Bacterial profile, their antibiotic susceptibility pattern, and associated factors of urinary tract infections in children at Hiwot Fana Specialized University Hospital, Eastern Ethiopia

Shambel Mekonnen; Tewodros Tesfa; Tadesse Shume; Fikru Tebeje; Kedir Urgesa; Fitsum Weldegebreal

doi:10.1371/journal.pone.0283637

Abstract

Background

Urinary tract infections (UTIs) are common pediatric infections and contribute to high morbidity and mortality. At present, the antimicrobial resistance emergency has quadrupled worldwide and poses a serious threat to the treatment of patients. However, there have been few studies on UTIs in children in Ethiopia, particularly in the east.

Objective

This study aimed to assess the bacterial profile of urinary tract infections, their susceptibility to antimicrobial agents, and associated factors in under-five children at Hiwot Fana Specialized University Hospital, eastern Ethiopia.

Method

We conducted hospital-based quantitative study on 332 consecutively selected under-five children from March 20 to June 10, 2021. Parents and guardians were interviewed to collect data using a structured questionnaire. Random urine samples were collected aseptically, and standard microbiological techniques were used to identify the bacteria and test for susceptibility to various antibiotics. Data were entered into Epi Info version 7 and exported to Statistical Package for the Social Sciences (SPSS) version 25 for analysis. Data were analyzed using descriptive analysis, bivariate, and multivariable logistic regression analysis. The crude odds ratio (COR) and adjusted odds ratio (AOR) with their respective 95% confidence intervals (CI) were used to determine the significance of the predictors. A p-value at a 95% confidence interval of less than 0.05 was considered statistically significant.

Results

The overall prevalence of bacterial urinary tract infections was 80 (24.1%) 95% CI:19.40–29.00%). Most of the bacterial isolates 55 (68.75%) were gram-negative bacteria, predominantly E. coli 23 (28.75%) and K. pneumoniae 10 (12.50%). Being a rural resident (AOR: 4.10, 95%CI: 1.45 11.54), uncircumcised male (AOR: 3.52, 95%CI: 1.33, 9.39), previous history of antibiotic usage (AOR: 7.32, 95%CI: 2.11, 25.37), indwelling catheterization (AOR: 10.35, 95%CI: 3.74, 28.63), previous history of urinary tract infections (AOR: 5.64, 95% CI: 1.36, 23.38), and urinary frequency (AOR: 5.56, 95%CI: 2.03, 15.25) had higher odds of culture positive result. The majority of the isolates have shown high levels of antibiotic resistance. Meropenem, ciprofloxacin, and amoxicillin-clavulanic acid were effective against gram-negative uropathogens, whereas rifampin and ciprofloxacin were the most sensitive drugs for gram-positive isolates. From the tested bacterial isolates, 53/86 (61.6%), 11/86 (11.6%), and 2/86 (2.3%) were found to have multidrug resistance (MDR), extreme drug resistance (XDR), and pan drug resistance (PDR), respectively.

Conclusions

About one-fourth of the children were culture-positive for many types of bacterial uropathogens; this is higher compared with most of the previous studies in Africa. Rural dwellers, uncircumcised males, indwelling catheterization, a history of antibiotic use and urinary tract infection, and frequent urination all had a higher risk of bacterial infections. Many isolates were resistant to multiple drugs, primarily beta-lactams. Urinary tract infections as well as the growth and spread of resistant bacterial pathogens should be monitor regularly.

Citation: Mekonnen S, Tesfa T, Shume T, Tebeje F, Urgesa K, Weldegebreal F (2023) Bacterial profile, their antibiotic susceptibility pattern, and associated factors of urinary tract infections in children at Hiwot Fana Specialized University Hospital, Eastern Ethiopia. PLoS ONE 18(4): e0283637. https://doi.org/10.1371/journal.pone.0283637

Editor: Ulrich Nübel, Leibniz-Institute DSMZ, GERMANY

Received: February 25, 2022; Accepted: March 14, 2023; Published: April 5, 2023

Copyright: © 2023 Mekonnen 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 paper and its Supporting Information files.

Funding: This research data collection finance was covered by Haramaya university's postgraduate directorate. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. None of the authors received a salary from the funders.

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

Abbreviations and acronyms: AST, Antimicrobial Susceptibility Test; ATCC, American Type Culture Collection; API, Analytical Profile Index; CFU, Colony Forming Units; CLED, Cysteine Lactose Electrolyte Deficient; CLSI, Clinical Laboratory Standards Institute; CoNS, Coagulase Negative Staphylococci; ECDC, European Centre for Disease Prevention and Control; ESBLs, Extended-spectrum Beta-Lactamases; HFSUH, Hiwot Fana Specialized University Hospital; KIA, Kligler Iron Agar; MDR, Multi-Drug Resistance; PBP2a, Penicillin-Binding Proteins 2a; PDR, Pan Drug Resistance; SOP, Standard Operating Procedures; SPSS, Statistical Package for the Social Sciences; UTI, Urinary Tract Infections; WHO, World Health Organization; XDR, Extremely Drug Resistance

Introduction

Infections of the urinary tract (UTIs) are some of the most common causes of acute morbidity and chronic medical conditions like hypertension, failure to thrive, and end-stage renal disease in children [1]. UTIs, which are caused by bacteria, are a serious public health problem and a significant cause of morbidity in infant boys, older men, women of all ages, and about 5% of girls and 2% of boys by the age of seven [1]. Virulence factors used by the main uropathogens are adherence, production of the toxin, immune evasion, and iron acquisition [2]. UTIs begin when bacterial uropathogens reside anywhere in the urinary tract: the kidney, ureter, bladder, and urethra. Expression of pili and adhesins results in colonization and invasion of the superficial umbrella cells. Host inflammatory responses begin to clear extracellular bacteria, though some bacteria evade the immune system through host cell invasion, morphological changes, multiplication, and biofilm formation, as well as by producing toxins and proteases that cause host cell damage, releasing essential nutrients that promote bacterial survival and ascent to the kidneys, and progressing to bacteremia [2, 3]. The clinical manifestations of UTIs depend on the causative agent, the severity of the infection, the parts of the urinary tract involved, and the immune response of patients [4]. UTIs can be lower (cystitis) or upper (pyelonephritis) UTIs based on the patient’s clinical manifestations [5]. Serious sequelae include frequent recurrences, Urosepsis, renal scarring, progressive kidney damage in young children, preterm birth, and high-level antibiotic resistance, which can lead to high health risks, mortality, and a considerable financial burden on society [2, 6]. Globally, UTIs are common bacterial infections in humans that affect more than 150 million people and require enormous antibiotic expenditure yearly, with a global cost of more than 6 billion US dollars [7, 8]. UTIs are a common disease in developing countries, with an estimated incidence of at least 8.3 million doctor visits annually [8].

The etiologic agents of UTIs are different and usually depend on the time, geographical area, and age of patients [9]. The most prevalent bacteria causing UTIs are Escherichia coli, followed by Klebsiella spp., Staphylococcus spp., Proteus spp., Pseudomonas aeruginosa, Enterobacter spp., Serratia spp., Citrobacter spp., Enterococcus spp., and Streptococci agalactiae, with variations in their sequence of prevalence in pediatric patients [10, 11].

Several associated factors have been identified in the literature; however, the studies are not reproducible. Age, gender, premature children, and young children with severe constipation are risk factors more commonly associated with bacterial UTIs and result in a high financial burden. Other risk factors include prolonged hospitalization, congenital urinary tract obstruction, males who have not undergone circumcision, malnutrition, a previous history of UTI, urinary catheterization, and malnutrition [12–15]. The antimicrobial resistance (AMR) emergence of bacterial uropathogenic has challenged the current therapies to treat and control the spread of infections [16], and treatment has not improved and does not prevent reinfections [17]. Especially, UTIs caused by resistant bacteria are an important global medical cause of severe infections with increasing rates of morbidity and mortality [18], and they can also result in prolonged hospital stays and poverty for pediatric patients [19, 20]. In third-world countries, the problem is immense, as most healthcare facilities lack culture-based diagnostic facilities [20, 21]. Recently, multidrug-resistant (MDR) and carbapenem-resistant Enterobacterales (CREs) have emerged and gradually become a significant public health challenge [22]. Several recent studies reported the emergence of MDR bacterial uropathogens [23–25] that increase the need for the routine application of antimicrobial susceptibility testing to detect the antibiotic of choice as well as the screening of the emerging MDR strains [14, 15]. MDR, extensively drug-resistant (XDR), and pan drug-resistant (PDR) bacteria have been clearly defined according to standardized international terminology developed by the European Centre for Disease Control (ECDC) and the Center for Disease Control and Prevention (CDC), Atlanta [26]. To qualify as MDR, an agent must have gained nonsusceptibility to at least one antimicrobial agent from three or more categories. Being resistant to at least one agent in all but two or fewer antimicrobial categories is XDR (i.e., bacterial isolates remain susceptible to only one or two antimicrobial categories). Non-susceptibility to any agent in any antimicrobial category is PDR. In Ethiopia, there are limited studies available on the prevalence, antibiotic susceptibility profiles, and associated factors of UTIs in children under the age of five, and this subject has never been addressed in the study area.

Materials and methods

Study area and period

We conducted the study in Harar town at Hiwot Fana Specialized University Hospital (HFSUH), eastern Ethiopia, from March 20 to June 10, 2021. HFSUH is the referral teaching hospital for Health and Medical Sciences students at Haramaya University that provides healthcare services to more than 5 million people around Harar and neighboring regions.

Study design and population

We conducted hospital-based quantitative study to assess the data and know the status of bacterial UTIs and associated factors in children hospitalized with suspected cases. All under-five children who were clinically suspected of UTIs and their parents or guardians who agreed to give consent to participate in the study were included from March 20 to June 10, 2021. Children under the age of five who had taken antibiotics within the previous 10 days of the data-collecting period were excluded. This study’s source population included all patients who visited HFSUH for a specific clinical condition diagnosis. However, during the study period, children who went to the Mother and Child Health (MCH) clinic for UTI diagnoses were regarded as the target population.

Sample size determination and sampling technique

The sample size of 332 under-five children was determined by taking the 26.8% prevalence [27] at a 95% confidence interval (CI), a 5% margin of error, and a 10% non-respondent rate. Study participants were recruited by convenient sampling technique until we got the required sample size.

Data and sample collection

Data on sociodemographic characteristics, clinical future, medical history, and associated factors were collected using a pretested, structured questionnaire adopted after reviewing various literature [12, 15, 28, 29] through a face-to-face interview of parents or guardians in their local languages and collecting urine samples from under-five children at the same time. The interviewer nurses performed an appropriate physical examination and card review of the child during medical registration. For toilet-trained children, a freshly cleaned random urine sample was collected in a wide-mouthed, sterile, leak-proof bottle after instructing the parents or guardians of the enrolled children to clean their genitals with soap and water. Urine samples were obtained from children who were not toilet trained by urethral catheterization, suprapubic aspiration (SPA), use of a pediatric urine collection bag, or leaving the child with the diaper off and obtaining a clean catch of urine when the child voids. Contamination was managed by giving proper instructions on how to handle the specimen correctly. The samples were delivered to the microbiology laboratory at Haramaya University College of Health and Medical Sciences within 30 minutes of collection [30], in a cold box.

Bacterial isolation and identification

We used Chesbrough’s recommended culture and biochemical procedures for bacterial isolation and phenotypic characterizations [31]. Well-mixed urine specimens were inoculated on 5% blood agar and Cysteine Lactose Electrolyte Deficient Medium (CLED) (HiMedia, Mumbai, India) plates [5, 32], using a 0.001 ml calibrated loop. After overnight aerobic incubation at 37°C, colony morphology, gram staining, and biochemical tests were used for phenotypic characterizations [31] (supplementary material).

Identifications of gram-negative bacterial species were determined by performing a total of eleven biochemical reactions (Oxoid Ltd, Basingstoke, UK), including triple sugar iron agar (sugar fermentation, gas, H2S production, and gas), indole, urease, citrate utilization, oxidase, lysine iron agar, methyl red/Voges Proskauer (MR/VP), phenylalanine deaminase, mannitol, ornithine decarboxylase, and motility test (supplementary material). Identifications of Enterobacterales and Pseudomonas bacterial isolates were confirmed using the Analytical Profile Index (API) 20E/20NE identification kit (BioMerieux, France) [33]. However, gram-positive isolates were identified by using nine biochemical tests (Oxoid Ltd, Basingstoke, UK), including catalase, coagulase, coagulase mannitol, DNase, novobiocin sensitivity, bacitracin sensitivity, bile esculin test, urase, ornithine decarboxylase, Pyrrolidonyl arylamidase (PYR), and hemolytic characteristics on blood agar [5, 31, 32], (supplementary material).

Antimicrobial susceptibility testing (AST)

Based on recommendations from the Clinical and Laboratory Standards Institute (CLSI) [34], modified Kirby-Bauer disk diffusion techniques were used for susceptibility testing. The suspension of bacterial inoculum, equivalent to 0.5 McFarland standards, was uniformly spread on Mueller–Hinton agar (HiMedia, Mumbai, India) plates using a sterile applicator cotton swab.

The following antimicrobial categories were tested (Oxoid, LTD, Basingstoke, and Hampshire, UK): aminoglycosides group (gentamicin (GN 10μg) and (tobramycin (TN 10μg), penicillin group (ampicillin (AMP 10μg), beta-lactamase inhibitor combination group (amoxicillin-clavulanic acid (AMC 10μg), cephalosporins class (ceftazidime (CAZ 30μg), (cefoxitin (CXT 30μg), and (cefazolin, Cz 30μg), fluoroquinolones group (ciprofloxacin (CIP 5μg), (nalidixic acid (NA 30μg), and (rifampin (RF 5μg), nitrofuran categories (nitrofurantoin (NI 300μg), competitive Inhibitors group (trimethoprim/sulphamethazole (TS 1.25/23.75μg), tetracycline (T 30μg), and phenicol (chloramphenicol (C 30μg), macrolides class (azithromycin (AZM 10 μg) and erythromycin (E 15μg), lincosamides class (clindamycin (CN 2μg), a carbapenem (meropenem (MEM 10μg), glycopeptides (vancomycin (VA 30μg), and (azetronam (ATM 30μg). These antibacterial disks were selected depending on local availability, pathogens, and 2020 CLSI recommendations. The interpretative guidelines set by the CLSI [34], were used to interpret the result as sensitive (S), intermediate (I), or resistant (R).

Data quality control

To ensure the validity of the questionnaire, the English version was translated into local languages (Amharic and Afan Oromo), and vice versa, by separate language experts and pretested at Jugol Hospital. Data collectors (laboratory personnel and nurses) were trained regarding all stages of the data collection process. To prepare the culture media, manufacturers’ directions were followed. The sterility of culture media was checked by incubating overnight at 35–37°C without specimen inoculation. The performance of the culture medium and drug disks was checked using reference strains such as E. coli (American Type Culture Collection, ATCC 25922), P. aeruginosa (ATCC 27853), and Staphylococcus aureus (ATCC 25923) [34]. To perform a drug susceptibility test, the turbidity of the bacterial suspension was adjusted to the 0.5 McFarland standard.

Method of data analysis

The data were double-entered into Epi Info version 7 and exported to Statistical Package for Social Science (SPSS) version 25 for analysis. A descriptive statistical tool was used to summarize the findings. The results were presented in words, graphs, and tables. Bivariate and multivariable logistic regression models were used to predict the relationship between dependent and independent variables. In the bivariate logistic regression model, independent variables with a P-value of less than 0.25 and clinical relevance of the variables were considered candidates for the multivariable logistic regression model [35]. The crude odds ratio (COR) and adjusted odds ratio (AOR) with their respective 95% CI were used to determine the significance of predictors. Finally, every variable with P-values less than 0.05 at a 95% confidence interval was considered statistically significant. Hosmer and Lemeshow goodness-of-fit-tests were used for adherence to multivariate logistic regression model assumptions, and a p-value > 0.05 was considered a good fit.

Ethical considerations

An ethical review was obtained from the Haramaya University Institutional Health Research Ethics Review Committee (IHRERC) of the College of Health and Medical Sciences before conducting research. The reference number of the ethical letter was "Ref No IHRERC /027/2021)". An official letter of support was written to HFSUH. Each parent or guardian of a child received information on the study, including its goals, methods, potential risks, and benefits. The study participants were informed of their right to refuse or withdraw from the study at any time. Each study was unaffected by participants’ refusal to take part. Informed, voluntary, written, and signed parental consent was obtained from all parents or guardians of children after explaining the purpose and objective of the study. Participants’ confidentiality was strictly assured. Moreover, the positive case was reported to the attending physician or health professional. Besides, both study participants and data collectors used sanitizer and wore face masks to protect them from COVID-19.

Result

Socio-demographic characteristics

A total of 332 study participants were enrolled in this study. Out of these participants, 64.2% were males. The median age of the children was 2 years. Most of them, 88.3%, were older than 12 months. About 69% of children were rural dwellers. Around 41.9% of study participants had parents or guardians who were unable to read and write, and 54.8% were farmers (Table 1).

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Table 1. Socio-demographic characteristics of under-five children at Hiwot Fana Specialized University Hospitals, eastern Ethiopia, 2021 (n = 332).

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Clinical future and medical history

About 139/213 (65.3%) of the males were circumcised. More than half of the participants were from inpatient wards. Most of the children (87.7%) did not have a previous history of antibiotic usage, 90.1% did not have a previous history of UTI, and 78.3% did not have a history or diagnosis of diabetes mellitus. About 29.5% of children have indwelling catheters. The majority of study participants did not complain about hematuria (78%), convulsion (74.4%), or urinary frequency (69.6%) during diagnosis. One-third of the children had a fever (Table 2).

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Table 2. Clinical future and medical history of under-five children at HFSUH, eastern Ethiopia, 2021 (n = 332).

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Prevalence of urinary tract infection

The overall prevalence of bacterial UTI was 24.1% (80/332; 95% CI: 19.4–29). A total of 86 bacterial isolates were identified. About 68.75% (55\80) of isolates were Gram-negative bacteria. In this study, the prevalence of UTI was 25.2% (30/119) in females, 28.2% (11/39) in the age <12 months, and 27.9% (64/229) in rural dwellers. There was also a higher frequency of UTI among those with a previous history of UTI (47.7%, 17/36), previous antimicrobial usage (43.9%, 18/39), children who had hematuria (42.5%, 31/73), uncircumcised boys (39.5%, 30/76), and catheterized patients (35.7%, 35/98).

Bacterial profile of uropathogens

Of the total 80 (24.1%) culture-positive bacteria, pure gram-negative bacterial species were predominant 55 (68.75%); the most frequently isolated were E. coli 23 (28.75%), followed by K. pnemumoniae 10 (12.5%). From gram-positive bacteria, S. aureus 5 (6.25%) has been isolated more commonly, followed by Enterococcus spp. 4 (5%), while 12 (15%) of the children had a mixed infection. Pathogens that cause mixed infections include Staphylococcus saprophyticus, Citrobacter spp., E. coli, K. pnemumoniae, Tatumella ptyseos, Enterobacter aerogenes, Streptococcus pyogenes, Salmonella paratypi A, S. aureus, Klebsiella ozaniae/Klebsiella rhinoscleromatis, and Enterococcus spp. (Fig 1).

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Fig 1. Frequency and type of bacterial isolated from the urine of under-five children at HFSUH, eastern Ethiopia, 2021.

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Associated factors

In the bivariate logistic regression analysis, 12 independent variables with a p-value of less than 0.25 were candidates for the multivariable logistic regression analysis (Table 3).

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Table 3. Factors associated with UTIs among under-five children at HFSUH, eastern Ethiopia, 2021.

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Antimicrobial susceptibility pattern

Gram-negative bacteria. The antimicrobial susceptibility test was performed on 86 bacterial isolates. About 92.7% of gram-negative isolates were susceptible to meropenem, 83.1% to ciprofloxacin, and 77.9% to amoxicillin-clavulanic acid. Additionally, 8.75% of the isolates showed sensitivity to all the antimicrobial agents used in the test panel. While, 90.5% of isolates exhibited resistance to ampicillin, 77.8% to tetracycline, 73% to cefazolin, and 72% to trimethoprim- trimethoprim-sulphamethoxazole. About 92.8% of E. coli were susceptible to meropenem, 75% to amoxicillin-clavulanic acid, and 71.4% to ciprofloxacin. However, it was 82% and 82.1% resistant to ampicillin and tetracycline, respectively (Table 4).

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Table 4. Antimicrobial susceptibility pattern of gram-negative bacteria isolated from the urine of under-five children attending at HFSUH, eastern Ethiopia, 2021.

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Gram-positive bacteria.

Among the tested antibiotics, rifampin (81.8%), ciprofloxacin (81.25%), and gentamycin (68.75%) were effective against gram-positive isolates. On the other hand, they showed resistance to tetracycline (56.2%), tobramycin (54.5%), and trimethoprim-sulphamethoxazole (54%). S. aureus was the most predominant isolate, which revealed 83.3% sensitivity to each of rifampin and ciprofloxacin. However, there is 83.3% resistance to each of the antibiotics, ampicillin and tetracycline (Table 5).

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Table 5. Antimicrobial susceptibility pattern of gram-positive bacteria isolated from the urine of under-five children at HFSUH, eastern Ethiopia, 2021.

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MDR patterns of bacterial isolates.

The overall MDR rate of the isolates was 61.6% (95% CI: 51–73). A higher rate of MDR was observed in gram-negative bacterial isolates compared to gram-positives. The majority of the gram-negative isolates 47/68 (69.1%) revealed MDR. Particularly, the highest MDR was observed in E. coli, 20/53(37.7%) followed by K. pneumoniae, 9/53 (17%), Citrobacter spp. 8/53 (15.1%). Multidrug resistance was also observed in a gram-positive bacterial isolate, which was 6/18(33.3%). About 3/53(5.7%) of MDR was observed in S. aureus (Table 6).

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Table 6. The pattern of MDR bacteria among under-five children at the HFSUH, eastern Ethiopia, 2021.

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Incidence of MDR, XDR, and PDR strains.

The antimicrobial susceptibility profiles of 86 bacterial isolates were identified. From the detected bacterial strains, 53(61.6%) bacterial strains were MDR, 10 (11.6%) were XDR, and 2 (2.3%) were PDR. Among the tested gram-negative isolates, 10/68(14.71%) were XDR, and 2/68(2.94%) were PDR. Almost all of the XDR was attributed to E. coli (8). However, the incidence of XDR and PDR strains was not observed in all identified gram-positive bacteria (Table 7).

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Table 7. Phenotypic resistance profile of bacteria isolated from the urine of under-five children at HFSUH, eastern Ethiopia, 2021.

https://doi.org/10.1371/journal.pone.0283637.t007

Discussion

Although UTIs can cause serious illness in children, the definitive diagnosis of UTIs is often overlooked in most developing countries due to a lack of facilities, high laboratory costs, and the challenges of obtaining urine from children, especially those who would not void voluntarily [14]. Presently, the effectiveness of commonly prescribed drugs is decreasing globally due to increasing resistant strains. As a result, an infection caused by those strains is challenging; it becomes difficult to treat [5, 36]. Colony counts below 10⁵ CFU/mL in random, clean urine samples for toilet trained children and below 5 x 10⁴ CFU/mL for children under 2 years old and catheterized or SPA urine are not considered significant for defining a UTI [37]; however, this cannot be ignored in patients with immunosuppressed.

In this study, the overall prevalence of bacterial UTIs in children was 24.1%, which is in agreement with other studies in Hawassa, Ethiopia (27.5%) [14], Uganda (26.8%) [27], and Tanzania (20.65%) [38]. However, this finding was higher than studies conducted in Bahirdar, Ethiopia (16.7%) [15], Abakaliki, Nigeria (3%) [39], Enugu, Nigeria (11%) [13], and Dar es Salaam, Tanzania (16.7%) [40]. The disparity between studies could result from the difference in nutritional status, immunity of the population, and method of lab diagnosis [41]. Other explanations could be variations in sample size, the definition of bacteriuria, and the duration of the study.

This study’s most common isolate was Escherichia coli (28.75%), which is comparable to some studies of Ethiopia [14, 15]. E. coli is the most common organism identified in nearly all UTI studies worldwide: 71.7% [13], 31.8% [38], 35.7% [42], and 41.2% [43]. The high rate of E. coli might be due to the high abundance of E. coli in the fecal flora, which ascends through the genitalia to cause UTI, in addition to having a unique structure such as P-fimbriae or pili adherence factors, which promote E. coli attachment to the uroepithelial cells, allowing for multiplication and tissue invasion [44]. But, this finding contradicts a study done in Abakaliki, Nigeria in which Klebsiella spp. (24.5%) were most commonly isolated [39], and in Uganda, Proteus spp. (39.5%) were most frequently isolated [27]. This could be due to variations in specimen collection techniques and the existence of many virulence factors [44–46].

On the analysis, being a rural resident was significantly associated with bacterial UTIs (p = 0.008) because the majority of study participants were from rural settings and host fecal flora might be the source of the infections [47]. Boys who were not circumcised had a nearly four-fold higher risk of UTIs. This could be because men with uncircumcision and obstructive uropathies have a higher risk of UTIs. As a result, a tight foreskin may interfere with the normal passage of urine and hinder the full emptying of the bladder [48]. patients who self-medicated without prescription were 7 times more likely to acquire UTIs; this finding contrast with another study conducted in Hawassa, Ethiopia [14]. These variations could be attributed to the low rate of self-medication in Hawassa (5.9%) when compared to this study’s (12%).

The history of previous UTIs shows six times more susceptibility to culture-positive results than the correlative one, similar to earlier studies in Bahirdar, Ethiopia [15]. It may be caused by the persistence of resistant strains from previous uropathogenic infections or by the recurrence of those illnesses [49]. Patients with indwelling catheterization have an eleven times higher risk of developing catheter associated UTIs than the non-indwelling catheterized group, which is contrary to the study in Gondar, Ethiopia [47]. Due to the presence of an indwelling catheter device and potentially pathogenic multidrug-resistant organisms in the hospital environment, catheter insertion predisposes to the development of catheter-associated UTIs by creating a new entry point for bacterial invasion and pushing bacteria into the bladder [50]. On the analysis, diabetic patients were an independent risk factor for the acquisition of bacterial UTIs when compared with non-diabetic patients (p = 0.014). This might be due to frequent urination and a high blood sugar level because the high sugar level gives a favorable growth environment to the pathogens [51]. Study participants with a body temperature of ≥ 38.5°C had 4 times more risk for bacterial UTI compared to their counterparts; this result is consistent with the study done in Tanzania [12]. Though it was contradicted by the study in Nigeria [52]. It could be due to geographical variation, climatic change, and differences in the number of study participants. Under-five children with symptoms of urinary frequency were six times more likely to have a culture-positive result. This finding was a disparity from the study in Nigeria [13]. Frequently urinating, infections, injuries, or irritation of the bladder, as well as changes in the muscles and nerves that regulate bladder function, could all be to blame for these variances [53].

Healthcare personnel’s ability to choose proper treatment for UTI has been affected by growing antibiotic resistance [54]. In the present study, meropenem (92.1%), ciprofloxacin (83.3%), and amoxicillin-clavulanic acid (75%) in the carbapenem, fluoroquinolone, and aminoglycoside classes of antibiotics, respectively, were more effective for gram-negative isolates. However, β-lactam antibiotics (ampicillin (10%), cefazolin (27%), and ceftazidime (32%)), tetracycline (22%), and trimethoprim-sulfamethoxazole (28%) were least effective for gram-negative pathogens. The increased rate of beta-lactam and other antibiotic resistance was probably associated with the continuous use of these drugs without prescription or susceptibility data, easy availability, limited diagnostic facilities, the tendency of a patient to use relatively low-cost drugs for all infections, and misuse of antibiotics [15, 55]. Contradictory results from a study in Gusau, Nigeria, showed susceptibility to Gentamycin (63.8%) and Nitrofurantoin (59.6%) [1]. It might be due to the gradual increase in drug resistance and poor adherence [29].

In this study, meropenem (92.8%), amoxicillin-clavulanic acid (75%), and ciprofloxacin (71.4%) were more effective for E. coli, as with some studies in Bahirdar, Ethiopia [15], Nigeria [1], and Tanzania [38], but it was resistant to the commonly prescribed penicillin drugs (ampicillin (82%)), cephalosporin antibiotics (cefazolin (75%), and ceftazidime (67.8%)), tetracycline (82.1%), and trimethoprim-sulfamethoxazole (75%). A similar finding has been reported from Bahirdar, Ethiopia [15], Hawassa, Ethiopia [14], Tanzania [40], and Kenya [29]. Some studies have found that trimethoprim-sulphamethoxazole, ceftazidime, and augmentin are more effective against E. coli [1, 24, 38, 47]. It is probably due to multiple factors, including recurrent UTIs, inappropriate prescribing, poor hygiene or fecal colonization, and the presence of extended-spectrum beta-lactamase (ESBL) producing E. coli [55–57]. In addition, drug resistance can exist naturally, such as through efflux pumps, alteration of the drug-binding site, membrane permeability, or degradation enzymes [36].

S. aureus was more resistant to the commonly prescribed beta-lactam antibiotics like ampicillin (83.3%) and tetracycline (83.3%), a similar finding was reported from other studies [14, 29], whereas tetracycline and chloramphenicol showed low resistance for S. aureus in the study from Gondar, Ethiopia [47]. This discordance could be due to S. aureus producing excessive β-lactamase, and acquiring resistance through plasmid-mediated transduction, transformation, and the insertion of drug-resistant genes of S.aureus [58].

Furthermore, the overall MDR rate of isolates in our study was 61.6% (95% CI: 51–73, N = 53). Specifically, gram-negative bacterial isolates showed a significant level of MDR 47/68 (69.1%) compared to gram-positive bacteria 6/18 (33.3%), in conjunction with others from Ethiopia [15, 24, 47]. the present study, 11.6% and 2.3% of the gram-negative species were XDR and PDR, respectively. Contradictory results from a study in Ethiopia for 22% XDR and 4% PDR [5] were observed. The use of broad-spectrum agents, increasing irrational antibiotics use, the easy availability of antimicrobials in non-controlled pharmacies, the transmission of resistance genes between people or between people and animals, and over-prescription are all factors that enhance the growth of resistance [5, 15]. And extremely high bacterial resistance in the general population, resulting in overuse of high-potency antibiotics for UTIs, thus increasing bacterial resistance. Antimicrobial resistance among uropathogens is alarmingly increasing with different resistance mechanisms [59, 60]. The commonest acquired antibiotic resistance mechanisms are: preventing the uptake of antibiotic agents (turning off the production of porin channel proteins), modifying a drug target, inactivating a drug through the production of enzymes, and enhancing drug efflux pumps [61]. E. coli isolate was the most common antibiotic-resistant pathogen in this study; it may produce a wide variety of β-lactamases, including ESBLs, penicillinase and carbapenemases, modification of lipopolysaccharides (LPS), and efflux pumps [62–64]. K. pneumoniae becomes resistant to commonly available drugs through the development of various first-generation β-lactamases (which are naturally resistant to penicillin); through the making of broad spectrum β-lactamases; through the yielding of ESBLs or penicillinases; and through non-carbapenemase mechanisms of resistance such as the turn of outer membrane proteins and the occurrence of efflux pumps, which can also act harmoniously with the overexpression of β-lactamases [63]. S. aureus has been able to develop resistance mechanisms to most antibiotics used against it through modification of penicillin-binding protein-2a (PBP2a), penicillinase, ribosomal methylation of binding sites, and efflux pumps. Similar to all β-lactam medications, S. aureus gained methicillin resistance through the development of PBP2a, which is resistant to all β-lactam antibiotics [65, 66].

Limitations of the study

One major limitation is the inability to identify some bacterial isolates into species and serotypes. In additions, that the possibility of contamination (especially of gram-negative organisms) exists in the bag or open diaper collection methods. Furthermore, the study could not indicate the molecular characteristics, ESBL and CRE of isolates due to a lack of resources.

Conclusion and recommendation

In comparison to the majority of other investigations conducted in Africa, more than one-fourth of the children had cultures that were positive for various bacterial uropathogens. UTIs were made more common by indwelling catheterization, a prior history of the condition, males who had not undergone circumcision, a history of using antibiotics without a prescription, rural dwellers, diabetes mellitus, children’s body temperatures, and urine frequency. Both gram-positive species and a variety of gram-negative species were documented, which yielded 24%. The most common isolates that cause UTIs are E. coli, K. pnemoniae, and S. aureus. These strains showed different percentages of susceptibility to the tested antibiotics. The current study points out that meropenem, ciprofloxacin, and amoxicillin-clavulanic acid are choices of drugs for UTI in the study area. Significantly high proportions of MDR strains were observed, especially against commonly used drugs. As patients are diagnosed and treated empirically in the study setting, hospitals should establish antimicrobial stewardship programs. Patients should be managed with microbiological evidence to avoid antimicrobial prescriptions for patients without bacterial infection and better control the spread of drug resistance. The careful prescribing of antibiotics is needed to halt the progress of drug resistance. Hence Working on the identified associated factors is vital to minimize the observed high prevalence of UTIs.

Supporting information

S1 Data set. Dataset used for the analysis of antimicrobial susceptibility result (SPSS).

https://doi.org/10.1371/journal.pone.0283637.s001

(SAV)

S2 Data set. Supplementary material.

https://doi.org/10.1371/journal.pone.0283637.s002

(SAV)

S3 Data set. Supplemental material for Bacterial profile, their antibiotic susceptibility pattern, and associated factors of urinary tract infections in children at Hiwot Fana specialized university hospital, Eastern Ethiopia.

https://doi.org/10.1371/journal.pone.0283637.s003

(XLSX)

Acknowledgments

We acknowledged Haramaya University Colleges of Health and Medical Sciences Institutional Health Research Ethical Review Committee for giving the ethical clearance. We also thank study participants and all individuals who have in one way or another contributed to the completion of this research.

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Figures

Abstract

Background

Objective

Method

Results

Conclusions

Introduction

Materials and methods

Study area and period

Study design and population

Sample size determination and sampling technique

Data and sample collection

Bacterial isolation and identification

Antimicrobial susceptibility testing (AST)

Data quality control

Method of data analysis

Ethical considerations

Result

Socio-demographic characteristics

Clinical future and medical history

Prevalence of urinary tract infection

Bacterial profile of uropathogens

Associated factors

Antimicrobial susceptibility pattern

Gram-positive bacteria.

MDR patterns of bacterial isolates.

Incidence of MDR, XDR, and PDR strains.

Discussion

Limitations of the study

Conclusion and recommendation

Supporting information

S1 Data set. Dataset used for the analysis of antimicrobial susceptibility result (SPSS).

S2 Data set. Supplementary material.

S3 Data set. Supplemental material for Bacterial profile, their antibiotic susceptibility pattern, and associated factors of urinary tract infections in children at Hiwot Fana specialized university hospital, Eastern Ethiopia.

Acknowledgments

References