Trends of antimicrobial resistance in patients with complicated urinary tract infection: Suggested empirical therapy and lessons learned from a retrospective observational study in Oman

Background: Complicated urinary tract infection (cUTI) is defined as an infection associated with structural, functional, or metabolic abnormalities of the genitourinary tract. These infections are caused frequently by multidrug-resistant Gram-negative bacilli. The rapid emergence of extended-spectrum beta-lactamase (ESBL), AmpC, and carbapenemase (CR) producers has made the treatment of such infections increasingly more challenging. Objectives: The aims of the present study were threefold: to assess the clinical profile, trends in etiology, and antimicrobial susceptibility profile in cUTI over the past 10 years at a tertiary care center in Oman as an interrupted time series on the one hand and to develop guidelines for empirical management of such cases on the other. Materials and Methods: We conducted a retrospective analysis of cUTI in patients presenting at Sultan Qaboos University Hospital over 3 years (2008, 2013, and 2018) covering a span of 10 years. Data were obtained from the patient's electronic records in the hospital information system. Analysis was done using the Statistical Package for Social Sciences program (SPSS), version 23. Results: Among the 650 cases of cUTI, 284 (44%) were males and 366 (56%) were females, with dysuria being the most common symptom (34%). The biggest risk factor for developing cUTI was diabetes (35%). The predominant pathogen was Escherichia coli (53%), followed by Klebsiella spp. (16%), Enterococcus faecalis (7%), Pseudomonas aeruginosa (7%), Candida spp. (2%), and Enterobacter cloacae (2%). Over the years, E. coli emerged as the predominant ESBL and AmpC producer, Acinetobacter baumannii as the multidrug-resistant bug, and Klebsiella pneumoniae as the major carbapenem-resistant Enterobacterales (CRE) producer. Nitrofurantoin emerged as the most effective drug for cystitis. Aminoglycosides, piperacillin-tazobactam, and carbapenems demonstrated the highest activity with an overall resistance of less than 10%. Higher resistance (30%) was observed against cephalosporins, fluoroquinolones, and trimethoprim/sulfamethoxazole. Analysis of the 10-year trend threw up some unexpected results. As expected, resistance increased from 2008 to 2013. Surprisingly, however, antimicrobial resistance in 2018 was lower against majority of the antimicrobials compared to 2013. Conclusion: There is a paucity of data for developing evidence-based guidelines management of cUTI. Targeted antibiograms and not cumulative antibiograms are essential for promoting appropriate prescribing and optimizing patient care. The welcome decline in resistance may be attributed cascade reporting, introduction of more ID physicians. Another possibility is increased utilization of fluoroquinolones which spared the other groups of antimicrobials. Judicious heterogeneous mixing of antimicrobials should be spearheaded in both cystitis and pyelonephritis so that there is no undue pressure on one drug. We strongly recommend carbapenem-sparing protocols in treatment of cUTI when anticipating augmented resistance due to AmpC production. Synergistic combinations such as piperacillin-tazobactam plus aminoglycosides/fluoroquinolones may be prescribed. In sepsis, however, carbapenems are the drugs of choice.

[1]  A. Gjelsvik,et al.  A Population-Based Assessment , 2022 .

[2]  R. Mkakosya,et al.  Carriage Prevalence of Extended-Spectrum β-Lactamase Producing Enterobacterales in Outpatients Attending Community Health Centers in Blantyre, Malawi , 2021, Tropical medicine and infectious disease.

[3]  H. Chambers,et al.  Trends in prevalence of extended-spectrum beta-lactamase-producing Escherichia coli isolated from patients with community- and healthcare-associated bacteriuria: results from 2014 to 2020 in an urban safety-net healthcare system , 2021, Antimicrobial resistance and infection control.

[4]  M. Rehman,et al.  Prevalence and antibiotic susceptibility pattern of uropathogens in outpatients at a tertiary care hospital , 2020, New microbes and new infections.

[5]  H. Mukae,et al.  Induction of plasmid-mediated AmpC β-lactamase DHA-1 by piperacillin/tazobactam and other β-lactams in Enterobacteriaceae , 2019, PloS one.

[6]  M. J. Cilleruelo Ortega,et al.  [Recommendations on the diagnosis and treatment of urinary tract infection]. , 2019, Anales de pediatria.

[7]  Jieun Kim,et al.  Clinical Practice Guidelines for the Antibiotic Treatment of Community-Acquired Urinary Tract Infections , 2018, Infection & chemotherapy.

[8]  G. Cornaglia,et al.  Multi-drug-resistant Gram-negative bacteria causing urinary tract infections: a review , 2017, Journal of chemotherapy.

[9]  Hao Ye,et al.  A 6-year study of complicated urinary tract infections in southern China: prevalence, antibiotic resistance, clinical and economic outcomes , 2017, Therapeutics and clinical risk management.

[10]  I. Beyer,et al.  Management of urinary tract infections in the elderly , 2001, Zeitschrift für Gerontologie und Geriatrie.

[11]  S. Hultgren,et al.  Urinary tract infections: epidemiology, mechanisms of infection and treatment options , 2015, Nature Reviews Microbiology.

[12]  R. Lynfield,et al.  Multistate point-prevalence survey of health care-associated infections. , 2014, The New England journal of medicine.

[13]  S. Calderwood,et al.  Catheter-associated urinary tract infection in adults , 2014 .

[14]  A. Shorr,et al.  Secular Trends in Gram-Negative Resistance among Urinary Tract Infection Hospitalizations in the United States, 2000–2009 , 2013, Infection Control & Hospital Epidemiology.

[15]  Jun Lin,et al.  Beta-lactamase induction and cell wall metabolism in Gram-negative bacteria , 2013, Front. Microbiol..

[16]  H. Goossens,et al.  The European Centre for Disease Prevention and Control (ECDC) pilot point prevalence survey of healthcare-associated infections and antimicrobial use. , 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[17]  S. Jaju,et al.  Health Survey : Part 1-Methodology , Sociodemographic Profile and Epidemiology of Non-Communicable Diseases in Oman , 2012 .

[18]  Sanjay Saint,et al.  Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. , 2010, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[19]  T. Cai,et al.  Guidelines on Urological Infections , 2009 .

[20]  D. Church,et al.  Community-onset Urinary Tract Infections: A Population-based Assessment , 2007, Infection.

[21]  L. Nicolle,et al.  Complicated urinary tract infection in adults. , 2005, The Canadian journal of infectious diseases & medical microbiology = Journal canadien des maladies infectieuses et de la microbiologie medicale.

[22]  J. Dieleman,et al.  Incidence and prevalence of lower urinary tract symptoms suggestive of benign prostatic hyperplasia in primary care--the Triumph project. , 2002, European urology.

[23]  W. Stamm,et al.  Antimicrobial resistance among uropathogens that cause community-acquired urinary tract infections in women: a nationwide analysis. , 2001, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[24]  W. Stamm,et al.  Urinary tract infections: disease panorama and challenges. , 2001, The Journal of infectious diseases.

[25]  M. Ferraro Performance standards for antimicrobial susceptibility testing , 2001 .

[26]  D. Scholes,et al.  Increasing prevalence of antimicrobial resistance among uropathogens causing acute uncomplicated cystitis in women. , 1999, JAMA.

[27]  A. Schaeffer,et al.  Evaluation of and antimicrobial therapy for recurrent urinary tract infections in women. , 1998, The Urologic clinics of North America.

[28]  M. Schumacher,et al.  Prevalence of nosocomial infections in representative German hospitals. , 1998, The Journal of hospital infection.

[29]  J. Bartlett,et al.  Evaluation of new anti-infective drugs for the treatment of intraabdominal infections. Infectious Diseases Society of America and the Food and Drug Administration. , 1992, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[30]  C. Keane,et al.  Circumcision and periurethral carriage of Proteus mirabilis in boys. , 1988, Archives of disease in childhood.

[31]  Z. Haider,et al.  Urinary tract infection in diabetics. , 1980, JPMA. The Journal of the Pakistan Medical Association.

[32]  W. Fair,et al.  Prostatic antibacterial factor. Identity and significance. , 1976, Urology.