The profile of bacteria isolated from urine culture of adults with urinary tract infection in Yogyakarta 2007-2022
Abstract
Local data regarding antimicrobial susceptibility patterns of bacteria from urine culture is limited in Indonesia, particularly in Yogyakarta. This study was conducted to provide epidemiology data of bacteria and their resistance profile, including the profile of bacteria that producing extended-spectrum beta-lactamase (ESBL) and carbapenemase in the urine of patients with urinary tract infection (UTI) in Yogyakarta. A descriptive retrospective study was conducted by assessing laboratory records of urine culture from adult patients at the Microbiology Laboratory, Department of Microbiology, Faculty of Medicine, Public Health, and Nursing, Universitas Gadjah Mada, Yogyakarta between 2007 and 2022. Of the 842 urine cultures, 464 (55.11%) isolates were recovered. Among thisolates, 50 (10.78%) were fungi, 67 (14.44%) were Gram-positive bacteria, and 347 (74.78%) were Gram-negative bacteria. Enterococcus sp. (41 (61.19%)) was the most bacteria found in the Gram-positive bacteria group, while Escherichia coli (38.90%) were the most bacteria found in the Gram-negative bacteria group. This study also identified Gram-negative bacteria producing ESBL enzymes (58.70%) and carbapenemases (27.94%). Gram-negative bacteria are the most common bacteria found in urine cultures of adult UTI patients in Yogyakarta, and the resistance profile of these bacteria is concerning.
References
Babich T, Eliakim-Raz N, Turjeman A, Pujol M, Carratala J, Shaw E, et al. Risk factors for hospital readmission following complicated urinary tract infection. Sci Rep 2021; 11(1):6926.
https://doi.org/10.1038/s41598-021-86246-7
Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015; 13(5):269-84.
https://doi.org/10.1038/nrmicro3432
Zalmanovich A, Katzir M, Chowers M, Matar A, Rodrig J, Alon D. Improving urinary tract infection treatment through a multifaceted antimicrobial stewardship intervention in the emergency department. Am J Emerg Med 2021; 49:10-3.
https://doi.org/10.1016/j.ajem.2021.05.037
Zhang H, Liang B, Wang J, Cai Y. Non-carbapenem beta-lactam/beta-lactamase inhibitors versus carbapenems for urinary tract infections caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae: a systematic review. Int J Antimicrob Agents 2021; 58(4):106410.
https://doi.org/10.1016/j.ijantimicag.2021.106410
Kang SW, Park S, Kim A, Han J, Lee J, Seo H, et al. Clinical characteristics of and risk factors for subsequent carbapenemase-producing enterobacterales (CPE) bacteremia in rectal CPE carriers. Int J Antimicrob Agents 2023; 62(5):106959.
https://doi.org/10.1016/j.ijantimicag.2023.106959
Goebel MC, Trautner BW, Grigoryan L. The five Ds of outpatient antibiotic stewardship for urinary tract infections. Clin Microbiol Rev 2021; 34(4):e0000320.
https://doi.org/10.1128/CMR.00003-20.
Lee ALH, Leung ECM, Lee MKP, Lai RWM. Diagnostic stewardship programme for urine culture: impact on antimicrobial prescription in a multi-centre cohort. J Hosp Infect 2021; 108:81-9.
https://doi.org/10.1016/j.jhin.2020.10.027.
Ginting F, Sugianli AK, Kusumawati RL, Parwati I, de Jong MD, Schultsz C, et al. Predictive value of the urinary dipstick test in the management of patients with urinary tract infection-associated symptoms in primary care in Indonesia: a cross-sectional study. BMJ Open 2018; 8(8):e023051.
https://10.1136/bmjopen-2018-023051
Bazaid AS, Saeed A, Alrashidi A, Alrashidi A, Alshaghdali K, Hammam SA, et al. Antimicrobial surveillance for bacterial uropathogens in Ha'il, Saudi Arabia: A five-year multicenter retrospective study. Infect Drug Resist 2021; 14:1455-65.
https://doi.org/10.2147/IDR.S299846
Lewis JS, Weinstein MP, Bobenchik AM, Campeau S, Cullen SK, Dingle T, et al. CLSI performance standards for antimicrobial susceptibility testing M100. USA: The Clinical and Laboratory Standards Institute 2023. 30th ed.
(EUCAST) ECoAST. EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. EUCAST. 2017; 1-43.
Sugianli AK, Ginting F, Kusumawati RL, Parwati I, de Jong MD, van Leth F, et al. Laboratory-based versus population-based surveillance of antimicrobial resistance to inform empirical treatment for suspected urinary tract infection in Indonesia. PLoS One 2020; 15(3):e0230489.
https://doi.org/10.1371/journal.pone.0230489
Quan J, Dai H, Liao W, Zhao D, Shi Q, Zhang L, et al. Etiology and prevalence of ESBLs in adult community-onset urinary tract infections in East China: A prospective multicenter study. J Infect 2021; 83(2):175-81.
https://doi.org/10.1016/j.jinf.2021.06.004
Rosana Y, Ocviyanti D, Halim M, Harlinda FY, Amran R, Akbar W, et al. Urinary tract infections among Indonesian pregnant women and its susceptibility pattern. Infect Dis Obstet Gynecol 2020; 2020:9681632.
https://doi.org/10.1155/2020/9681632
Norafika, Arbianti N, Prihatiningsih S, Indriani DW, Indriati DW. A retrospective cross-sectional study of urinary tract infections and prevalence of antibiotic resistant pathogens in patients with diabetes mellitus from a public hospital in Surabaya, Indonesia. Germs 2020; 10(4):157-66.
https://doi.org/10.18683/germs.2020.1201
Dufke S, Kunze-Kronawitter H, Schubert S. Pyelonephritis and urosepsis caused by Streptococcus pneumoniae. J Clin Microbiol 2004; 42(9):4383-5.
https://doi.org/10.1128/JCM.42.9.4383-4385.2004
Burckhardt I, Panitz J, van der Linden M, Zimmermann S. Streptococcus pneumoniae as an agent of urinary tract infections - a laboratory experience from 2010 to 2014 and further characterization of strains. Diagn Microbiol Infect Dis 2016; 86(1):97-101.
https://doi.org/10.1016/j.diagmicrobio.2016.06.009
Pougnet R, Sapin J, De Parscau L, Pougnet L. Streptococcus pneumoniae urinary tract infection in pedeatrics. Ann Biol Clin (Paris) 2017; 75(3):348-50.
https://doi.org/10.1684/abc.2017.1241
Kubone PZ, Mlisana KP, Govinden U, Abia ALK, Essack SY. Antibiotic susceptibility and molecular characterization of uropathogenic Escherichia coli associated with community-acquired urinary tract infections in urban and rural settings in South Africa. Trop Med Infect Dis 2020; 5(4):176.
https://doi.org/10.3390/tropicalmed5040176
Ohnishi T, Mishima Y, Naito T, Matsuda N, Ariji S, Umino D, et al. Clinical features and treatment strategies of febrile urinary tract infection caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae in children: A multicenter retrospective observational study in Japan. Int J Infect Dis 2022; 125:97-102.
https://doi.org/10.1016/j.ijid.2022.09.033
Azami M, Jaafari Z, Masoumi M, Shohani M, Badfar G, Mahmudi L, et al. The etiology and prevalence of urinary tract infection and asymptomatic bacteriuria in pregnant women in Iran: a systematic review and meta-analysis. BMC Urol 2019; 19(1):43.
https://doi.org/10.1186/s12894-019-0454-8
Drekonja DM, Trautner B, Amundson C, Kuskowski M, Johnson JR. Effect of 7 vs 14 days of antibiotic therapy on resolution of symptoms among afebrile men with urinary tract infection: A randomized clinical trial. JAMA 2021; 326(4):324-31.
https://doi.org/10.1001/jama.2021.9899
Rawat D, Nair D. Extended-spectrum beta-lactamases in Gram-negative bacteria. J Glob Infect Dis 2010; 2(3):263-74.
https://10.4103/0974-777X.68531
Ghafourian S, Sadeghifard N, Soheili S, Sekawi Z. Extended spectrum beta-lactamases: definition, classification and epidemiology. Curr Issues Mol Biol 2015; 17:11-21.
Karlowsky JA, Lob SH, DeRyke CA, Siddiqui F, Young K, Motyl MR, et al. Prevalence of ESBL non-CRE Escherichia coli and Klebsiella pneumoniae among clinical isolates collected by the SMART global surveillance programme from 2015 to 2019. Int J Antimicrob Agents 2022; 59(3):106535.
https://doi.org/10.1016/j.ijantimicag.2022.106535
Apostolakos I, Mughini-Gras L, Fasolato L, Piccirillo A. Impact of selective and non-selective media on prevalence and genetic makeup of ESBL/pAmpC-producing Escherichia coli in the broiler production pyramid. Vet Microbiol 2020; 240:108536.
https://doi.org/10.1016/j.vetmic.2019.108536
Al-Jamei SA, Albsoul AY, Bakri FG, Al-Bakri AG. Extended-spectrum beta-lactamase producing Escherichia coli in urinary tract infections: A two-center, cross-sectional study of prevalence, genotypes and risk factors in Amman, Jordan. J Infect Public Health 2019; 12(1):21-5.
https://doi.org/10.1016/j.jiph.2018.07.011.
Tufa TB, Fuchs A, Tufa TB, Stotter L, Kaasch AJ, Feldt T, et al. High rate of extended-spectrum beta-lactamase-producing Gram-negative infections and associated mortality in Ethiopia: a systematic review and meta-analysis. Antimicrob Resist Infect Control 2020; 9(1):128.
https://doi.org/10.1186/s13756-020-00782-x.
Wijaya C, Eriata AH, Rustawan INT, Candra IKBA, Budayanti NNS. Prevalence of uropathogen producing extended spectrum beta lactamase (ESBL) at urinary tract infection in chronic kidney disease patient. J Clin Microbiol Infect Dis (JCMID) 2023; 3(1):12-5.
https://doi.org/10.51559/jcmid.v3i1.29
Anggi A, Wijaya DW, Ramayani OR. Risk Factors for Catheter-associated urinary tract infection and uropathogen bacterial profile in the Intensive Care Unit in Hospitals in Medan, Indonesia. Open Access Maced J Med Sci 2019; 7(20):3488-92.
https://doi.org/10.3889/oamjms.2019.684
Hosu MC, Vasaikar SD, Okuthe GE, Apalata T. Detection of extended spectrum beta-lactamase genes in Pseudomonas aeruginosa isolated from patients in rural Eastern Cape Province, South Africa. Sci Rep 2021; 11(1):7110.
https://doi.org/10.1038/s41598-021-86570-y
Wagenlehner FME, Bjerklund Johansen TE, Cai T, Koves B, Kranz J, Pilatz A, et al. Epidemiology, definition and treatment of complicated urinary tract infections. Nat Rev Urol 2020; 17(10):586-600.
https://doi.org/10.1038/s41585-020-0362-4
Aurilio C, Sansone P, Barbarisi M, Pota V, Giaccari LG, Coppolino F, et al. Mechanisms of action of carbapenem resistance. Antibiotics (Basel) 2022; 11(3):421.
https://doi.org/10.3390/antibiotics11030421
Hansen GT. Continuous evolution: perspective on the epidemiology of carbapenemase resistance among enterobacterales and other Gram-negative bacteria. Infect Dis Ther 2021; 10(1):75-92.
https://doi.org/10.1007/s40121-020-00395-2
Chen Y, Marimuthu K, Teo J, Venkatachalam I, Cherng BPZ, De Wang L, et al. Acquisition of plasmid with carbapenem-resistance gene bla(KPC2) in hypervirulent Klebsiella pneumoniae, Singapore. Emerg Infect Dis 2020; 26(3):549-59.
https://doi.org/10.3201/eid2603.191230
Chen L, Mathema B, Chavda KD, DeLeo FR, Bonomo RA, Kreiswirth BN. Carbapenemase-producing Klebsiella pneumoniae: molecular and genetic decoding. Trends Microbiol 2014; 22(12):686-96.
https://doi.org/10.1016/j.tim.2014.09.003
Nordmann P, Poirel L. Epidemiology and diagnostics of carbapenem resistance in Gram-negative bacteria. Clin Infect Dis 2019; 69(Suppl 7):S521-S8.
https://doi.org/10.1093/cid/ciz824
Gomides MDA, Fontes AMS, Silveira A, Matoso DC, Ferreira AL, Sadoyama G. The importance of active surveillance of carbapenem-resistant Enterobacterales (CRE) in colonization rates in critically ill patients. PLoS One 2022; 17(1):e0262554.
https://doi.org/10.1371/journal.pone.0262554
Kelly AM, Mathema B, Larson EL. Carbapenem-resistant enterobacteriaceae in the community: A scoping review. Int J Antimicrob Agents 2017; 50(2):127-34.
https://doi.org/10.1016/j.ijantimicag.2017.03.012
Karlowsky JA, Wise MG, Hsieh TC, Lu HC, Chen WT, Cheng MH, et al. Temporal and geographical prevalence of carbapenem-resistant Pseudomonas aeruginosa and the in vitro activity of ceftolozane/tazobactam and comparators in Taiwan-SMART 2012-2021. J Glob Antimicrob Resist 2023; 34:106-12.
https://doi.org/10.1016/j.jgar.2023.06.013
Perez F, Villegas MV. The role of surveillance systems in confronting the global crisis of antibiotic-resistant bacteria. Curr Opin Infect Dis 2015; 28(4):375-83.
https://doi.org/10.1097/QCO.0000000000000182
Iskandar K, Molinier L, Hallit S, Sartelli M, Hardcastle TC, Haque M, et al. Surveillance of antimicrobial resistance in low- and middle-income countries: A scattered picture. Antimicrob Resist Infect Control 2021; 10(1):63.
https://doi.org/10.1186/s13756-021-00931-w
Khatri D, Freeman C, Falconer N, de Camargo Catapan S, Gray LC, Paterson DL. Clinical impact of antibiograms as an intervention to optimize antimicrobial prescribing and patient outcomes: A systematic review. Am J Infect Control 2024; 52(1):107-22.