Sudan Journal of Medical Sciences Volume 17, Issue no. 1, DOI 10.18502/sjms.v17i1.10685 Production and Hosting by Knowledge E Original Article The Antibiotic Resistance and Multidrug Resistance Pattern of Uropathogenic Escherichia coli at Soba University Hospital: A Descriptive Retrospective Survey Hagir Mohamed Eezzeldin1, Safaa Badi2, and Bashir Alsiddig Yousef3* 1Department of Clinical Pharmacy, Faculty of Pharmacy, University of Khartoum, Al-Qasr Ave, Khartoum, Sudan 2Department of Clinical Pharmacy, Faculty of Pharmacy, Omdurman Islamic University, Aboseid Street, Khartoum, Sudan 3Department of Pharmacology, Faculty of Pharmacy, University of Khartoum, Al-Qasr Ave, Khartoum, Sudan ORCID: Bashir Alsiddig Yousef: https://orcid.org/0000-0001-7832-4556 Abstract Background: The irrational use of antibiotics for the treatment of urinary tract infections (UTIs) may lead to increased antimicrobial resistance among uropathogenic Escherichia coli (E. coli), as well as multidrug resistance worldwide, which will limit available treatment options for UTIs caused by these organisms. This study aimed to determine the resistance pattern of E. coli causing UTIs in out-patients and in-patients of Soba University Hospital. Methods: Data were collected from the laboratory records in the Department of Microbiology in Soba Teaching Hospital by using a predesigned checklist and then analyzed using the statistical package for social sciences. Bivariate analysis (Chi- square test) was used to compare between variables. Results: Out of the 231 E. coli urine cultures, 160 (69.3%) were collected from females. The results showed high resistance to ampicillin (92.4%), amoxicillin-clavulanic acid (83.3%), cephalexin (90.6%), cefuroxime (72%), ceftazidime (71%), ceftriaxone (72%), ciprofloxacin (68%), and co-trimoxazole (75.3%). Collectively, around 188 (81.4%) were multidrug-resistant. On the other hand, the sensitivities of E. coli isolates were 68.8%, 93.1%, 89.4%, and 100% to gentamicin, amikacin, nitrofurantoin, and carbapenems, respectively. Conclusion: The rate of E. coli resistance was observed to be high to the commonly prescribed drugs for UTIs, including ampicillin, amoxicillin/clavulanic acid, different cephalosporins, fluoroquinolones, and co-trimoxazole. However, E. coli showed lower resistance rates to nitrofurantoin, amikacin, and carbapenems. Thus, these drugs can be reserved for the empirical treatment of UTIs caused by E. coli. Keywords: Escherichia coli, urinary tract infection, multidrug resistance, Soba University Hospital How to cite this article: Hagir Mohamed Eezzeldin, Safaa Badi, and Bashir Alsiddig Yousef* (2022) “The Antibiotic Resistance and Multidrug Resistance Pattern of Uropathogenic Escherichia coli at Soba University Hospital: A Descriptive Retrospective Survey,” Sudan Journal of Medical Sciences, vol. 17, Issue no. 1, pages 56–69. DOI 10.18502/sjms.v17i1.10685 Page 56 Corresponding Author: Bashir Alsiddig Yousef; email: bashiralsiddiq@gmail.com Received 07 May 2021 Accepted 02 March 2022 Published 31 March 2022 Production and Hosting by Knowledge E Hagir Mohamed Eezzeldin et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Editor-in-Chief: Prof. Mohammad A. M. Ibnouf http://www.knowledgee.com mailto:bashiralsiddiq@gmail.com https://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/ Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al 1. Introduction Urinary tract infections (UTIs) are one of the most frequent infectious diseases that affect humans and is considered a critical public health problem [1, 2]. In United States, UTIs are responsible for around 7 million clinic visits per year and cost $2 billion annually [1]. The main etiology of UTIs is the microbial invasion to different tissues of the urinary tract system [3]. Among bacteria causing UTIs, Escherichia coli (E. coli) is considered as the most predominant cause of both community and nosocomial UTIs. Other UTI- causing bacteria include Proteus spp, Staphylococcus Saprophyticus, Klebsiella spp, and other Enterobacteriaceae [2, 4]. Clinically, E. coli can cause uncomplicated and complicated UTIs. In uncomplicated UTIs, individuals develop infection without any structural or neurological abnormalities in the urinary tract; it can either be upper UTIs (pyelonephritis) or lower UTIs (cystitis) [5]. Many risk factors are associated with UTIs, including a previous UTI, female gender, vaginal infection, obesity, diabetes, and genetic susceptibility [6]. In complicated UTIs, other factors such as compromised immune system, urinary obstruction, neurological disease, renal failure, and foreign bodies can predispose to UTI [7, 8]. Treatment of UTIs requires assessment of the patient by evaluating the symptoms or signs, determining the type of UTI, and knowing the previous antimicrobial therapy in case of recurrent infection [9]. Many antibiotics commonly prescribed for the treatment of UTIs include ciprofloxacin, nitrofurantoin, co-trimoxazole, and ampicillin [10]. According to clinical practice guidelines, fluoroquinolones have been recommended for lower UTIs, whereas intravenous cephalosporins are commonly administered for upper UTIs. More- over, the recommended first-line antimicrobial for acute uncomplicated bacterial infec- tion is nitrofurantoin or fosfomycin or co-trimoxazole; the second-line options include fluoroquinolones and β-lactams antibiotics, while for β-lactamase-producing organisms, it recommends using fosfomycin or fluoroquinolones or piperacillin-tazobactam or car- bapenems. Whereas, for multi-drug resistance (MDR), the recommended antibiotics are fluoroquinolones, ceftazidime, piperacillin-tazobactam, carbapenems, aminoglycosides, and colistin [11]. However, extensive use of antibiotics in treating UTIs is highly correlated to antimicrobial resistance [1, 12] and the emergence of MDR that is defined as organisms being resistant to at least three classes of antimicrobial agents [13]. Moreover, antibiotic resistance is a public health problem, which may result in treatment failure and poor clinical outcomes such as development of complications, prolonged hospitalization, and need for intravenous therapy [14, 15]. DOI 10.18502/sjms.v17i1.10685 Page 57 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al Knowledge of the causative organisms and their sensitivity pattern is crucial for empirical therapy for various infections. Since E. coli is the most predominant causative agent for UTIs, regular antibiogram of E. coli strains at different hospitals is crucial for better adaptation of empirical antibiotic therapy. Hence, our study aimed to explore the pattern of antibiotic resistance by uropathogenic E.coli isolate from urine samples at Soba University Hospital in Khartoum State. 2. Materials and Methods 2.1. Study setting This retrospective cross-sectional hospital-based survey used medical records of the patients visiting Soba Hospital in Khartoum, Sudan between January and December 2017, who underwent the antibiotic sensitivity test (disc-diffusion method) for the E. coli isolates. 2.2. Inclusion and exclusion criteria All medical records of patients for whom E. coli antibiogram was done were included, while patient records with incomplete information were excluded. 2.3. Sample size and sampling method A total of 231 patients met the inclusion criteria and were included in the study. 2.4. Data collection tool Data were collected retrospectively from patient records using a data collection sheet, which consisted of the sociodemographic data of the patient, and the list of used medications with the sensitivity findings (sensitive or resistant). DOI 10.18502/sjms.v17i1.10685 Page 58 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al 2.5. Data analysis Data were analyzed by the International Business Machines (IBM) Statistical Package for Social Sciences [SPSS] for Windows, v.22.0 software [Armonk, NY: IBM Corp]. Descrip- tive statistics (frequency tables) and bivariate analysis (Chi-square) was done. P-value ≤ 0.05 was considered significant in comparative data. 3. Results Of the 231 urine culture samples, 160 (69.3%) were of females and 71 (30.7%) of males. Additionally, while 159 (68.8%) samples were of adults, 72 (31.6%) were of pediatric patients. Regarding patient age, 20.8% of the participants were aged 1–6 years, and 28.6% were >60 years (Table 1) Regarding the antibiotics sensitivity pattern for different antibiotics, as shown in Table 2, the pattern to β-lactams antibiotics were varied, E. coli was resistant to ampicillin in 91.5% of the participants, and it was resistant to amoxicillin-clavulanic acid in 84.6%. Furthermore, the resistance rates for E. coli strains against cephalexin, cefuroxime, ceftazidime, and ceftriaxone were 69%, 73.1%, 71.7%, and 71.8%, respectively. More- over, E. coli bacteria were resistant to ciprofloxacin in around two-thirds (65.9%) of the participants, and to gentamicin in about one-third (32.2%) of them. However, it was resistant to nitrofurantoin in only 10.6% of the samples. Interestingly, 99.6% of E. coli samples were sensitive to carbapenems (Table 2). On the other hand, the frequency of E. coli stains with MDR (with resistance to at least three classes of the antimicrobial agents) were 188 (81.4%) (Figure 1). Furthermore, E. coli samples from pediatric or adult patients showed different resistance and sensitivity patterns toward various antibacterial agents (Tables 3 and 4). When chi-square was performed to determine the association of the antibiotic resis- tance and sociodemographic characteristics of the participants, the study showed no significant association between the sensitivity to antibacterial drugs and the gen- der or the age groups. However, the admission status (in- or outpatient) was signifi- cantly associated with the sensitivity to cephalexin, cefuroxime, ceftazidime, ceftriaxone, ciprofloxacin, gentamicin, and nitrofurantoin (0.041, 0.009, 0.003, 0.006, 0.000, 0.042, 0.012), respectively. DOI 10.18502/sjms.v17i1.10685 Page 59 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al Figure 1: Distribution of study sample according to multiple antibiotics resistance. Table 1: Demographic characteristics of the participants (n = 231). Variable Number (frequency %) Gender Male 71 (30.7%) Female 160 (69.3%) Age category Adult 159 (68.8%) Pediatric 72 (31.2%) Age group (yr) 1–6 48 (20.8%) 7–12 20 (8.6%) 13–18 4 (1.7%) 19–30 13 (5.6) 31–40 19 (8.4) 41–50 29 (12.5) 51–60 32 (13.8) >60 66 (28.6) Admission unit Inpatient 160 (69.3%) Outpatient 71 (30.7%) 4. Discussion The emergence of antibiotic resistance in E. coli and other microorganisms that cause UTIs is increasing day by day, making it a critical health problem. Thus, in order to provide proper treatment for UTIs, it is crucial to measure the antibiotic resistance patterns in E. coli isolates [16]. In the present study, the total E.coli samples isolated within the study period were 231. We found that the occurrence of Uropathogenic E. coli frequency was higher in females than in males; this may occur due to the difference in the anatomy of the urinary tract of the females, and the hormonal effects, pregnancy, certain type of birth control, and behavioral patterns [17–20]. Regarding the resistant pattern, 91.5% DOI 10.18502/sjms.v17i1.10685 Page 60 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al Table 2: Distribution of study sample according to sensitivity pattern (n = 231). Antibiotic class Antibiotic Sensitivity test N (%) β-lactams Ampicillin NRST† (n = 43) RST∗ (n = 188) Resistance 172 (91.5%) Sensitive 16 (8.5%) Amoxicillin + Clavulanic acid NRST (n = 10) RST (n = 221) Resistance 187 (84.6%) Sensitive 34 (15.4%) Cephalosporin Cephalexin NRST (n = 173) RST (n = 58) Resistance 40 (69%) Sensitive 18 (31%) Cefuroxime NRST (n = 8) RST (n = 223) Resistance 163 (73.1%) Sensitive 60 (26.9%) Ceftazidime NRST (n = 8) RST (n = 223) Resistance 160 (71.7%) Sensitive 63 (28.3%) Ceftriaxone NRST (n = 4) RST (n = 227) Resistance 163 (71.8%) Sensitive 64 (28.2%) Flouroquinolones Ciprofloxacin NRST (n = 8) RST (n = 223) Resistance 147 (65.9%) Sensitive 77 (34.1%) Aminoglycosides Gentamycin NRST (n = 60) RST (n = 171) Resistance 55 (32.2%) Sensitive 116 (67.8%) Amikacin NRST (n = 4) RST (n = 227) Resistance 20 (8.8%) Sensitive 208 (91.2%) Carbapenems Meropenem and imipenem NRST (n = 2) RST (n = 229) Resistance 1 (0.4%) Sensitive 228 (99.6%) Sulphonamides Co-trimoxazole NRST (n = 4) RST (n = 227) Resistance 169 (73.2%) Sensitive 58 (26.8%) Others Nitrofurantoin NRST (n = 5) RST (n = 226) Resistance 24 (10.6%) Sensitive 202 (89.4%) ∗RST: Requested sensitivity test; †NRST: Not requested sensitivity test. DOI 10.18502/sjms.v17i1.10685 Page 61 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al Table 3: Distribution of pediatric patients’ sample according to sensitivity pattern (n = 72). Antibiotic class Antibiotic Sensitivity test N (%) β-lactams Ampicillin NRST† (n = 14) RST* (n =58) Resistance 55 (94.8%) Sensitive 3 (5.2%) Amoxicillin + Clavulanic acid NRST (n = 2) RST (n = 70) Resistance 59 (84.3%) Sensitive 11 (15.7%) Cephalosporin Cefuroxime NRST (n = 4) RST (n = 68) Resistance 51 (75%) Sensitive 17 (25%) Ceftazidime NRST (n = 4) RST (n = 68) Resistance 48 (70.6%) Sensitive 20 (29.4%) Ceftriaxone NRST (n = 0) RST (n = 72) Resistance 51 (70.8%) Sensitive 21 (29.2%) Flouroquinolones Ciprofloxacin NRST (n = 1) RST (n = 71) Resistance 46 (64.8%) Sensitive 25 (35.2%) Aminoglycosides Gentamycin NRST (n = 16) RST (n = 56) Resistance 19 (33.9%) Sensitive 37 (66.1%) Amikacin NRST (n = 0) RST (n = 72) Resistance 7 (9.9%) Sensitive 65 (90.1%) Carbapenems Meropenem and imipenem NRST (n = 2) RST (n = 70) Resistance 1 (1.4%) Sensitive 69 (98.6%) Sulphonamides Co-trimoxazole NRST (n = 1) RST (n = 71) Resistance 56 (78.9%) Sensitive 15 (21.1%) Others Nitrofurantoin NRST (n = 2) RST (n = 70) Resistance 11 (15.7%) Sensitive 59 (84.3%) *RST: requested sensitivity test; † NRST: not requested sensitivity test. and 84.6% of E.coli samples were resistant to ampicillin and co-amoxiclav, respectively, which indicated a cautious use of these antibiotics for the treatment of UTIs. Similar findings were seen in India and Pakistan [21–23]. The resistance rates were also high for cephalosporin antibiotics, including cephalexin (90.6%), ceftazidime (71%), cefuroxime DOI 10.18502/sjms.v17i1.10685 Page 62 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al Table 4: Distribution of adult patients’ sample according to sensitivity pattern (n = 159). Antibiotic class Antibiotic Sensitivity test N (%) β-lactams Ampicillin NRST† (n = 29) RST* (n = 130) Resistance 117 (90%) Sensitive 13 (10%) Amoxicillin + Clavulanic acid NRST (n = 8) RST (n = 151) Resistance 128 (84.7%) Sensitive 23 (15.3%) Cephalosporin Cephalexin NRST (n = 113) RST (n = 46) Resistance 32 (69.6%) Sensitive 14 (30.4%) Cefuroxime NRST (n = 4) RST (n = 155) Resistance 112 (72.3%) Sensitive 43 (27.7%) Ceftazidime NRST (n = 4) RST (n = 155) Resistance 112 (72.3%) Sensitive 43 (27.7%) Ceftriaxone NRST (n = 4) RST (n = 155) Resistance 112 (72.3%) Sensitive 43 (27.7%) Flouroquinolones Ciprofloxacin NRST (n = 7) RST (n = 152) Resistance 101 (66.4%) Sensitive 52 (33.6%) Aminoglycosides Gentamycin NRST (n = 44) RST (n = 115) Resistance 36 (31.3%) Sensitive 79 (68.7%) Amikacin NRST (n = 3) RST (n = 156) Resistance 13 (8.3%) Sensitive 143 (91.7%) Carbapenems Meropenem and imipenem NRST (n= 0) RST (n = 159) Resistance 0 (0%) Sensitive 159 (100%) Sulphonamides Co-trimoxazole NRST (n = 3) RST (n = 156) Resistance 113 (72.4%) Sensitive 43 (27.6%) Others Nitrofurantoin NRST (n = 3) RST (n = 156) Resistance 13 (8.3%) Sensitive 143 (91.7%) *RST: Requested sensitivity test; †NRST: Not requested sensitivity test DOI 10.18502/sjms.v17i1.10685 Page 63 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al (72%), and ceftriaxone (72%), which renders them inefficient as empirical therapy against UTIs. The main reason for that is the irrational prescribing of these classes of drugs in different hospitals in Sudan [24–26]. However, in United States, due to the rational prescribing of antibiotics, the resistance rates to penicillin and cephalosporins were comparatively low [27]. Trimethoprim-sulfamethoxazole (co-trimoxazole) has been widely used for the treat- ment of UTIs, but our results showed high resistance (74.4%), this result is inconsistent with other studies [21, 27]. Among aminoglycosides, the observed resistance rate for gentamicin and amikacin were 32.2% and 8.8%, respectively, with a significant associ- ation with the kind of admission (p < 0.05). Similar results were observed in a hospital in Tamil Nadu, India, where gentamicin and amikacin resistance rates were 30.4% and 10.5%, respectively [19]. However, even with high sensitivities for these antibiotics, the utilization of aminoglycosides is low, due to their nephrotoxicity and ototoxicity [28]. On the other hand, fluoroquinolones, especially ciprofloxacin, have been the most frequently used antibiotic for UTIs in the recent past [29]. In the present study, E. coli strains were highly resistant (65.9%) to ciprofloxacin, this finding is concerning, as fluoroquinolones are frequently used empirically to treat UTIs, especially compli- cated infections. Interestingly, the resistance to nitrofurantoin was very low (10.6%) in comparison to other antibiotics, which suggest using this drug as the first-line option in the empirical treatment of uncomplicated cystitis and other lower UTIs. This low rate of resistance may be due to the limited use of nitrofurantoin in the last years. These findings were also observed worldwide [21, 30]. Among the carbapenems class of antibiotics, this study demonstrated there was only one resistant case for all tested isolates, as these drugs are restricted for severe infections. In contrast to another study done in a tertiary care hospital in India that showed relatively high resistance (43.3%) to carbapenems, these may have resulted due to misuse and overuse of this class in the hospital [31]. In addition, the current study showed a high rate (81.4%) of MDR of E. coli in comparison to another study done in the United States that showed only 7.1% of MDR [32]. A high occurrence of MDR could result from many factors including hospitalization, diabetes, chronic renal disease, and catheterization [33, 34]. Limitations The limitations of the current study are: firstly, the cross-sectional design in one hos- pital may not allow generalization of the findings to all hospitals in Sudan. Secondly, DOI 10.18502/sjms.v17i1.10685 Page 64 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al many incomplete and missed data were also reported. Despite these limitations, this surveillance is essential, as it demonstrates the situation of the E. coli resistance to antibiotics which will help a lot in the proper selection of empirical therapy to treat UTIs. However, prospective studies are urgently needed in other Sudanese Hospitals in order to determine the resistance and sensitivity patterns for E. coli and microorganisms. 5. Conclusion The uropathogenic E.coli are highly resistant to the majority of antibiotics commonly used in the clinical practice in inpatients and outpatients. The E. coli resistance rate was observed to be high for ampicillin, combination B-lactamase inhibitor (amoxi- cillin/clavulanic acid), and cephalosporin (cefuroxime, ceftazidime, and ceftriaxone), fluoroquinolones, and co-trimoxazole. However, E. coli showed lower resistance to nitrofurantoin, amikacin, and carbapenems; this can be reserved for empirical treatment of UTIs. According to our findings, we recommend using nitrofurantoin as an empirical therapy for the treatment of lower UTIs. Acknowledgements The authors would like to thank all members of the Department of Microbiology at Soba University Hospital for their help and collaboration. Ethical Considerations The ethical clearance was obtained from the Ethical Committee of the Faculty of Phar- macy, University of Khartoum. Additional approval was taken from the administration of Soba University Hospital and the Department of Microbiology in the hospital before starting data collection. All collected data were coded while ensuring confidentiality throughout the study. Competing Interests There are no conflicts of interest. DOI 10.18502/sjms.v17i1.10685 Page 65 Sudan Journal of Medical Sciences Hagir Mohamed Eezzeldin et al Availability of Data and Material All relevant data of this study are available to any interested researchers upon reason- able request to the corresponding author. Funding None. 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Emergency Medicine International, vol. 2013, article 258517. [34] Tenney, J., Hudson, N., Alnifaidy, H., et al. (2018). Risk factors for aquiring multidrug- resistant organisms in urinary tract infections: a systematic DOI 10.18502/sjms.v17i1.10685 Page 69 Introduction Materials and Methods Study setting Inclusion and exclusion criteria Sample size and sampling method Data collection tool Data analysis Results Discussion Limitations Conclusion Acknowledgements Ethical Considerations Competing Interests Availability of Data and Material Funding References