1478 | Miscellaneous Changes in Bacterial Species and Antibiotic Sensitivity in Intensive Care Unit: Acquired Urinary Tract Infection during 10 Years Inter- val (2001-2011 ) Byung Il Yoon,1 Hyo Sin Kim,2 Sung Dae Kim,3 Kang Jun Cho,2 Sun Wook Kim,4 U-Syn Ha,4 Yong-Hyun Cho,4 Dong Wan Sohn4 Corresponding Author: Department of Urology, Yeouido St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea. Tel: +82 2 3779 1038 Fax: +82 2 761 1626 E-mail address: uroking@naver.com Received September, 2012 Accepted December, 2013 1 Department of Urology, In- ternational St. Mary’s Hospital, Incheon, Korea. 2 Department of Urology, Bucheon St. Mary’s Hospital, College of Medicine, The Catho- lic University of Korea, Bucheon, Korea. 3 Department of Urology, School of Medicine, Jeju Na- tional University, Jeju, Korea. 4 Department of Urology, Yeo- uido St. Mary’s Hospital, College of Medicine, The Catholic Uni- versity of Korea, Seoul, Korea. MISCELLANEOUS Purpose:‎Patients‎in‎the‎intensive‎care‎unit‎(ICU)‎are‎usually‎at‎greater‎risk‎for‎acquiring‎uri- nary‎tract‎infections‎(UTIs).‎Few‎studies‎have‎focused‎on‎UTIs‎specifically‎acquired‎within‎ the‎ICU.‎We‎studied‎the‎change‎in‎bacterial‎species‎causing‎UTIs‎in‎ICU‎admitted‎patients‎ in 2001 and 2011. Materials and Methods:‎We‎reviewed‎the‎medical‎records‎of‎a‎total‎of‎2,890‎ICU‎patients‎ who‎had‎undergone‎urine‎culture‎in‎2001‎and‎2011‎at‎the‎Yeouido‎and‎Bucheon‎St.‎Mary’s‎ hospitals.‎Changes‎in‎causative‎organisms‎and‎their‎antibiotic‎sensitivity‎between‎the‎years‎ 2001 and 2011 were analyzed. Results:‎Escherichia‎coli‎(E.‎coli)‎was‎the‎most‎common‎organism‎in‎ICU-acquired‎UTIs‎in‎ 2001‎and‎2011‎in‎our‎study.‎The‎pathogens‎that‎significantly‎increased‎in‎2011‎compared‎to‎ 2001‎were‎Pseudomonas,‎and‎Klebsiella‎species‎(P‎<‎.05).‎In‎2011gram-negative‎organisms‎ showed‎relatively‎higher‎sensitivities‎to‎amikacin,‎imipenem,‎and‎tazocin‎(72.0%,‎77.5%‎and‎ 76.1%,‎respectively),‎whereas‎they‎showed‎relatively‎lower‎sensitivities‎to‎third-generation‎ cephalosporins‎and‎ciprofloxacin‎(55.2%‎and‎45.0%,‎respectively).‎In‎2011gram-positive‎ organisms‎showed‎high‎sensitivities‎to‎teicoplanin‎and‎vancomycin‎(91.1%‎and‎87.9%,‎re- spectively),‎whereas‎they‎showed‎low‎sensitivities‎to‎ampicillin‎and‎ciprofloxacin‎(24.1%‎ and‎25.5%,‎respectively).‎The‎antibiotic‎resistance‎rate‎of‎Pseudomonas‎species‎was‎nearly‎ doubles‎that‎of‎E.‎coli.‎‎ Conclusion:‎Infections‎caused‎by‎Pseudomonas‎and‎Klebsiella‎species‎were‎found‎to‎have‎ increased‎significantly‎in‎2011.‎Pseudomonas‎species‎had‎a‎significantly‎lower‎susceptibility‎ to‎antibiotic‎sensitivity‎than‎other‎identified‎organisms. Keywords:‎bacterial‎infections;‎drug‎resistance;‎intensive‎care‎units;‎microbial‎sensitivity‎ tests;‎retrospective‎studies. 1479Vol. 11 | No. 02 | March- April 2014 |U R O LO G Y J O U R N A L Bacterial Species and Antibiotic Sensitivity in ICU | Yoon et al INTRODUCTION Patients‎ admitted‎ to‎ intensive‎ care‎ unit‎ (ICU)‎ are‎prone‎to‎various‎infections‎i.e.‎lung,‎urinary‎tract,‎skin,‎oral‎mucosal‎and‎etc.‎A‎huge‎number‎of‎infec- tions‎are‎device-associated‎health-care-associated‎infection‎ (DA-HAI),‎or‎nosocomial‎infections.(1)‎As‎is‎known‎to‎all,‎ due‎to‎the‎specificity‎of‎pathogens‎and‎high‎drug‎resistance,‎ nosocomial‎infection‎is‎often‎difficult‎to‎control,‎and‎asso- ciates‎with‎poor‎outcome.(2) Urinary‎tract‎infections‎(UTIs)‎are‎one‎of‎the‎most‎common‎ types‎of‎nosocomial‎infections‎encountered‎in‎the‎inpatient‎ settings‎including‎ICU.‎Amongst‎patients‎admitted‎to‎ICU,‎ studies‎have‎revealed‎the‎incidence‎of‎nosocomial‎UTIs‎to‎ range‎from‎9%‎to‎29%.(3,4)‎The‎risk‎of‎patients‎acquiring‎a‎ UTIs‎in‎an‎ICU‎is‎approximately‎2.5-fold‎higher‎than‎that‎of‎ patients‎in‎a‎general‎hospital‎ward.‎Complicated‎nosocomial‎ UTIs‎may‎lead‎to‎urosepsis,‎and‎increase‎patient‎morbidity‎ and‎mortality.(5) The‎primary‎cause‎for‎nosocomial‎UTIs‎is‎catheterization‎of‎ the‎urinary‎system.‎Since‎most‎ICU‎patients‎are‎monitored‎ with‎regard‎to‎the‎amount‎of‎intake‎and‎output‎by‎the‎Foley‎ catheter,‎they‎are‎easily‎exposed‎to‎the‎risk‎of‎infection‎due‎ to‎its‎indwelling‎characteristic.‎To‎date,‎many‎studies‎have‎ been‎conducted‎to‎examine‎the‎causative‎bacteria‎for‎UTIs‎ among‎outpatients‎and‎hospitalized‎patients.‎However,‎few‎ studies‎have‎focused‎on‎UTI‎causative‎organisms‎or‎their‎sen- sitivity‎to‎antibiotics‎in‎ICU‎patients.‎In‎UTI‎cases,‎empirical‎ antibiotics should be used until the bacterial culture is con- firmed;‎therefore,‎it‎is‎essential‎to‎examine‎the‎antibiogram‎ of‎the‎causative‎organism.‎Sensitivity‎to‎antibiotics‎may‎vary‎ depending‎on‎the‎hospital‎and‎the‎region.‎Particularly‎for‎pa- tients‎in‎the‎ICU,‎causative‎bacteria‎for‎UTIs‎may‎be‎different‎ from‎those‎isolated‎from‎the‎regular‎outpatient‎and‎general‎ ward‎patients.‎Specifically,‎in‎ICU‎patients‎the‎sensitivity‎to‎ antibiotics‎may‎be‎lower‎compared‎to‎other‎patients. Based‎on‎this‎information,‎we‎comparatively‎analyzed‎the‎ major‎causative‎bacteria‎of‎UTIs‎and‎investigated‎disparity‎in‎ the‎sensitivity‎to‎antibiotics‎between‎isolates‎from‎2001‎and‎ 2011‎in‎the‎ICUs‎of‎two‎medical‎institutions. MATERIALS AND METHODS A‎ retrospective‎ analysis‎ was‎ performed‎ on‎ urine‎ cultures‎ performed‎in‎2001‎and‎2011‎in‎ICU‎patients‎in‎two‎hospi- tals.‎Four‎ICUs‎included‎in‎this‎study:‎surgical‎ICU‎(25‎bed),‎ medical‎ ICU‎ (24‎ bed),‎ neurosurgical‎ ICU‎ (20‎ beds)‎ and‎ cardiac‎ICU‎(16‎beds).‎We‎defined‎ICU‎acquired‎UTI‎when‎ urine‎culture‎is‎positive‎[urine‎culture‎with‎a‎bacterial‎count‎ >100,000‎colony-forming‎units‎(CFU)/mL]‎within‎48‎hours‎ or‎later‎after‎admission‎in‎ICU.(6)‎We‎excluded‎the‎patients‎ who‎showed‎a‎positive‎urine‎culture‎within‎30‎days‎to‎mini- mize‎the‎duplication‎of‎test‎results‎such‎as‎reinfections‎of‎first‎ UTI.‎The‎medical‎records‎of‎patients‎were‎reviewed‎to‎make‎ a‎ differential‎ diagnosis‎ between‎ asymptomatic‎ bacteriuria‎ and‎UTI.‎Dysuria‎and‎fever‎at‎the‎time‎of‎urine‎culture‎test- ing‎were‎considered‎as‎symptomatic‎of‎UTI.‎Asymptomatic‎ bacteriuria‎was‎excluded‎from‎the‎study.‎ Urine‎collection‎was‎conducted‎according‎to‎the‎following‎ methods.‎The‎tip‎of‎the‎catheter‎was‎cleaned‎using‎a‎boric‎ sponge, and then the urine was collected using a sterilized syringe‎from‎patients‎with‎an‎indwelling‎catheter.‎From‎the‎ patients‎without‎indwelling‎catheters,‎the‎middle‎urine‎was‎ collected‎after‎cleaning‎of‎the‎urethral‎meatus‎and‎the‎per- ineal‎region‎using‎a‎boric‎sponge.‎If‎self-voiding‎was‎impos- sible,‎urine‎samples‎were‎obtained‎by‎catheterization.‎The‎ midstream‎urine‎was‎collected‎from‎pediatric‎patients‎with‎ the‎ability‎of‎voiding‎control.‎In‎other‎cases,‎urine‎samples‎ were‎obtained‎by‎catheterization.‎Bacterial‎identification‎was‎ conducted‎with‎the‎use‎of‎ATB‎kits‎(BioMérieux,‎Mumbai,‎ India).‎Species‎identification‎for‎yeast‎was‎done‎on‎VITEK‎ 2‎Compact‎system‎(BioMérieux,‎Mumbai,‎India)‎as‎per‎the‎ manufacturers’‎instruction.‎Antimicrobial‎susceptibility‎tests‎ were‎performed‎using‎the‎Kirby-Bauer‎method.‎The‎proto- col‎of‎the‎study‎was‎approved‎by‎a‎central‎ethical‎committee‎ (Catholic‎Medical‎Center,‎The‎Catholic‎University‎of‎Korea‎ College‎of‎Medicine,‎Seoul,‎Korea,‎No.‎HIRB-00145_2-002)‎ and‎by‎the‎respective‎local‎ethical‎committees. Statistical Analysis Sigmastat‎for‎Windows‎(Systat‎Inc.,‎Chicago,‎IL,‎USA)‎was‎ used‎for‎statistical‎analysis.‎To‎make‎a‎comparison‎of‎the‎rate‎ of‎bacterial‎culture‎between‎the‎two‎years,‎a‎Fisher's‎exact‎ test‎was‎performed.‎A‎P value‎<‎.05‎was‎considered‎statisti- cally‎significant. RESULTS The‎number‎of‎ICU‎patients‎who‎underwent‎urine‎culture‎ testing‎was‎1,007‎in‎2001‎and‎1,883‎in‎2011,‎for‎a‎total‎of‎ 2,890‎ICU‎patients‎who‎underwent‎urine‎culture‎testing.‎Of‎ these‎patients,‎208‎in‎2001‎and‎256‎in‎2011‎met‎study‎criteria‎ and enrolled into the study. 1480 | Miscellaneous The‎male‎to‎female‎ratio‎was‎93:129‎in‎2001‎and‎107:120‎ in 2011 (P =‎.689).‎The‎mean‎ages‎were‎57.4‎±‎21.7‎years‎in‎ 2001‎and‎60.7‎±‎24.4‎years‎in‎2011‎(P =‎.854).‎In‎both‎years,‎ the‎most‎common‎bacterial‎strain‎isolated‎from‎UTI‎patients‎ was‎E.‎coli‎(Table‎1).‎In‎2001,‎the‎causative‎bacterial‎spe- cies‎that‎were‎cultured‎included‎E.‎coli‎(24.5%),‎Enterococ- cus‎(15.5%),‎Pseudomonas‎(10.5%),‎Staphylococcus‎(8.2%),‎ coagulase‎ negative‎ Staphylococcus‎ (CNS)‎ (7.2%)‎ and‎ Klebsiella‎(4.2%).‎In‎2011,‎the‎causative‎bacteria‎that‎were‎ cultured‎ included‎ E.‎ coli‎ (23.1%),‎ Pseudomonas‎ (19.0%),‎ Enterococcus‎ (17.2%),‎ Klebsiella‎ (10.1%),‎ CNS‎ (4.2%),‎ and‎Staphylococcus‎(4.2%).‎For‎yeast‎species,‎Candida‎and‎ Trichosporon‎species‎were‎identified.‎Other‎bacterial‎strains‎ included,‎Enterobacter,‎Serratia,‎Stenotrophomonas,‎Strepto- coccus,‎Myroides,‎Proteus,‎Providencia,‎Morganella,‎Citro- bacter,‎Acinetobacter‎and‎Alcaligenes.‎Overall,‎ the‎propor- tion‎of‎gram-negative‎bacteria‎was‎35.0%‎in‎2001‎and‎50.1%‎ in 2011 (P‎<‎.05)‎and‎the‎proportion‎of‎gram-positive‎bac- teria‎was‎30.9%‎in‎2001‎and‎39.6%‎in‎2011‎(P‎=‎.748).‎The‎ proportion‎of‎yeast‎was‎13.7%‎in‎2001‎and‎15.5%‎in‎2011.‎ The‎proportion‎of‎Pseudomonas‎and‎Klebsiella‎significantly‎ increased‎from‎2001‎to‎2011‎(P‎<‎.05).‎Despite‎a‎lack‎of‎sta- tistical‎significance,‎the‎proportion‎of‎Enterococcus‎increased‎ from‎15.5%‎to‎17.2%‎and‎Staphylococcus‎aureus‎decreased‎ from‎8.2%‎to‎4.2%‎in‎2011‎compared‎to‎2001.‎ In‎each‎bacterial‎strain,‎antibiotic‎sensitivity‎was‎analyzed‎ (Table‎2).‎Ampicillin‎showed‎low‎sensitivity‎to‎gram-negative‎ bacteria‎(24.5%‎in‎2001‎and‎23.4%‎in‎2011).‎Ceftazidime,‎a‎ third-generation‎cephalosporin,‎showed‎relatively‎high‎sen- sitivity‎to‎gram-negative‎bacteria‎(33.0%‎in‎2001‎and‎62.0%‎ in‎2011).‎Of‎the‎aminoglycosides‎in‎gram-negative‎bacteria,‎ amikacin‎(70.2%‎in‎2001‎and‎72.0%‎in‎2011)‎showed‎high‎ sensitivity‎as‎compared‎to‎gentamicin‎(60.1%‎in‎2001‎and‎ 57.2%‎in‎2011)‎or‎tobramycin‎(54.5%‎in‎2001‎and‎60.1%‎in‎ 2011).‎Quinolones‎such‎as‎ciprofloxacin‎showed‎relatively‎ low‎ sensitivity‎ (50.1%‎ in‎ 2001‎ and‎ 55.2%‎ in‎ 2011)‎ com- pared‎to‎the‎aminoglycosides‎in‎gram-negative‎bacteria.‎In‎ addition,‎the‎Bactrim‎(sulfamethoxazole‎and‎trimethoprim)‎ showed‎a‎low‎degree‎of‎antibiotic‎sensitivity‎at‎30.2%‎and‎ 40.1%,‎respectively.‎ In‎a‎meticulous‎review‎of‎the‎data,‎Escherichia‎coli‎(E.‎coli)‎ had‎a‎lower‎degree‎of‎antibacterial‎sensitivity‎to‎ampicillin‎ in‎2001‎and‎in‎2011,‎but‎it‎had‎a‎relatively‎higher‎degree‎of‎ antibacterial‎sensitivity‎to‎the‎third-generation‎cephalosporin‎ ceftazidime‎in‎2001‎and‎in‎2011.‎In‎the‎case‎of‎aminoglyco- sides,‎amikacin‎showed‎a‎very‎high‎antibacterial‎sensitivity.‎ Ciprofloxacin‎had‎a‎relatively‎higher‎degree‎of‎antibacterial‎ sensitivity‎in‎2001‎and‎in‎2011.‎Klebsiella‎had‎a‎very‎low‎ degree‎of‎antibacterial‎sensitivity‎to‎ampicillin‎in‎2001‎and‎in‎ 2011.‎Pseudomonas‎was‎found‎to‎have‎almost‎no‎sensitivity‎ to‎cefotaxime‎and‎then‎showed‎a‎relatively‎lower‎degree‎of‎ antibacterial‎sensitivity‎to‎ceftazidime,‎the‎aminoglycosides,‎ and‎quinolone‎at‎a‎rate‎of‎30-40%.‎In‎particular,‎there‎was‎a‎ low‎degree‎of‎antibacterial‎sensitivity‎to‎imipenem‎at‎a‎rate‎of‎ 45%‎in‎2011‎(Table‎3). According‎to‎the‎results‎obtained‎for‎2011,‎Enterococcus‎had‎ a‎lower‎degree‎of‎antibacterial‎sensitivity‎to‎ampicillin‎and‎ ciprofloxacin‎but‎had‎a‎higher‎degree‎of‎antibacterial‎sensi- tivity‎to‎tetracycline,‎teicoplanin,‎and‎vancomycin.‎Staphy- lococcus‎had‎a‎higher‎degree‎of‎antibacterial‎sensitivity‎to‎ Table 1. Species distribution of urine isolates from patients with urinary tract infections. Organisms 2001 (%) 2011 (%) P Escherichia coli 24.5 23.1 .475 Enterococcus 15.5 17.2 .308 Yeast 13.7 15.5 .530 Coagulase negative staphylococcus 7.2 4.2 .176 Pseudomonas 10.5 19.0 .003 Klebsiella 4.2 10.1 .04 Staphylococcus aureus 8.2 4.2 .054 Others* 16.2 6.7 .005 Totals 100.0 100.0 ----- * Enterobacter, Serratia, Stenotrophomonas, Streptococcus, Myroides, Proteus, Providencia, Morganella, Citrobacter, Acinetobacter and Alcaligenes genera. 1481Vol. 11 | No. 02 | March- April 2014 |U R O LO G Y J O U R N A L teicoplanin‎and‎vancomycin‎in‎2001‎and‎in‎2011.‎Some‎an- tibiotics‎were‎not‎considered‎for‎drug‎sensitivity‎testing‎and‎ thus‎had‎no‎available‎results.‎In‎the‎tested‎drugs,‎sensitivity‎ was‎shown‎to‎change‎with‎time‎(Table‎4). DISCUSSION The‎major‎findings‎of‎our‎study‎were‎as‎follows;‎E.‎coli‎was‎ the‎most‎common‎organism‎in‎ICU-acquired‎UTIs‎both‎in‎ 2001‎and‎2011;‎Pseudomonas,‎and‎Klebsiella‎species‎signif- icantly‎increased‎in‎2011‎compared‎to‎2001‎and‎infections‎ with‎Pseudomonas,‎the‎antibiotics‎resistance‎rates‎were‎high- er‎than‎that‎of‎other‎bacterial‎strains.‎UTI‎is‎one‎of‎the‎most‎ common‎infectious‎diseases,‎only‎second‎to‎respiratory‎infec- tions‎in‎clinical‎practice‎of‎internal‎medicine.‎Despite‎the‎rap- idly‎updated‎treatment‎modalities‎for‎UTI,‎some‎patients‎with‎ refractory‎UTIs‎and‎complicated‎UTIs‎are‎difficult‎to‎treat.(7)‎ A‎nosocomial‎UTI‎is‎one‎of‎the‎most‎common‎types‎of‎infec- tions‎and‎accounts‎for‎the‎highest‎incidence‎of‎total‎nosoco- mial‎infections.‎According‎to‎a‎survey‎that‎was‎conducted‎to‎ examine‎disease‎status‎in‎1996,‎the‎incidence‎of‎UTIs‎consti- tuted‎30.3%‎of‎total‎nosocomial‎infection‎cases.(8) Accord- ing‎to‎clinical‎guidelines‎proposed‎by‎the‎European‎Associa- tion‎of‎Urology‎(EAU)‎in‎2006,‎cases‎in‎which‎a‎UTI‎was‎ acquired‎in‎a‎hospital‎setting‎were‎established‎as‎one‎of‎the‎ indicators‎associated‎with‎complex‎UTIs(9) because patients who‎have‎been‎hospitalized‎were‎typically‎older‎in‎age‎and‎ had‎complicating‎chronic‎diseases‎such‎as‎diabetes‎mellitus‎ or‎hypertension.‎In‎addition,‎they‎had‎a‎higher‎frequency‎of‎ exposure‎to‎other‎infectious‎diseases.‎These‎characteristics‎ are‎more‎prevalently‎seen‎in‎ICU‎patients‎in‎particular.‎ Most‎cases‎of‎ICU-acquired‎UTIs‎occur‎as‎the‎result‎of‎sin- gle‎bacterial‎strain‎infections.‎Complex-type‎infections‎due‎to‎ more‎than‎two‎bacterial‎strains‎have‎been‎reported‎to‎occur‎at‎ an‎incidence‎rate‎of‎5-12%.(5,10) In the current study the inci- dence‎of‎complex-type‎infections‎was‎approximately‎18%,‎ most‎of‎ them‎were‎due‎ to‎contamination‎during‎ the‎urine‎ sampling‎ procedure.‎According‎ to‎ studies‎ about‎ infectious‎ diseases‎occurring‎in‎an‎ICU‎setting‎in‎North‎America‎and‎ Europe,‎E.‎coli,‎Pseudomonas,‎and‎Enterococcus‎are‎the‎most‎ common‎bacterial‎strains‎in‎cases‎of‎ICU‎infections.(11)‎Can- dida‎species‎have‎been‎reported‎to‎be‎present‎at‎a‎maximal‎ frequency‎of‎1/3‎of‎total‎cases‎of‎ICU‎infections.(12) In the current‎study,‎bacterial‎cultures‎showed‎an‎order‎of‎incidence‎ of‎E.‎coli‎(23.1%),‎Pseudomonas‎(19.0%)‎and‎Enterococcus‎ (17.2%)‎in‎2011.‎Yeasts‎including‎Candida‎were‎detected‎at‎ a‎rate‎of‎15.5%.‎In‎comparison‎with‎the‎results‎that‎were‎ob- tained‎in‎2001,‎E.‎coli‎showed‎no‎great‎difference.‎Enterococ- cus‎showed‎a‎detection‎rate‎of‎15.5-17.2%‎despite‎a‎lack‎of‎ statistical‎significance.‎In‎particular,‎Pseudomonas‎infections‎ greatly‎increased‎from‎10.5‎to‎19.0%‎and‎Klebsiella‎also‎in- creased‎from‎4.2‎to‎10.1%.‎These‎results‎were‎in‎agreement‎ with‎the‎latest‎Korean‎reports‎that‎identified‎the‎major‎causa- tive‎bacteria‎for‎UTIs‎in‎Korea.‎The‎incidence‎of‎infections‎ due‎to‎gram-positive‎bacteria‎was‎greatly‎increased.‎With‎re- gard‎to‎gram-negative‎bacterial‎infections,‎the‎incidence‎of‎ infections‎due‎to‎E.‎coli‎decreased,‎and‎infections‎due‎to‎other‎ gram-negative‎bacteria‎such‎as‎Pseudomonas,‎Klebsiella,‎and‎ Enterobacter‎increased.(13,14) Table 2. Antibiotic sensitivities for gram-stained pathogens in 2001 versus 2011. Variables Antibiotic Susceptibility (%) Year AC CL CZ CT GM AK TM CF LF IP BT TZ Gram (-) 2001 24.5 51.8 33.0 60.1 70.2 54.5 50.1 55.8 90.8 30.2 70.2 2011 23.4 45.5 62.0 44.0 57.2 72.0 60.1 55.2 82.1 77.5 40.1 76.1 P .982 .731 < .05 .684 .963 .741 .891 <0.05 < .05 .061 .794 Antibiotic Susceptibility (%) Year EM GM TC AC CL TP VM CF Gram (+) 2001 24.5 24.1 60.1 9.2 20.4 85.4 85.7 39.5 2011 27.1 10.2 54.2 24.1 19.1 91.1 87.9 25.5 P .891 < .05 .641 < .05 .941 .791 .912 < .05 Keys: AC = ampicillin, CL = cephalothin, CZ = ceftazidime, CT = cefotaxime, GM = gentamicin, AK = amikacin, TM = tobramycin, CF = ciprofloxacin, LF = levofloxacin, IP = imipenem, BT = bactrim, TZ = tazocin, EM = erythromycin, TC = tetracycline, TP = teicoplanin and VM = vancomycin. Bacterial Species and Antibiotic Sensitivity in ICU | Yoon et al 1482 | Miscellaneous In‎regard‎to‎antibiotic‎sensitivity,‎the‎emergence‎of‎bacterial‎ resistant‎to‎antibiotics‎has‎greatly‎increased‎since‎the‎1990s.‎ Ko‎and‎colleagues(13)‎reported‎that‎ampicillin‎had‎antibacte- rial‎sensitivity‎in‎gram-negative‎bacteria‎at‎a‎rate‎of‎15.6%‎ in‎1994‎and‎11.6%‎in‎1998.‎With‎ciprofloxacin,‎antibacterial‎ sensitivity‎has‎been‎reported‎to‎be‎87.8%‎and‎78.8%‎in‎those‎ same‎years.‎Ryu‎and‎colleagues(15)‎reported‎that‎the‎sensitiv- ity‎of‎gram-negative‎bacteria‎to‎ciprofloxacin‎decreased‎from‎ 53.9%‎in‎2000‎to‎42.6%‎in‎2005.‎In‎the‎current‎study,‎sen- sitivity‎to‎ciprofloxacin‎was‎similarly‎shown‎a‎decrease‎at‎a‎ rate‎of‎50.1%‎in‎2001‎and‎55.2%‎in‎2011.‎The‎sensitivity‎to‎ ampicillin‎and‎Bactrim‎was‎shown‎to‎be‎23.4%‎and‎40.1%,‎ respectively.‎These‎results‎indicate‎that‎ampicillin‎and‎Bac- trim‎should‎not‎be‎further‎used‎as‎the‎primary‎treatment‎for‎ ICU‎patients‎with‎UTIs.‎It‎is‎also‎assumed‎that‎special‎atten- tion‎should‎be‎paid‎to‎the‎use‎of‎quinolones.‎In‎2005,‎Ryu‎and‎ colleagues(15)‎ reported‎that‎ the‎sensitivity‎to‎penicillin‎and‎ ampicillin‎ was‎ 40%,‎ and‎ sensitivity‎ to‎ the‎ first-generation‎ cephalosporin‎was‎16%‎in‎gram-positive‎microorganisms.‎In‎ the‎current‎study,‎gram-positive‎bacterial‎sensitivity‎to‎am- picillin,‎ the‎ first-generation‎ cephalosporin,‎ quinolone,‎ and‎ erythromycin‎all‎showed‎a‎sensitivity‎rate‎of‎10-20%‎in‎2011.‎ These‎rates‎were‎overall‎lower‎than‎those‎in‎the‎report‎made‎ by Ryu and colleagues.(15)‎This‎might‎be‎because‎only‎ICU‎ patients‎were‎enrolled‎in‎the‎relevant‎studies.‎ An‎analysis‎of‎sensitivity‎was‎performed‎for‎each‎bacterial‎ strain.‎In‎2011,‎E.‎coli‎had‎sensitivity‎to‎ampicillin,‎cipro- floxacin,‎and‎the‎third-generation‎cephalosporin‎at‎a‎rate‎of‎ 32.1%,‎63.8%‎and‎76-78%,‎respectively.‎Of‎the‎aminoglyco- sides,‎amikacin‎had‎a‎higher‎degree‎of‎antibacterial‎sensitiv- ity‎as‎compared‎to‎gentamicin‎or‎tobramycin.‎However,‎anti- biotic‎sensitivity‎for‎Pseudomonas‎was‎shown‎to‎be‎30-45%.‎ It‎was‎found‎that‎Pseudomonas‎have‎antibiotic‎resistance‎ap- proximately‎two‎times‎higher‎than‎E.‎coli.‎In‎particular,‎the‎ sensitivity‎of‎E.‎coli‎or‎Klebsiella‎to‎imipenem‎and‎tazocin‎ was‎found‎to‎be‎at‎most‎40-55%.‎According‎to‎Ryu‎and‎col- leagues(15)‎the‎sensitivity‎of‎Pseudomonas‎to‎ceftazidime,‎ce- fotaxime,‎ofloxacin‎and‎imipenem‎abruptly‎increased‎in‎2005‎ as‎compared‎to‎2000.‎These‎results‎make‎it‎difficult‎to‎select‎ empirical‎antibiotics‎in‎ICU‎patients‎with‎catheterization. In‎the‎UTI‎cases‎that‎arose‎in‎the‎ICU,‎the‎most‎important‎ risk‎factor‎was‎catheterization‎of‎the‎urinary‎system.‎Richards‎ and colleagues(16)‎reported‎that‎more‎than‎95%‎of‎total‎ICU- acquired‎nosocomial‎UTI‎cases‎were‎associated‎with‎cath- eterization. Recent reports showed that catheter-associated UTI‎in‎ICU‎is‎also‎very‎common,‎only‎secondary‎to‎ventila- tor-associated‎pneumonia‎both‎in‎developing‎and‎developed‎ countries.(2,17) This‎study‎had‎several‎limitations.‎Firstly,‎the‎results‎were‎ based‎on‎a‎single‎group‎of‎patients‎from‎two‎hospitals.‎There- fore,‎the‎finding‎may‎not‎be‎representative‎of‎all‎ICU‎patients‎ in‎our‎country‎hospitals.‎The‎sample‎size‎was‎small,‎observa- tional‎nature‎of‎this‎study‎may‎also‎have‎affected‎the‎findings‎ of‎this‎study.‎The‎small‎sample‎size‎might‎also‎explain‎why‎ the‎results‎of‎our‎antibacterial‎testing‎were‎not‎in‎agreement‎ with‎previous‎reports.‎Second,‎ the‎patients‎ types,‎duration‎ of‎ICU‎stay,‎changes‎of‎devices,‎trends‎of‎Simplified‎Acute‎ Physiology‎Score‎II‎ (SAPS‎II),‎antibiotics‎usage‎duration,‎ Table 3. Antibiotic sensitivities for gram-stained pathogens in 2001 versus 2011. Variables Antibiotic Susceptibility (%) Year AC CL CZ CT GM AK TM CF LF IP BT TZ Gram (-) 2001 24.5 51.8 33.0 60.1 70.2 54.5 50.1 55.8 90.8 30.2 70.2 2011 23.4 45.5 62.0 44.0 57.2 72.0 60.1 55.2 82.1 77.5 40.1 76.1 P .982 .731 < .05 .684 .963 .741 .891 < .05 < .05 .0 .794 Antibiotic Susceptibility (%) Year EM GM TC AC CL TP VM CF Gram (+) 2001 24.5 24.1 60.1 9.2 20.4 85.4 85.7 39.5 2011 27.1 10.2 54.2 24.1 19.1 91.1 87.9 25.5 P .891 < .05 .641 < .05 .941 .791 .912 < .05 Keys: AC = ampicillin, CL = cephalothin, CZ = ceftazidime, CT = cefotaxime, GM = gentamicin, AK = amikacin, TM = tobramycin, CF = ciprofloxacin, LF = levofloxacin, IP = imipenem, BT = bactrim, TZ = tazocin, EM = erythromycin, TC = tetracycline, TP = teicoplanin and VM = vancomycin. 1483Vol. 11 | No. 02 | March- April 2014 |U R O LO G Y J O U R N A L REFERENCES 1. Edwards JR, Peterson KD, Mu Y, et al. National Healthcare Safety Network (NHSN) report: data summary for 2006 through 2008, is- sued December 2009. Am J Infect Control. 2009;37:783-805. 2. Dudeck MA, Horan TC, Peterson KD, et al. National Healthcare Safe- ty Network (NHSN) Report, data summary for 2010, device- associ- ated module. Am J Infect Control. 2011;39:798-816. 3. Moreno CA, Rosenthal VD, Olarte N, et al. Device-associated infec- tion rate and mortality in intensive care units of 9 Colombian hos- pitals: findings of the International Nosocomial Infection Control Consortium. Infect Control Hosp Epidemiol. 2006;27:349-56. 4. Rosenthal VD, Maki DG, Salomao R, et al. Device-associated nosoco- mial infections in 55 intensive care units of 8 developing countries. Ann Intern Med. 2006;145:582-91. 5. Laupland KB, Bagshaw SM, Gregson DB, Kirkpatrick AW, Ross T, Church DL. Intensive care unit-acquired urinary tract infections in a regional critical care system. Crit Care. 2005;9:R60-5. 6. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC defi- nitions for nosocomial infections, 1988. Am J Infect Control. 1988;16:128-40. 7. Di Filippo A, Casini A, de Gaudio AR. Infection prevention in the intensive care unit: review of the recent literature on the manage- ment of invasive devices. Scand J Infect Dis. 2011;43:243-50. 8. Kim JM, Park ES, Jeong JS, et al. Multicenter surveillance study for nosocomial infections in major hospitals in Korea. Nosocomial In- fection Surveillance Committee of the Korean Society for Nosoco- mial Infection Control. Am J Infect Control. 2000;28:454-8. 9. Naber K, Bishop M, Bjerklund-Johansen T, et al. EAU guidelines on the management of urinary and male genital tract infections. EAU Working Group on Urinary and Male Genital Tract Infections. In: Eu- ropean Association of Urology Guidelines, 2006 ed. Arnhem: Druk- kerij Gelderland; 2006. p. 1-126. trends‎of‎antibiotics‎consumption‎and‎etc.‎during‎10‎years‎ may‎have‎changed.‎But‎we‎overlooked‎these‎factors‎and‎this‎ can‎be‎selection‎bias‎for‎our‎result.‎Third,‎we‎think‎that‎short‎ term‎trends‎(e.g.‎3-5‎years‎investigations)‎of‎organisms‎and‎ antibiotic‎sensitivity‎would‎be‎more‎reliable‎and‎interesting.‎ Fourth,‎the‎absence‎data‎about‎extended‎spectrum‎of‎beta‎lac- tamase‎(ESBL)‎is‎another‎limitations‎of‎present‎study.‎The‎ ESBL‎is‎the‎hot‎issues‎in‎UTI‎related‎part‎from‎the‎3-5‎years‎ before.‎ Our‎ study‎ was‎ comparing‎ the‎ periods‎ of‎ 10‎ years‎ before‎(2001).‎So‎we‎could‎not‎collect‎the‎accurate‎data‎of‎ ESBL‎in‎that‎period.‎ Future‎studies‎should‎involve‎more‎ICUs‎with‎many‎institu- tions;‎treatment‎regimens‎and‎comparisons‎of‎antibiotic‎re- sistance‎patterns‎between‎ICUs‎and‎general‎wards‎and‎across‎ institutions‎should‎also‎be‎carried‎out‎to‎further‎evaluate‎pa- tients‎with‎ICU-acquired‎UTI‎in‎Korea. CONCLUSION The‎most‎common‎bacteria‎responsible‎for‎the‎occurrence‎of‎ UTIs‎in‎the‎ICU‎include‎E.‎coli,‎Pseudomonas,‎Klebsiella,‎ and‎Enterococcus.‎In‎particular,‎Pseudomonas‎and‎Klebsiella‎ infections‎were‎greatly‎increased‎in‎2011‎compared‎to‎2001.‎ In‎cases‎of‎Pseudomonas‎infection,‎the‎sensitivity‎to‎antibiot- ics‎was‎approximately‎two‎times‎lower‎than‎in‎other‎types‎ of‎gram-negative‎bacterial‎strains.‎This‎signifies‎that‎atten- tion‎should‎be‎paid‎to‎selecting‎optimal‎empirical‎antibiotics.‎ Hence,‎further‎multi-center‎studies‎are‎required‎to‎examine‎ the‎antibacterial‎sensitivity‎of‎bacteria‎causing‎UTIs‎in‎the‎ ICU‎setting. CONFLICT OF INTEREST None declared. Table 4. Antibiotic sensitivities for Gram-positive organisms in 2001 versus 2011. Variables Antibiotic Susceptibility (%) Year AC CL CZ CT GM AK TM CF LF IP BT TZ Gram (-) 2001 24.5 51.8 33.0 60.1 70.2 54.5 50.1 55.8 90.8 30.2 70.2 2011 23.4 45.5 62.0 44.0 57.2 72.0 60.1 55.2 82.1 77.5 40.1 76.1 P .982 .731 < .05 .684 .963 .741 .891 < .05 < .05 .061 .794 Antibiotic Susceptibility (%) Year EM GM TC AC CL TP VM CF Gram (+) 2001 24.5 24.1 60.1 9.2 20.4 85.4 85.7 39.5 2011 27.1 10.2 54.2 24.1 19.1 91.1 87.9 25.5 P .891 < .05 .641 < .05 .941 .791 .912 < .05 Keys: AC = ampicillin, CL = cephalothin, CZ = ceftazidime, CT = cefotaxime, GM = gentamicin, AK = amikacin, TM = tobramycin, CF = ciprofloxacin, LF = levofloxacin, IP = imipenem, BT = bactrim, TZ = tazocin, EM = erythromycin, TC = tetracycline, TP = teicoplanin and VM = vancomycin. Bacterial Species and Antibiotic Sensitivity in ICU | Yoon et al 1484 | 10. Tissot E, Limat S, Cornette C, Capellier G. Risk factors for catheter- associated bacteriuria in a medical intensive care unit. Eur J Clin Microbiol Infect Dis. 2001;20:260-2. 11. Gaynes R, Edwards JR, National Nosocomial Infections Surveillance S. Overview of nosocomial infections caused by gram-negative ba- cilli. Clin Infect Dis. 2005;41:848-54. 12. Alvarez-Lerma F, Nolla-Salas J, Leon C, et al. Candiduria in critically ill patients admitted to intensive care medical units. Intensive Care Med. 2003;29:1069-76. 13. Ko HS, Choi DY, Han YT. A Study of the Changes of Antibiotic Sensi- tivity to the Causative Organisms of Urinary Tract Infection for Re- cent 5 Years. Korean J Urol. 1999;40:809-16. 14. Ko YH, Oh JS, Cho DY, Bea JH, Koh SK. Changes of Causative Organ- isms and Antimicrobial Sensitivity of Urinary Tract Infection be- tween 1979 and 2001. Korean J Urol. 2003;44:342-50. 15. Ryu KH, Kim MK, Jeong YB. A Recent Study on the Antimicrobial Sensitivity of the Organisms that Cause Urinary Tract Infection. Ko- rean J Urol. 2007;48:638-45. 16. Richards MJ, Edwards JR, Culver DH, Gaynes RP. Nosocomial infec- tions in combined medical-surgical intensive care units in the Unit- ed States. Infect Control Hosp Epidemiol. 2000;21:510-5. 17. Tao L, Hu B, Rosenthal VD, Gao X, He L. Device-associated infection rates in 398 intensive care units in Shanghai, China: International Nosocomial Infection Control Consortium (INICC) findings. Int J In- fect Dis. 2011;15:e774-80. Miscellaneous