1 Carle Foundation Hospital, Urbana, IL, USA. 2 University of Illinois College of Medicine, Urbana, IL, USA

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1 588822CPJXXX / Clinical PediatricsAhmed et al research-article2015 Article First-Line Antimicrobial Resistance Patterns of Escherichia coli in Children With Urinary Tract Infection in Emergency Department and Primary Care Clinics Clinical Pediatrics 2016, Vol. 55(1) The Author(s) 2015 Reprints and permissions: sagepub.com/journalspermissions.nav DOI: / cpj.sagepub.com M. Nadeem Ahmed, MD, PhD 1,2, Debby Vannoy, MA 1, Ann Frederick, BS 1, Sandy Chang, BS 2, and Elisabeth Lawler, MS, MD 3 Abstract Objective: To identify risk factors for antibiotic resistance to Escherichia coli (E. coli) in children with urinary tract infections (UTIs) in emergency room and primary care clinics. Method: This is a cross-sectional study of children 0 to 18 years of age reported to have E coli positive UTIs whose medical and laboratory records were systematically reviewed. Result: Compared with girls, boys were 2.29 times (confidence interval [CI] = ) more likely to have E coli isolates resistant to ampicillin and 2 times more likely (CI = ) to have isolates resistant to trimethoprim-sulfamethoxazole (TMP/SMX). Patients with genitourinary abnormalities were 1.57 times more likely to be resistant to ampicillin (CI = ) and 1.86 times to TMP/SMX (CI = ). Conclusion: Higher rates of ampicillin and TMP/SMX resistant urinary E coli isolates were observed among boys and children with a history of genitourinary abnormality. Age and recent antibiotic prescription are also potential risk factors for resistance. Keywords urinary tract infection, antibiotic resistance, antibiotics, pediatrics, children, risk factors, ampicillin, trimethoprimsulfamethoxazole, cefazolin, Escherichia coli Introduction Urinary tract infection (UTI) is one of the most prevalent infectious diseases that is commonly encountered in children in ambulatory care settings. Children with UTIs constitute 1.5 million to 1.75 million doctor visits annually. 1 Overall, there are nearly 8 million patient visits to physicians for UTIs per year in the United States, and approximately one-fifth of those visits are to emergency departments. 2 Among outpatients, Escherichia coli (E coli) is the primary urinary tract pathogen, accounting for 75% to 95% of isolates from uncomplicated UTIs. 3 Frequently, a clinician prescribes antibiotics empirically because it is vital to initiate antibiotics pending urine culture results for children suffering from UTIs. Various factors are involved in antibiotic selection, including patient age, allergies, cost, compliance, dosing frequency, and resistance patterns. 1-3 Often amoxicillin with clavulanate, trimethoprim/sulfamethoxazole (TMP/SMX), and cephalosporins are used as first-line empirical therapy for young children. 4 However, management of UTIs has been complicated by the emergence of resistance to most commonly used antibiotics. 1-5 Adult studies reported that among uropathogens, E coli antimicrobial resistance has been associated with lower likelihood of clinical cure and increased risk of infection recurrence. 5,6 Studies of US surveillance data over 12 million urinary E coli isolates reported that nearly 1 in 2 isolates was resistant to ampicillin and 1 in 4 to TMP/SMX, the second most commonly prescribed antimicrobials for UTIs. 7-9 Recently revised published guidelines by the Infectious Disease Society of America (IDSA) recommended TMP/SMX therapy only in communities where the prevalence of TMP/SMX resistance 1 Carle Foundation Hospital, Urbana, IL, USA 2 University of Illinois College of Medicine, Urbana, IL, USA 3 Southern Illinois University Medical Center, Springfield, IL, USA Corresponding Author: M. Nadeem Ahmed, Pediatric Hospital Medicine, Carle Foundation Hospital, 611 West Park Street, Urbana, IL 61801, USA. nadeem.ahmed@carle.com

2 20 Clinical Pediatrics 55(1) is below 20%. 10 Studies have also shown that the TMP/ SMX resistance rate varies by region, ranging from 18% to 50% worldwide and from 18% to 25% in North America. 7-9,11 Therefore, knowledge of the spectrum of pathogens and their patterns of resistance in the local community is critical for clinicians to empirically select an effective therapeutic agent and reduce the risk of treatment failure. In the literature, very few studies have reviewed the potential risk factors and resistance pattern of urinary tract pathogens among children in emergency department and primary care settings. Patients age, gender, history of prior UTI, genitourinary tract abnormalities, and recent use of antibiotics are reported to be contributing factors in antibiotic resistance But data were often limited and sparse either because of small sample size or use of surveillance records. The purpose of this study is to determine the spectrum of risk factors associated with antibiotics resistant to commonly prescribed agents for E coli infected pediatric UTIs in emergency room and outpatient clinics. Methods Study Design We performed a retrospective cross-sectional study examining urinary E coli isolates of patients up to age 18 years collected in the emergency department and primary care clinics. The study was conducted at a university-affiliated hospital serving 1.5 million people in east central and southern Illinois. Primary care clinics were defined as nonspecialty care clinic within the Pediatrics and Family Medicine departments. The medical records of these identified patients who were being evaluated in emergency room and primary care clinics were then reviewed to collect demographic and clinical data. All medical information was in electronic format. Patients were excluded if their records were not available, if urine culture grew more than one organism, or if a urine contamination was suspected. Voided cultures with greater than 100, 000 colony forming units (cfu)/ml and cultures obtained from a catheterized specimen with greater than 10, 000 cfu/ml were not considered contaminants. Urine cultures positive for E coli that were drawn from patients with visits in the primary care clinics and the emergency room from January 1, 2011, to December 31, 2012, were eligible for inclusion in the analysis. Measurement Variables Demographic data collected included patient age, date of birth, gender, race/ethnicity, and insurance status. Clinical data consisted of date of encounters, methods of urine specimen collection, urinalysis and culture and sensitivity results, history of genitourinary abnormality, chronic medical conditions, previous history of UTI, clinical symptoms suggestive of UTI (including fever, dysuria, frequency, urgency, vomiting, irritability, and abdominal or flank pain/tenderness), physician specialty, place of visit (primary care clinics, and emergency department), and history of antibiotic prescriptions in the past 6 months. Collected data included diagnosis, disposition, treatment, and imaging studies as well. All urinary tract isolates of E coli were identified and subjected to susceptibility testing with the Vitek 2 automated system (Bio Merieux Vitek, Inc, Hazelwood, MO). Vitek 2 is an automated computerized instrument that provides specific quantitative results of urine cultures faster when compared with conventional methods. It is reported to be highly sensitive (92.8%) and specific (99.4%), with average predictive value of 92%. 15 The breakpoints (µg/ml) for E coli isolates were based on Clinical Laboratory Standard Institute guidelines formerly known as the National Committee on Clinical Laboratory Standards. 16 The data set was then limited to the first isolate tested for antibiotic susceptibilities per patient to minimize potential bias resulting from repeat cultures. Statistical Analysis SAS Enterprise Guide for Windows Version 4.3 statistical software was used for data analysis. Summary statistics were performed for frequencies and proportions for categorical variables. Univariate statistics were calculated using the χ 2 test at a 5% significance level to measure unadjusted association between predictor variables and antibiotic resistance. Finally, multivariate logistic regression models were developed to determine the association between E coli urinary isolate resistance to a specific antibiotic and predictor variables. Results are presented as odds ratios (ORs) with 95% confidence intervals (CIs). Results During the study period 1,159 urinary tract isolates of E coli from 886 different individuals were examined for susceptibility patterns. Laboratory data were matched with the corresponding individual s medical record to obtain a descriptive distribution of the study population. The median patient age was 10 years, and body mass index was kg/m 2. The pattern of antibiotic resistance in E coli positive urinary isolates identified is shown in Table 1. Overall, 43.9% of E coli isolates were resistant to ampicillin,

3 Ahmed et al 21 Table 1. Antimicrobial Susceptibility Results for Escherichia coli Urinary Isolates. Number of Isolates (%) Antimicrobial Agent Total Number of Isolates (n) Resistant Susceptible Ampicillin (43.9) 650 (56.1) Ciprofloxacin (4.2) 1108 (95.8) Ceftriaxone (1.1) 1143 (98.9) Cefazolin (3.7) 1116 (96.3) Ampicillin/sulbactam (15.8) 972 (84.2) Ceftazidime (1.1) 1146 (98.9) Nitrofurantoin (0.4) 1155 (99.6) Gentamycin (6.0) 1089 (94.0) Levofloxacin (4.2) 1108 (95.8) TMP/SMX (20.5) 922 (79.5) Tobramycin (0.6) 1152 (99.4) Abbreviation: TMP/SMX, trimethoprim/sulfamethoxazole. Table 2. Resistance to One or More Antibiotics Among 1155 Escherichia coli Urinary Isolates Against Commonly Prescribed Antimicrobials. Number of Agents to Which Isolates Were Resistant Total Number of Isolates (%) Ampicillin TMP/SMX Number of Isolates (%), Resistant to Ampicillin/ Sulbactam Cefazolin Nitrofurantoin Levofloxacin a (53.1) (17.3) 168 (84.0) 25 (12.5) 1 (0.5) 0 (0.0) 0 (0.0) 6 (3.0) (20.8) 236 (98.3) 139 (57.9) 94 (39.2) 1 (0.4) 2 (0.8) 8 (3.3) 3 b 74 (6.4) 74 (100.0) 50 (67.6) 61 (82.4) 21 (28.4) 1 (1.4) 15 (20.3) 4 b 24 (2.1) 24 (100.0) 18 (75.0) 23 (95.8) 16 (66.7) 1 (4.2) 14 (58.3) 5 b 4 (0.4) 4 (100.0) 4 (100.0) 4 (100.0) 4 (100.0) 0 (0.0) 4 (100.0) Abbreviation: TMP/SMX, trimethoprim/sulfamethoxazole. a Susceptibility pattern was identical for levofloxacin and ciprofloxacin. b In all, 8.9% (102 of 1155) of isolates were resistant to 3 or more antibiotics among the listed 6 antibiotics and defined as multidrug resistant. 20.5% to TMP/SMX, and 15.8% to ampicillin/sulbactam. Resistance rates were varied, from 1.1% to 6% for ceftriaxone, ceftazidime, cefazolin, ciprofloxacin, levofloxacin, and gentamycin. Nitrofurantoin (0.4%) and tobramycin (0.6%) demonstrated the lowest rates of resistance. About 18% of urinary isolates (208/1159) were found to be resistant to both ampicillin and TMP/ SMX and 3.6% (42/1159) to ampicillin and cefazolin. Among the 1,159 urinary isolates that were tested against all antimicrobial agents, resistance patterns of the 6 most commonly prescribed antibiotics are shown in Table 2. The majority (53.1%) were susceptible to all the agents shown in the table, of which 17.3% were resistant to a single agent, and 20.8% were resistant to 2 agents, predominantly ampicillin. Multidrug resistance (MDR) was defined as if the urinary isolates were resistant to 3 or more antimicrobials. MDR isolates accounted for 8.9% (n = 102) of the 1,155 isolates. The majority of MDR isolates (n = 74; 72.5%) were resistant to 3 antimicrobials, and these accounted for 6.4% of all isolates. The susceptibility pattern was identical for levofloxacin and ciprofloxacin. The rates of resistance to ampicillin and TMP/SMX for E coli-infected uropathogen by potential risk factors are shown in Tables 3 and 4. According to univariate analysis in Table 3, E coli resistance to ampicillin was significantly higher among boys (P <.0007) and patients younger than 4 years of age (P <.0006). Patients cared for either in the emergency department (OR = 1.43; CI = ) or admitted in hospital (OR = 2.07; CI = ) were 1.43 times and 2.07 times, respectively, more likely to have ampicillin-resistant urinary isolates when compared with clinic patients. Previous history of genitourinary abnormality (P <.01) and fever at presentation (P <.02) appeared to be significantly influenced by E coli resistance to ampicillin.

4 22 Clinical Pediatrics 55(1) Table 3. Factors Associated With Resistance to Ampicillin as Assessed by Univariate Analysis. Number (%) of Isolates Risk Factor Susceptible Resistant OR (95% CI) P Value Overall Location Emergency department 86 (13.2) 89 (17.5) 1.43 ( ).03 Inpatient 14 (2.2) 21 (4.1) 2.07 ( ).04 Outpatient 550 (84.6) 399 (78.4) 1 Gender Male 22 (3.4) 41 (8.1) 2.50 ( ).0007 Female 628 (96.6) 468 (91.9) 1 Race Black 68 (10.5) 69 (13.6) 1.35 ( ).1 Others 91 (14.0) 72 (14.2) 1.06 ( ).75 White 491 (75.5) 368 (72.3) 1 Age (12.8) 103 (20.2) 1.72 ( ) (87.2) 406 (79.8) 1 Health insurance Government 336 (51.7) 285 (56.0) 1.19 ( ).15 Private 314 (48.3) 224 (44.0) 1 History of genitourinary abnormality Yes 45 (6.9) 57 (11.2) 1.70 ( ).01 No 605 (93.1) 452 (88.8) 1 Previous diagnosis of UTI Yes 19 (2.9) 16 (3.1) 1.08 ( ).83 No 631 (97.1) 493 (96.9) 1 History of chronic medication Yes 22 (3.4) 23 (4.5) 1.35 ( ).32 No 628 (96.6) 486 (95.5) 1 Antibiotics prescribed in past 6 months Yes 275 (42.3) 230 (45.2) 1.12 ( ).33 No 375 (57.7) 279 (54.8) 1 Fever Yes 125 (19.2) 127 (25.0) 1.40 ( ).02 No 525 (80.8) 382 (75.1) 1 Dysuria Yes 352 (54.2) 266 (52.3) 0.93 ( ).52 No 298 (45.9) 243 (47.7) 1 Frequency Yes 238 (36.6) 194 (38.1) 1.07 ( ).6 No 412 (63.4) 315 (61.9) 1 Urgency Yes 113 (17.4) 92 (18.1) 1.05 ( ).76 No 537 (82.6) 417 (81.9) 1 Vomiting Yes 69 (10.6) 67 (13.2) 1.28 ( ).18 No 581 (89.4) 442 (86.8) 1 Irritability Yes 21 (3.2) 23 (4.5) 1.42 ( ).26 No 629 (96.8) 486 (95.5) 1 Abdominal/flank pain Yes 237 (36.5) 177 (34.8) 0.93 ( ).55 No 413 (63.5) 332 (65.2) 1 Mode of urine collection Catheterized 49 (7.5) 55 (10.8) 1.49 ( ).055 Void 601 (92.5) 454 (89.2) 1 Abbreviations: OR, odds ratio; CI, confidence interval; UTI, urinary tract infection.

5 Ahmed et al 23 Table 4. Factors Associated With Resistance to TMP/SMX as Assessed by Univariate Analysis. Number (%) of Isolates Risk Factor Susceptible Resistant OR (95% CI) P Value Location Emergency department 136 (14.8) 39 (16.5) 1.13 ( ).54 Inpatient 29 (3.2) 6 (2.5) 0.82 ( ).66 Outpatient 757 (82.1) 192 (81.0) 1 Gender Male 40 (4.3) 23 (9.7) 2.37 ( ).001 Female 882 (95.7) 214 (90.3) 1 Race Black 105 (11.4) 32 (13.5) 1.25 ( ).3 Others 126 (13.7) 37 (15.6) 1.21 ( ).36 White 691 (75.0) 168 (70.9) 1 Age (15.2) 46 (19.4) 1.35 ( ) (84.8) 191 (80.6) 1 Health insurance Government 481 (52.2) 140 (59.1) 1.32 ( ).06 Private 441 (47.8) 97 (40.9) 1 History of genitourinary abnormality Yes 67 (7.3) 35 (14.8) 2.21 ( ).0004 No 855 (92.7) 202 (85.2) 1 Previous diagnosis of UTI Yes 27 (2.9) 8 (3.4) 1.16 ( ).72 No 895 (97.1) 229 (96.6) 1 History of chronic medication Yes 34 (3.7) 11 (4.6) 1.27 ( ).5 No 888 (96.3) 226 (95.4) 1 Antibiotics prescribed in the past 6 months Yes 384 (41.7) 121 (51.1) 1.46 ( ).009 No 538 (58.4) 116 (49.0) 1 Fever Yes 200 (21.7) 52 (21.9) 1.05 ( ).93 No 722 (78.3) 185 (78.1) 1 Dysuria Yes 500 (54.2) 118 (49.8) 0.84 ( ).22 No 422 (45.8) 119 (50.2) 1 Frequency Yes 354 (38.4) 78 (32.9) 0.79 ( ).12 No 568 (61.6) 159 (67.1) 1 Urgency Yes 166 (18.0) 39 (16.5) 0.90 ( ).58 No 756 (82.0) 198 (83.5) 1 Vomiting Yes 110 (11.9) 26 (11.0) 0.91 ( ).68 No 812 (8.1) 211 (89.0) 1 Irritability Yes 36 (3.9) 8 (3.4) 0.86 ( ).7 No 886 (96.1) 229 (96.6) 1 Abdominal/flank pain Yes 338 (36.7) 76 (32.1) 0.82 ( ).19 No 584 (63.3) 161 (67.9) 1 Mode of urine collection Catheterized 72 (7.8) 32 (13.5) 1.84 ( ).007 Void 850 (92.2) 205 (86.5) 1 Abbreviations: TMP/SMX, trimethoprim/sulfamethoxazole; OR, odds ratio; CI, confidence interval; UTI, urinary tract infection.

6 24 Clinical Pediatrics 55(1) Table 5. Multivariate Analysis of Independent Risk Factors for Escherichia coli Isolate Resistance to Ampicillin and TMP/SMX. Ampicillin TMP/SMX Risk Factor Number (%) of Resistant Isolates Unadjusted Odds Ratio Estimate/95% CI Adjusted Odds Ratio Estimate/95% CI Number (%) of Resistant Isolates Unadjusted Odds Ratio Estimate/95% CI Adjusted Odds Ratio Estimate/95% CI Location ED versus 89 (17.5) 1.43 ( ) 1.26 ( ) 39 (16.5) 1.13 ( ) 0.97 ( ) outpatient Inpatient versus 21 (4.1) 2.07 ( ) 1.73 ( ) 6 (2.5) 0.82 ( ) 0.71( ) outpatient Gender Male versus female 41 (8.1) 2.50 ( ) 2.29 ( ) 23 (9.7) 2.37 ( ) 2.02 ( ) Race Black versus white 69 (13.6) 1.35 ( ) 1.26 ( ) 32 (13.5) 1.25 ( ) 1.26 ( ) Others versus 72 (14.2) 1.06 ( ) 0.99 ( ) 37 (15.6) 1.21 ( ) 1.23 ( ) white Age 0-4 Versus (20.2) 1.72 ( ) 1.61 ( ) 46 (19.4) 1.35 ( ) 1.37 ( ) Health insurance Government versus private 285 (56.0) 1.19 ( ) 1.05 ( ) 140 (59.1) 1.32 ( ) 1.27 ( ) History of genitourinary abnormality Yes versus no 57 (11.2) 1.70 ( ) 1.57 ( ) 35 (14.8) 2.21 ( ) 1.86 ( ) History of chronic medication Yes versus no 23 (4.5) 1.35 ( ) 1.13 ( ) 11 (4.6) 1.27 ( ) 1.03 ( ) Antibiotics prescribed in past 6 months Yes versus no 230 (45.2) 1.12 ( ) 1.08 ( ) 121 (51.1) 1.46 ( ) 1.33 ( ) Symptoms (yes vs no) Fever 127 (25.0) 1.40 ( ) 1.18 ( ) 52 (21.9) 1.05 ( ) 0.91 ( ) Irritability 23 (4.5) 1.42 ( ) 0.74 ( ) 8 (3.4) 0.86 ( ) 0.61 ( ) Urinary symptoms 310 (60.9) 0.89 ( ) 1.13 ( ) 133 (56.1) 0.72 ( ) 0.82 ( ) Vomiting/ Abdominal pain 211 (41.5) 1.02 ( ) 1.00 ( ) 89 (37.6) 0.83 ( ) 0.84 ( ) Abbreviations: TMP/SMX, trimethoprim/sulfamethoxazole; CI, confidence interval; ED, emergency department. Table 4 indicated that boys, when compared with girls, are more susceptible to developing UTIs with TMP/SMX-resistant E coli (P <.001). Also, catheterized urine specimens were reported to be more resistant to TMP/SMX (P <.007) than voided samples. Prior prescription of antibiotics in the past 6 months (P <.009) and history of genitourinary abnormality (P <.0004) were found to be significant factors associated with TMP/SMX-resistant E coli. A high collinearity was observed between previous diagnosis of UTI and history of genitourinary abnormality (Pearson correlation coefficient = 0.27). Therefore, we removed previous diagnosis of UTI from the logistic regression models. In multivariate analysis (Table 5), boys were 2.29 times more likely to have E coli isolates resistant to ampicillin than were girls (CI = ). Similarly, boys also had twice the risk of being resistant to TMP/SMX than girls (CI = ). When all explanatory variables were included in the model, children <4 years of age were more likely to have ampicillin-resistant E coli compared with children older than 4 years (OR = 1.61; CI = ). Patients with a history of genitourinary abnormality were 1.57 times more likely to be resistant to ampicillin (CI = ) and 1.86 times more likely to have TMP/SMX resistance (CI = ) than those without such abnormalities. Patients who had antibiotics prescribed in the past 6 months were 1.33 times more likely to be resistant to TMP/SMX (CI = ). Discussion Antibiotic resistance is now becoming a serious clinical problem in treating uncomplicated UTI patients in

7 Ahmed et al 25 ambulatory care settings. In pediatrics, the goal of treatment of UTIs is to prevent urosepsis and to reduce the risk of renal scarring. Ampicillin, TMP/SMX, and cefazolin are commonly prescribed first-line antimicrobial therapy for uncomplicated urinary infections. 4 Knowledge of local susceptibility patterns is vital for the selection of appropriate empirical therapy for UTIs. This study provided the distribution of demographic and clinical data along with antibiotic susceptibility patterns of E coli isolated from patients with communityacquired UTIs at a local university-affiliated hospital. The study population included children managed in emergency room and outpatient clinics. To date, there are limited studies that have reviewed the resistance of E coli uropathogen to commonly prescribed antibiotics among children in ambulatory care settings for UTIs. Our results revealed that a high proportion of E coli urinary isolates from children were resistant to first line agents: 43.9% for ampicillin, 20.5% for TMP/SMX, and 3.7% for cefazolin. McLoughlin and Joseph 12 reported a resistance of 45.5% to ampicillin, 6.5% to Bactrim, and 5.2% to cefazolin against Gram-negative pathogens in children evaluated in the emergency department. More recently, Edlin et al 13 published an article where they examined the current national patterns of antibiotic resistance of outpatient pediatric patients using an electronic surveillance database from 195 US hospitals. The authors reported an increasing trend in E coli resistance rates for TMP/SMX, from 23% to 31% in male patients and from 20% 23% in female patients, which are consistent with our results. In addition to ampicillin, ampicillin/sulbactum, and cefazolin, our institution s antibiogram data for children also demonstrated a similar gradual increase in TMP/SMXresistant E coli isolates over time (Figure 1). It should be noted that the MDR pattern is emerging in pediatric UTI patients as well. Our study showed that about 21% of E coli isolates were resistant to at least 2 antibiotics, and 8.9% of isolates were resistant to 3 or more antibiotics. Not only that, within isolates that are resistant to ampicillin, 41% were also found to be resistant to TMP/SMX (n = 208/509) and 8.2% (n = 42/509) to cefazolin. One approach to resolve the issue would be to develop an individual patient profile matrix by incorporating local antibiotic susceptibility patterns and patient s risk factor in determining the likelihood of resistance to an individual. Compared with children 4 years old, patients younger than 4 years were more likely to have isolates resistant to ampicillin but not to TMP/SMX. Studies have shown that, often, children in this age group go to child care facilities and are prone to be in contact with the resistant strain of E coli. 17 They are also more likely to be contracting respiratory tract infections and otitis media at higher rates and, therefore, likely to be prescribed multiple and 50.0% 45.0% 40.0% 35.0% 30.0% 25.0% 20.0% 15.0% 10.0% 5.0% 0.0% Ampicillin Cefazolin Ampicillin/Sulb TMP/SMX 2012 Figure 1. Selected antibiotic resistance trend for urinary Escherichia coli isolates from 2007 to 2012 for patients seen in emergency rooms and primary care clinics. prolonged courses of antibiotics by health care providers. 18,19 Often, physicians prescribe amoxicillin for such infections, which may make patients resistant more to ampicillin than to TMP/SMX. Our data set, unfortunately, lacks adequate documentation on day care attendance. Unlike in other studies, gender was found to be a significant risk factor for E coli isolate resistance to both ampicillin and TMP/SMX. Despite the fact regarding the higher prevalence of UTIs among girls than boys because of anatomical and physiological factors, the reason why boys were more prone to antibiotic-resistant E coli isolates was not clearly understood. One likely explanation could be the tendency for boys to present more often with complicated UTIs, which may be associated with more antimicrobial-resistant uropathogens. 20 Patients evaluated in the emergency department were reported to be more prone to have ampicillin-resistant E coli isolate compared with clinic patients. Often, the emergency department is a part of a hospital facility; therefore, there is an increase in likelihood that it shares similar risks as hospitals in carrying more resistant variant E coli isolates. Also, the catheterized method of urine collection appeared to be another risk factor associated with antibiotic-resistant isolates. A more reasonable explanation could be that these children were likely to be younger in age; be ill appearing; have multiple comorbidities, including genitourinary abnormalities; have multiple episodes of UTI; or be on antimicrobial prophylaxis. We found a strong association between history of genitourinary abnormality and E coli isolates resistant to ampicillin and TMP/SMX in our study. The findings are consistent with those of the Canadian study by Allen

8 26 Clinical Pediatrics 55(1) et al, 14 where the authors demonstrated that patients with a history of genitourinary tract abnormality were 2.4 times more likely to have resistant isolates than patients without such abnormalities. 14 Our study reported a high correlation between history of genitourinary tract abnormality and previous history of UTIs, and thereby precluded incorporating this potential risk factor in our analysis. Many studies reported that children receiving prophylactic antibiotics were at increased risk for resistant organisms. 17,21,22 Our study, however, found a marginal association between receiving antibiotic prescriptions in the past 6 months and increased risk for TMP/SMX-resistant UTI, with an adjusted OR of 1.33 (CI = ) when the crude OR was 1.46 (CI = ). The finding is consistent with a case-control study done in the United Kingdom by Hillier et al, 23 where the authors reported that previous exposure to antibiotics was a significant risk factor for resistant E coli. Previously, the relationship between prior antibiotic prescription and the risk of subsequent development of resistant infection, particularly for E coli driven UTIs, has not been well characterized for pediatric patients at the individual level. Although study outcomes from surveillance data provides a snapshot of antimicrobial susceptibility patterns to commonly used agents for UTIs in different geographical locations, they are inadequate in providing any meaningful association between the two. For example, the North American Urinary Tract Collaborative Alliance (NAUTICA) conducted a study collecting outpatient E coli urinary isolates from 30 US and 10 Canadian medical centers and concluded that overall resistance rates for antimicrobials were higher in US than Canadian medical centers. 24 The application of study outcomes, however, to local levels could be problematic because there is often a nonuniformity in data collection methods, and also, data were aggregated irrespective of age, gender, race, and locality. In contrast, the current study was uniquely able to examine the relationship of demographical and clinical variables as risk factors for ampicillin- and TMP/SMX-resistant urinary E coli isolates in children in the ambulatory care setting. All urinary samples were analyzed in one central location, and the laboratory data were merged with the electronic clinical data set, which was later validated systematically with individual patients medical records. The results of our investigation must be interpreted in light of the following considerations. The management of acute uncomplicated UTIs has changed dramatically recently. Empirical broad-spectrum antibiotic selection, when a narrower-spectrum agent would suffice, became the norm in order to reduce medical costs, which discouraged health care providers from ordering for routine urine cultures and subsequent susceptibility testing for otherwise healthy patients with uncomplicated UTIs. Hence, there might be a potential for overestimating the resistance rates because urinary isolates that are tested in the laboratory may be predominantly from patients for whom previous antimicrobial treatment failed or from patients with underlying risk factors. Dahle et al 25 recommended the use of caution with hospital antibiogram data, which may provide inaccurate information regarding antibiotic resistance patterns for ambulatory pediatric patients. However, our patient-based study corroborated the laboratory data systematically with patients medical records and, hence, minimized that potential. In a retrospective review of medical records, certain variables such as previous diagnosis of UTI, history of chronic medication, certain symptoms such as irritability, were often incomplete or missing and, therefore, hindered our ability to evaluate the significance of those risk factors in complete detail. Finally, although the study results are useful to our health care practitioners at the local level, caution must be used when applied to other geographic areas. In conclusion, we observed a higher rate of ampicillin- and TMP/SMX-resistant urinary E coli isolates among boys and children with a history of genitourinary abnormality who were evaluated either in emergency departments or primary care clinics. Age <4 years was reported to be a significant risk factor for ampicillinresistant E coli, whereas antibiotic prescribed in the past 6 months was found to be associated with TMP/SMX resistance. Regional variability in resistance to single and multiple agents and the increase in ampicillin and TMP/SMX resistance among uropathogens over time stresses the importance of local population-specific surveillance to select appropriate empirical antimicrobials for UTIs in children. This study serves as a guideline in reviewing existing antibiotic prescription patterns in order to better determine optimal empirical antibiotic selection in ambulatory care settings. We, therefore, recommend that children in the risk groups identified by our study should have their antimicrobial regimens periodically reassessed in relation to proposed surveillance data. Also, it would be prudent to alternate antimicrobials in patients who require a prolonged course of antibiotics. Further longitudinal studies are warranted to identify specific risk factors and virulence of organisms to better understand the potential forces that trigger the resistance. In an era of increasing antibiotic resistance, a multidisciplinary, effective educational intervention for patients, parents, and health care providers should be adopted at community and national levels to bring about rational antibiotic use in order to prolong the clinical effectiveness of existing agents.

9 Ahmed et al 27 Acknowledgment This study is approved by Carle IRB. We thank Xuan Bi and Dr Peiyong Qu from University of Illinois Statistical Department for helping with the statistical analysis and Dr Anna Keck from Carle Research Institute for logistical support in conducting this study. Author Contributions MNA participated in study design, data collection, data analysis, literature review, wrote the manuscript, and approved the final version as submitted. DV participated in data integration, compilation, and manuscript revision. A Fparticipated in laboratory data compilation and preliminary laboratorty data analysis. SC participated in data collection and review. EL participated in data collection and review. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by the Carle Foundation Research Institute. References 1. Copp HL, Shapiro DJ, Hersh AL. National ambulatory antibiotic prescribing patterns for pediatric urinary tract infection, Pediatrics. 2011;127: Warren JW, Abrutyn E, Hebel JR, Schaeffer AJ, Stamm WE. Guidelines for antimicrobial treatment of uncomplicated acute bacterial cystitis and acute pyelonephritis in women. Infectious Diseases Society of America (IDSA). Clin Infect Dis. 1999;29: Nicolle LE. Epidemiology of urinary tract infection. Infect Med. 2001;18: American Academy of Pediatrics, Committee on Quality Improvement, Subcommittee on Urinary Tract Infection. Urinary tract infection: clinical practice guideline for the diagnosis and management of the initial UTI in febrile infants and children 2 to 24 months. Pediatrics. 2011;128: Gupta K, Scholes D, Satmm WE. Increasing prevalence of antimicrobial resistance among uropathogens causing acute uncomplicated cystitis in young women. JAMA. 1999;281: Sham DF, Thornsberry C, Mayfield DC, Jones ME. Multidrug-resistance urinary tract isolates of Escherichia coli prevalence and patient demographics in United States in J Antimicrob Chemother. 2001;45: Gales AC, Jones RN, Gordon KA, et al. Activity and spectrum of 22 antimicrobial agents tested against urinary tract infection pathogens in hospitalized patients in Latin America: report from the second year of the SENTRY antimicrobial surveillance program (1998). J Antimicrob Chemother. 2000;45: Jones RN, Kugler KC, Pfaller MA, WinoKur PI. Characteristics of pathogens causing urinary tract infections in hospitals in North America: results from the SENTRY antimicrobial surveillance program (1997). Diagn Microbiol Infect Dis. 1999;35: Sanchez GV, Master RN, Karlowsky JA, Bordon JM. In vitro antimicrobial resistance of urinary Escherichia coli isolates among U.S. outpatients from 2000 to J Antimicrob Chemother. 2012;56: Gupta K, Hooton TM, Naber KG, et al. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis. 2011,52:e103-e Zhanel GG, Karlowsky JA, Harding GKM, et al. A Canadian national surveillance study of urinary tract isolates from outpatients: comparison of the activities of trimethoprim-sulfamethoxazole, ampicillin, mecillinam, nitrofurantoin, and ciprofloxacin. Antimicrob Agents Chemother. 2000;44: McLoughlin TG, Joseph MM. Antibiotic resistance patterns of uropathogens in pediatric emergency department patients. Acad Emerg Med. 2003;10: Edlin RS, Shapiro DJ, Hersh AL, Copp HL. Antibiotic resistance patterns of outpatient pediatric urinary tract infections. J Urol. 2013;190: Allen UD, MacDonald N, Fuite L, Chan F, Stephens D. Risk factors for resistance to first-line antimicrobials among urinary tract isolates of Escherichia coli in children. CMAJ. 1999;160: Smith PB, Gavan TL, Isenberg HD, et al. Multi-laboratory evaluation of an automated microbial detection/identification system. J Clin Microbiol. 1978;8: Clinical and Laboratory Standards Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. Approved standard, 8th ed. Wayne, PA: Clinical and Laboratory Standards Institute; CLSI publication M07-A Reeves ER, Fong M, Pickering LK, Bartlett A III, Alvarez M, Murray BE. Risk factors for fecal colonization with trimethoprim-resistant and multi-resistant Escherichia coli among children in day-care centers in Houston, Texas. Antimicrob Agents Chemother. 1990;34: Wald ER, Dashefsky B, Byers C, Guerra N, Taylor F. 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10 28 Clinical Pediatrics 55(1) 21. Paris D, Staussberg RA, Vitzur YN, Nussinovitch M, Hare L, Amir J. Bacterial susceptibility to oral antibiotics in community acquired urinary tract infections. Arch Dis Child. 2003;88: Murray BE, Rensimer ER, DuPont HL. Emergence of high-level trimethoprim resistance in fecal Escherichia coli during oral administration of trimethoprim or trimethoprim-sulfamethoxazole. N Engl J Med. 1982;306: Hillier S, Roberts Z, Dunstan F, Butler C, Howard A, Palmer S. Prior antibiotics and risk of antibiotic-resistant community-acquired urinary tract infection: a case-control study. J Antimicrob Chemother. 2007;60: Zhanel GG, Hisanaga TL, Laing NM, et al. Antibiotic resistance in outpatient Escherichia coli urinary isolates: final results from the North American Urinary Tract Infection Collaborative Alliance (NAUTICA). Int J Antimicrob Agents. 2006;27(6): Dahle KW, Korgenski EK, Hersh AL, Srivastava R, Gesteland PH. Clinical value of an ambulatory-based antibiogram for uropathogens in children. J Pediatr Infect Dis Soc. 2012;1:

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