1(100.0) | 0(0.0) | 1(100) | 0(0.0) | 0(0.0) | 1(100) | NA | 0(0.0) | 0(0.0) | 0(0.0) | NA |
| I | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | NA | 1(100) | 0(0.0) | 1(100) | NA | |
| R | 0(0.0) | 1(100.0) | 1(100.0) | 0(0.0) | 1(100) | 0(0.00 | 1(100) | 1(100) | 0(0.0) | NA | 0(0.0) | 1(100) | 09)0.0) | NA | |
| P.aeruginosa (N) = 2 | S | NA | 1(50.0) | 2(100.0) | NA | 2(100) | 2(100) | NA | NA | 2(100) | 1(50.0) | 1(50) | 1(50) | 1(50.0) | NA |
| I | NA | 0(0.0) | 0(0.0) | NA | 0(0.0) | 0(0.0) | NA | NA | 0(0.0) | 0 | 0(0.00 | 0(0.0) | 0(0.0) | NA | |
| R | NA | 1(50.0) | 0(0.0) | NA | 0(0.0) | 0(0.0) | NA | NA | 0(0.0) | 1(50) | 1(50) | 1(50) | 1(50.0) | NA | |
| Total for Gram negative isolates (n = 21) | S | 2(10.0) | 14(66.7) | 10(47.6) | 13(68.4) | 12(57.1) | 21(100) | 5(26.3) | 6(31.6) | 19(90.5) | 1(50) | 8(38.1) | 10(46.6) | 8(38.1) | NA |
| I | 3(15.8) | 2(9.5) | 3(14.3) | 0(0.0) | 3(14.3) | 0(0.0) | 3(15.8) | 4(21.1) | 0(0.0) | 0 | 5(23.8) | 4(19.0) | 5(23.8) | NA | |
| R | 14(73.7) | 5(23.8) | 8(38.1) | 6(31.6) | 6(28.6) | 0(0.0) | 11(57.9) | 9(47.4) | 2(9.5) | 1(50) | 8(38.2) | 7(33.3) | 8(38.1) | NA | |
| Gram Positive Isolates | |||||||||||||||
| S.aureus(n = 5) | S | NA | NA | 3(60) | 4(80.0) | 4(80) | 5(100) | 4(80) | NA | 5(100) | NA | NA | NA | 3(60) | 0(0.0) |
| I | NA | NA | 1(20) | 0(0.0) | 0(0.0) | 0(0.0) | 0(0.0) | NA | 00.00) | NA | NA | NA | 0(0.0) | 0(0.0) | |
| R | NA | NA | 1(20) | 1(20.0) | 1(20) | 0(0.0) | 1(20) | NA | 0(0.0) | NA | NA | NA | 2(40) | 5(100) | |
| CONS(n = 7) | S | NA | NA | 4(57.1) | 2(28.6) | 4(57) | 7(100) | 1(14.3) | NA | 4(71.4) | NA | NA | NA | NA | 1(14.3) |
| I | NA | NA | 2(28.6) | 1(14.3) | 0(0.0) | 0(0.0) | 2(28.6) | NA | 1(14.3) | NA | NA | NA | NA | 0(0.0) | |
| R | NA | NA | 1(14.3) | 4(57.1) | 3(42.9) | 0(0.0) | 4(57.1) | NA | 1(14.3) | NA | NA | NA | NA | 6(85.7) | |
| Total for Gram positive isolates | S | NA | NA | 7(58.3) | 6(50.0) | 8(66.7) | 12(100) | 5(41.7) | NA | 9(75.0) | NA | NA | NA | 3(60) | 1(8.3) |
| I | NA | NA | 3(25.0) | 1(8.3) | 0(0.0) | 0(0.00 | 2(16.7) | NA | 1(8.3) | NA | NA | NA | 0(0.0) | 0(0.0) | |
| R | NA | NA | 2(16.7) | 5(41.7) | 4(33.3) | 0(0.0) | 5(41.7) | NA | 1(8.3) | NA | NA | NA | 2(40) | 11(91.7) | |
{AMP: ampicillin; CAZ: Ceftazidime; CIP: ciprofloxacin CRO: Ceftriaxone ; CTX: Cefotaxime ; FOX: Cefoxitin; nitrofurantoin; GN: gentamicin; NAL: nalidixic acid; I: intermediate; MEM: meropenem; NOR: norfloxacin; PIP: piperacillin; R: resistant; S:sensitive; SXT: trimethoprim-sulfamethoxazole; TE: tetracycline; NA: not applicable; PEN: penicillin}
E. coli, the most frequently isolated bacteria, showed high resistance to ampicillin (73.3%), and tetracycline (60%). On the other hand, E.coli showed high susceptibility to gentamycin (100%) followed by nitrofurantoin (86.7%). k.pneumoniae isolates were found to have high resistance (100%) to Ampicillin and ciprofloxacin and cephalosporin groups (Table 4).
P. aeruginosa showed the highest level of sensitivity (100%) to gentamycin, ciprofloxacine, and nitrofurantoin, and 50% sensitivity to meropenem, piperacillin, and cephalosporins groups (Table 4).
K.oxytoca isolates were found 100% resistant to norfloxacin, tetracycline, ciprofloxacin, and nalidixic acid, whereas the highest rate of sensitivity (100%) to gentamycin, ampicillin, trimethoprim-sulfamethoxazole, and nitrofurantoin (Table 4).
Regarding the gram-positive bacteria, high degree of resistance was seen to penicillin, (91.7%). In contrast, a high rate of susceptibility to gentamycin (100%) followed by nitrofurantoin (75%) and norfloxacin (66.7%) was observed. Whereas S. aureus showed high susceptibility (100%) to nitrofurantoin and gentamycin, it also showed high resistance (100%) to penicillin (Table 4).
Multidrug resistance pattern of the isolates
Multidrug resistance (MDR), defined as nonsusceptibility to at least one agent in three or more antimicrobial categories [23], was observed in 14 (42.4%) of all isolated bacterial uropathogens. Among Gram-negative isolates, 11 (52.4%) exhibited MDR, whereas 4 (33.3%) of Gram-positive isolates were MDR.
Among the Gram-negative bacterial isolates, the predominant isolate was E. coli, with 8 (53.3%) showing MDR. Among the Gram-positive bacterial isolates, MDR was observed in 3 (42.9%) cases of coagulase-negative staphylococci, followed by S.aureus, which exhibited MDR in 1 (20%) case (Table 5).
Table 5.
Multidrug resistance patterns among diabetic patients at Debre Markos comprehensive specialized Hospital, Ethiopia, 2023
| Bacterial isolates | Total N (%) | Antimicrobial resistance pattern | R3 N (%) | R4 N (%) | R5 N (%) | MDR N (%) |
||
|---|---|---|---|---|---|---|---|---|
| R0 N (%) |
R1 N (%) | R2 N (%) | ||||||
| Gram-negative | 21(63.6) | 5(23.8) | 4(19.0) | 2(9.5) | 3(14.3) | 5(23.8) | 3(14.3) | 11(52.4) |
| E. coli | 15(45.5) | 3(20) | 3(203) | 1(13,3) | 2(13.3) | 4(26.7) | 2(13.3) | 8(53.3) |
| K pneumoniae | 2(6.1) | 0(0) | 0(0) | 1(3) | 1(3.0) | 0 (0) | 0(0) | 1(50.0) |
| P. aeruginos | 2(6.1) | 2(100) | 0(0) | 0(0) | 0(0) | 0(0) | 0(0) | 0(0) |
| K. oxytoca | 1(3.0) | 0(0) | 0(0) | 0(0) | 0(0) | 1(3.0) | 0(0) | 1(100) |
| Citrobacter spp | 1(3.0) | 0(0) | 1(3.0) | 0(0) | 0(0) | 0(0) | 0(0) | 0(0) |
| Gram-positive | 12(36.4) | 0(0) | 5(41.6) | 3(25) | 0(0) | 2(16.7) | 2(16.7) | 4(33.3) |
| S. aureus | 5(15.1) | 0(0) | 3(9.1) | 1(3.0) | 0(0) | 0(0) | 1(3.0) | 1(20.0) |
| CONS | 7(21.2) | 0(0) | 2(6.2) | 2(6.1) | 0(0) | 2(6.1) | 1(3.0) | 3(42.9) |
| Total | 33(100) | 5(15.2) | 9(27.3) | 6(18.2) | 3(9.0) | 7(21.2) | 4(12.1) | 14(42.4) |
{R0 - No antibiotic resistance, R1- Resistance to one drug, R2-Resistance to two drugs, R3- Resistance to three drugs, R4- Resistance to four drugs, R5- Resistance to five drugs, MDR- Resistance to three or more classes of drugs}
ESBL-producing gram-negative uropathogens
A total 13/19(68.4%) of Enterobacteria isolated in this study were positive for the ESBL production screening test. The combination disk test confirmed that 84.6% (11/13) of the suspected isolates were capable of producing ESBL, leading to an overall ESBL positivity rate of 57.9% (11/19) (Table 6).
Table 6.
Distribution of ESBL producing Enterobacteriaceae (n = 19) among diabetic patients at Debre Markos comprehensive specialized Hospital, Ethiopia, 2023
| Bacteria isolates Total (N) |
Total (N) | Positive for ESBL Screening | ESBL Phenotype Confirmation Test Positivity |
|---|---|---|---|
| E.coli | 15 | 9(60%) | 7/9(77.8%) |
| K.pneumonae | 2 | 2(100%) | 2/2(100%) |
| Citrobacter spp | 1 | 1(100%) | 1/1(100%) |
| K. oxytoca | 1 | 1(100%) | 1/1(100%) |
| Total | 19 | 13/19 (68.4%) | 11/19 (57.9) |
The majority of ESBL producing isolates were E. coli (7/11(63.6%)) followed by K.pneumoniae, (2/11(18.2%)), Citrobacter Spp (1/11(9.1%)) and K. oxytoca (1/11(9.1%) (Fig. 1).
Fig. 1.
Distribution of ESBL producer bacterial uropathogen isolates (n = 11) among diabetic patients at Debre Markos Comprehensive Specialized Hospital, Ethiopia, 2023
Antibiotics susceptibility pattern of ESBLs
In our study, ESBL-positive isolates exhibited a high level of resistance to ampicillin (90.9%), tetracycline (81.8%), and ciprofloxacin, ceftazidime, and cefotaxime (each 72.7%), and while demonstrating greater sensitivity to gentamicin (100%), nitrofurantoin (81.8%), and meropenem (54.5%). E. coli was the most prominent producer of ESBL., showing 85.7% resistance to trimethoprim-sulfamethoxazole, tetracycline, ampicillin, and 71.4% to ceftazidime, respectively. K. pneumoniae exhibited 100% resistance to trimethoprim-sulfamethoxazole, norfloxacin, and the cephalosporin group. Citrobacter spp. showed 100% resistance to meropenem, ampicillin, and cefotaxime. K. ozanae exhibited 100% resistance to meropenem, ampicillin, tetracycline, and norfloxacin (Table 7).
Table 7.
Antimicrobial resistance among the phenotypically confirmed ESBL producer (N = 11) among DM patient in DMCSH Ethiopia, 2023
| Antimicrobial gents tested | ||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Bacteria isolates | Pattern | SXT | NOR | F | TE | CIP | GEN | NAL | MEM | AMP | PRC | CAZ | CRO | CTX |
| E.coli (n = 7) | S | 1(14.3) | 2(28.6) | 5(71.4) | 1(14.3) | 1(14.3) | 7(100) | 2(28.6) | 5(71.4) | 0 | ND | 0 | 0 | 1(14.3) |
| I | 0 | 1(14.3) | 0 | 0 | 1(14.3) | 0 | 0 | 0 | 1(14.3) | ND | 2(28.6) | 3(42.9) | 2(28.6) | |
| R | 6(85.7) | 4(57.1) | 2(28.6) | 6(85.7) | 5(71.4) | 0 | 5(71.4) | 2(28.6) | 6(85.7) | ND | 5(71.4) | 4(57.1) | 4(57.1) | |
|
K.pneumoniae (n = 2) |
S | 2(100) | 0 | 2(100) | 0 | 0 | 2(100) | 1(50) | 1(50) | 0 | ND | 0 | 0 | 0 |
| I | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1(50) | 0 | ND | 0 | 0 | 0 | |
| R | 0 | 2(100) | 0 | 2(100) | 2(100) | 0 | 1(50) | 0 | 2(100) | ND | 2(100) | 2(100) | 2(100) | |
| Citrobacter Spp (n = 1) | S | 1(100) | 1(100) | 1(100) | 1(100) | 1(100) | 1(100) | 0 | 0 | 0 | ND | 1(100) | 1(100) | 0 |
| I | 0 | 0 | 0 | 0 | 0 | 0 | 1(100) | 0 | 0 | ND | 0 | 0 | 0 | |
| R | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1(100) | 1(00) | ND | 0 | 0 | 1(100) | |
| K. ozanae (n = 1) | S | 1(100) | 0 | 1(100) | 0 | 0 | 1(100) | 0 | 0 | 0 | ND | 1(100) | 0 | 0 |
| I | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | ND | 0 | 1(100) | 1(100) | |
| R | 0 | 1(1000 | 0 | 1(100) | 1(100) | 0 | 1(100) | 1(100) | 1(100) | ND | 0 | 0 | 0 | |
| Total (n = 1 11) | S | 5(45.5) | 3(27.3) | 9(81.8) | 2(18.2) | 2(18.2) | 11(100) | 3(27.3) | 6(54.5) | 0 | 0 | 2(18.2) | 1(9.1) | 1(9.1) |
| I | 0 | 1(9.1) | 0 | 0 | 1(9.1) | 0 | 1(9.1) | 1(9.1) | 1(9.1) | 0 | 2(18.2) | 4(36.4) | 3(27.3) | |
| R | 6(54.5) | 7(63.6) | 2(18.2) | 9(81.8) | 8(72.7) | 0 | 7(63.6) | 5(45.5) | 10(90.9) | 1(9.1) | 8(72.7) | 7(63.6) | 8(72.7) | |
{AMP: ampicillin; CAZ: Ceftazidime; CIP: ciprofloxacin CRO: Ceftriaxone ; CTX: Cefotaxime ; F: nitrofurantoin; GN: gentamicin; NAL: nalidixic acid; I: intermediate; MEM: meropenem; NOR: norfloxacin; PIP: piperacillin; R: resistant; S:sensitive; SXT: trimethoprim-sulfamethoxazole; TE: tetracycline; NA: not applicable; PEN: penicillin}
Discussion
Diabetes mellitus is a well-known risk factor for urinary tract infections (UTIs), often leading to more complicated and recurrent cases [10]. In this study, the overall prevalence of significant bacteriuria among diabetic patients was 17.5% (95% CI: 12.7%–22.9%), which is consistent with other studies in Ethiopia and elsewhere, showing a range between 14.7% and 22.9% [24–26]. However, it was higher than studies conducted in Addis Ababa, Ethiopia (9.8%) [8], and Ghana (9.2%) [27], but lower than the prevalence reported in Arba Minch, Ethiopia (33.9%) [10]. These variations may result from differences in population characteristics, sample size, geographic location, hygiene practices, and healthcare access.
In this study, Gram-negative bacteria (63.6%) were more prevalent than Gram-positive (36.4%), consistent with previous studies from Metu (64.1% vs. 35.9%) [28] and Arba Minch (72.7% vs. 27.3% for gram negative and positive, respectively) [10]. The most frequently isolated uropathogen was Escherichia coli (45.5%), followed by coagulase-negative staphylococci (21.2%) and Staphylococcus aureus (15.2%). These findings align with reports from Ethiopia and other regions, which consistently identify E. coli as the primary cause of UTI, with prevalence rates of 46.7% to 51.4% [29–31]. Its dominance may be attributed to virulence factors such as fimbriae, capsules, and lipopolysaccharides that enable adherence and colonization to uroepithelial cells [32].
Among Gram-positive bacteria, coagulase-negative staphylococci (CONS) accounted for 21.2%, comparable to findings in Metu (15.4%) [28], Harar (15%) [29], and Hawassa (26.9%) [30]. Staphylococcus aureus was isolated in 15.2% of case, aligning with studies from Metu (17.9%) [28] and Kombolcha (18.4%) [24]. The increasing detection of Gram-positive pathogens, particularly CONS and S. aureus, may be attributed to growing use of urinary catheters and invasive procedures [33].
Urinary tract infections appear to be multifactorial in diabetes, influenced by various diabetes-related risk factors. Significant bacteriuria was significantly associated with female sex [AOR = 3.9], age 25–34 years [AOR = 5.4], previous UTI history [AOR = 4.97], and hospitalization [AOR = 5.97]. The association with female sex is supported by other Ethiopian studies [24, 28, 29]. This may be due to the shorter female urethra, its proximity to the rectum, the absence of bacteriostatic prostatic secretions, poor hygienic condition, and sexual intercourse, all of which facilitate bacterial entry into the bladder [12]. These factors may be more pronounced in resource-limited settings, including Ethiopia, where access to adequate sanitation and health education is limited and sociocultural practices may further increase the risk of urinary tract infections.
The higher odds among patients aged 25–34 years may relate to increased sexual activity in this age group, which has also been identified as a risk factor for UTI in other studies [15, 30, 33]. In the Ethiopian context, this age group represents a highly active and mobile population, which may increase exposure to infection and delay healthcare seeking.
Similarly, patients with a prior history of UTI were almost five times more likely to be infected again, consistent with findings from other studies [28, 29, 32]. This recurrence may result from incomplete eradication, reinfection, or persistent colonization. In diabetic patients, glycosuria may further support bacterial proliferation [31, 34].
Hospitalization was also significantly associated with bacteriuria, possibly due to increased exposure to nosocomial pathogens, invasive procedures such as catheterization, and prolonged hospital stays. In Ethiopia, limited infection prevention resources and overcrowding in healthcare facilities may further contribute to this increased risk.
Antimicrobial resistance among bacterial uropathogens to commonly used antibiotics is on the rise, leaving clinicians with very few options for treating UTIs [34]. The increase in resistance may be attributed to inappropriate and incorrect administration of antimicrobial agents in empiric therapies and a lack of appropriate infection control strategies. S. aureus showed 100% resistance to penicillin, consistent with studies from Addis Ababa and Arba Minch [8, 10]. Resistance mechanisms include penicillinase production and alternative PBPs like PBP-2 A [35]. Gram-negative isolates were highly resistant to ampicillin (73.7%) and tetracycline (57.9%), similar to results from Kombolcha (ampicillin 72.5%, tetracycline 62.9%) [24].
Despite these resistance trends, E. coli remained 100% sensitive to gentamicin and 86.7% to nitrofurantoin, possibly due to less frequent use. These findings agree with reports from Hawassa (100% sensitivity to nitrofurantoin) [36] and Addis Ababa (85.7% sensitivity to gentamicin, 100% to nitrofurantoin) [8].
Multidrug resistance (MDR) was observed in 14 (42.4%) of the isolates, which is comparable to the rate reported in Kombolcha (50.88%) [24]. Among MDR isolates, 52.4% were Gram-negative and 33.3% were Gram-positive, similar to those from echoing studies from Hawassa (57.6% and 42.1% for gram-negative and gram-positive bacteria, respectively) [36] and Dessie (50.0% and 36.4% for gram-negative and gram-positive bacteria, respectively) [37]. E. coli was the most common MDR isolate (53.3%), followed by CONS (42.9%), similar to studies in Kombolcha and Dessie [24, 37].
The prevalence of ESBL-producing Enterobacteriaceae uropathogens was 57.9%, consistent with findings from Ethiopia (51.3%–58%) [25, 38, 39], though higher than reports from Jimma (38.4%) [40], Dessie (8.7%) [37], but lower than Addis Ababa (78.7%) [41]. These variations may be explained by differences in antibiotic prescribing practices, particularly the frequent use of third-generation cephalosporins, inappropriate antibiotic use without susceptibility testing and prescription, limited antimicrobial stewardship programs, and suboptimal infection prevention and control measures. Additionally, differences in study populations, healthcare settings, and laboratory methodologies may contribute to the observed discrepancies.
E. coli (63.6%) was the leading ESBL producer, followed by K. pneumoniae (18.2%), consistent with studies across Ethiopia [25, 38]. While some studies found Klebsiella to be the only ESBL producer, others report it as the predominant isolate over E. coli [41–45].
ESBL-producing isolates exhibited high resistance to ampicillin (90.9%), tetracycline (81.8%), and ciprofloxacin, ceftazidime, and cefotaxime (each 72.7%), as well as to norfloxacin, nalidixic acid, and ceftriaxone (each 63.6%). These findings echo reports from Jimma, where resistance to ampicillin and tetracycline was 100% and 60.8%, respectively [46], and from Dessie [47], where all ESBL-producing isolates were non-susceptible to ampicillin.This highlights the limited effectiveness of commonly used antibiotics against ESBL strains, underscoring the urgent need for antibiotic stewardship and routine ESBL screening.
In conclusion, this study found a UTI prevalence of 17.5% among diabetic patients, with E. coli as the predominant and resistant uropathogen. Key risk factors included female sex, age 25–34, prior UTI, and hospitalization. High antimicrobial resistance, particularly among ESBL-producing organisms, complicates empiric treatment. We recommend routine urine culture and ESBL screening in diabetic patients, implementation of antimicrobial stewardship programs, and strengthening laboratory capacity and resistance surveillance in the hospital setting.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
The authors acknowledge Debremarkos University College of Medicine and Health sciences and the study participants who took part in the study.
Abbreviations
- CLSI
Clinical and Laboratory Standard Institute
- DM
Diabetes Mellitus
- ESBL
Extended-Spectrum Beta-Lactamase
- MDR
Multidrug-Resistant
- MHA
Mueller-Hinton Agar
- UTI
Urinary Tract Infection
Author contributions
YM: Conceived the idea for this study, and participated in conception and design, data collection, and data analysis. YA: Conceived the idea for this study, Participated in conception and design, and conducted data analysis. AM: Conceived the idea for this study, participated in conception and design, conducted data analysis, and drafted and finalized the manuscript for publication.
Funding
No funding was received for this research.
Data availability
The data used to support the findings of this study are included in the article.
Declarations
Ethics approval and consent to participate
This research was conducted in accordance with the Declaration of Helsinki. Ethical clearance was obtained from the Ethical Review Committee (ERC) of Debre Markos University (No: HSC/RCS/135/11/12; Date: 04/04/2023), College of Medicine and Health Sciences, along with a support letter from the Amhara Public Health Institution and the Debre Markos Comprehensive Specialized Hospital medical director. Written informed consent was obtained from all the participants and from the legal guardians of the illiterate participants. Moreover, the confidentiality of the patient’s information was safeguarded.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Bloom DE, Cafiero E, Jané-Llopis E, Abrahams-Gessel S, Bloom LR, Fathima S, et al. The global economic burden of noncommunicable diseases. Program on the Global Demography of Aging; 2012.
- 2.Carracher AM, Marathe PH, Close KL. International diabetes federation 2017. J Diabetes. 2018;10(5):353–6. [DOI] [PubMed] [Google Scholar]
- 3.Lin X, Xu Y, Pan X, Xu J, Ding Y, Sun X, et al. Global, regional, and National burden and trend of diabetes in 195 countries and territories: an analysis from 1990 to 2025. Sci Rep. 2020;10(1):14790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Wolde HF, Derso T, Biks GA, Yitayal M, Ayele TA, Gelaye KA, et al. High hidden burden of diabetes mellitus among adults aged 18 years and above in urban Northwest Ethiopia. J Diabetes Res. 2020;2020:9240398. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Yu S, Fu AZ, Qiu Y, Engel SS, Shankar R, Brodovicz KG, et al. Disease burden of urinary tract infections among type 2 diabetes mellitus patients in the U.S. J Diabetes Complications. 2014;28(5):621–6. [DOI] [PubMed] [Google Scholar]
- 6.Yismaw G, Asrat D, Woldeamanuel Y, Unakal CG. Urinary tract infection: bacterial etiologies, drug resistance profile and associated risk factors in diabetic patients attending Gondar university Hospital, Gondar, Ethiopia. Eur J Experimental Biology. 2012;2(4):889–98. [Google Scholar]
- 7.Yeshitela B, Gebre-Selassie S, Feleke Y. Asymptomatic bacteriuria and symptomatic urinary tract infections (UTI) in patients with diabetes mellitus in Tikur Anbessa specialized university Hospital, addis Ababa, Ethiopia. Ethiop Med J. 2012;50(3):239–49. [PubMed] [Google Scholar]
- 8.Yenehun Worku G, Belete Alamneh Y, Erku Abegaz W. Prevalence of bacterial urinary tract infection and antimicrobial susceptibility patterns among diabetes mellitus patients attending Zewditu memorial Hospital, addis Ababa, Ethiopia. Infect Drug Resist. 2021;14:1441–54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.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. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Mama M, Manilal A, Gezmu T, Kidanewold A, Gosa F, Gebresilasie A. Prevalence and associated factors of urinary tract infections among diabetic patients in Arba minch Hospital, Arba minch province, South Ethiopia. Turkish J Urol. 2019;45(1):56. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Nayaju T, Upreti MK, Ghimire A, Shrestha B, Maharjan B, Joshi RD, et al. Higher prevalence of extended spectrum β-Lactamase producing uropathogenic Escherichia coli among patients with diabetes from a tertiary care hospital of Kathmandu, Nepal. Am J Trop Med Hyg. 2021;105(5):1347–55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Vasudevan R. Urinary tract infection: an overview of the infection and the associated risk factors. J Microbiol Exp. 2014;1(2):00008. [Google Scholar]
- 13.Nigussie D, Amsalu A. Prevalence of uropathogen and their antibiotic resistance pattern among diabetic patients. Turkish J Urol. 2017;43(1):85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Chaudhary B, Charu C, Shukla S. Bacteriology of urinary tract infection and antibiotic susceptibility pattern among diabetic patients. Int J Bioassays. 2014;3(08):3224–7. [Google Scholar]
- 15.Woldemariam HK, Geleta DA, Tulu KD, Aber NA, Legese MH, Fenta GM, et al. Common uropathogens and their antibiotic susceptibility pattern among diabetic patients. BMC Infect Dis. 2019;19:1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Bitew A, Tsige E. High prevalence of multidrug-resistant and extended-Spectrum β-lactamase-producing Enterobacteriaceae: a cross-sectional study at Arsho advanced medical laboratory, Addis Ababa, Ethiopia. Journal of Tropical Medicine. 2020;2020. [DOI] [PMC free article] [PubMed]
- 17.Abayneh M, Worku T. Prevalence of multidrug-resistant and extended-spectrum beta-lactamase (ESBL)-producing gram-negative bacilli: A meta-analysis report in Ethiopia. Drug Target Insights. 2020;14:16–25. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Bono MJ, Leslie SW, Reygaert WC. Uncomplicated urinary tract infections. StatPearls [Internet]: StatPearls Publishing; 2023. [Google Scholar]
- 19.Karah N, Rafei R, Elamin W, Ghazy A, Abbara A, Hamze M, et al. Guideline for urine culture and biochemical identification of bacterial urinary pathogens in low-resource settings. Diagnostics. 2020;10(10):832. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Priest AL. Development of a nutrition education workbook for Local, Regional, and Over-the-Road (OTR) truck drivers. California State University, Long Beach; 2021.
- 21.Derese B, Kedir H, Teklemariam Z, Weldegebreal F, Balakrishnan S. Bacterial profile of urinary tract infection and antimicrobial susceptibility pattern among pregnant women attending at Antenatal Clinic in Dil Chora Referral Hospital, Dire Dawa, Eastern Ethiopia. Therapeutics and clinical risk management. 2016:251 – 60. [DOI] [PMC free article] [PubMed]
- 22.Clinical ILS. M100. Performance standards for antimicrobial susceptibility testing 32nd. Clinical and Laboratory Standards Institute; 2022.
- 23.Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81. [DOI] [PubMed] [Google Scholar]
- 24.Oumer O, Metaferia Y, Gebretsadik D. Bacterial uropathogens, their associated factors, and antimicrobial susceptibility pattern among adult diabetic patients in two health centers at Kombolcha town, Northeastern Ethiopia. SAGE Open Med. 2022;10:20503121221139149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Assegu D. Prevalence of Extended-Spectrum Beta-Lactamase producing bacteria isolated from urine of diabetes Patients, their drug resistance profile and associated factors at Hawassa university comprehensive specialized hospital Sidama. Hawassa, Ethiopia: HU; 2022. [Google Scholar]
- 26.Mageto VM, Gatwiri MS, Njoroge W. Uropathogens antibiotic resistance patterns among type 2 diabetic patients in Kisii teaching and referral Hospital, Kenya. Pan Afr Med J. 2018;30(1). [DOI] [PMC free article] [PubMed]
- 27.Forson AO, Menkah DA, Quarchie MN, Dhikrullahi SB, Olu-Taiwo M, Codjoe FS. Bacterial drug-resistance patterns and genetic diversity of bacteria-associated bacteriuria in diabetic patients in Ghana. IJID Reg. 2021;1:142–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Gutema T, Weldegebreal F, Marami D, Teklemariam Z. Prevalence, antimicrobial susceptibility pattern, and associated factors of urinary tract infections among adult diabetic patients at Metu Karl heinz referral Hospital, Southwest Ethiopia. Int J Microbiol. 2018;2018(1):7591259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Abate D, Kabew G, Urgessa F, Meaza D. Bacterial etiologies, antimicrobial susceptibility patterns and associated risk factors of urinary tract infection among diabetic patients attending diabetic clinics in Harar, Eastern Ethiopia. East Afr J Health Biomedical Sci. 2017;1(2):11–20. [Google Scholar]
- 30.Mohammed A, Beyene G, Teshager L, Daka D. Urinary pathogenic bacterial profile, antibiogram of isolates and associated risk factors among diabetic patients in Hawassa town, Southern ethiopia: a cross-sectional study. Urol Nephrol Open Access J. 2020;8(4):84–91. [Google Scholar]
- 31.Borj M, Taghizadehborojeni S, Shokati A, Sanikhani N, Pourghadamyari H, Mohammadi A, et al. Urinary tract infection among diabetic patients with regard to the risk factors, causative organisms and their antimicrobial susceptibility profiles at Firoozgar Hospital, Tehran, Iran. Int J Life Sci Pharma Res. 2017;7(3):L38–47. [Google Scholar]
- 32.Kebamo S, Dabso R, Deressa A, Gebrie M. Urinary tract infection: bacterial etiologies, drug resistance profile and associated risk factors among diabetic patients attending Nekemte referral Hospital, Ethiopia. Am J Curr Microbiol. 2017;5(1):19–31. [Google Scholar]
- 33.Odoki M, Almustapha Aliero A, Tibyangye J, Nyabayo Maniga J, Wampande E, Drago Kato C, et al. Prevalence of bacterial urinary tract infections and associated factors among patients attending hospitals in Bushenyi district, Uganda. Int J Microbiol. 2019;2019(1):4246780. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Denekew Y. Food, medicine and health care administration and control authority. 2014.
- 35.Samuel O, Mathew A, Agboola D, Mopelola A, Joshua O, Tosin A. Asymptomatic urinary tract infection in diabetic patients in Ago–Iwoye, Ogun State, Nigeria. J Am Sci. 2014;10(4):72–8. [Google Scholar]
- 36.Mohammed A, Beyene G, Teshager L. Urinary pathogenic bacterial profile, antibiogram of isolates and associated risk factors among diabetic patients in Hawassa town, Southern ethiopia: a cross-sectional study. Urol Nephrol Open Access J. 2020;8(4):84–91. [Google Scholar]
- 37.Alemu M, Belete MA, Gebreselassie S, Belay A, Gebretsadik D. Bacterial profiles and their associated factors of urinary tract infection and detection of extended spectrum beta-lactamase producing gram-negative uropathogens among patients with diabetes mellitus at Dessie referral Hospital, Northeastern Ethiopia. Diabetes Metabolic Syndrome Obesity: Targets Therapy. 2020;13:2935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Yakubu H, Muhammed B, Mukhtar M, Kalgo Z. Prevalence of extended-spectrum beta lactamase and AmpC producing Enterobacteriaceae among diabetic patients in Bauchi State, Nigeria. Bayero J Pure Appl Sci. 2022;13(1):546–53. [Google Scholar]
- 39.Ouedraogo A-S, Sanou M, Kissou A, Sanou S, Solaré H, Kaboré F, et al. High prevalence of extended-spectrum ß-lactamase producing Enterobacteriaceae among clinical isolates in Burkina Faso. BMC Infect Dis. 2016;16(1):1–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Siraj SM, Ali S, Wondafrash B. Extended-spectrum β-lactamase production in Klebsiella pneumoniae and Escherichia coli at Jimma university specialized hospital, south-west, Ethiopia. Mol Microbiol Res. 2015;5.
- 41.Legese MH, Weldearegay GM, Asrat D. Extended-spectrum beta-lactamase-and carbapenemase-producing Enterobacteriaceae among Ethiopian children. Infect Drug Resist. 2017;10:27–34. [DOI] [PMC free article] [PubMed]
- 42.Thapa R, Lamichhane P, Banjara MR, Acharya GP. Prevalence of extended spectrum beta lactamase producing uropathogens in pregnant women. Prevalence. 2015;8(1).
- 43.Moyo SJ, Aboud S, Kasubi M, Lyamuya EF, Maselle SY. Antimicrobial resistance among producers and non-producers of extended spectrum beta-lactamases in urinary isolates at a tertiary hospital in Tanzania. BMC Res Notes. 2010;3:1–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Gebremariam G, Legese H, Woldu Y, Araya T, Hagos K, GebreyesusWasihun A. Bacteriological profile, risk factors and antimicrobial susceptibility patterns of symptomatic urinary tract infection among students of Mekelle University, Northern Ethiopia. BMC Infect Dis. 2019;19:1–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Al Yousef SA, Younis S, Farrag E, Moussa HS, Bayoumi FS, Ali AM. Clinical and laboratory profile of urinary tract infections associated with extended spectrum β-lactamase producing Escherichia coli and Klebsiella pneumoniae. Annals Clin Lab Sci. 2016;46(4):393–400. [PubMed] [Google Scholar]
- 46.Abayneh M, Tesfaw G, Abdissa A. Isolation of Extended-Spectrum β-lactamase- (ESBL-) producing Escherichia coli and Klebsiella pneumoniae from patients with Community-Onset urinary tract infections in Jimma university specialized Hospital, Southwest Ethiopia. Can J Infect Dis Med Microbiol. 2018;2018:4846159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Alemu M, Belete MA, Gebreselassie S, Belay A, Gebretsadik D. Bacterial profiles and their associated factors of urinary tract infection and detection of extended spectrum beta-lactamase producing gram-negative uropathogens among patients with diabetes mellitus at Dessie Referral Hospital, Northeastern Ethiopia. Diabetes, Metabolic Syndrome and Obesity. 2020:2935-48. [DOI] [PMC free article] [PubMed]
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