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Efficacy of Urine Dipstick Test in Diagnosing Urinary Tract Infection

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Efficacy of Urine Dipstick Test in Diagnosing Urinary Tract Infection diseases Article Efficacy of Urine Dipstick Test in Diagnosing Urinary Tract Infection and Detection of the blaCTX-M Gene among ESBL-Producing Escherichia coli Rubina Gurung 1,†, Sanjib Adhikari 1,† , Nabaraj Adhikari 1, Sanjeep Sapkota 2, Jid Chani Rana 3, Binod Dhungel 1 , Upendra Thapa Shrestha 1 , Megha Raj Banjara 1, Prakash Ghimire 1 and Komal Raj Rijal 1,* 1 Central Department of Microbiology, Tribhuvan University, Kirtipur 44600, Kathmandu, Nepal; [email protected] (R.G.); [email protected] (S.A.); [email protected] (N.A.); [email protected] (B.D.); [email protected] (U.T.S.); [email protected] (M.R.B.); [email protected] (P.G.) 2 Department of Microbiology, Birendra Multiple Campus, Tribhuvan University, Bharatpur 44200, Chitwan, Nepal; [email protected] 3 Department of Microbiology, Bharatpur Hospital, Bharatpur 44200, Chitwan, Nepal; [email protected] * Correspondence: [email protected] or [email protected] † These authors contributed equally to this work. Abstract: A urine dipstick test used for prompt diagnosis of urinary tract infection (UTI) is a rapid and cost-effective method. The main objective of this study was to compare the efficacy of the urine dipstick test with culture methods in screening for UTIs along with the detection of the blaCTX-M Citation: Gurung, R.; Adhikari, S.; gene in extended spectrum β-lactamase (ESBL)-producing Escherichia coli. A total of 217 mid-stream Adhikari, N.; Sapkota, S.; Rana, J.C.; urine samples were collected from UTI-suspected patients attending Bharatpur Hospital, Chitwan, Dhungel, B.; Thapa Shrestha, U.; and tested by dipstick test strip (COMBI-10SL, Germany) prior to the culture. E. coli isolates were Banjara, M.R.; Ghimire, P.; Rijal, K.R. Efficacy of Urine Dipstick Test in identified by standard microbiological procedures and subjected to antimicrobial susceptibility Diagnosing Urinary Tract Infection testing by Kirby Bauer disc diffusion method following CLSI guideline. Primary screening of ESBL- and Detection of the blaCTX-M Gene producing E. coli isolates was conducted using ceftriaxone, cefotaxime and ceftazidime discs and among ESBL-Producing Escherichia phenotypically confirmed by combined disk diffusion test. Plasmid DNA of ESBL-producing strains coli. Diseases 2021, 9, 59. https:// was extracted by phenol-chloroform method and subjected to PCR for detection of the blaCTX-M gene. doi.org/10.3390/diseases9030059 Out of 217 urine samples, 48 (22.12%) showed significant bacteriuria. Among 46 (21.20%) Gram negative bacteria recovered, the predominant one was E. coli 37 (77.08%) of which 33 (89.19%) were Academic Editor: St Patrick Reid multidrug resistant (MDR). E. coli isolates showed a higher degree of resistance towards cefazolin (62.16%) while 81.08% of the isolates were sensitive towards amikacin followed by nitrofurantoin Received: 26 June 2021 (70.27%). Among 14 (37.84%) phenotypically confirmed ESBL isolates, only eight (21.62%) isolates Accepted: 26 August 2021 carried the bla gene. Sensitivity, specificity, positive predictive value (PPV) and negative Published: 27 August 2021 CTX-M predictive value (NPV) of urine dipstick test were 43.75%, 77.51%, 35.59% and 82.91%, respectively. Publisher’s Note: MDPI stays neutral Besides, the use of dipstick test strip for screening UTI was associated with many false positive and with regard to jurisdictional claims in negative results as compared to the gold standard culture method. Hence, dipstick nitrite test alone published maps and institutional affil- should not be used as sole method for screening UTIs. iations. Keywords: Escherichia coli; ESBL; sensitivity; specificity; PPV; NPV; blaCTX-M Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. 1. Introduction This article is an open access article Urinary tract infection is the second most frequent infectious disease that probably distributed under the terms and affects one-half of all people during their lifetimes. UTIs simply mean the presence of conditions of the Creative Commons microbial pathogens causing the infection within the urinary tract [1]. Each year, approxi- Attribution (CC BY) license (https:// mately 150 million people are diagnosed with UTI, costing the global economy of billions creativecommons.org/licenses/by/ of US dollars [2]. It has been estimated that at least 40% to 50% of women will experience 4.0/). Diseases 2021, 9, 59. https://doi.org/10.3390/diseases9030059 https://www.mdpi.com/journal/diseases Diseases 2021, 9, 59 2 of 11 a minimum of one symptomatic UTI with roughly 27% to 48% of affected women expe- riencing recurrent UTIs [3]. A UTI is a severe public health problem caused by a variety of pathogens, but most frequently by Escherichia coli followed by Klebsiella pneumoniae, Proteus mirabilis, Enterococcus faecalis, Staphylococcus saprophyticus, Staphylococcus aureus, and Pseudomonas aeruginosa [4–6]. Urine culture is used as the reference standard to detect UTI; however, the culture method is expensive and time-consuming [7]. Urinalysis is one of the rapid screening techniques that have been used to diagnose UTIs, proteinuria, haematuria, and some other conditions [8]. Several tests are available for the diagnosis of UTIs, but the semi-quantitative culture of urine specimen is the only method for the detailed documentation of a bacterial urine infection [9]. The dipstick strip is considered to be one of the qualitative diagnostic tools [10] which include reagent pads such as nitrite, leukocyte esterase, specific gravity, pH, protein, glucose, ketones, bilirubin, urobilinogen and blood [11]. It is nevertheless associated with many false positive and negative results as compared to the gold standard culture method. Beta-lactam drugs are among the most prescribed antibiotics that are used to treat diseases caused by MDR Enterobacteriaceae [12]. The excessive use of beta-lactam antibi- otics has increased the expansion of resistant Enterobacteriaceae. Usually, ESBLs confer resistance to all penicillin, cephalosporins (except for cephamycins), and monobactams, being inhibited by β-lactam inhibitors [13,14] and they are the predominant sources of enterobacterial resistance to third and fourth generation cephalosporins. Among ESBLs observed in E. coli, the most commonly identified are enzymes from the family CTX-M (mostly CTX-M-1 lineage), followed by SHVs, and TEMs [15,16]. Plasmids have been found to confer drug resistance in their host bacteria by various mating processes such as conjuga- tion, transduction and transformation with plasmid size [17]. They are responsible for the spread of antibiotic resistant genes in bacterial populations and the release of antibiotics into the environment will boost up R-plasmids, integrons and multidrug resistance [18]. In a developing country such as Nepal, specialised laboratories with diagnostic tools and techniques are limited and hence rapid tests such as urine dipstick tests are employed for the patients suspected of having UTIs. However, very few studies have reported the accuracy of these tests. Moreover, there is increasing evidence of drug resistant isolates in hospitals/clinical settings in Nepal [19–22]. The data available in the country necessary for marking the resistant patterns are not sufficient to describe the trend of antibiotic resistance. Therefore, the current study was designed to evaluate the efficacy of the urine dipstick test and for the detection of blaCTX-M gene in Extended Spectrum β-lactamase (ESBL)-producing E. coli isolates. 2. Materials and Methods 2.1. Study Design and Setting This was a hospital-based cross-sectional study conducted at Bharatpur hospital, Chitwan, Nepal, from January to April 2019. Bharatpur hospital is a government-funded tertiary care hospital situated in Bagmati Province in the mid-southern part of the country. The hospital has 600 beds and has been providing health services to around a 35 hundred- thousand population of eight major surrounding districts besides Chitwan itself. 2.2. Sample Collection, Processing and Identification A total of 217 midstream urine samples were collected from UTI suspected patients of all ages and sexes visiting the hospital and processed in the Microbiology Laboratory of Bharatpur Hospital, Chitwan. Patients were asked to collect 10–20 mL of clean first-voided morning mid-stream urine in a sterile, dry, wide-necked, leakproof container and, once brought to the laboratory, the urine was tested first by using a dipstick test strip (COMBI- 10SL, Analyticon Biotechnologies, Germany). Nitrite was considered as positive if there was a change in the colour of the dipstick from colourless to pink within 60 s. Urine culture was performed by using the strips calibrated to deliver 0.02 µL of urine on MacConkey Diseases 2021, 9, 59 3 of 11 and blood agar plates and incubated at 37 ◦C for 24 to 48 h. Following enumeration of the colonies, it was reported that there was significant bacteriuria if the growth was ≥105 CFU/mL. The identification of bacterial isolates was conducted by conventional microbiological techniques that involved studying the colonial morphology, Gram staining and various biochemical tests [23]. The culture method was considered as gold standard to evaluate the performance of dipstick test. 2.3. Antimicrobial Susceptibility Testing Antibiotic susceptibility tests of E. coli isolates were performed using a modified Kirby– Bauer disc diffusion method on Mueller Hinton Agar (MHA), as recommended by CLSI guidelines using an array of commonly prescribed antibiotics
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