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Overtreatment of asymptomatic bacteriuria: a qualitative study
Accepted Manuscript Overtreatment of asymptomatic bacteriuria: a qualitative study M.M. Eyer, M. Läng, D. Aujesky, J. Marschall PII:
S0195-6701(16)30044-5
DOI:
10.1016/j.jhin.2016.04.007
Reference:
YJHIN 4800
To appear in:
Journal of Hospital Infection
Received Date: 31 March 2016 Accepted Date: 8 April 2016
Please cite this article as: Eyer MM, Läng M, Aujesky D, Marschall J, Overtreatment of asymptomatic bacteriuria: a qualitative study, Journal of Hospital Infection (2016), doi: 10.1016/j.jhin.2016.04.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Overtreatment of Asymptomatic Bacteriuria: A Qualitative Study
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Myriam M. Eyer1,2, Matthias Läng1, Drahomir Aujesky3, Jonas Marschall1
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Department of Infectious Diseases, Bern University Hospital, Bern, Switzerland
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Division of Infectious Diseases, Valais Hospital, Sion, Switzerland
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Division of General Internal Medicine, Bern University Hospital, Bern, Switzerland
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Keywords: Asymptomatic bacteriuria; overtreatment; urinary tract infection; qualitative
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research
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Running title: Overtreatment of Asymptomatic Bacteriuria
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Authors
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Myriam M. Eyer
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Department of Infectious Diseases, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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and
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Division of Infectious Diseases, Valais Hospital
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Av. du Grand-Champsec 86, CH-1951 Sion
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Phone +41 27 603 4863
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[email protected]
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Matthias Läng
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Department of Infectious Diseases, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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Phone +41 33 826 22 07
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[email protected] 1
Drahomir Aujesky
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Division of General Internal Medicine, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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Phone +41 31 632 88 84
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[email protected]
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Jonas Marschall
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Department of Infectious Diseases, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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Phone +41 31 632 27 45
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[email protected]
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Corresponding author and reprint requests to:
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Myriam M. Eyer, MD
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Division of Infectious Diseases, Valais Hospital
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Av. du Grand-Champsec 86, CH-1951 Sion
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Phone +41 27 603 4863
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Mobile telephone number +41 79 750 4814
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Fax +41 27 603 4789
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[email protected]
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Word count: Text: 3953 Tables: 1
Summary: 229
References: 29
Appendix: 1
Figures: 0
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ACCEPTED MANUSCRIPT SUMMARY
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Background: Overtreatment of asymptomatic bacteriuria (ASB) is common and can result in
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antibiotic side effects, excess costs to the healthcare system, and potentially trigger
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antimicrobial resistance. According to international management guidelines, ASB is not an
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indication for antibiotic treatment (with few exceptions).
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Aim: To determine reasons for using antibiotics to treat ASB in the absence of a treatment
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indication.
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Methods: We conducted a qualitative study at a tertiary care hospital in Switzerland during
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2011. We interviewed 21 internal medicine residents and attending physicians selected by
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purposive sampling, using a semi-structured questionnaire. Responses were analysed in an
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inductive thematic content approach using dedicated software (MAXQDA®).
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Findings: In the 21 interviews, the following thematic rationales for antibiotic overtreatment
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of ASB were reported (in order of reporting frequency): 1) Treating laboratory findings
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without taking the clinical picture into account (n=17); 2) Psychological factors such as
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anxiousness, overcautiousness or anticipated positive impact on patient outcomes (n=13); 3)
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External pressors such as institutional culture, peer pressure, patient expectation, and
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excessive workload that interferes with proper decision-making (n=9); 4) Difficulty with
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interpreting clinical signs and symptoms (n=8).
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Conclusions: In this qualitative study we identified both physician-centred factors (e.g.,
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overcautiousness) and external pressors (e.g., excessive workload) as motivators for
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prescribing unnecessary antibiotics. Also, we interpreted the frequently cited practice of
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treating asymptomatic patients based on laboratory findings alone as lack of awareness of
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evidence-based best practices.
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INTRODUCTION
79 The prevalence of asymptomatic bacteriuria (ASB), defined as urine culture with significant
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bacterial growth in an asymptomatic individual, increases with age and may reach 50% in
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nursing home residents.1 In contrast to urinary tract infection (UTI), ASB is not an indication
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for antibiotic treatment (with very few exceptions).2 However, multiple studies have shown
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that at least a third of patients with ASB are unnecessarily treated with antibiotics.3-6 This
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practice corresponds to significant antimicrobial consumption.7, 8 Consequences of
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inappropriate antibiotic use include the development of antimicrobial resistance, side effects
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of antibiotics, and additional costs to the healthcare system. The 2005 practice guideline by
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Nicolle and colleagues was an important effort to reduce antibiotic overuse for ASB in that
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the authors discarded all but two treatment indications (i.e., ASB in pregnancy and ASB in
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patients about to undergo urogenital surgery). In the same vein, a recent IDSA practice
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guideline by Hooton and colleagues differentiated between catheter-associated UTI and
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catheter-associated ASB, and recommended against both screening and antibiotic treatment
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for the latter.9 Regarding UTI management, we know that guideline adherence is a concern.10,
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adherence for ASB (i.e., screening, diagnosis and treatment). In light of the above-mentioned
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reports on antibiotic overuse, we must assume that ASB guidelines are not well observed.
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Very few studies have examined the psychological mechanisms for antibiotic misuse and
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barriers for guideline implementation. In the long-term care setting, Walker et al. identified
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misleading or non-specific clinical signs, ordering of urine cultures without clear indication,
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and the lack of education among providers in interpreting urine culture findings as the main
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contributors towards antibiotic overuse.12 For the acute care setting data are lacking. Our
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objective was to elicit factors that drive antibiotic misuse for ASB in a tertiary care hospital.
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We are, however, unaware of published studies determining the degree of guideline
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METHODS
105 Design, setting, and study population
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We conducted a qualitative evaluation of physician interviews using a semi-structured
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approach. Interviews were performed during November 2011 at the Bern University Hospital,
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a 950-bed tertiary care hospital located in Switzerland, which offers all medical specialties.
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This hospital operates a large general medicine house staff, which consists of residents and
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senior physicians who serve general medicine floors and a broad range of medical and
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surgical subspecialties. For the purpose of this study, we approached 69 physicians (49
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residents and 20 senior physicians) based on their availability for interviews. Of these, 21
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voluntary participants were recruited (12 residents and 9 senior physicians). By purposive
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sampling, we made sure that both genders and all training levels were represented among the
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interviewees. The sample size attempted to reach data saturation (i.e., the point where no
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further material can be obtained) across the full dataset.
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Interview structure
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We performed case-based, semi-structured, individual interviews with open-ended
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questions.13 In order to elicit information about the motivators for prescribing unnecessary
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antibiotics for ASB, a case mirroring a typical clinical course was presented to participants at
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the start of the interviews. The purpose of this case was to serve as discussion basis to
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highlight how difficult it is to distinguish UTI from ASB. The interview questions followed a
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pre-defined “topic guide” (Appendix) and focused on 1) determinants of starting antibiotic
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treatment for suspected UTI, 2) knowledge of scientific evidence and resulting evidence-
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based guidelines and adherence thereto, and 3) understanding and awareness of the concept of
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“asymptomatic bacteriuria”. The topic guide was developed and piloted by one of the authors
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(ME, fellow in infectious disease) and, to ensure its applicability, subsequently reviewed by
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ACCEPTED MANUSCRIPT an infectious disease senior physician, an epidemiologist, and a behavioural psychologist.
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Before the interview started, participants were informed that the objective was to understand
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their knowledge background, management concepts, and behaviour, and we obtained their
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informed consent. We also reminded participants that their identity would not be revealed
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outside the research team, and that their responses were stored in an anonymous fashion and
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not used for individual assessment. Each interview lasted approximately 30 minutes, was
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audio-taped, and then transcribed verbatim. Participants confirmed the accuracy of the written
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transcripts by signature which we kept in our files. In consultation with the local ethics
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committee, formal ethical approval was not required as the study was deemed a quality
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control project without immediate impact on patient care.
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140 Data analysis
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We undertook a computer-assisted analysis (MAXQDA® software, version 10, VERBI
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Software Consult Sozialforschung GmbH, Berlin) with inductive thematic content approach
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according to Mayring.13 Interview transcripts represented the material in which thematic
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categories were identified. Coding was inductively created according to new themes emerging
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from the material. We repeatedly revised the codebook as result of a continuous comparative
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approach to identify similar or distinct perceptions, attitudes, and experiences. Two data
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abstractors (ME and ML) systematically coded the material in an independent way. In order to
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improve the consistency and reliability of the analyses, ME and ML discussed emergent
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themes between each other; the ultimately selected interpretation was supported by consensus
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in all cases. For illustration purposes, we extracted typical examples from the material (i.e.,
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“anchor examples”). Finally, frequency analysis summarized the prevalence of identified
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codes.
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ACCEPTED MANUSCRIPT RESULTS
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We conducted and analysed a total of 21 interviews with the recruited physicians. The themes
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that were used to create categories were: “Treatment of laboratory results without considering
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the clinical picture”, “Physician-centred factors”, “External factors”, “Therapy in light of
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ambiguous or non-attributable signs and symptoms“, “Lack of attention to detail or analytical
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thinking, particularly under time constraints“, and “Overtreatment due to trivialization of
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UTI”. We arranged the categories according to the frequency in which they were mentioned
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and their distribution according to the level of training (Table I) and illustrated each category
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with an „anchor example“. The order in which themes are listed does not imply a weighting
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by the authors. There was a substantial difference between residents and senior physicians in
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reporting nonspecific signs and symptoms as reason for overtreatment. Otherwise, the two
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groups identified similar topics of concern.
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„Treatment of laboratory results without considering the clinical picture“
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The interviewees reported a reflex treatment of pathological urinalyses suggestive of UTI,
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notably nitrite-positivity. The same was reported with positive urine cultures. In those cases
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the providers said they tended to initiate antimicrobial treatment solely based on laboratory
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findings.
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Int.7; § 62-64:
S: I think the trend is that the providers when they see a positive urinalysis they will treat it S: This is a bit more the tenor, as I recollect. Many may say: „So, yes, she has a UTI, so we will treat
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her“. And then you ask: „Does she have any complaints, yes, no, ongoing?“ Then they will say: „ No,
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actually not, she doesn’t have symptoms at all“.
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The repeatedly mentioned thought that routine examination of urine may lead to
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overtreatment of ASB supports our hypothesis that antimicrobial therapy may be prescribed
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mainly due to pathological lab results. Also, leucocytosis and an elevated CRP in combination 7
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with a pathological urinalysis were considered to be indicative of a UTI and, per the
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interviewees’ responses, would likely be treated with antibiotics.
183 „Physician-centred factors“
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In this category we combined findings concerning psychological factors and motivations
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leading to overtreatment of ASB. Anxiousness, insecurity and overcautiousness of the treating
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physician may cause a more “generous” management in terms of antimicrobial therapy. The
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need for personal reassurance is particularly prominent in ambiguous clinical situations and
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when of the physician has little clinical experience. In addition, there is often fear of
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complications. Having witnessed poor patient outcomes when antibiotics were used too
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restrictively is another factor which appears to lead to overtreatment.
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Int.3; § 60:
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S: Yes, that is it,-- if you receive a pathological result but cannot clearly correlate it with the clinical
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picture and then you are afraid, so to speak, to treat a patient not sufficiently or to give no treatment at
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all and so you decide to always opt in favour of antibiotics and never against if there is a doubt.
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S: Because I cannot really tell what... probably it is overcautiousness...
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S:...which is pushing you…
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S: That is what you think,--- hopefully it should not get worse if one does not treat it, or I don’t know...
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S: But I experience it like that. That you will treat is anyway even though you tell yourself “Mm, I don’t
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quite have a clear indication”.
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Occasionally, antibiotic prescription is driven by the hope of improving the patient’s
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condition.
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Int.7; § 50:
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S: It is not always very easy and sometimes one is, maybe, one is tempted to treat it anyway, because
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after all, it is somehow the only thing you have where you can say: “Yes, maybe this might explain [the
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symptoms] somehow and it helps a little with the discomfort”.
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may be the last conceivable intervention in a setting of therapeutic powerlessness. Also,
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respondents reported an expectation towards themselves to treat every „UTI“ and never to
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miss this diagnosis. Furthermore, some stated that they felt better if they could at least treat
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something in a polymorbid patient.
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Int.16; § 150-152:
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S:…Ok, but a UTI that you can treat, of course. The rest you have to watch, how is her heart […] and
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how does it improve and so on and so forth. But alright, we have a UTI that can be treated; in that case
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we are already doing something. It also gives you a good feeling. Gives you a good feeling, doesn’t it?
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S: you now are doing something and you treat something.
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„External factors“
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Some residents who were interviewed indicated difficulties to justify restrictive use of
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antimicrobial therapy and to find arguments against their attending physician’s more
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permissive attitude. To argue against an intention to treat often seems to be more difficult than
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to defend a therapeutic decision that is based on pathological laboratory findings. This aspect
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may allow for the already mentioned “knee-jerk reflex” to treat any pathological laboratory
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findings, irrespective of clinical symptoms.
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Int.16; § 134-136:
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S: yes, when, when one is discussing [the case], and then the attending comes…
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S: … and says: What did you do with the findings? Then you have to justify yourself: yes but - what do I know- [the patient] is asymptomatic and then you have to discuss. S: And then - that is something you sometimes would like to bypass and say: ok good, well, I don’t want to discuss it in detail here and now, why I didn’t treat the [laboratory] results...
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Int.16; § 257-259:
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S: Yes. I think so. Yes, I mean, it is a reflex- the reflex arises just because, because, - because opposing
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it is too much effort, against – the whole system.
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S: I don’t want to waste my energy, everyday, because of such a – trivial thing – to generate too much
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stress, losing your time, discussing, and then- causes me to get into trouble, or maybe not. – It happens
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rarely that you hear: “Yes, good, very good that you did not give any antibiotics”. But one will always
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review critically, then weigh against, well, certainly. That costs time and nerves.
Pressure to start antimicrobial therapy may not only come from senior physicians but also
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from nursing staff. The latter may influence patient management by demanding antibiotic
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treatment for what they think is a UTI. Still another factor is the expectation of the patients
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and their family toward the physician to offer some form of therapy. Our interview partners
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expressed that some family members wish that the indication for antimicrobial therapy is
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made generously, while others even claim such therapy. The patient himself may expect
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antibiotic therapy, too. However, considering that patients with ASB have, per definition, no
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urinary tract symptoms, this factor may be negligible.
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Some physicians reported the observation that the clinical management is often adapted to
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that of colleagues and senior physicians, particularly if there is a “generous” antibiotic
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prescribing environment.
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Int.16; § 144-148:
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S: ...yes, that is often like this, that it is not, you give [antibiotics], you adapt yourself to where you are
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and so.
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S: to the, the environment, where you are, right.
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S: And when you know, there will be more, so there will be done a lot, then- you’re not going to be the
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first to say, yes, but I won’t do that. Hum- that’s the - the tenor then.
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„Therapy in light of ambiguous or non-attributable signs and symptoms“
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Repeatedly, interviewees reported that they would like to prescribe antibiotics, especially in
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elderly patients with ambiguous clinical findings or unclear clinical deterioration in the
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context of pathological findings in the urine.
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Int.8; § 93:
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S: Yes, I believe there is also an uncertainty on the floors.—The patient is doing poorly, for whatever
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reason, and then you prefer to give an antibiotic, in case the patient has a UTI, which might be the
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cause. I believe this is a bit the train of thought […] when the case is unclear. Then it’s better to cover
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it…
268 „Lack of attention to detail or analytical thinking, particularly under time constraints“
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In our interviews it was conveyed that the need for antimicrobial therapy is sometimes
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evaluated in an insufficient manner. An important reason for this might be a lack of time for
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decision-making, which occurs during clinical rounds and night shifts.
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Int.3; § 105-107:
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S: I think to myself, you have become extremely generous with antibiotic therapy. That is, you’re very
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fast with [norfloxacin] or [trimethoprim-sulfamethoxazole] or [amoxicillin-clavulanate] in your hand.
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M: And do you have an explanation for that? (laughs) a little bit of a difficult question...
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S: --- is difficult, yes, ehm---, yes, that’s maybe a cheap excuse, but sometimes it is also a bit of time
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pressure, it is easier, hum, to prescribe an antibiotic for three days when rounding, instead of dealing
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with the concrete situation, hum, and analysing it thoroughly and then trying to figure out the evidence
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for this situation.
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„Overtreatment due to trivialization of UTI”
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Some consider a UTI to be of trivial concern, for which reason the indication for antibiotics
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would be generous. For the same reason there would be less consultation between residents
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and senior physicians.
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Int.16; § 320/328:
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S: -- Yes I guess… that is never of such interest to anybody here. – Or, this is a small UTI, that is -- that
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gets treated, period, end of discussion!
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S: People don’t make a big deal out of it [treating ASB].
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DISCUSSION
294 The main objective of antimicrobial stewardship is to reduce unnecessary antibiotic treatment,
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which saves costs, limits adverse events due to antibiotics, and may prevent the emergence of
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antibiotic resistance. Overtreatment in the context of urine culture findings is particularly
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common and has been the subject of dedicated practice guidelines.2 Despite the publication of
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such guidelines almost a decade ago, overtreatment is an ongoing issue. Reasons for
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overtreating ASB, however, are not well-characterized. In this qualitative study we identified
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both physician-centred factors (e.g., overcautiousness) and external pressors (e.g., excessive
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workload) as motivators for prescribing unnecessary antibiotics. Also, we interpreted the
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commonly cited practice of treating asymptomatic patients based on laboratory findings alone
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as lack of awareness of evidence-based best practices.
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Physician-centred factors
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Among the physician-centred factors, a number of psychological factors emerged as drivers of
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overtreatment. Most notably, anxiousness, overcautiousness, and a need for personal security,
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were cited in our interviews. Physicians indicated that they were afraid of complications and
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that this prompted them to generously prescribe antibiotics for bacteriuria, even if they
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suspected that treatment was not indicated. Prescribing drugs because of personal reassurance
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has already been reported by hospital paediatricians. De Brasi et al. evaluated reasons for
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prescribing drugs to infants with bronchiolitis and found that this practice was linked to the
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perceived clinical severity of this diagnosis, however, there was no correlation between
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objective clinical severity and likelihood of drug prescription.14 For healthcare providers at
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long-term care facilities, Walker et al. reported that “being on the safe side” often justified the
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decision to order antibiotics for ASB.12 In their qualitative study certain physicians explicitly
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later.
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Physicians may be hesitant to use practice guidelines as they question their applicability to an
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individual patient. They frequently use anecdotal experience to justify individual decisions for
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their own patients.15-17 In our study, some indicated the willingness to prescribe antibiotics for
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ASB was a result of adverse outcomes they had witnessed in their professional career with
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restrictive antibiotic use. Other authors mentioned concerns about potential complications of
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ASB as a reason for overtreatment. In a qualitative study on patterns of antibiotic prescription
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for sore throat, a general practitioner explained his high volume of prescribing was a
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consequence of the serious complications he had seen when withholding antibiotics.18 In
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terms of guideline implementation, to stop doing something, such as withholding antibiotics,
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seems to be much more difficult than continue or intensify doing something.16, 19
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Another trigger of permissive use of antibiotics we elicited was the lack of sufficient clinical experience. According to our interviewees, the need for personal reassurance is
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particularly noticeable in residents. The less clinical experience physicians have, the more
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likely they are to be unfamiliar with the exact content of guidelines, which may increase
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permissive use of antibiotics, as mentioned by Cabana et al.15 Others authors also reported a
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strong association between knowledge of ASB management guidelines and level of training.16
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Moreover, younger physicians have yet to build experience in how to use their knowledge, to
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interpret clinical findings, and finally to translate such findings into a management plan.
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There are also “positive” psychological factors that may lead to overtreatment of ASB.
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For example, prescribing a medical treatment can be seen as a confirmation of the physician’s
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role, and trigger the perception that at least something was done. Antibiotics may act as
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beacon of hope, as they hold promise of a clinical improvement even in serious clinical
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situations. Kumar et al. reported the positive feedback on doctor’s feelings associated with
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antibiotic prescription for sore throat because prescribing them made the consultation quick
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by offering a straightforward plan.18
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Of note, interviewees in our study used the term “asymptomatic urinary tract infection” remarkably frequently. The term asymptomatic bacteriuria was less commonly
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used. Thus, it is possible that even the choice of words could unconsciously induce antibiotic
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prescribing.
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Therapy in light of ambiguous or non-attributable signs and symptoms
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Particularly in the context of UTIs, there is often uncertainty as to whether subtle and atypical signs and symptoms can be attributed to a UTI. Some interviewees stated they would
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readily prescribe antibiotics in unclear situations.15 This concern was mainly reported by our
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senior physicians in an attempt to explain residents’ ordering behaviour. In the setting of long-
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term care facilities, Walker et al. emphasized the difficulty to evaluate nonspecific signs and
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symptoms, especially in situations where patients are cognitively impaired and unable to
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articulate their symptoms well.12 Although there is no evidence to support the practice of
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treating a positive urine culture when nonspecific indicators are present, they will often lead
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to antibiotic prescription.20 In her commentary of Walker’s study, Dr. Nicolle emphasized the
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contribution of misinterpreting nonspecific clinical presentations as potentially caused by UTI
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to antibiotic overuse, particularly in institutionalized elderly people; she felt that optimization
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of antibiotic use in the of long-term care setting was an unrealistic goal due to understaffing,
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insufficient diagnostic accuracy and outcome uncertainty.21, 22 However, in acute care
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watchful waiting with continuous reassessment of clinical signs and symptoms may be more
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feasible and could be the best strategy.
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Treatment of laboratory results (without considering the clinical picture)
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Another important reason for overtreatment of ASB is the lack of considering the clinical 14
ACCEPTED MANUSCRIPT picture in the interpretation of laboratory results. Our sample of hospitalists who may only see
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certain patients when on call or when covering for colleagues is comparable to the physicians
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Walker et al. interviewed.12 Decisions were often made independent of the clinical context.
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Based on this study and previous ones, one can say that in the initial phase of ASB
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management a generous diagnostic policy predisposes to permissive treatment, particularly in
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situations of uncertain diagnostic criteria.12 As previously reported by others, our interviews
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confirm that positive results of urinalysis, notably nitrite positivity (data not shown), positive
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urine cultures and systemic leucocytosis trigger cognitive bias which drives inappropriate
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antibiotic use.16, 23 Thus, to improve concordance with international ASB management
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guidelines, screening for ASB without treatment indication should be discouraged.24-26
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379 External pressures
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Even if physicians are willing to adopt evidence-based recommendations, external pressors
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can affect their ability to follow them. Time pressure is a well-described obstacle. In one
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cross-sectional survey, it was the most frequently reported barrier to the implementation of
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guidelines.27 Furthermore, being in conflict with senior physicians and the nursing staff, i.e.,
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arguing against an antimicrobial therapy for ASB seems to be more difficult than giving in,
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and thus can act as external barrier.
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The institutional culture and an institution’s antimicrobial stewardship program can both
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interfere with prescribing practices. Some interviewees mentioned that they adjusted their
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behaviour to an environment of generous antibiotic administration, possibly a common
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occurrence among residents. Two qualitative studies about barriers to antimicrobial treatment
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guidelines highlighted that residents do not make independent decisions in a teaching hospital
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setting because they are constantly supervised in their prescribing practice.17, 28 They may also
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rotate between different wards and departments and need to quickly adapt to the respective
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“subculture” and its antibiotic policy. Thus, strategies for guideline implementation should
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guideline acceptance among physicians of different age; they found that those with <10 years’
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clinical experience were more likely to have a positive attitude towards guidelines and to
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observe them, compared with physicians with >25 years’ experience who often considered
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guidelines as too complicated and restrictive regarding treatment options and flexibility.27
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Expectations of patients and their relatives can also act as obstacles to guideline adherence.15,
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influence the prescribing practice, since these patients are by definition asymptomatic.
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However, regarding practice guideline for ASB, patients’ preferences are less likely to
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We think that our study method with individual interviews reduced mutual interference
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between study participants as seen in focus groups. Another strength is the diverse clinical
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experience in our interview partners. Our qualitative study offers an overview of the main
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contributors towards overtreatment of ASB in the acute care setting and can act as framework
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for further interventions to improve evidence-based best practices in the management of ASB.
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We conducted our qualitative research in a rigorous way in order to ensure reliability and
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validity. Nevertheless, this research has limitations inherent in any qualitative study, namely
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its limited generalizability to other hospital settings with different antibiotics prescribing
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cultures. In addition, despite the fact that two researchers coded the material independently,
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the qualitative method is always a subjective one, as it reflects the observers’ interpretations.
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Lastly, the voluntary study participation may have selected participants who are particularly
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concerned with the issue of antibiotic overtreatment. Furthermore, basic understanding of the
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concept of “asymptomatic bacteriuria” in those who volunteered might differ from those who
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declined participation and therefore limit the study generalizability.
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CONCLUSIONS
422 We believe our study to be the first qualitative investigation into reasons for overtreatment of
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ASB in the acute care setting. We identified different factors that drive overtreatment. Lack of
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awareness regarding the existence of guidelines and insufficient familiarity with their exact
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content are major barriers to implementing evidence-based best practices. But even if
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physicians are willing to adopt recommendations, physician-centred factors and external
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pressures influence their prescribing behaviour. In order to reduce overtreatment effectively
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and sustainably, we think that factors as those identified in our work should be targeted in
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intervention studies.
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Contributorship: Study conception and development of the study design: ME. Acquisition of
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data: ME, DA. Conducting interviews: ME. Data analysis and interpretation: ME, ML, JM.
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Drafting the article: ME. Critical revision of the manuscript and final approval of the version
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to be published: ME, ML, DA, JM. Study supervision: JM.
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This research project served as master thesis for Matthias Läng, medical student. He defended
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his master thesis on April 25, 2014.
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Ethics approval: In consultation with the local ethics committee, formal ethical approval was
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not required as the study was deemed a quality control project without immediate impact on
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patient care.
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Funding: None.
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Conflicts of interest: None.
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ACKNOWLEDGEMENTS
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We appreciate Kathrin Mühlemann†, MD PhD and Martin Egger, MD, for concepting this
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study and stimulating discussions. Unfortunately, Kathrin passed away prematurely in 2012.
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We thank Dr. phil Heinz Bolliger-Salzmann for reviewing the interview topic guide.
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REFERENCES
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1. Colgan R, Nicolle LE, McGlone A, Hooton TM. Asymptomatic bacteriuria in adults. Am fam physician 2006; 74: 985-990. 2. Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton TM, et al. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis 2005; 40: 643-654. 3. Cope M, Cevallos ME, Cadle RM, Darouiche RO, Musher DM, Trautner BW. Inappropriate treatment of catheter-associated asymptomatic bacteriuria in a tertiary care hospital. Clinical Infect Dis 2009; 48: 1182-1188. 4. Chowdhury F, Sarkar K, Branche A, Kim J, Dwek P, Nangit A, et al. Preventing the inappropriate treatment of asymptomatic bacteriuria at a community teaching hospital. J Community Hosp Intern Med Perspect 2012; 2: 17814. 5. Rotjanapan P, Dosa D, Thomas KS. Potentially inappropriate treatment of urinary tract infections in two Rhode Island nursing homes. Arch Intern Med 2011; 171: 438-443. 6. Loeb M, Simor AE, Landry L, Walter S, McArthur M, Duffy J, et al. Antibiotic use in Ontario facilities that provide chronic care. J Gen Intern Med 2001; 16: 376-383. 7. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 2002; 113: 5S-13S. 8. Ansari F, Erntell M, Goossens H, Davey P. The European surveillance of antimicrobial consumption (ESAC) point-prevalence survey of antibacterial use in 20 European hospitals in 2006. Clin Infect Dis 2009; 49: 1496-1504. 9. Hooton TM, Bradley SF, Cardenas DD, Colgan R, Geerlings SE, Rice JC, 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. Clin Infect Dis 2010; 50: 625-663. 10. Grover ML, Bracamonte JD, Kanodia AK, Bryan MJ, Donahue SP, Warner AM, et al. Assessing adherence to evidence-based guidelines for the diagnosis and management of uncomplicated urinary tract infection. Mayo Clin Proc 2007; 82: 181-185. 11. Taur Y, Smith MA. Adherence to the Infectious Diseases Society of America guidelines in the treatment of uncomplicated urinary tract infection. Clin Infect Dis 2007; 44: 769-774. 12. Walker S, McGeer A, Simor AE, Armstrong-Evans M, Loeb M. Why are antibiotics prescribed for asymptomatic bacteriuria in institutionalized elderly people? A qualitative study of physicians' and nurses' perceptions. CMAJ 2000; 163: 273-277. 13. Mayring P. Qualitative Inhaltsanalyse, Grundlagen und Techniken. In: Beltz, editors. 11th ed. Basel/Weinheim 2010:48-109. 14. De Brasi D, Pannuti F, Antonelli F, de Seta F, Siani P, de Seta L. Therapeutic approach to bronchiolitis: why pediatricians continue to overprescribe drugs? Ital J Pediatr 2010; 36: 67. 15. Cabana MD, Rand CS, Powe NR, Wu AW, Wilson MH, Abboud PA, et al. Why don't physicians follow clinical practice guidelines? A framework for improvement. JAMA 1999; 282: 1458-1465. 16. Trautner BW, Petersen NJ, Hysong SJ, Horwitz D, Kelly PA, Naik AD. Overtreatment of asymptomatic bacteriuria: identifying provider barriers to evidence-based care. Am J Infect Control 2014; 42: 653-658. 17. Charani E, Castro-Sanchez E, Sevdalis N, Kyratsis Y, Drumright L, Shah N, et al. Understanding the determinants of antimicrobial prescribing within hospitals: the role of "prescribing etiquette". Clin Infect Dis 2013; 57: 188-196.
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18. Kumar S, Little P, Britten N. Why do general practitioners prescribe antibiotics for sore throat? Grounded theory interview study. BMJ 2003; 326: 138. 19. Arnold SR, Straus SE. Interventions to improve antibiotic prescribing practices in ambulatory care. Cochrane Database Syst Rev 2005: CD003539. 20. Boscia JA, Kobasa WD, Knight RA, Abrutyn E, Levison ME, Kaye D. Epidemiology of bacteriuria in an elderly ambulatory population. Am J Med 1986; 80: 208-214. 21. Nicolle LE. Asymptomatic bacteriuria in institutionalized elderly people: evidence and practice. CMAJ 2000; 163: 285-286. 22. Nicolle LE. Urinary tract infection in geriatric and institutionalized patients. Curr Opin Urol 2002; 12: 51-55. 23. Trautner BW, Bhimani RD, Amspoker AB, Hysong SJ, Garza A, Kelly PA, et al. Development and validation of an algorithm to recalibrate mental models and reduce diagnostic errors associated with catheter-associated bacteriuria. BMC Med Inform Decis Mak 2013; 13: 48. 24. Nicolle LE. Asymptomatic bacteriuria: when to screen and when to treat. Infect Dis Clin North Am 2003; 17: 367-394. 25. Leis JA, Rebick GW, Daneman N, Gold WL, Poutanen SM, Lo P, et al. Reducing antimicrobial therapy for asymptomatic bacteriuria among noncatheterized inpatients: a proofof-concept study. Clin Infect Dis 2014; 58: 980-983. 26. Jones CW, Culbreath KD, Mehrotra A, Gilligan PH. Reflect urine culture cancellation in the emergency department. J Emerg Med 2014; 46: 71-76. 27. Taba P, Rosenthal M, Habicht J, Tarien H, Mathiesen M, Hill S, et al. Barriers and facilitators to the implementation of clinical practice guidelines: a cross-sectional survey among physicians in Estonia. BMC Health Serv Res 2012; 12: 455. 28. Mol PG, Rutten WJ, Gans RO, Degener JE, Haaijer-Ruskamp FM. Adherence barriers to antimicrobial treatment guidelines in teaching hospital, the Netherlands. Emerg Infect Dis 2004; 10: 522-525. 29. Lugtenberg M, Burgers JS, Besters CF, Han D, Westert GP. Perceived barriers to guideline adherence: a survey among general practitioners. BMC Fam Pract 2011; 12: 98.
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ACCEPTED MANUSCRIPT Table I: Frequency in which reasons for overtreatment of ASB were mentioned (of 21 interviewees) Frequency
Laboratory oriented management
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Reasons for overtreatment of ASB
Reflex treatment of pathological urinalysis (in asymptomatic patient)
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Broad screening urinalysis
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Treatment based on inflammatory blood parameters
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Insufficient consideration of symptoms by interpretation of lab results
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Physician-centered psychological factors
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Anxiousness, insecurity and overcautiousness
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Fear of complications
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Need for personal reassurance when physician has little clinical
Having witnessed poor patient outcomes when antibiotics were
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Anxiousness in ambiguous situations
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Hope of improving the patient’s condition
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Last conceivable intervention in a setting of therapeutic powerlessness
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Expectation towards oneself to treat „every UTI“
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Better feeling to „at least“ treat something
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External factors
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Difficulties to justify restrictive use of antimicrobial therapy
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Difficulties to justify oneself to senior physicians
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Difficulties to justify oneself to nursing staff
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Patient’s expectations
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Family members’ expectations
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Adaptation to institutional culture and its antibiotic policy
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Time pressure on duty
Treatment in light of ambiguous or non-attributable signs and
Lack of attention to detail or analytical thinking
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Overtreatment due to trivialization of UTI
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Appendix: Topic guide
How do you make a clinical decision to prescribe antibiotics, or not, in a case of suspected UTI. Which factors do you take into account? What do you associate with the term “asymptomatic bacteriuria”?
To what extent do you base your therapeutic decision making upon scientific
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evidence?
Are there any circumstances where you decide not to follow guidance derived from
What difficulties and obstacles do you encounter when attempting to observe evidence-based best practices?
Which conditions would have to be met in order to facilitate the implementation of evidence-based best practices?
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scientific evidence?
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S0195-6701(16)30044-5
DOI:
10.1016/j.jhin.2016.04.007
Reference:
YJHIN 4800
To appear in:
Journal of Hospital Infection
Received Date: 31 March 2016 Accepted Date: 8 April 2016
Please cite this article as: Eyer MM, Läng M, Aujesky D, Marschall J, Overtreatment of asymptomatic bacteriuria: a qualitative study, Journal of Hospital Infection (2016), doi: 10.1016/j.jhin.2016.04.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Overtreatment of Asymptomatic Bacteriuria: A Qualitative Study
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Myriam M. Eyer1,2, Matthias Läng1, Drahomir Aujesky3, Jonas Marschall1
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Department of Infectious Diseases, Bern University Hospital, Bern, Switzerland
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Division of Infectious Diseases, Valais Hospital, Sion, Switzerland
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Division of General Internal Medicine, Bern University Hospital, Bern, Switzerland
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Keywords: Asymptomatic bacteriuria; overtreatment; urinary tract infection; qualitative
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research
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Running title: Overtreatment of Asymptomatic Bacteriuria
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Authors
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Myriam M. Eyer
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Department of Infectious Diseases, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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and
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Division of Infectious Diseases, Valais Hospital
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Av. du Grand-Champsec 86, CH-1951 Sion
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Phone +41 27 603 4863
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[email protected]
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Matthias Läng
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Department of Infectious Diseases, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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Phone +41 33 826 22 07
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[email protected] 1
Drahomir Aujesky
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Division of General Internal Medicine, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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Phone +41 31 632 88 84
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[email protected]
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Jonas Marschall
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Department of Infectious Diseases, Bern University Hospital
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Freiburgstrasse 18, CH-3010 Bern
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Phone +41 31 632 27 45
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[email protected]
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Corresponding author and reprint requests to:
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Myriam M. Eyer, MD
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Division of Infectious Diseases, Valais Hospital
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Av. du Grand-Champsec 86, CH-1951 Sion
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Phone +41 27 603 4863
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Mobile telephone number +41 79 750 4814
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Fax +41 27 603 4789
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[email protected]
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Word count: Text: 3953 Tables: 1
Summary: 229
References: 29
Appendix: 1
Figures: 0
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ACCEPTED MANUSCRIPT SUMMARY
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Background: Overtreatment of asymptomatic bacteriuria (ASB) is common and can result in
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antibiotic side effects, excess costs to the healthcare system, and potentially trigger
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antimicrobial resistance. According to international management guidelines, ASB is not an
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indication for antibiotic treatment (with few exceptions).
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Aim: To determine reasons for using antibiotics to treat ASB in the absence of a treatment
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indication.
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Methods: We conducted a qualitative study at a tertiary care hospital in Switzerland during
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2011. We interviewed 21 internal medicine residents and attending physicians selected by
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purposive sampling, using a semi-structured questionnaire. Responses were analysed in an
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inductive thematic content approach using dedicated software (MAXQDA®).
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Findings: In the 21 interviews, the following thematic rationales for antibiotic overtreatment
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of ASB were reported (in order of reporting frequency): 1) Treating laboratory findings
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without taking the clinical picture into account (n=17); 2) Psychological factors such as
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anxiousness, overcautiousness or anticipated positive impact on patient outcomes (n=13); 3)
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External pressors such as institutional culture, peer pressure, patient expectation, and
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excessive workload that interferes with proper decision-making (n=9); 4) Difficulty with
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interpreting clinical signs and symptoms (n=8).
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Conclusions: In this qualitative study we identified both physician-centred factors (e.g.,
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overcautiousness) and external pressors (e.g., excessive workload) as motivators for
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prescribing unnecessary antibiotics. Also, we interpreted the frequently cited practice of
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treating asymptomatic patients based on laboratory findings alone as lack of awareness of
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evidence-based best practices.
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INTRODUCTION
79 The prevalence of asymptomatic bacteriuria (ASB), defined as urine culture with significant
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bacterial growth in an asymptomatic individual, increases with age and may reach 50% in
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nursing home residents.1 In contrast to urinary tract infection (UTI), ASB is not an indication
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for antibiotic treatment (with very few exceptions).2 However, multiple studies have shown
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that at least a third of patients with ASB are unnecessarily treated with antibiotics.3-6 This
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practice corresponds to significant antimicrobial consumption.7, 8 Consequences of
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inappropriate antibiotic use include the development of antimicrobial resistance, side effects
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of antibiotics, and additional costs to the healthcare system. The 2005 practice guideline by
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Nicolle and colleagues was an important effort to reduce antibiotic overuse for ASB in that
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the authors discarded all but two treatment indications (i.e., ASB in pregnancy and ASB in
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patients about to undergo urogenital surgery). In the same vein, a recent IDSA practice
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guideline by Hooton and colleagues differentiated between catheter-associated UTI and
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catheter-associated ASB, and recommended against both screening and antibiotic treatment
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for the latter.9 Regarding UTI management, we know that guideline adherence is a concern.10,
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adherence for ASB (i.e., screening, diagnosis and treatment). In light of the above-mentioned
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reports on antibiotic overuse, we must assume that ASB guidelines are not well observed.
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Very few studies have examined the psychological mechanisms for antibiotic misuse and
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barriers for guideline implementation. In the long-term care setting, Walker et al. identified
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misleading or non-specific clinical signs, ordering of urine cultures without clear indication,
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and the lack of education among providers in interpreting urine culture findings as the main
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contributors towards antibiotic overuse.12 For the acute care setting data are lacking. Our
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objective was to elicit factors that drive antibiotic misuse for ASB in a tertiary care hospital.
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We are, however, unaware of published studies determining the degree of guideline
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METHODS
105 Design, setting, and study population
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We conducted a qualitative evaluation of physician interviews using a semi-structured
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approach. Interviews were performed during November 2011 at the Bern University Hospital,
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a 950-bed tertiary care hospital located in Switzerland, which offers all medical specialties.
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This hospital operates a large general medicine house staff, which consists of residents and
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senior physicians who serve general medicine floors and a broad range of medical and
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surgical subspecialties. For the purpose of this study, we approached 69 physicians (49
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residents and 20 senior physicians) based on their availability for interviews. Of these, 21
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voluntary participants were recruited (12 residents and 9 senior physicians). By purposive
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sampling, we made sure that both genders and all training levels were represented among the
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interviewees. The sample size attempted to reach data saturation (i.e., the point where no
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further material can be obtained) across the full dataset.
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Interview structure
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We performed case-based, semi-structured, individual interviews with open-ended
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questions.13 In order to elicit information about the motivators for prescribing unnecessary
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antibiotics for ASB, a case mirroring a typical clinical course was presented to participants at
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the start of the interviews. The purpose of this case was to serve as discussion basis to
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highlight how difficult it is to distinguish UTI from ASB. The interview questions followed a
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pre-defined “topic guide” (Appendix) and focused on 1) determinants of starting antibiotic
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treatment for suspected UTI, 2) knowledge of scientific evidence and resulting evidence-
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based guidelines and adherence thereto, and 3) understanding and awareness of the concept of
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“asymptomatic bacteriuria”. The topic guide was developed and piloted by one of the authors
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(ME, fellow in infectious disease) and, to ensure its applicability, subsequently reviewed by
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ACCEPTED MANUSCRIPT an infectious disease senior physician, an epidemiologist, and a behavioural psychologist.
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Before the interview started, participants were informed that the objective was to understand
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their knowledge background, management concepts, and behaviour, and we obtained their
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informed consent. We also reminded participants that their identity would not be revealed
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outside the research team, and that their responses were stored in an anonymous fashion and
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not used for individual assessment. Each interview lasted approximately 30 minutes, was
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audio-taped, and then transcribed verbatim. Participants confirmed the accuracy of the written
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transcripts by signature which we kept in our files. In consultation with the local ethics
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committee, formal ethical approval was not required as the study was deemed a quality
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control project without immediate impact on patient care.
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140 Data analysis
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We undertook a computer-assisted analysis (MAXQDA® software, version 10, VERBI
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Software Consult Sozialforschung GmbH, Berlin) with inductive thematic content approach
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according to Mayring.13 Interview transcripts represented the material in which thematic
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categories were identified. Coding was inductively created according to new themes emerging
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from the material. We repeatedly revised the codebook as result of a continuous comparative
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approach to identify similar or distinct perceptions, attitudes, and experiences. Two data
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abstractors (ME and ML) systematically coded the material in an independent way. In order to
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improve the consistency and reliability of the analyses, ME and ML discussed emergent
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themes between each other; the ultimately selected interpretation was supported by consensus
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in all cases. For illustration purposes, we extracted typical examples from the material (i.e.,
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“anchor examples”). Finally, frequency analysis summarized the prevalence of identified
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codes.
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We conducted and analysed a total of 21 interviews with the recruited physicians. The themes
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that were used to create categories were: “Treatment of laboratory results without considering
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the clinical picture”, “Physician-centred factors”, “External factors”, “Therapy in light of
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ambiguous or non-attributable signs and symptoms“, “Lack of attention to detail or analytical
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thinking, particularly under time constraints“, and “Overtreatment due to trivialization of
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UTI”. We arranged the categories according to the frequency in which they were mentioned
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and their distribution according to the level of training (Table I) and illustrated each category
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with an „anchor example“. The order in which themes are listed does not imply a weighting
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by the authors. There was a substantial difference between residents and senior physicians in
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reporting nonspecific signs and symptoms as reason for overtreatment. Otherwise, the two
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groups identified similar topics of concern.
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„Treatment of laboratory results without considering the clinical picture“
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The interviewees reported a reflex treatment of pathological urinalyses suggestive of UTI,
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notably nitrite-positivity. The same was reported with positive urine cultures. In those cases
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the providers said they tended to initiate antimicrobial treatment solely based on laboratory
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findings.
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Int.7; § 62-64:
S: I think the trend is that the providers when they see a positive urinalysis they will treat it S: This is a bit more the tenor, as I recollect. Many may say: „So, yes, she has a UTI, so we will treat
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her“. And then you ask: „Does she have any complaints, yes, no, ongoing?“ Then they will say: „ No,
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actually not, she doesn’t have symptoms at all“.
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The repeatedly mentioned thought that routine examination of urine may lead to
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overtreatment of ASB supports our hypothesis that antimicrobial therapy may be prescribed
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mainly due to pathological lab results. Also, leucocytosis and an elevated CRP in combination 7
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with a pathological urinalysis were considered to be indicative of a UTI and, per the
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interviewees’ responses, would likely be treated with antibiotics.
183 „Physician-centred factors“
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In this category we combined findings concerning psychological factors and motivations
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leading to overtreatment of ASB. Anxiousness, insecurity and overcautiousness of the treating
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physician may cause a more “generous” management in terms of antimicrobial therapy. The
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need for personal reassurance is particularly prominent in ambiguous clinical situations and
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when of the physician has little clinical experience. In addition, there is often fear of
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complications. Having witnessed poor patient outcomes when antibiotics were used too
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restrictively is another factor which appears to lead to overtreatment.
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Int.3; § 60:
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S: Yes, that is it,-- if you receive a pathological result but cannot clearly correlate it with the clinical
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picture and then you are afraid, so to speak, to treat a patient not sufficiently or to give no treatment at
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all and so you decide to always opt in favour of antibiotics and never against if there is a doubt.
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Int.8; § 127-133:
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S: Because I cannot really tell what... probably it is overcautiousness...
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S:...which is pushing you…
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S: That is what you think,--- hopefully it should not get worse if one does not treat it, or I don’t know...
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S: But I experience it like that. That you will treat is anyway even though you tell yourself “Mm, I don’t
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quite have a clear indication”.
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Occasionally, antibiotic prescription is driven by the hope of improving the patient’s
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condition.
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Int.7; § 50:
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S: It is not always very easy and sometimes one is, maybe, one is tempted to treat it anyway, because
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after all, it is somehow the only thing you have where you can say: “Yes, maybe this might explain [the
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symptoms] somehow and it helps a little with the discomfort”.
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may be the last conceivable intervention in a setting of therapeutic powerlessness. Also,
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respondents reported an expectation towards themselves to treat every „UTI“ and never to
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miss this diagnosis. Furthermore, some stated that they felt better if they could at least treat
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something in a polymorbid patient.
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Int.16; § 150-152:
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S:…Ok, but a UTI that you can treat, of course. The rest you have to watch, how is her heart […] and
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how does it improve and so on and so forth. But alright, we have a UTI that can be treated; in that case
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we are already doing something. It also gives you a good feeling. Gives you a good feeling, doesn’t it?
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S: you now are doing something and you treat something.
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„External factors“
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Some residents who were interviewed indicated difficulties to justify restrictive use of
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antimicrobial therapy and to find arguments against their attending physician’s more
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permissive attitude. To argue against an intention to treat often seems to be more difficult than
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to defend a therapeutic decision that is based on pathological laboratory findings. This aspect
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may allow for the already mentioned “knee-jerk reflex” to treat any pathological laboratory
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findings, irrespective of clinical symptoms.
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Int.16; § 134-136:
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S: yes, when, when one is discussing [the case], and then the attending comes…
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S: … and says: What did you do with the findings? Then you have to justify yourself: yes but - what do I know- [the patient] is asymptomatic and then you have to discuss. S: And then - that is something you sometimes would like to bypass and say: ok good, well, I don’t want to discuss it in detail here and now, why I didn’t treat the [laboratory] results...
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Int.16; § 257-259:
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S: Yes. I think so. Yes, I mean, it is a reflex- the reflex arises just because, because, - because opposing
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it is too much effort, against – the whole system.
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S: I don’t want to waste my energy, everyday, because of such a – trivial thing – to generate too much
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stress, losing your time, discussing, and then- causes me to get into trouble, or maybe not. – It happens
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rarely that you hear: “Yes, good, very good that you did not give any antibiotics”. But one will always
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review critically, then weigh against, well, certainly. That costs time and nerves.
Pressure to start antimicrobial therapy may not only come from senior physicians but also
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from nursing staff. The latter may influence patient management by demanding antibiotic
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treatment for what they think is a UTI. Still another factor is the expectation of the patients
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and their family toward the physician to offer some form of therapy. Our interview partners
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expressed that some family members wish that the indication for antimicrobial therapy is
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made generously, while others even claim such therapy. The patient himself may expect
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antibiotic therapy, too. However, considering that patients with ASB have, per definition, no
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urinary tract symptoms, this factor may be negligible.
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Some physicians reported the observation that the clinical management is often adapted to
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that of colleagues and senior physicians, particularly if there is a “generous” antibiotic
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prescribing environment.
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Int.16; § 144-148:
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S: ...yes, that is often like this, that it is not, you give [antibiotics], you adapt yourself to where you are
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and so.
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S: to the, the environment, where you are, right.
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S: And when you know, there will be more, so there will be done a lot, then- you’re not going to be the
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first to say, yes, but I won’t do that. Hum- that’s the - the tenor then.
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„Therapy in light of ambiguous or non-attributable signs and symptoms“
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Repeatedly, interviewees reported that they would like to prescribe antibiotics, especially in
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elderly patients with ambiguous clinical findings or unclear clinical deterioration in the
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context of pathological findings in the urine.
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Int.8; § 93:
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S: Yes, I believe there is also an uncertainty on the floors.—The patient is doing poorly, for whatever
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reason, and then you prefer to give an antibiotic, in case the patient has a UTI, which might be the
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cause. I believe this is a bit the train of thought […] when the case is unclear. Then it’s better to cover
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it…
268 „Lack of attention to detail or analytical thinking, particularly under time constraints“
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In our interviews it was conveyed that the need for antimicrobial therapy is sometimes
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evaluated in an insufficient manner. An important reason for this might be a lack of time for
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decision-making, which occurs during clinical rounds and night shifts.
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Int.3; § 105-107:
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S: I think to myself, you have become extremely generous with antibiotic therapy. That is, you’re very
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fast with [norfloxacin] or [trimethoprim-sulfamethoxazole] or [amoxicillin-clavulanate] in your hand.
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M: And do you have an explanation for that? (laughs) a little bit of a difficult question...
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S: --- is difficult, yes, ehm---, yes, that’s maybe a cheap excuse, but sometimes it is also a bit of time
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pressure, it is easier, hum, to prescribe an antibiotic for three days when rounding, instead of dealing
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with the concrete situation, hum, and analysing it thoroughly and then trying to figure out the evidence
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for this situation.
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„Overtreatment due to trivialization of UTI”
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Some consider a UTI to be of trivial concern, for which reason the indication for antibiotics
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would be generous. For the same reason there would be less consultation between residents
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and senior physicians.
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Int.16; § 320/328:
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S: -- Yes I guess… that is never of such interest to anybody here. – Or, this is a small UTI, that is -- that
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gets treated, period, end of discussion!
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S: People don’t make a big deal out of it [treating ASB].
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DISCUSSION
294 The main objective of antimicrobial stewardship is to reduce unnecessary antibiotic treatment,
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which saves costs, limits adverse events due to antibiotics, and may prevent the emergence of
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antibiotic resistance. Overtreatment in the context of urine culture findings is particularly
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common and has been the subject of dedicated practice guidelines.2 Despite the publication of
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such guidelines almost a decade ago, overtreatment is an ongoing issue. Reasons for
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overtreating ASB, however, are not well-characterized. In this qualitative study we identified
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both physician-centred factors (e.g., overcautiousness) and external pressors (e.g., excessive
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workload) as motivators for prescribing unnecessary antibiotics. Also, we interpreted the
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commonly cited practice of treating asymptomatic patients based on laboratory findings alone
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as lack of awareness of evidence-based best practices.
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Physician-centred factors
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Among the physician-centred factors, a number of psychological factors emerged as drivers of
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overtreatment. Most notably, anxiousness, overcautiousness, and a need for personal security,
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were cited in our interviews. Physicians indicated that they were afraid of complications and
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that this prompted them to generously prescribe antibiotics for bacteriuria, even if they
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suspected that treatment was not indicated. Prescribing drugs because of personal reassurance
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has already been reported by hospital paediatricians. De Brasi et al. evaluated reasons for
313
prescribing drugs to infants with bronchiolitis and found that this practice was linked to the
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perceived clinical severity of this diagnosis, however, there was no correlation between
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objective clinical severity and likelihood of drug prescription.14 For healthcare providers at
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long-term care facilities, Walker et al. reported that “being on the safe side” often justified the
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decision to order antibiotics for ASB.12 In their qualitative study certain physicians explicitly
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later.
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Physicians may be hesitant to use practice guidelines as they question their applicability to an
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individual patient. They frequently use anecdotal experience to justify individual decisions for
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their own patients.15-17 In our study, some indicated the willingness to prescribe antibiotics for
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ASB was a result of adverse outcomes they had witnessed in their professional career with
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restrictive antibiotic use. Other authors mentioned concerns about potential complications of
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ASB as a reason for overtreatment. In a qualitative study on patterns of antibiotic prescription
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for sore throat, a general practitioner explained his high volume of prescribing was a
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consequence of the serious complications he had seen when withholding antibiotics.18 In
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terms of guideline implementation, to stop doing something, such as withholding antibiotics,
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seems to be much more difficult than continue or intensify doing something.16, 19
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Another trigger of permissive use of antibiotics we elicited was the lack of sufficient clinical experience. According to our interviewees, the need for personal reassurance is
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particularly noticeable in residents. The less clinical experience physicians have, the more
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likely they are to be unfamiliar with the exact content of guidelines, which may increase
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permissive use of antibiotics, as mentioned by Cabana et al.15 Others authors also reported a
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strong association between knowledge of ASB management guidelines and level of training.16
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Moreover, younger physicians have yet to build experience in how to use their knowledge, to
337
interpret clinical findings, and finally to translate such findings into a management plan.
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There are also “positive” psychological factors that may lead to overtreatment of ASB.
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For example, prescribing a medical treatment can be seen as a confirmation of the physician’s
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role, and trigger the perception that at least something was done. Antibiotics may act as
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beacon of hope, as they hold promise of a clinical improvement even in serious clinical
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situations. Kumar et al. reported the positive feedback on doctor’s feelings associated with
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antibiotic prescription for sore throat because prescribing them made the consultation quick
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by offering a straightforward plan.18
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Of note, interviewees in our study used the term “asymptomatic urinary tract infection” remarkably frequently. The term asymptomatic bacteriuria was less commonly
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used. Thus, it is possible that even the choice of words could unconsciously induce antibiotic
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prescribing.
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Therapy in light of ambiguous or non-attributable signs and symptoms
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Particularly in the context of UTIs, there is often uncertainty as to whether subtle and atypical signs and symptoms can be attributed to a UTI. Some interviewees stated they would
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readily prescribe antibiotics in unclear situations.15 This concern was mainly reported by our
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senior physicians in an attempt to explain residents’ ordering behaviour. In the setting of long-
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term care facilities, Walker et al. emphasized the difficulty to evaluate nonspecific signs and
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symptoms, especially in situations where patients are cognitively impaired and unable to
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articulate their symptoms well.12 Although there is no evidence to support the practice of
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treating a positive urine culture when nonspecific indicators are present, they will often lead
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to antibiotic prescription.20 In her commentary of Walker’s study, Dr. Nicolle emphasized the
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contribution of misinterpreting nonspecific clinical presentations as potentially caused by UTI
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to antibiotic overuse, particularly in institutionalized elderly people; she felt that optimization
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of antibiotic use in the of long-term care setting was an unrealistic goal due to understaffing,
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insufficient diagnostic accuracy and outcome uncertainty.21, 22 However, in acute care
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watchful waiting with continuous reassessment of clinical signs and symptoms may be more
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feasible and could be the best strategy.
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366 367
Treatment of laboratory results (without considering the clinical picture)
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Another important reason for overtreatment of ASB is the lack of considering the clinical 14
ACCEPTED MANUSCRIPT picture in the interpretation of laboratory results. Our sample of hospitalists who may only see
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certain patients when on call or when covering for colleagues is comparable to the physicians
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Walker et al. interviewed.12 Decisions were often made independent of the clinical context.
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Based on this study and previous ones, one can say that in the initial phase of ASB
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management a generous diagnostic policy predisposes to permissive treatment, particularly in
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situations of uncertain diagnostic criteria.12 As previously reported by others, our interviews
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confirm that positive results of urinalysis, notably nitrite positivity (data not shown), positive
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urine cultures and systemic leucocytosis trigger cognitive bias which drives inappropriate
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antibiotic use.16, 23 Thus, to improve concordance with international ASB management
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guidelines, screening for ASB without treatment indication should be discouraged.24-26
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379 External pressures
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Even if physicians are willing to adopt evidence-based recommendations, external pressors
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can affect their ability to follow them. Time pressure is a well-described obstacle. In one
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cross-sectional survey, it was the most frequently reported barrier to the implementation of
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guidelines.27 Furthermore, being in conflict with senior physicians and the nursing staff, i.e.,
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arguing against an antimicrobial therapy for ASB seems to be more difficult than giving in,
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and thus can act as external barrier.
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The institutional culture and an institution’s antimicrobial stewardship program can both
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interfere with prescribing practices. Some interviewees mentioned that they adjusted their
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behaviour to an environment of generous antibiotic administration, possibly a common
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occurrence among residents. Two qualitative studies about barriers to antimicrobial treatment
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guidelines highlighted that residents do not make independent decisions in a teaching hospital
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setting because they are constantly supervised in their prescribing practice.17, 28 They may also
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rotate between different wards and departments and need to quickly adapt to the respective
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“subculture” and its antibiotic policy. Thus, strategies for guideline implementation should
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guideline acceptance among physicians of different age; they found that those with <10 years’
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clinical experience were more likely to have a positive attitude towards guidelines and to
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observe them, compared with physicians with >25 years’ experience who often considered
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guidelines as too complicated and restrictive regarding treatment options and flexibility.27
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Expectations of patients and their relatives can also act as obstacles to guideline adherence.15,
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29
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influence the prescribing practice, since these patients are by definition asymptomatic.
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However, regarding practice guideline for ASB, patients’ preferences are less likely to
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We think that our study method with individual interviews reduced mutual interference
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between study participants as seen in focus groups. Another strength is the diverse clinical
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experience in our interview partners. Our qualitative study offers an overview of the main
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contributors towards overtreatment of ASB in the acute care setting and can act as framework
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for further interventions to improve evidence-based best practices in the management of ASB.
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We conducted our qualitative research in a rigorous way in order to ensure reliability and
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validity. Nevertheless, this research has limitations inherent in any qualitative study, namely
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its limited generalizability to other hospital settings with different antibiotics prescribing
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cultures. In addition, despite the fact that two researchers coded the material independently,
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the qualitative method is always a subjective one, as it reflects the observers’ interpretations.
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Lastly, the voluntary study participation may have selected participants who are particularly
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concerned with the issue of antibiotic overtreatment. Furthermore, basic understanding of the
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concept of “asymptomatic bacteriuria” in those who volunteered might differ from those who
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declined participation and therefore limit the study generalizability.
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CONCLUSIONS
422 We believe our study to be the first qualitative investigation into reasons for overtreatment of
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ASB in the acute care setting. We identified different factors that drive overtreatment. Lack of
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awareness regarding the existence of guidelines and insufficient familiarity with their exact
426
content are major barriers to implementing evidence-based best practices. But even if
427
physicians are willing to adopt recommendations, physician-centred factors and external
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pressures influence their prescribing behaviour. In order to reduce overtreatment effectively
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and sustainably, we think that factors as those identified in our work should be targeted in
430
intervention studies.
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ACCEPTED MANUSCRIPT STATEMENTS
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Contributorship: Study conception and development of the study design: ME. Acquisition of
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data: ME, DA. Conducting interviews: ME. Data analysis and interpretation: ME, ML, JM.
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Drafting the article: ME. Critical revision of the manuscript and final approval of the version
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to be published: ME, ML, DA, JM. Study supervision: JM.
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This research project served as master thesis for Matthias Läng, medical student. He defended
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his master thesis on April 25, 2014.
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Ethics approval: In consultation with the local ethics committee, formal ethical approval was
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not required as the study was deemed a quality control project without immediate impact on
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patient care.
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Funding: None.
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Conflicts of interest: None.
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ACKNOWLEDGEMENTS
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We appreciate Kathrin Mühlemann†, MD PhD and Martin Egger, MD, for concepting this
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study and stimulating discussions. Unfortunately, Kathrin passed away prematurely in 2012.
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We thank Dr. phil Heinz Bolliger-Salzmann for reviewing the interview topic guide.
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REFERENCES
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1. Colgan R, Nicolle LE, McGlone A, Hooton TM. Asymptomatic bacteriuria in adults. Am fam physician 2006; 74: 985-990. 2. Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton TM, et al. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis 2005; 40: 643-654. 3. Cope M, Cevallos ME, Cadle RM, Darouiche RO, Musher DM, Trautner BW. Inappropriate treatment of catheter-associated asymptomatic bacteriuria in a tertiary care hospital. Clinical Infect Dis 2009; 48: 1182-1188. 4. Chowdhury F, Sarkar K, Branche A, Kim J, Dwek P, Nangit A, et al. Preventing the inappropriate treatment of asymptomatic bacteriuria at a community teaching hospital. J Community Hosp Intern Med Perspect 2012; 2: 17814. 5. Rotjanapan P, Dosa D, Thomas KS. Potentially inappropriate treatment of urinary tract infections in two Rhode Island nursing homes. Arch Intern Med 2011; 171: 438-443. 6. Loeb M, Simor AE, Landry L, Walter S, McArthur M, Duffy J, et al. Antibiotic use in Ontario facilities that provide chronic care. J Gen Intern Med 2001; 16: 376-383. 7. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 2002; 113: 5S-13S. 8. Ansari F, Erntell M, Goossens H, Davey P. The European surveillance of antimicrobial consumption (ESAC) point-prevalence survey of antibacterial use in 20 European hospitals in 2006. Clin Infect Dis 2009; 49: 1496-1504. 9. Hooton TM, Bradley SF, Cardenas DD, Colgan R, Geerlings SE, Rice JC, 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. Clin Infect Dis 2010; 50: 625-663. 10. Grover ML, Bracamonte JD, Kanodia AK, Bryan MJ, Donahue SP, Warner AM, et al. Assessing adherence to evidence-based guidelines for the diagnosis and management of uncomplicated urinary tract infection. Mayo Clin Proc 2007; 82: 181-185. 11. Taur Y, Smith MA. Adherence to the Infectious Diseases Society of America guidelines in the treatment of uncomplicated urinary tract infection. Clin Infect Dis 2007; 44: 769-774. 12. Walker S, McGeer A, Simor AE, Armstrong-Evans M, Loeb M. Why are antibiotics prescribed for asymptomatic bacteriuria in institutionalized elderly people? A qualitative study of physicians' and nurses' perceptions. CMAJ 2000; 163: 273-277. 13. Mayring P. Qualitative Inhaltsanalyse, Grundlagen und Techniken. In: Beltz, editors. 11th ed. Basel/Weinheim 2010:48-109. 14. De Brasi D, Pannuti F, Antonelli F, de Seta F, Siani P, de Seta L. Therapeutic approach to bronchiolitis: why pediatricians continue to overprescribe drugs? Ital J Pediatr 2010; 36: 67. 15. Cabana MD, Rand CS, Powe NR, Wu AW, Wilson MH, Abboud PA, et al. Why don't physicians follow clinical practice guidelines? A framework for improvement. JAMA 1999; 282: 1458-1465. 16. Trautner BW, Petersen NJ, Hysong SJ, Horwitz D, Kelly PA, Naik AD. Overtreatment of asymptomatic bacteriuria: identifying provider barriers to evidence-based care. Am J Infect Control 2014; 42: 653-658. 17. Charani E, Castro-Sanchez E, Sevdalis N, Kyratsis Y, Drumright L, Shah N, et al. Understanding the determinants of antimicrobial prescribing within hospitals: the role of "prescribing etiquette". Clin Infect Dis 2013; 57: 188-196.
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18. Kumar S, Little P, Britten N. Why do general practitioners prescribe antibiotics for sore throat? Grounded theory interview study. BMJ 2003; 326: 138. 19. Arnold SR, Straus SE. Interventions to improve antibiotic prescribing practices in ambulatory care. Cochrane Database Syst Rev 2005: CD003539. 20. Boscia JA, Kobasa WD, Knight RA, Abrutyn E, Levison ME, Kaye D. Epidemiology of bacteriuria in an elderly ambulatory population. Am J Med 1986; 80: 208-214. 21. Nicolle LE. Asymptomatic bacteriuria in institutionalized elderly people: evidence and practice. CMAJ 2000; 163: 285-286. 22. Nicolle LE. Urinary tract infection in geriatric and institutionalized patients. Curr Opin Urol 2002; 12: 51-55. 23. Trautner BW, Bhimani RD, Amspoker AB, Hysong SJ, Garza A, Kelly PA, et al. Development and validation of an algorithm to recalibrate mental models and reduce diagnostic errors associated with catheter-associated bacteriuria. BMC Med Inform Decis Mak 2013; 13: 48. 24. Nicolle LE. Asymptomatic bacteriuria: when to screen and when to treat. Infect Dis Clin North Am 2003; 17: 367-394. 25. Leis JA, Rebick GW, Daneman N, Gold WL, Poutanen SM, Lo P, et al. Reducing antimicrobial therapy for asymptomatic bacteriuria among noncatheterized inpatients: a proofof-concept study. Clin Infect Dis 2014; 58: 980-983. 26. Jones CW, Culbreath KD, Mehrotra A, Gilligan PH. Reflect urine culture cancellation in the emergency department. J Emerg Med 2014; 46: 71-76. 27. Taba P, Rosenthal M, Habicht J, Tarien H, Mathiesen M, Hill S, et al. Barriers and facilitators to the implementation of clinical practice guidelines: a cross-sectional survey among physicians in Estonia. BMC Health Serv Res 2012; 12: 455. 28. Mol PG, Rutten WJ, Gans RO, Degener JE, Haaijer-Ruskamp FM. Adherence barriers to antimicrobial treatment guidelines in teaching hospital, the Netherlands. Emerg Infect Dis 2004; 10: 522-525. 29. Lugtenberg M, Burgers JS, Besters CF, Han D, Westert GP. Perceived barriers to guideline adherence: a survey among general practitioners. BMC Fam Pract 2011; 12: 98.
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ACCEPTED MANUSCRIPT Table I: Frequency in which reasons for overtreatment of ASB were mentioned (of 21 interviewees) Frequency
Laboratory oriented management
17
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Reasons for overtreatment of ASB
Reflex treatment of pathological urinalysis (in asymptomatic patient)
10
Broad screening urinalysis
4 4
Treatment based on inflammatory blood parameters
3
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Treatment solely based on positive urine cultures (ASB)
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Insufficient consideration of symptoms by interpretation of lab results
2
Physician-centered psychological factors
13
Anxiousness, insecurity and overcautiousness
10
Fear of complications
experience
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Need for personal reassurance when physician has little clinical
Having witnessed poor patient outcomes when antibiotics were
6 4
2
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used too restrictively
Anxiousness in ambiguous situations
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Hope of improving the patient’s condition
2 7
Last conceivable intervention in a setting of therapeutic powerlessness
3
Expectation towards oneself to treat „every UTI“
2
Better feeling to „at least“ treat something
2
External factors
9
Difficulties to justify restrictive use of antimicrobial therapy
3
Difficulties to justify oneself to senior physicians
3
Difficulties to justify oneself to nursing staff
1
ACCEPTED MANUSCRIPT Expectations toward the physician
3
Patient’s expectations
3
Family members’ expectations
1 2
Adaptation to institutional culture and its antibiotic policy
2
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Time pressure on duty
Treatment in light of ambiguous or non-attributable signs and
Lack of attention to detail or analytical thinking
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Overtreatment due to trivialization of UTI
4
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symptoms
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NOTE. ASB, asymptomatic bacteriuria; UTI, urinary tract infection.
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Appendix: Topic guide
How do you make a clinical decision to prescribe antibiotics, or not, in a case of suspected UTI. Which factors do you take into account? What do you associate with the term “asymptomatic bacteriuria”?
To what extent do you base your therapeutic decision making upon scientific
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evidence?
Are there any circumstances where you decide not to follow guidance derived from
What difficulties and obstacles do you encounter when attempting to observe evidence-based best practices?
Which conditions would have to be met in order to facilitate the implementation of evidence-based best practices?
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scientific evidence?
1