Skip to main content
Top
Published in: BMC Urology 1/2021

Open Access 01-12-2021 | Nitrofurantoin | Research article

Current antibiotic resistance patterns of rare uropathogens: survey from Central European Urology Department 2011–2019

Authors: Jan Hrbacek, Pavel Cermak, Roman Zachoval

Published in: BMC Urology | Issue 1/2021

Login to get access

Abstract

Background

While the resistance rates of commonly detected uropathogens are well described, those of less frequent Gram-negative uropathogenic bacteria have seldom been reported. The aim of this study was to examine the resistance rates of less frequent uropathogenic Gram-negatives in a population of patients treated in a Department of Urology of a tertiary referral centre in Central Europe over a period of 9 years.

Methods

Data on all positive urine samples from urological in- and out-patients were extracted form the Department of Clinical Microbiology database from 2011 to 2019. Numbers of susceptible and resistant isolates per year were calculated for these uropathogens: Acinetobacter spp. (n = 74), Citrobacter spp. (n = 60), Enterobacter spp. (n = 250), Morganella morganii (n = 194), Providencia spp. (n = 53), Serratia spp. (n = 82) and Stenotrophomonas maltophilia (n = 27). Antimicrobial agents selected for the survey included: ampicillin, amoxicillin/clavulanic acid, piperacillin/tazobactam; cefuroxime, cefotaxime, ceftazidime and cefepime; ciprofloxacin and ofloxacin; gentamicin and amikacin; ertapenem, meropenem and imipenem; trimethoprim-sulfamethoxazole (co-trimoxazole), nitrofurantoin and colistin.

Results

Penicillin derivatives have generally poor effect except piperacillin/tazobactam. Cefuroxime is not efficient unlike cefotaxime (except against Acinetobacter spp. and S. maltophilia). Susceptibility to fluoroquinolones is limited. Amikacin is somewhat more efficient than gentamicine but susceptibilities for both safely exceed 80%. Nitrofurantoin shows virtually no efficiency. Cotrimoxazole acts well against Citrobacter spp., Serratia spp. and it is the treatment of choice for S. maltophilia UTIs. Among carbapenems, ertapenem was less efficient than meropenem and imipenem except for S. maltophilia whose isolates were mostly not suceptible to any carbapenems.

Conclusions

Uropathogenic microorganisms covered in this report are noteworthy for their frequently multi-drug resistant phenotypes. Knowledge of resistance patterns helps clinicians choose the right empirical antibiotic treatment when the taxonomical assignment of the isolate is known but sensitivity results are pending.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gajdács M, Urbán E. Resistance trends and epidemiology of Citrobacter—Enterobacter—Serratia in urinary tract infections of inpatients and outpatients (RECESUTI): a 10-year survey. Medicina (B Aires). 2019;55(285):1–13. Gajdács M, Urbán E. Resistance trends and epidemiology of Citrobacter—Enterobacter—Serratia in urinary tract infections of inpatients and outpatients (RECESUTI): a 10-year survey. Medicina (B Aires). 2019;55(285):1–13.
3.
go back to reference Schaeffer A, Schaeffer E. Infections of the urinary tract. In: Wein A, Kavoussi L, editors. Campbell-Walsh Urology. 10th ed. 2012. p. 258–60. Schaeffer A, Schaeffer E. Infections of the urinary tract. In: Wein A, Kavoussi L, editors. Campbell-Walsh Urology. 10th ed. 2012. p. 258–60.
5.
go back to reference Vallejo-Torres L, Pujol M, Shaw E, Wiegand I, Vigo JM, Stoddart M, et al. Cost of hospitalised patients due to complicated urinary tract infections: a retrospective observational study in countries with high prevalence of multidrug-resistant Gram-negative bacteria: The COMBACTE-MAGNET, RESCUING study. BMJ Open. 2018;8(4):1–9.CrossRef Vallejo-Torres L, Pujol M, Shaw E, Wiegand I, Vigo JM, Stoddart M, et al. Cost of hospitalised patients due to complicated urinary tract infections: a retrospective observational study in countries with high prevalence of multidrug-resistant Gram-negative bacteria: The COMBACTE-MAGNET, RESCUING study. BMJ Open. 2018;8(4):1–9.CrossRef
7.
go back to reference Cullen IM, Manecksha RP, Mccullagh E, Ahmad S, Kelly FO, Flynn RJ, et al. The changing pattern of antimicrobial resistance within 42 033 Escherichia coli isolates from nosocomial, community and urology patient-specific urinary tract infections, Dublin, 1999–2009. BJUI Int. 2011;109(109):1198–206. Cullen IM, Manecksha RP, Mccullagh E, Ahmad S, Kelly FO, Flynn RJ, et al. The changing pattern of antimicrobial resistance within 42 033 Escherichia coli isolates from nosocomial, community and urology patient-specific urinary tract infections, Dublin, 1999–2009. BJUI Int. 2011;109(109):1198–206.
8.
go back to reference Iacchini S, Sabbatucci M, Gagliotti C, Rossolini GM, Moro ML, Iannazzo S, et al. Bloodstream infections due to carbapenemas eproducing Enterobacteriaceae in Italy: results from nationwide surveillance, 2014 to 2017. Eurosurveillance. 2019;24(5):66.CrossRef Iacchini S, Sabbatucci M, Gagliotti C, Rossolini GM, Moro ML, Iannazzo S, et al. Bloodstream infections due to carbapenemas eproducing Enterobacteriaceae in Italy: results from nationwide surveillance, 2014 to 2017. Eurosurveillance. 2019;24(5):66.CrossRef
9.
go back to reference Lob SH, Nicolle LE, Hoban DJ, Kazmierczak KM, Badal RE, Sahm DF. Susceptibility patterns and ESBL rates of Escherichia coli from urinary tract infections in Canada and the United States, SMART 2010–2014. Diagn Microbiol Infect Dis. 2016;85(4):459–65.CrossRef Lob SH, Nicolle LE, Hoban DJ, Kazmierczak KM, Badal RE, Sahm DF. Susceptibility patterns and ESBL rates of Escherichia coli from urinary tract infections in Canada and the United States, SMART 2010–2014. Diagn Microbiol Infect Dis. 2016;85(4):459–65.CrossRef
11.
go back to reference Sierra-Díaz E, Hernández-ríos CJ, Bravo-cuellar A. Antibiotic resistance: microbiological profile of urinary tract infections in Mexico. Circ Circ. 2019;87:176–82. Sierra-Díaz E, Hernández-ríos CJ, Bravo-cuellar A. Antibiotic resistance: microbiological profile of urinary tract infections in Mexico. Circ Circ. 2019;87:176–82.
12.
go back to reference Okeke IN, Laxminarayan R, Bhutta ZA, Duse AG, Jenkins P, Brien TFO, et al. AMR Resistance in developing countries. Lancet Infect Dis. 2005;5(August):481–93.CrossRef Okeke IN, Laxminarayan R, Bhutta ZA, Duse AG, Jenkins P, Brien TFO, et al. AMR Resistance in developing countries. Lancet Infect Dis. 2005;5(August):481–93.CrossRef
13.
go back to reference Fasugba O, Mitchell BG, Mnatzaganian G, Das A, Collignon P, Gardner A. Five-year antimicrobial resistance patterns of urinary Escherichia coli at an Australian Tertiary Hospital: time series analyses of prevalence data. PLoS ONE. 2016;11(10):1–14.CrossRef Fasugba O, Mitchell BG, Mnatzaganian G, Das A, Collignon P, Gardner A. Five-year antimicrobial resistance patterns of urinary Escherichia coli at an Australian Tertiary Hospital: time series analyses of prevalence data. PLoS ONE. 2016;11(10):1–14.CrossRef
14.
go back to reference Hyun M, Noh CI, Ryu SY, Kim HA. Changing trends in clinical characteristics and antibiotic susceptibility of Klebsiella pneumoniae bacteremia. Korean J Intern Med. 2018;33:595–603.CrossRef Hyun M, Noh CI, Ryu SY, Kim HA. Changing trends in clinical characteristics and antibiotic susceptibility of Klebsiella pneumoniae bacteremia. Korean J Intern Med. 2018;33:595–603.CrossRef
15.
go back to reference Karlowsky JA, Hoban DJ, Hackel MA, Lob SH, Sahm DF. Antimicrobial susceptibility of Gram-negative ESKAPE pathogens isolated from hospitalized patients with intra-abdominal and urinary tract infections in Asia-Pacific countries: SMART 2013–2015. J Med Microbiol. 2017;66(1):61–9.CrossRef Karlowsky JA, Hoban DJ, Hackel MA, Lob SH, Sahm DF. Antimicrobial susceptibility of Gram-negative ESKAPE pathogens isolated from hospitalized patients with intra-abdominal and urinary tract infections in Asia-Pacific countries: SMART 2013–2015. J Med Microbiol. 2017;66(1):61–9.CrossRef
16.
go back to reference Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA. 2018;115(15):E3463–70.CrossRef Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA. 2018;115(15):E3463–70.CrossRef
17.
go back to reference Stapleton PJ, Lundon DJ, McWade R, Scanlon N, Hannan MM, O’Kelly F, et al. Antibiotic resistance patterns of Escherichia coli urinary isolates and comparison with antibiotic consumption data over 10 years, 2005–2014. Ir J Med Sci. 2017;186(3):733–41.CrossRef Stapleton PJ, Lundon DJ, McWade R, Scanlon N, Hannan MM, O’Kelly F, et al. Antibiotic resistance patterns of Escherichia coli urinary isolates and comparison with antibiotic consumption data over 10 years, 2005–2014. Ir J Med Sci. 2017;186(3):733–41.CrossRef
19.
go back to reference Fleming-Dutra K, Hersh AL, Shapiro DJ. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010–2011. JAMA. 2016;315(17):1865–73.CrossRef Fleming-Dutra K, Hersh AL, Shapiro DJ. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010–2011. JAMA. 2016;315(17):1865–73.CrossRef
20.
go back to reference Chardavoyne PC, Kasmire KE. Appropriateness of Antibiotic Prescriptions for urinary tract infections. West J Emerg Med. 2020;21(3):633–9.CrossRef Chardavoyne PC, Kasmire KE. Appropriateness of Antibiotic Prescriptions for urinary tract infections. West J Emerg Med. 2020;21(3):633–9.CrossRef
21.
go back to reference Harris PNA, Wei JY, Shen AW, Abdile AA, Paynter S, Huxley RR, et al. Carbapenems versus alternative antibiotics for the treatment of bloodstream infections caused by Enterobacter, Citrobacter or Serratia species: a systematic review with meta-analysis. J Antimicrob Chemother. 2016;71(2):296–306.CrossRef Harris PNA, Wei JY, Shen AW, Abdile AA, Paynter S, Huxley RR, et al. Carbapenems versus alternative antibiotics for the treatment of bloodstream infections caused by Enterobacter, Citrobacter or Serratia species: a systematic review with meta-analysis. J Antimicrob Chemother. 2016;71(2):296–306.CrossRef
23.
go back to reference Bergogne-Bérézin E, Towner KJ. Acinetobacter spp as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clin Microbiol Rev. 1996;9(2):148–65.CrossRef Bergogne-Bérézin E, Towner KJ. Acinetobacter spp as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clin Microbiol Rev. 1996;9(2):148–65.CrossRef
24.
go back to reference Brooke JS. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev. 2012;25(1):2–41.CrossRef Brooke JS. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev. 2012;25(1):2–41.CrossRef
25.
go back to reference Hrbacek J, Cermak P, Zachoval R. Current antibiotic resistance trends of uropathogens in central europe: survey from a tertiary hospital urology department 2011–2019. Antibiotics. 2020;9(9):1–11.CrossRef Hrbacek J, Cermak P, Zachoval R. Current antibiotic resistance trends of uropathogens in central europe: survey from a tertiary hospital urology department 2011–2019. Antibiotics. 2020;9(9):1–11.CrossRef
26.
go back to reference Gajdács M, Urbán E. Comparative epidemiology and resistance trends of proteae in urinary tract infections of inpatients and outpatients: a 10-year retrospective study. Antibiotics. 2019;8(91):1–13. Gajdács M, Urbán E. Comparative epidemiology and resistance trends of proteae in urinary tract infections of inpatients and outpatients: a 10-year retrospective study. Antibiotics. 2019;8(91):1–13.
27.
go back to reference Fajfr M, Louda M, Paterová P, Ryšková L, Pacovský J, Košina J, et al. The susceptibility to fosfomycin of Gram-negative bacteria isolates from urinary tract infection in the Czech Republic: data from a unicentric study. BMC Urol. 2017;17(1):1–6.CrossRef Fajfr M, Louda M, Paterová P, Ryšková L, Pacovský J, Košina J, et al. The susceptibility to fosfomycin of Gram-negative bacteria isolates from urinary tract infection in the Czech Republic: data from a unicentric study. BMC Urol. 2017;17(1):1–6.CrossRef
28.
go back to reference Jiménez-Guerra G, Borrego-Jiménez J, Gutiérrez-Soto B, Expósito-Ruiz M, Navarro-Marí JM, Gutiérrez-F, et al. Evolución de la sensibilidad a los antibióticos de Enterobacter cloacae, Morganella morganii, Klebsiella aerogenes y Citrobacter freundii causantes de infecciones del tracto urinario: un estudio de vigilancia epidemiológica de 11 años. Enferm Infecc Microbiol Clin. 2019. https://doi.org/10.1016/j.eimc.2019.07.010. Jiménez-Guerra G, Borrego-Jiménez J, Gutiérrez-Soto B, Expósito-Ruiz M, Navarro-Marí JM, Gutiérrez-F, et al. Evolución de la sensibilidad a los antibióticos de Enterobacter cloacae, Morganella morganii, Klebsiella aerogenes y Citrobacter freundii causantes de infecciones del tracto urinario: un estudio de vigilancia epidemiológica de 11 años. Enferm Infecc Microbiol Clin. 2019. https://​doi.​org/​10.​1016/​j.​eimc.​2019.​07.​010.
29.
go back to reference Jiménez-Guerra G, Heras-Cañas V, Gutiérrez-Soto M, Aznarte-Padial M del P, Expósito-Ruiz M, Navarro-Marí JM, et al. Urinary tract infection by acinetobacter baumannii and pseudomonas aeruginosa: evolution of antimicrobial resistance and therapeutic alternatives. J Med Microbiol. 2018;67(6):790–7. Jiménez-Guerra G, Heras-Cañas V, Gutiérrez-Soto M, Aznarte-Padial M del P, Expósito-Ruiz M, Navarro-Marí JM, et al. Urinary tract infection by acinetobacter baumannii and pseudomonas aeruginosa: evolution of antimicrobial resistance and therapeutic alternatives. J Med Microbiol. 2018;67(6):790–7.
30.
go back to reference de Lemos MC, de Paixao EF, de Souza Santos MAR. Stenotrophomonas maltophilia isolates in a tertiary care hospital in Northeastern Brazil. Braz J Hea Rev. 2019;2(4):3373–84.CrossRef de Lemos MC, de Paixao EF, de Souza Santos MAR. Stenotrophomonas maltophilia isolates in a tertiary care hospital in Northeastern Brazil. Braz J Hea Rev. 2019;2(4):3373–84.CrossRef
31.
go back to reference Nyc O, Matejková J. Stenotrophomonas maltophilia: significant contemporary hospital pathogen—review. Folia Microbiol Praha. 2010;55(3):286–94.CrossRef Nyc O, Matejková J. Stenotrophomonas maltophilia: significant contemporary hospital pathogen—review. Folia Microbiol Praha. 2010;55(3):286–94.CrossRef
32.
go back to reference Munoz-Price S, Weinstein RA. Acinetobacter infection. N Engl J Med. 2008;358(12):1271–81.CrossRef Munoz-Price S, Weinstein RA. Acinetobacter infection. N Engl J Med. 2008;358(12):1271–81.CrossRef
33.
go back to reference Moy S, Sharma R. Treatment outcomes in infections caused by “SPICE” (Serratia, Pseudomonas, Indole-positive Proteus, Citrobacter, and Enterobacter) organisms: Carbapenem versus Noncarbapenem Regimens. Clin Ther. 2017;39(1):170–6.CrossRef Moy S, Sharma R. Treatment outcomes in infections caused by “SPICE” (Serratia, Pseudomonas, Indole-positive Proteus, Citrobacter, and Enterobacter) organisms: Carbapenem versus Noncarbapenem Regimens. Clin Ther. 2017;39(1):170–6.CrossRef
34.
go back to reference Chassin-Trubert CA-M. Síndrome de la bolsa de orina púrpura: un fenómeno inusual y muy llamativo. Rev Med Chile. 2014;142:1482–4.CrossRef Chassin-Trubert CA-M. Síndrome de la bolsa de orina púrpura: un fenómeno inusual y muy llamativo. Rev Med Chile. 2014;142:1482–4.CrossRef
35.
go back to reference Davin-Regli A, Pagès J. Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Front Microbiol. 2015;6:392.CrossRef Davin-Regli A, Pagès J. Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Front Microbiol. 2015;6:392.CrossRef
36.
go back to reference Chang C-L, Su L-H, Lu C-M, Tai F-T, Huang Y-C, Chang K-K. Outbreak of ertapenem-resistant Enterobacter cloacae urinary tract infections due to a contaminated ureteroscope. J Hosp Infect. 2013;85(2):118–24.CrossRef Chang C-L, Su L-H, Lu C-M, Tai F-T, Huang Y-C, Chang K-K. Outbreak of ertapenem-resistant Enterobacter cloacae urinary tract infections due to a contaminated ureteroscope. J Hosp Infect. 2013;85(2):118–24.CrossRef
37.
go back to reference Mahlen SD. Serratia infections: from military experiments to current practice. Clin Microbiol Rev. 2011;24(4):755–91.CrossRef Mahlen SD. Serratia infections: from military experiments to current practice. Clin Microbiol Rev. 2011;24(4):755–91.CrossRef
38.
go back to reference Su L, Ou JT, Leu H, Chiang P, Chiu Y, Chia J, et al. Extended epidemic of nosocomial urinary tract infections caused by Serratia marcescens. J Clin Microbiol. 2003;41(10):4726–32.CrossRef Su L, Ou JT, Leu H, Chiang P, Chiu Y, Chia J, et al. Extended epidemic of nosocomial urinary tract infections caused by Serratia marcescens. J Clin Microbiol. 2003;41(10):4726–32.CrossRef
39.
go back to reference O'Hara CM, Brenner FW, Miller JM. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev. 2000;13(4):534–46. O'Hara CM, Brenner FW, Miller JM. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev. 2000;13(4):534–46.
40.
go back to reference Choi HK, Kim YK, Kim HY, Park JE, Uh Y. Clinical and microbiological features of Providencia bacteremia: experience at a tertiary care hospital. Korean J Intern Med. 2015;30:219–25.CrossRef Choi HK, Kim YK, Kim HY, Park JE, Uh Y. Clinical and microbiological features of Providencia bacteremia: experience at a tertiary care hospital. Korean J Intern Med. 2015;30:219–25.CrossRef
Metadata
Title
Current antibiotic resistance patterns of rare uropathogens: survey from Central European Urology Department 2011–2019
Authors
Jan Hrbacek
Pavel Cermak
Roman Zachoval
Publication date
01-12-2021

Other articles of this Issue 1/2021

BMC Urology 1/2021 Go to the issue