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A decade of trends in the distribution and antimicrobial susceptibility of prevalent uropathogens among pediatric patients from Tehran, Iran during 2005-2016 |
Ali Reza Nateghiana,Sina Karajib,Khosrow Zamanic,d,*()
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a Ali Asghar Clinical Research Development Center (AACRDC), Ali Asghar Children’s Hospital, Iran University of Medical Sciences, Tehran, Iran b General PractitionerAli Asghar Children’s Hospital, Iran University of Medical Sciences, Tehran, Iran c Student Research Committee, Iran University of Medical Sciences, Tehran, Iran d Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran |
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Abstract Objectives: To determine changes in the distribution of uropathogens and their antimicrobial resistance in pediatric patients in a children's hospital from 2005 to 2016. Methods: A cross-sectional analysis of uropathogens and their antimicrobial resistance within inpatient children was performed over the 11-year period, 2005 to 2016, in Ali Asghar children's hospital. The rate of antibiotic resistance among patients was evaluated according to demographic data including age, sex, urinary tract abnormities and history of antibiotic consumption. Results: In total, 958 female and 349 male positive cultures were analyzed. Escherichia coli (E. coli) (77.6%) was the most common causative agent of urinary tract infection (UTI) in children and Klebsiella pneumoniae (10.4%), Pseudomonas aeruginosa (2.4%), and Enterococcus spp (2.4%) were less frequent isolated bacteria. The resistance rates of E. coli isolates were increased against amikacin, ceftriaxone, ceftazidime, ciprofloxacin, cotrimoxazole and imipenem from 2005 to 2010. However, we observed a decreasing trend for some of antibiotics including amikacin, gentamicin, imipenem, ceftazidime and cotrimoxazole during 2014-2016. The rate of antibiotic resistance was greater in boys than in girls against many antibiotics. The rate of resistance to amikacin, gentamicin, nitrofurantoin and cotrimoxazole in patients aged <1 year was higher than other age groups (p<0.001). A higher antibiotic resistance rate was observed in patients with anatomical abnormality and those who have had a history of antibiotic consumption. Conclusion: The study indicated the significant decrease in E. coli antibiotic resistance in the last 3 years. An effective empirical treatment regime should be based on local epidemiology and antimicrobial susceptibility testing.
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Received: 05 November 2019
Available online: 29 May 2020
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Corresponding Authors:
Khosrow Zamani
E-mail: zamanikh@yahoo.com
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Microorganisms | Number (%) | Gram-negative bacteria | Escherichia coli | 1014 (77.6) | Klebsiella pneumoniae | 140 (10.71) | Pseudomonas aeruginosa | 32 (2.44) | Proteus spp | 15 (1.14) | Enterobacter spp | 13 (1.0) | Acinetobacter spp | 3 (0.23) | Other Gram-negative bacteria | 8 (0.61) | Gram-positive bacteria | Enterococcus spp | 32 (2.44) | Coagulase-negative staphylococci | 29 (2.21) | Staphylococcus aureus | 5 (0.4) | Other streptococci | 14 (1.07) | Other Gram-positive bacteria | 2 (0.15) | Total | 1307 (100) |
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Frequency of uropathogens isolated from urine cultures.
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Antibiotics | Escherichia coli | Klebsiella pneumoniae | Pseudomonas aeruginosa | Enterococcus spp | %R | TN | %R | TN | %R | TN | %R | TN | Amikacin | 6.95 | 950 | 24.62 | 130 | 6.9 | 29 | 71.43 | 7 | Gentamicin | 19.02 | 936 | 29.46 | 129 | 24.14 | 29 | 85 | 20 | Ampicillin | 78.75 | 607 | 88.68 | 106 | 100 | 14 | 40.91 | 22 | Cefazolin | 56.33 | 529 | 76.09 | 100 | 82.35 | 17 | - | - | Cephalexin | 52.28 | 329 | 57.14 | 21 | 100 | 7 | - | - | Cefuroxime | 53.23 | 387 | 60 | 70 | 92.31 | 13 | - | - | Ceftizoxime | 29.09 | 55 | 33.33 | 3 | - | - | - | - | Ceftazidime | 28.38 | 613 | 41.94 | 93 | 20.83 | 24 | - | - | Cefotaxime | 37.75 | 355 | 55.56 | 27 | 75.0 | 12 | - | - | Ceftriaxone | 36.08 | 898 | 46.28 | 121 | 46.15 | 26 | - | - | Cefepime | 15.58 | 552 | 24.72 | 89 | 11.11 | 18 | - | - | Imipenem | 13.16 | 395 | 4.55 | 44 | 6.25 | 16 | - | - | Ciprofloxacin | 19.66 | 829 | 7.89 | 114 | 4 | 25 | 60 | 20 | Ofloxacin | 31.11 | 135 | 15.38 | 13 | 0 | 4 | 20 | 5 | Cotrimoxazole | 60.24 | 835 | 40.17 | 117 | 81.82 | 22 | 73.68 | 19 | Nitrofurantoin | 2.93 | 957 | 17.42 | 132 | 83.87 | 31 | 16.67 | 18 | Nalidixic acid | 46.43 | 420 | 18.42 | 38 | 76.92 | 13 | 42.86 | 7 | Erythromycin | - | - | - | - | - | - | 76.92 | 26 |
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The pattern of antibiotic resistance for selected uropathogens.
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Antibiotics | Boys | Girls | p-Value | Number (%) of resistant isolates | Total number of isolates | Number (%) of resistant isolates | Total number of isolates | Amikacin | 51 (16.8) | 303 | 64 (7.5) | 859 | <0.001 | Ampicillin | 169 (83.7) | 202 | 443 (75.9) | 584 | <0.021 | Ceftriaxone | 140 (47.5) | 295 | 285 (34.9) | 816 | <0.001 | Ceftazidime | 81 (38.9) | 208 | 147 (26.5) | 554 | <0.001 | Nitrofurantoin | 47 (14.8) | 317 | 50 (5.6) | 891 | <0.001 | Gentamicin | 98 (31.8) | 308 | 160 (18.3) | 874 | <0.001 | Ciprofloxacin | 60 (21.5) | 279 | 134 (17.5) | 765 | <0.142 | Imipenem | 20 (16.1) | 124 | 38 (10.7) | 355 | <0.11 | Cotrimoxazole | 156 (54.4) | 287 | 456 (58.3) | 782 | <0.247 |
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Distribution and frequency of antibiotic resistance uropathogens by gender.
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Antimicrobial agent | 2005-2007 | 2008-2010 | 2011-2013 | 2014-2016 | p-Value | Resistance percentage | Total number | Resistance percentage | Total number | Resistance percentage | Total number | Resistance percentage | Total number | Amikacin | 9.2% | 142 | 13.6% | 213 | 7.6% | 249 | 1.4% | 346 | <0.001 | Ampicillin | 66.7% | 6 | 90% | 50 | 81% | 211 | 75.9% | 340 | 0.058 | Ceftriaxone | 30.5% | 128 | 42.6% | 216 | 44.7% | 215 | 28.6% | 339 | <0.001 | Ceftazidime | 25.8% | 62 | 46.3% | 41 | 40.5% | 173 | 20.5% | 337 | <0.001 | Ciprofloxacin | 14.1% | 64 | 21.4% | 187 | 23% | 243 | 17.3% | 335 | 0.027 | Cotrimoxazole | 65.5% | 139 | 70.8% | 192 | 70.6% | 221 | 42.4% | 283 | <0.001 | Gentamycin | 18.4% | 136 | 28.4% | 211 | 24.2% | 260 | 9.1% | 329 | <0.001 | Imipenem | 8.3% | 36 | 18.2% | 214 | 10.5% | 86 | 1.7% | 59 | 0.005 | Nitrofurantoin | 6.7% | 134 | 6% | 216 | 2.3% | 263 | 0.0% | 344 | <0.001 |
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Antimicrobial resistance trends among Escherichia coli isolates from Ali Asghar Hospital, 2005 to 2016.
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Organisms | Patients with abnormalities, n (percent of isolates, %) | Patients without anatomical abnormalities, n (percent of isolates, %) | Escherichia coli | 350 (73.3) | 618 (80.7) | Klebsiella pneumoniae | 51 (10.6) | 79 (10.3) | Pseudomonas aeruginosa | 23 (4.8) | 7 (0.9) | Enterococcus. spp | 11 (2.3) | 17 (2.2) | Enterobacter. spp | 9 (1.8) | 4 (0.5) | Proteus. spp | 6 (1.2) | 9 (1.2) | Coagulase-negative staphylococci | 8 (1.6) | 9 (1.2) | Others | 19 (3.9) | 23 (3) |
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Distribution of UTI etiological agents in patients with and without anatomical abnormalities.
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Antimicrobial agent | Patients without anatomical abnormalities | Patients with anatomical abnormalities | p-Value | Number (%) of resistant isolates | Total number of isolates | Number (%) of resistant isolates | Total number of isolates | Amikacin | 57 (8.4) | 677 | 51 (12.0) | 426 | 0.053 | Ampicillin | 366 (76.3) | 480 | 215 (79.9) | 269 | 0.247 | Cefazolin | 221 (53.3) | 415 | 157 (72.7) | 216 | 0.0002 | Cefepime | 65 (15.6) | 417 | 55 (22.2) | 248 | 0.032 | Cephalexin | 103 (45.8) | 225 | 95 (67.4) | 141 | 0.0005 | Ceftriaxone | 208 (32.3) | 644 | 196 (47.2) | 415 | 0.0001 | Ceftazidime | 118 (26.8) | 441 | 101 (35.4) | 285 | 0.0128 | Ciprofloxacin | 94 (15.0) | 627 | 83 (22.7) | 365 | 0.0021 | Cotrimoxazole | 361 (57.6) | 627 | 224 (57.6) | 389 | 0.998 | Gentamicin | 130 (18.6) | 699 | 111 (26.2) | 424 | 0.0027 | Imipenem | 27 (10.1) | 267 | 28 (15.1) | 185 | 0.108 | Nitrofurantoin | 45 (6.3) | 715 | 44 (10.1) | 434 | 0.0181 |
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Distribution of resistant isolates of Escherichia coli among patients with and without anatomical abnormalities.
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Antibiotics | Previous antibiotic consumption (+) | Previous antibiotic consumption (-) | p-Value | Number (%) of resistant isolates | Total number | Number (%) of resistant isolates | Total number | Ampicillin | 16 (8.9) | 180 | 6 (4.9) | 22 | 0.192 | Amikacin | 103 (82.4) | 125 | 66 (68.8) | 96 | 0.017 | Cefepime | 25 (23.4) | 107 | 5 (5.5) | 91 | 0.0004 | Cephalexin | 36 (52.9) | 68 | 9 (32.1) | 28 | 0.063 | Cefotaxime | 31 (43.7) | 71 | 7 (24.1) | 29 | 0.067 | Ceftriaxone | 73 (42.2) | 173 | 33 (27) | 122 | 0.008 | Ceftazidime | 34 (31.8) | 107 | 14 (15.4) | 91 | 0.007 | Ciprofloxacin | 36 (21.1) | 171 | 15 (12.9) | 116 | 0.077 | Cotrimoxazole | 102 (60.7) | 168 | 43 (41.3) | 104 | 0.002 | Gentamicin | 40 (20.8) | 192 | 19 (15.4) | 123 | 0.231 | Imipenem | 10 (11.4) | 88 | 2 (4.3) | 47 | 0.166 | Nalidixic acid | 41 (49.4) | 83 | 8 (22.9) | 35 | 0.008 | Nitrofurantoin | 16 (8.3) | 193 | 4 (3.2) | 126 | 0.065 |
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Association of previous antibiotic consumption and antibiotic resistance.
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[1] |
Bitsori M, Maraki S, Galanakis E. Long-term resistance trends of uropathogens and association with antimicrobial prophylaxis. Pediatr Nephrol 2014; 29:1053-8.
doi: 10.1007/s00467-013-2719-x
pmid: 24362645
|
[2] |
Aghamahdi F, Hashemian H, Shafiei M, Akbarian Z, Rostam NM, Fallah KM. Etiologies and antibiotic resistance patterns in infants with urinary tract infections hospitalized in children medical center. Rasht IJN 2013; 4:21-5.
|
[3] |
Sobel JD, Kaye D. Urinary tract infections. In: Bennett JE, Dolin R, Blaser MJ, editors. Principles and practice of infectious diseases. Philadelphia: Elsevier saunder; 2015. P897-9.
|
[4] |
Kock R, Siemer Ph, Esser J, Kampmeier S, Berends MS, Glasner C, et al. Defining multidrug resistance of gramnegative bacteria in the Dutch-German border region-impact of national guidelines. Microorganisms 2018; 6: 11. https://doi.org/10.3390/microorganisms6010011.
doi: 10.3390/microorganisms6010011
|
[5] |
Nateghian AR, Robinson JL, Mohanddesi SH, Hooman N. Resistance pattern of breakthrough urinary tract infections in children on antibiotic prophylaxis. J Infect Public Health 2009; 2:147-52.
doi: 10.1016/j.jiph.2009.08.002
|
[6] |
Zellweger RM, Basnyat B, Shrestha P, Prajapati KG, Dongol S, Sharma PK, et al. Changing antimicrobial resistance trends in Kathmandu, Nepal: a 23-year retrospective analysis of bac-teraemia. Front Med (Lausanne) 2018; 5:262-70.
|
[7] |
Karchmer AW. Bloodstream infections: the problem and the challenge. Int J Antimicrob Agents 2009; 34:S2-4. https://doi.org/10.1016/S0924-8579(09)70556-4.
|
[8] |
Renda R. Diagnosis and antibiotic resistance distribution in children with urinary tract infection: a single center experience. Int J Pediatr 2018; 6:6815-22.
|
[9] |
Tseng MH, Lo WT, Lin WJ, Teng CS, Chu ML, Wang CS. Changing trend in antimicrobial resistance of pediatric uropathogens in Taiwan. Pediatr Int 2008; 50:797-800.
doi: 10.1111/ped.2008.50.issue-6
|
[10] |
Mutlu M, Aslan Y, Akturk Acar F, Kader S, Bayramoglu G, Yilmaz G. Changing trend of microbiologic profile and antibiotic susceptibility of the microorganisms isolated in the neonatal nosocomial sepsis: a 14years analysis. J Matern Fetal Neonatal Med 2019; 4:1-8.
doi: 10.3109/14767059509017287
|
[11] |
Wagenlehner FM, Weidner W, Perletti G, Naber KG. Emerging drugs for bacterial urinary tract infections. Expet Opin Emerg Drugs 2010; 15:375-97.
|
[12] |
Armin S, Fallah F, Hoseini-Alfatemi SM. Antimicrobial susceptibility pattern of six threatening pathogens at Mofid children's hospital, Tehran, Iran. Arch Clin Infect Dis 2018; 13:e15576. https://doi.org/10.5812/archcid.15576.
|
[13] |
Saderi H, Oulia P, Jalali NM, Zaeri F, Zandieh E. A 3-year study of demographic characteristics of patients with urinary tract infection, microbial etiology, and susceptibility of isolated bacteria to antibiotics in Shaheed Mostafa Khomeini hospital. IJP 2006; 1:99-104.
|
[14] |
Valavi E, Nikfar R, Ahmadzadeh A, Kompani F, Najafi R, The last three years antibiotic susceptibility patterns of uropathogens in southwest of Iran. Jundishapur J Microbiol 2013; 6:e4958. https://doi.org/10.5812/jjm.4958.
|
[15] |
Erol B, Culpan M, Caskurlu H, Sari U, Cag Y, Vahaboglu H, et al. Changes in antimicrobial resistance and demographics of UTIs in pediatric patients in a single institution over a 6-year period. J Pediatr Urol 2018; 14:176.e1-5. https://doi.org/10.1016/j.jpurol.2017.12.002.
doi: 10.1016/j.jpurol.2017.12.002
|
[16] |
Gökçe i, Çiçek N, Güven S, Altuntaş Ü, Bıyıklı N, Yıldız N, et al. Changes in bacterial resistance patterns of pediatric urinary tract infections and rationale for empirical antibiotic therapy. Balkan Med J 2017; 34:432-5.
doi: 10.4274/balkanmedj
|
[17] |
McLellan LK, Hunstad DA. Urinary tract infection: pathogenesis and outlook. Trends Mol Med 2016; 22:946-57.
doi: S1471-4914(16)30118-6
pmid: 27692880
|
[18] |
Motamedifar M, Zamani KH, Hassanzadeh Y, Pashoutan S. Bacterial etiologies and antibiotic susceptibility pattern of urinary tract infections at the pediatric ward of Dastgheib hospital, Shiraz, Iran: a Three-Year Study (2009-2011). Arch Clin Infect Dis 2016; 11:e28973. https://doi.org/10.5812/archcid.28973.
|
[19] |
Azimi T, Maham S, Fallah F, Azimi L, Gholinejad Z. Evaluating the antimicrobial resistance patterns among major bacterial pathogens isolated from clinical specimens taken from patients in Mofid Children’s Hospital, Tehran, Iran: 2013-2018. Infect Drug Resist 2019; 12:2089-102.
doi: 10.2147/IDR
|
[20] |
Mirsoleymani SR, Salimi M, Shareghi Brojeni M, Ranjbar M, Mehtarpoor M. Bacterial pathogens and antimicrobial resistance patterns in pediatric urinary tract infections: a four-year Surveillance Study (2009-2012). Int J Pediatr 2014; 2014:125142. https://doi.org/10.1155/2014/126142.
|
[21] |
Taheri PA, Navabi B, Khatibi E. Frequency and susceptibility of bacteria caused urinary tract infection in Neonates: eight-year study at neonatal division of Bahrami children’s hospital, Tehran Iran. Iran J Public Health 2013; 42:1126-33.
|
[22] |
Grude N, Tveten Y, Kristiansen BE. Urinary tract infections in Norway: bacterial etiology and susceptibility. A retrospective study of clinical isolates. Clin Microbiol Infect 2001; 7:543-7.
doi: 10.1111/j.1469-0691.2001.00306.x
|
[23] |
McGregor JC, Elman MR, Bearden DT, Smith DH. Sex- and age-specific trends in antibiotic resistance patterns of Escherichia coli urinary isolates from outpatients. BMC Fam Pract 2013; 14:25. https://doi.org/10.1186/1471-2296-14-25.
doi: 10.1186/1471-2296-14-25
pmid: 23433241
|
[24] |
Lee LC, Lorenzo AJ, Koyle MA. The role of voiding cystourethrography in the investigation of children with urinary tract infections. Can Urol Assoc J 2016; 10:210-4.
doi: 10.5489/cuaj.3610
|
[25] |
Asensio A, Alvarez-Espejo T, Fernandez-Crehuet J, Ramos A, Vaque-Rafart J, Bishopberger C, et al. Trends in yearly prevalence of third-generation cephalosporin and fluoroquinolone resistant Enterobacteriaceae infections and antimicrobial use in Spanish hospitals, Spain, 1999 to 2010. Euro Surveill 2011; 16:19983. https://doi.org/10.2807/ese.16.40.19983-en.
|
[26] |
Amini M, Ansari I, Vaseie M, Vahidian M. Pattern of antibiotic resistance in nosocomial infections with Gram-negative bacilli in ICU patients (Tehran, Iran) during the ears 2012-2014. JBCP 2018; 6:23-30.
|
[27] |
Olesen SW, Barnett ML, MacFadden DR, Brownstein JS, Her-nández-Díaz S, Lipsitch M, et al. The distribution of antibiotic use and its association with antibiotic resistance. Elife 2018; 18:e39435. https://doi.org/10.7554/eLife.39435.
|
[28] |
Bryce A, Hay AD, Lane IF, Thornton HV, Costelloe C. Global prevalence of antibiotic resistance in paediatric urinary tract infections caused by Escherichia coli and association with routine use of antibiotics in primary care: systematic review and meta-analysis. BMJ 2016; 352:i939. https://doi.org/10.1136/bmj.i939.
|
[29] |
Hickling DR, Sun TT, Wu XR. Anatomy and physiology of the urinary tract: relation to host defense and microbial Infection. Microbiol Spectr 2015; 3:10. https://doi.org/10.1128/microbiolspec.UTI-0016-2012.
|
[30] |
Ahmed MN, Vannoy D, Frederick A, Chang S, Lawler E. First-line antimicrobial resistance patterns of Escherichia coli in children with urinary tract infection in emergency department and primary care clinics. Clin Pediatr (Phila) 2016; 55:19-28.
doi: 10.1177/0009922815588822
|
[31] |
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; 160:1436-40.
|
[32] |
Lutter SA, Currie ML, Mitz LB, Greenbaum LA. Antibiotic resistance patterns in children hospitalized for urinary tract infections. Arch Pediatr Adolesc Med 2005; 159:924-8.
doi: 10.1001/archpedi.159.10.924
|
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