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Article

Assessment of the Compliance of Cystitis Management According to French Recommendations through the Analysis of Prescriptions Collected in Community Pharmacies

by
Arthur Piraux
1,*,
Ramy Hammoud
2,
Jérémie Riou
3,
Souhil Lebdai
4 and
Sébastien Faure
1
1
University of Angers, Inserm, CNRS, MINT, SFR ICAT, F-49000 Angers, France
2
Methodology and Biostatistics Department, University of Angers, F-49000 Angers, France
3
University of Angers, Inserm, CHU Angers, CNRS, MINT, SFR ICAT, F-49000 Angers, France
4
Department of Urology, Angers University Hospital, F-49000 Angers, France
*
Author to whom correspondence should be addressed.
Antibiotics 2022, 11(7), 976; https://doi.org/10.3390/antibiotics11070976
Submission received: 26 June 2022 / Revised: 13 July 2022 / Accepted: 18 July 2022 / Published: 20 July 2022
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Abstract

:
Urinary tract infections, especially cystitis, are common infections; they are the second most prevalent cause of antibiotic prescriptions in community pharmacies. To reduce antimicrobial resistance, guidelines are revised regularly. This study aims to assess compliance between prescriptions collected in community pharmacies and French cystitis guidelines. A treatment is considered compliant if the nature, dosage, and duration of the antibiotics are correct. Only women aged 18–65 years with a diagnosis of cystitis were eligible. The participation of 16 pharmacies resulted in 303 prescriptions. Most infections were classified as uncomplicated cystitis (79.2%), general practitioners were the prescribers in more than 9 out of 10 cases, and fosfomycin trometamol was the antibiotic dispensed for 1 in 2 women. An average compliance of 66% was observed, but with disparities according to the type of cystitis. Two-thirds of cases of uncomplicated cystitis and recurrent cystitis followed the recommendations, whereas only 15% of cystitis cases that were at risk of complication did so. The inclusion of a urine examination in uncomplicated cystitis decreased the overall compliance rate to 5.8%. These results show the essential role played by pharmacists; they are the last line of defence before dispensing antibiotics. They must know the recommendations in order to apply them.

1. Introduction

Urinary tract infections (UTIs) are the second most common cause of antibiotic prescriptions after respiratory infections [1,2,3,4]. Each year, 150 million people are treated for this condition [5]. UTIs include several conditions, such as cystitis, pyelonephritis, urethritis, and prostatitis [6,7]. Cystitis in women is characterized by an inflammation of the bladder caused by germs such as Escherichia coli (E. coli). It is a commensal pathogen, naturally found in the urinary tract, responsible for 75–95% of infections [6]. The imbalance of its environment can cause its proliferation and lead to an infection [8]. E. coli is the most frequently found bacteria. Symptoms such as pollakiuria (urinary frequency) with an urgent need to urinate, dysuria (burning and pain during urination), and hematuria (blood in urine) are frequently observed [8,9].
Three different types of cystitis are described in [3,7,10]. Simple or uncomplicated cystitis is the most common diagnosis, when there are no identified risk factors. Cystitis at risk of complication is diagnosed when a patient presents with at least one risk factor. The most common risk factors are urinary tract abnormality, pregnancy, being elderly (≥75 years old), severe chronic renal failure, and severe immunodeficiency [9,10]. Recurrent cystitis occurs when a patient has at least four episodes of cystitis in the same year. This definition has evolved recently. UTIs are considered recurrent if they occur at least three times a year or twice within the last six months [11].
A urine dipstick is the only test recommendedfor uncomplicated cystitis, but a urine culture is needed for the two other types of cystitis [10,12]. The negative predictive value of a urine dipstick is very high (>95%). It allows the detection of two compounds: leukocytes (evidence of infection) and nitrites (presence of an enterobacteria with a nitrate reductase, such as E. coli, Proteus mirabilis, or Klebsiella spp.). In the case of recurrent cystitis, urine cultures are only requested during the initial episode.
The high frequency of this infection results in the regular consumption of antibiotics, sometimes in the same patient. In France, the choice of the antibiotic is guided by three parameters: efficacity, tolerability, and the ecological impact on the gut microbiota [10]. The most recent studies have shown that a shorter duration of antibiotics improves the above parameters, without limiting the treatment of the infection [13]. These results explain why the duration of the antibiotics to treat a simple acute cystitis is 3 days, and no longer 5 days, with pivmecillinam, or with a single dose of fosfomycin trometamol [9,14]. To reduce the antimicrobial resistance (AMR), the nature of the antibiotic must be considered, and guidelines must be reviewed regularly [15]. For example, the overuse of fluoroquinolones created a resistance to these drugs in uropathogenic E. coli. This resistance is particularly marked in developed countries (55–85% resistance), compared with developing countries (5–30% resistance) [16].
A precedent study analysed the impact of new recommendations on antibiotic-prescribing behaviour in France [17]. Several antibiotics are still commonly prescribed, despite their withdrawal from recommendations (lomefloxacin and norfloxacin, in particular). This reflects the length of time it takes for recommendations to reach prescribers. This observation is confirmed by other studies. Hecker et al. report low adherence to UTI guidelines in the emergency department (42%), which led to a stewardship intervention [18]. Adherence to the guidelines increased to 68% (period 1) and 82% (period 2). Grave et al. reported similar adherence to French guidelines for UTIs (66%) [19]. This rate varied significantly depending on the condition; 66% (n = 71) of acute cystitis cases were conformed, but only 20% (n = 3) of cystitis at risk of complication did so. In line with these results, this study aimed to assess compliance between prescriptions collected in community pharmacies and respective French cystitis guidelines.

2. Materials and Methods

The development of this study required the completion of a preliminary study to determine the necessary sample size, and to verify its feasibility. Its goal was to propose an overview of the situation to obtain an estimation of the compliance between the treatment and the French guidelines to treat cystitis.

2.1. Preliminary Study

A preliminary study was conducted in four community pharmacies to obtain approximately 50 response forms. Each pharmacist was trained prior to the data collection to ensure a proper understanding of the form (Appendix A). It was available online, on the LimeSurvey® platform, and on paper. Before completing the form, it was necessary to check the following inclusion/non-inclusion criteria. Only women aged 18–65 years with a diagnosis of cystitis (uncomplicated cystitis, cystitis at risk of complication, or recurrent cystitis) were eligible. In addition, the lack of pregnancy or another UTI (i.e., pyelonephritis) was required. Each incomplete form was considered non-responsive.
This preliminary study aimed to evaluate the accordance between the guidelines and the treatment prescribed for a UTI. The prescription was considered compliant if, and only if, the nature, the dosage, and the duration of the antibiotics were correct. Current recommendations at the time of the study were used as a reference; they were published by the French Infectious Diseases Society (Société de Pathologie Infectieuse de Langue Française—SPILF) in 2018 [10]. Specific guidelines were edited for each type of cystitis (Table 1).
The pilot study was conducted from 22 September to 18 October 2020. In total, 56 forms were collected but only 52 were retained (1 patient was pregnant, 1 patient was older than 65 years, and there were 2 incomplete forms). A total of 41 prescriptions were in compliance with the recommendations regarding the nature of the antibiotic. However, only 36 prescriptions were fully compliant with national recommendations, representing an observed compliance percentage of 69.2%.

2.2. Main Study

The main study was conducted from 14 January to 1 June 2021. All data had to be entered into the LimeSurvey® platform, but pharmacists had the possibility to use a paper questionnaire with the patient before completing the online questionnaire. The inclusion and non-inclusion criteria were the same as those used in the pilot study (women, aged between 18 and 65 years old, a diagnosis of cystitis, no pregnancy, and no other UTIs present).
The prescription of antibiotics in a woman was a sign that the patient would require the pharmacy team’s attention. As with any prescription, it was the pharmacist’s responsibility to confirm the match between the prescription and the condition by asking questions. The patients who received an antibiotic to treat or prevent cystitis were invited to participate in the study. Participation was free and voluntary. Verbal approval indicated consent to participate in the study. One or two minutes were required to complete the survey (Appendix A).
Community pharmacists were recruited through the Regional Union of Health Professionals (Union Régionale des Profesionnels de Santé—URPS). This organization sent an e-mail to all community pharmacists in the Pays de la Loire region of France. A virtual meeting was organized to present the study in detail and to explain the process. Sixteen community pharmacists agreed to participate in the study. This study aimed to assess compliance with the French guidelines, using the same modalities as the preliminary study.

2.3. Sample Size and Statistical Analysis

The percentage of compliance observed for the preliminary study (69%) was consistent with the literature. Grave et al. produced a similar study and obtained a compliance of 58% [19]. As a precaution, a margin was taken, and the theoretical percentage of compliance retained was 60%. Considering a theoretical proportion of 60%, an observed proportion of 69%, a type I error rate, α of 5%, and a power of 95%, the required sample size was 303 patients.
GraphPad® (Prism 8.4.3 version) was used for the statistical analysis of the data [20]. The data were presented as frequency and percentages. The chi-square test and Fisher’s t-test were used to appreciate the association between the conformity and some factors. A p-value of <0.05 indicated a statistically significant difference, which became highly significant if the p-value was <0.001. R software (version 4.1.3) was also used to perform a logistic regression analysis [21]. A variable selection was determined to minimize the AIC, while focusing on known confounders. The absence of collinearity was also checked.

3. Results

A total of 375 forms were received, but 62 were not complete and 10 were rejected because the inclusion criteria were not verified (two women were pregnant and eight women were over the age of 65). In total, 303 forms were retained for analysis.

3.1. Patients’ Characteristics

The sample seems heterogenous, with a representativity of each age range but also of several profiles, including the risk factor and the first infection (Table 2). While 22.4% of women suffered from cystitis for the first time, nearly one in two (47.8%) had experienced at least one in the past 12 months. For 11.9% of them, it was even a recurrent cystitis. The risk of reporting a new episode within 3 months of the first one seemed to be verified; 31.7% of patients had at least one episode in the last 3 months. Most infections were classified as uncomplicated cystitis (79.2%) and some women were reported to be at risk of complication (8.9%).
Hygiene rules were explained for most of the women (56.4%). A urine culture was performed for 35.5% of patients, but a urine dipstick was performed for only 14.5% of them. Only a small proportion of patients received prescriptions containing an additional box of antibiotics (11.9%).

3.2. Prescriptions’ Characteristics

General practitioners were the prescribers in more than nine out of ten cases (Figure 1). Fosfomycin trometamol was the antibiotic prescribed for one in two women, while pivmecillinam was in second place (with 16.3% of prescriptions). Cefixime and ciprofloxacin shared third place (at 6.5%). The other antibiotics were anecdotic with less than 5% for each of them.

3.3. Compliance between Cystitis Management and Guidelines

The compliance of the prescriptions was assessed according to the valid recommendations at the time of the survey (Figure 2). A global average compliance of 61.4% was observed, with some disparities according to the type of cystitis. Approximately two-thirds of the cases of uncomplicated cystitis and recurrent cystitis followed the recommendations, whereas only 14.8% of the cases of cystitis at risk of complication did so. For the latter, a decrease in compliance was observed for each additional criterion (the compliance rate divided by two between the nature and the dosage, and then halved again with the addition of the duration).
To assess the association between some variables and the compliance of antibiotic therapy (nature, dosage, and duration), a logistic regression was performed (Figure 3). Ages between 56 and 65 years and having a prescription left with the office secretary increased the risk of non-compliance (with an OR of 2.6 and 4.52, respectively). Conversely, the absence of a urine culture slightly but significantly reduced non-compliance (with an OR between 0.58 and 0.99). Finally, the absence of a risk factor in the patient remains the criterion that most reduced non-compliance with antibiotic therapy (with an OR of 0.08).
A focus was placed on uncomplicated cystitis (n = 240). For this specific indication, the compliance between guidelines and antibiotic therapy was 66.3% (nature, dosage, and duration) (Figure 4). A dipstick test was performed in only 35 cases (14.6%), and a urine culture was performed twice as often (33.3%). Compliance with the antibiotic therapy and the urine examination led to a compliance rate of 5.8% (n = 14), ten times lower than compliance with the antibiotic prescription alone. Explanation of hygienic rules by the physician reduced this compliance to 2.9% (n = 7) (Figure 3).

4. Discussion

This study aimed to assess the compliance between prescriptions collected in community pharmacies and the French cystitis guidelines. An average compliance of 66% was observed. Two-thirds of cases of uncomplicated cystitis and cystitis at risk of complication were compliant for the antibiotic therapy, while only 15% of cases of recurrent cystitis were. These results appeared to be in line with the international literature. For example, even though Grave et al. conducted their study in a hospital, they reported similar compliance rates (58% and 61.4%, respectively) [19]. In this study, a similar finding was observed for the management of cystitis at risk of complication, with a compliance rate of 20% (14.8% in the study). The management of this type of infection seems to be less known to physicians. Several factors should be considered in determining whether antibiotic therapy is appropriate for the guidelines. The presence of risk factors, and therefore the type of cystitis, are factors that influence compliance with the recommendations, considering the type of urinary examination performed for uncomplicated cystitis decreased compliance with guidelines by a factor of 10.
The nature of the antibiotic appeared to be a major factor of compliance (Figure 2). For uncomplicated cystitis and recurrent cystitis, a quarter of the prescriptions were not in compliance with the nature of the microbial agent alone. Considering that almost 80% of cystitis cases were uncomplicated, it was expected that fosfomycin trometamol would be the first antibiotic prescribed (54.9%). However, it was even more surprising that quinolones were prescribed in 14.3% of cases, even though they are no longer indicated for this type of infection. In France, a focus on the good use of fluoroquinolones was published by the SPILF in 2015 [22]. This study highlights that they are very effective but must be prescribed sparingly to limit resistance and preserve the intestinal microbiota. Therefore, they should not be prescribed when another antibiotic can be used. Previous treatments must be considered (contraindication to prescribe a fluoroquinolone, if prescribed within the last 6 months), and the recommended dosage must be respected [23]. Similar studies have been conducted in other countries and found comparable difficulties in compliance with treatment guidelines [24,25,26,27,28]. In France, a clear decrease in lomefloxacin and norfloxacin prescriptions has been observed since they are no longer reimbursed [17]. Even if the recommendations might vary from one country to another, the fight against AMR is a major issue. The over-prescription of quinolones might lead to resistance and limited efficacy and should be restricted. In some countries, these antibiotics are prescribed in the majority of cases (51% of prescriptions in Houston, TX, USA) [25].
The nature of the antibiotic was not the only criteria considered. The addition of dosage to compliance had little impact on uncomplicated cystitis and recurrent cystitis, with a decrease in compliance of three points. A new decrease in compliance of six points was observed with the addition of the duration criteria (nature, dosage, and duration). The management of cystitis at risk of complication was a real problem, as each parameter reduced compliance with recommendations by half. Regarding the duration of antibiotic therapy, a Cochrane review by Lutters et al. reported the added value of short treatments [29]. They found that there was no significant difference in efficacy between short and long treatments, but that the latter caused more adverse effects. For this reason, many international recommendations tended to reduce the duration of antibiotic treatments used to limit AMR [30,31,32,33]. These recommendations should also be communicated to prescribers in the best possible way.
The next step is to bring the new recommendations to prescribers so that they may better manage these infections. A systematic meta-review from Francke et al. provided some answers [34]. The characteristics of healthcare providers, patients, and the environment must be considered. In addition, simple but varied strategies appeared to be more effective. In our case, the frequent updating of the recommendations seemed to be an obstacle to their application. It would be relevant to conduct the same study, with the new recommendations currently in effect, and to observe whether the reduction in the duration of the prescription of pivmecillinam has been retained.
According to Llor et al., the adherence of physicians to guidelines for the management of lower UTIs in women is poor [35]. It is reported that first-choice drug schedules were prescribed in only 17.5% of cases. A recent qualitative study was conducted to analyse primary-care provider decisions in the management of UTIs [36]. In this study, physicians were not familiar with fosfomycin trometamol, which explained its low prescription rate. The same problem was observed in France with pivmecillinam. Since 2015, in uncomplicated cystitis, pivmecillinam was really prescribed only 2–3 years later [17]. The authors noted that beliefs may lead healthcare providers to prescribe one antibiotic over another. For example, they believed that infection control was faster with fluoroquinolones than with trimethoprim-sulfamethoxazole or nitrofurantoin. They also added that the recommendations should be integrated into the medical software to ensure compliance.
Our study had several limitations. Even though we highlighted existing practice flaws, unfortunately our methodology did not allow us to help improve them. In addition, our study suffered from a collection and a recall bias because of the lack of contact between the pharmacist and the physician, as well as the inability to access the patient’s medical records. Indeed, the pharmacists had to collect all the information from the patients themselves. It can explain the collection of contradictory data in some rare cases (e.g., one episode was indicated in the current year, while the last episode was more than a year ago). Some questions must be approached with caution, especially those involving the patient’s history (such as previous infections, or previous treatment with a quinolone). Nevertheless, the use of the patient’s history via the business software or the pharmaceutical files (available with the patient’s health card in France), allowed us to limit this lack of information. Only pharmacists who volunteered to participate in the study were included, without randomization. Their motivation and the extension of the collection period provided the expected sample. Moreover, as it is impossible to be sure of the completeness of the reporting of UTI cases in each pharmacy during the study period, a patient-selection bias can be assumed. This bias seems limited by the proportion of each type of UTI collected; that is consistent with the epidemiology of this infection [3].
The pharmacist is the last line of defence before a patient takes a drug. Thus, the pharmacist must be aware of the recommendations in force and ensure that they are respected. If necessary, the pharmacist can contact the prescriber to adapt the prescription. As with physicians, it may be appropriate to assess pharmacists’ knowledge in this area. A study that assessed pharmacists’ knowledge of current recommendations would estimate the rate of prescribing that could be improved. This study provided an overview of compliance with antibiotic prescriptions for cystitis in women. Uncomplicated cystitis and recurrent cystitis benefitted from average management (concordance of approximately 66% between recommendations and prescriptions) but cystitis at risk of complication should be improved with a concordance rate of 15%. The management of UTIs also involved an examination. The example of simple cystitis showed us that urine cultures were performed instead of urine dipstick tests. Taking this criterion into account, in addition to antibiotic therapy, reduced the compliance rate for the management of uncomplicated cystitis to less than 10%.
Following this study, an intervention for prescribers should be considered to provide them with the tools to implement the new recommendations. The frequent updating of recommendations complicates their application. The availability of computer tools on the prescription software, mobile phone applications, or simple online tools might be one solution [37,38,39]. These tools can improve the knowledge translation from the guidelines to the physicians [40]. Interprofessional education, continuing professional development, or multifaceted, education-focused interventions are other proposals to improve adherence to recommendations [41,42]. A post-intervention analysis would then be appropriate to measure the effects of this intervention. Furthermore, because uncomplicated cystitis is such a common and simple UTI, its management by a pharmacist would be relevant. A dispensation under protocol by the pharmacist would allow them to answer this need of care, but also to respect the recommendations with the protocol used [43,44,45,46].

Author Contributions

Conceptualization, R.H.; methodology, R.H.; validation, A.P. and S.F.; formal analysis, J.R. and A.P.; investigation, R.H.; writing—original draft preparation, A.P.; writing—review and editing, R.H., S.L., J.R. and S.F.; supervision, S.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

This research was conducted in accordance with French regulations. This study was approved by the Institutional Review Board of the Groupe Nantais d’Ethique dans le Domaine de la Santé (GNEDS) under IRB #22062022.

Informed Consent Statement

Participants agreed to give oral informed consent before they completed the survey.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We thank all the pharmacists who participated in this study and the Union régionale des professionnels de santé Pharmaciens des Pays de la Loire for its support. Editorial assistance was provided by Speak the Speech Consulting.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A. Data Collection Form

Antibiotics 11 00976 i001
Antibiotics 11 00976 i002

References

  1. Porter, H.; Choutet, P.; Peyramond, D.; Saimot, A.G.; Soussy, C.J.; Stahl, J.P. Société de pathologie infectieuse de langue française Deuxième conférence de consensus en thérapeutique anti-infectieuse. Méd. Mal. Infect. 1990, 20, 620–623. [Google Scholar] [CrossRef]
  2. Stamm, W.E.; Norrby, S.R. Urinary Tract Infections: Disease Panorama and Challenges. J. Infect. Dis. 2001, 183, S1–S4. [Google Scholar] [CrossRef] [PubMed]
  3. Geerlings, S.E. Clinical Presentations and Epidemiology of Urinary Tract Infections. Microbiol. Spectr. 2016, 4, 27–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Foxman, B. Epidemiology of urinary tract infections: Incidence, morbidity, and economic costs. Am. J. Med. 2002, 113, 5–13. [Google Scholar] [CrossRef]
  5. McLellan, L.K.; Hunstad, D.A. Urinary Tract Infection: Pathogenesis and Outlook. Trends Mol. Med. 2016, 22, 946–957. [Google Scholar] [CrossRef] [Green Version]
  6. Gupta, K.; Hooton, T.M.; Naber, K.G.; Wullt, B.; Colgan, R.; Miller, L.G.; Moran, G.J.; Nicolle, L.E.; Raz, R.; Schaeffer, A.J.; et al. International Clinical Practice Guidelines for the Treatment of Acute Uncomplicated Cystitis and Pyelonephritis in Women: A 2010 Update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin. Infect. Dis. 2011, 52, e103–e120. [Google Scholar] [CrossRef] [Green Version]
  7. Johansen, T.E.B.; Botto, H.; Cek, M.; Grabe, M.; Tenke, P.; Wagenlehner, F.M.; Naber, K.G. Critical review of current definitions of urinary tract infections and proposal of an EAU/ESIU classification system. Int. J. Antimicrob. Agents 2011, 38, 64–70. [Google Scholar] [CrossRef]
  8. Flores-Mireles, A.L.; Walker, J.N.; Caparon, M.; Hultgren, S.J. Urinary tract infections: Epidemiology, mechanisms of infection and treatment options. Nat. Rev. Microbiol. 2015, 13, 269–284. [Google Scholar] [CrossRef]
  9. Haute autorité de Santé. Cystite Aiguë Simple, à Risque de Complication ou Récidivante, de la Femme; Haute autorité de Santé: Saint-Denis, France, 2021. [Google Scholar]
  10. Caron, F.; Galperine, T.; Flateau, C.; Azria, R.; Bonacorsi, S.; Bruyère, F.; Cariou, G.; Clouqueur, E.; Cohen, R.; Doco-Lecompte, T.; et al. Practice guidelines for the management of adult community-acquired urinary tract infections. Méd. Mal. Infect. 2018, 48, 327–358. [Google Scholar] [CrossRef]
  11. EAU. EAU Guidelines. Edn. Presented at the EAU Annual Congress Amsterdam, The Netherlands 2022, 22/03; EAU: Arnhem, The Netherlands, 2022; ISBN 978-94-92671-16-5. [Google Scholar]
  12. Meister, L.; Morley, E.J.; Scheer, D.; Sinert, R. History and Physical Examination Plus Laboratory Testing for the Diagnosis of Adult Female Urinary Tract Infection. Acad. Emerg. Med. 2013, 20, 631–645. [Google Scholar] [CrossRef]
  13. Wintenberger, C.; Guery, B.; Bonnet, E.; Castan, B.; Cohen, R.; Diamantis, S.; Lesprit, P.; Maulin, L.; Péan, Y.; Peju, E.; et al. Proposal for shorter antibiotic therapies. Méd. Mal. Infect. 2017, 47, 92–141. [Google Scholar] [CrossRef] [PubMed]
  14. Gauzit, R.; Castan, B.; Bonnet, E.; Bru, J.; Cohen, R.; Diamantis, S.; Faye, A.; Hitoto, H.; Issa, N.; Lebeaux, D.; et al. Anti-infectious treatment duration: The SPILF and GPIP French guidelines and recommendations. Infect. Dis. Now 2021, 51, 114–139. [Google Scholar] [CrossRef] [PubMed]
  15. Bell, B.G.; Schellevis, F.; Stobberingh, E.; Goossens, H.; Pringle, M. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect. Dis. 2014, 14, 13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Kot, B. Antibiotic Resistance Among Uropathogenic Escherichia coli. Pol. J. Microbiol. 2019, 68, 403–415. [Google Scholar] [CrossRef] [Green Version]
  17. Piraux, A.; Faure, S.; Naber, K.G.; Alidjanov, J.F.; Ramond-Roquin, A. Changes in the management of urinary tract infections in women: Impact of the new recommendations on antibiotic prescribing behavior in France, between 2014 and 2019. BMC Health Serv. Res. 2021, 21, 612. [Google Scholar] [CrossRef]
  18. Hecker, M.T.; Fox, C.J.; Son, A.H.; Cydulka, R.K.; Siff, J.E.; Emerman, C.L.; Sethi, A.K.; Muganda, C.P.; Donskey, C.J. Effect of a Stewardship Intervention on Adherence to Uncomplicated Cystitis and Pyelonephritis Guidelines in an Emergency Department Setting. PLoS ONE 2014, 9, e87899. [Google Scholar] [CrossRef] [Green Version]
  19. Grave, E. Prise en Charge des Infections Urinaires au Service d’accueil des Urgences du Centre Hospitalier de Dunkerque Selon les Recommandations de la SPILF; Université du droit et de la santé Lille 2: Lille, France, 2017. [Google Scholar]
  20. GraphPad Software, GraphPad Software: San Diego, CA, USA, 2020.
  21. R Core Team. R: A Language and Environment for Statistical Computing; R Core Team: Vienna, Austria, 2022. [Google Scholar]
  22. Chidiac, C.; Cavallo, J.D.; Cohen, R.; Dupon, M.; Galperine, T.; Garraffo, R.; Garo, B.; Gauzit, R.; Gavazzi, G.; Kouzan, S.; et al. Focus on the Good Use of Systemic Fluoroquinolones Administered in Adults (Ciprofloxacin, Levofloxacin, Moxifloxacin, Norfloxacin, Ofloxacin, Pefloxacin). 2015, p. 64. Available online: https://www.infectiologie.com/UserFiles/File/medias/Recos/2015-MAP-fluoroquinolones-SPILF.pdf (accessed on 30 December 2020).
  23. van der Starre, W.E.; van Nieuwkoop, C.; Paltansing, S.; van’t Wout, J.W.; Groeneveld, G.H.; Becker, M.J.; Koster, T.; Wattel-Louis, G.H.; Delfos, N.M.; Ablij, H.C.; et al. Risk factors for fluoroquinolone-resistant Escherichia coli in adults with community-onset febrile urinary tract infection. J. Antimicrob. Chemother. 2010, 66, 650–656. [Google Scholar] [CrossRef] [Green Version]
  24. Kabbara, W.K.; Meski, M.M.; Ramadan, W.H.; Maaliki, D.S.; Salameh, P. Adherence to International Guidelines for the Treatment of Uncomplicated Urinary Tract Infections in Lebanon. Can. J. Infect. Dis. Med Microbiol. 2018, 2018, 7404095. [Google Scholar] [CrossRef]
  25. Grigoryan, L.; Zoorob, R.; Wang, H.; Trautner, B.W. Low Concordance with Guidelines for Treatment of Acute Cystitis in Primary Care. Open Forum Infect. Dis. 2015, 2, ofv159. [Google Scholar] [CrossRef]
  26. Kim, M.; Lloyd, A.; Condren, M.; Miller, M.J. Beyond antibiotic selection: Concordance with the IDSA guidelines for uncomplicated urinary tract infections. Infection 2015, 43, 89–94. [Google Scholar] [CrossRef]
  27. Zatorski, C.; Zocchi, M.; Cosgrove, S.E.; Rand, C.; Brooks, G.; May, L. A single center observational study on emergency department clinician non-adherence to clinical practice guidelines for treatment of uncomplicated urinary tract infections. BMC Infect. Dis. 2016, 16, 638. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Durkin, M.J.; Keller, M.; Butler, A.M.; Kwon, J.H.; Dubberke, E.R.; Miller, A.C.; Polgreen, P.M.; Olsen, M.A. An Assessment of Inappropriate Antibiotic Use and Guideline Adherence for Uncomplicated Urinary Tract Infections. Open Forum Infect. Dis. 2018, 5, ofy198. [Google Scholar] [CrossRef] [PubMed]
  29. Lutters, M.; Vogt-Ferrier, N.B. Antibiotic duration for treating uncomplicated, symptomatic lower urinary tract infections in elderly women. Cochrane Database Syst. Rev. 2008, CD001535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. IACG. No Time to Wait: Securing the Future from Drug-Resistant Infections. Report to the Secretary-General of the United Nations; IACG: Geneva, Switzerland, 2019. [Google Scholar]
  31. Butler, C.C.; Hillier, S.; Roberts, Z.; Dunstan, F.; Howard, A.; Palmer, S. Antibiotic-resistant infections in primary care are symptomatic for longer and increase workload: Outcomes for patients with E. coli UTIs. Br. J. Gen. Pract. 2006, 56, 686–692. [Google Scholar]
  32. Spoorenberg, V.; Hulscher, M.E.J.L.; Akkermans, R.P.; Prins, J.M.; Geerlings, S.E. Appropriate Antibiotic Use for Patients with Urinary Tract Infections Reduces Length of Hospital Stay. Clin. Infect. Dis. 2014, 58, 164–169. [Google Scholar] [CrossRef] [Green Version]
  33. World Health Organisation (WHO). Antimicrobial Resistance: Global Report on Surveillance; WHO: Geneva, Switzerland, 2014; ISBN 9789241564748.
  34. Francke, A.L.; Smit, M.C.; de Veer, A.J.; Mistiaen, P. Factors influencing the implementation of clinical guidelines for health care professionals: A systematic meta-review. BMC Med. Inform. Decis. Mak. 2008, 8, 38. [Google Scholar] [CrossRef] [Green Version]
  35. Llor, C.; Rabanaque, G.; López, A.; Cots, J.M. The adherence of GPs to guidelines for the diagnosis and treatment of lower urinary tract infections in women is poor. Fam. Pract. 2011, 28, 294–299. [Google Scholar] [CrossRef]
  36. Grigoryan, L.; Nash, S.; Zoorob, R.; Germanos, G.J.; Horsfield, M.S.; Khan, F.M.; Martin, L.; Trautner, B.W. Qualitative Analysis of Primary Care Provider Prescribing Decisions for Urinary Tract Infections. Antibiotics 2019, 8, 84. [Google Scholar] [CrossRef] [Green Version]
  37. Antibioclic. Antibiothéraphie Rationnelle En Soins Primaires. Available online: https://antibioclic.com/ (accessed on 16 September 2020).
  38. Yoon, C.H.; Ritchie, S.R.; Duffy, E.J.; Thomas, M.G.; McBride, S.; Read, K.; Chen, R.; Humphrey, G. Impact of a smartphone app on prescriber adherence to antibiotic guidelines in adult patients with community acquired pneumonia or urinary tract infections. PLoS ONE 2019, 14, e0211157. [Google Scholar] [CrossRef] [Green Version]
  39. VIDAL—Recommandations. Available online: https://www.vidal.fr/recommandations/ (accessed on 4 November 2020).
  40. Abidi, S.; Vallis, M.; Piccinini-Vallis, H.; Imran, S.A.; Abidi, S.S.R. Diabetes-Related Behavior Change Knowledge Transfer to Primary Care Practitioners and Patients: Implementation and Evaluation of a Digital Health Platform. JMIR Med Inform. 2018, 6, e25. [Google Scholar] [CrossRef]
  41. Willems, L.; Denckens, P.; Philips, H.; Henriquez, R.; Remmen, R. Can we improve adherence to guidelines for the treatment of lower urinary tract infection? A simple, multifaceted intervention in out-of-hours services. J. Antimicrob. Chemother. 2012, 67, 2997–3000. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Lam, T.T.; Dang, D.A.; Tran, H.H.; Do, D.V.; Le, H.; Negin, J.; Jan, S.; Marks, G.B.; Nguyen, T.A.; Fox, G.J.; et al. What are the most effective community-based antimicrobial stewardship interventions in low- and middle-income countries? A narrative review. J. Antimicrob. Chemother. 2021, 76, 1117–1129. [Google Scholar] [CrossRef] [PubMed]
  43. Erni, P.; von Overbeck, J.; Reich, O.; Ruggli, M. netCare, a new collaborative primary health care service based in Swiss community pharmacies. Res. Soc. Adm. Pharm. 2016, 12, 622–626. [Google Scholar] [CrossRef] [PubMed]
  44. Stewart, F.; Caldwell, G.; Cassells, K.; Burton, J.; Watson, A. Building capacity in primary care: The implementation of a novel ‘Pharmacy First’ scheme for the management of UTI, impetigo and COPD exacerbation. Prim. Health Care Res. Dev. 2018, 19, 531–541. [Google Scholar] [CrossRef] [Green Version]
  45. Booth, J.L.; Mullen, A.B.; Thomson, D.A.M.; Johnstone, C.; Galbraith, S.J.; Bryson, S.M.; McGovern, E.M. Antibiotic treatment of urinary tract infection by community pharmacists: A cross-sectional study. Br. J. Gen. Pract. 2013, 63, e244–e249. [Google Scholar] [CrossRef]
  46. Ministry of Solidarites and Health. Arrêté Du 6 Mars 2020 Relatif à L’autorisation Du Protocole de Coopération « Prise En Charge de La Pollakiurie et de La Brûlure Mictionnelle Chez La Femme de 16 à 65 Ans Par l’infirmier Diplômé d’Etat et Le Pharmacien d’officine Dans Le Cadre d’une Structure Pluri-Professionnelle »; Ministry of Solidarites and Health: Paris, France, 2020.
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Figure 1. The origin of the prescriber (A) and the nature of the antibiotic prescribed (B) among the 303 selected prescriptions. In three cases, two antibiotics were prescribed at the same time for the same patient (n = 306).
Figure 1. The origin of the prescriber (A) and the nature of the antibiotic prescribed (B) among the 303 selected prescriptions. In three cases, two antibiotics were prescribed at the same time for the same patient (n = 306).
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Antibiotics 11 00976 g002 550
Figure 2. The compliance of antibiotic prescription, depending on the type of cystitis: uncomplicated cystitis, cystitis at risk of complication, and recurrent cystitis (n = 303). Compliance was examined based on the nature of the antibiotic, the nature and dosage of the antibiotic, or the nature, the dosage, and the duration of the antibiotic with the guidelines.
Figure 2. The compliance of antibiotic prescription, depending on the type of cystitis: uncomplicated cystitis, cystitis at risk of complication, and recurrent cystitis (n = 303). Compliance was examined based on the nature of the antibiotic, the nature and dosage of the antibiotic, or the nature, the dosage, and the duration of the antibiotic with the guidelines.
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Antibiotics 11 00976 g003 550
Figure 3. The impacts of the different factors which influenced the risk of non-compliance with antibiotic therapy for cystitis. Logistic regression was conducted with an α risk of 5%. A p-value of <0.05 was considered significant, a p-value of <0.01 was considered very significant, and a p-value of <0.001 was considered highly significant.
Figure 3. The impacts of the different factors which influenced the risk of non-compliance with antibiotic therapy for cystitis. Logistic regression was conducted with an α risk of 5%. A p-value of <0.05 was considered significant, a p-value of <0.01 was considered very significant, and a p-value of <0.001 was considered highly significant.
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Figure 4. The compliance of uncomplicated cystitis management with recommendations using cumulative criteria (n = 240). Each column represented a new compliance criterion. The starting point was the compliance of the nature of the antibiotic, then its dosage, and its duration. Then, the compliance of the urine examination, urine culture, and urine dipstick were added. Finally, the explanation of hygiene rules was included.
Figure 4. The compliance of uncomplicated cystitis management with recommendations using cumulative criteria (n = 240). Each column represented a new compliance criterion. The starting point was the compliance of the nature of the antibiotic, then its dosage, and its duration. Then, the compliance of the urine examination, urine culture, and urine dipstick were added. Finally, the explanation of hygiene rules was included.
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Table
Table 1. French guidelines for cystitis management *, according to the type of cystitis, during the preliminary study and the study.
Table 1. French guidelines for cystitis management *, according to the type of cystitis, during the preliminary study and the study.
Uncomplicated CystitisCystitis at Risk of ComplicationRecurrent Cystitis
  • Fosfomycin trometamol 3 g, single dose
  • Pivmecillinam 400 mg, twice daily for 5 days
If the result of urine culture is known:
  • Amoxicillin 1 g, three daily for 7 days
  • Pivmecillinam 400 mg, twice daily for 7 days
  • Nitrofurantoin 100 mg, three daily for 7 days
  • Fosfomycin trometamol 3 g, three doses each administered 48 h apart (D1-D3-D5)
  • Trimethoprim 150 mg, once daily for 5 days
Curative treatment (<1 episode per month)
  • Fosfomycin trometamol 3 g, single dose
  • Pivmecillinam 400 mg, twice daily for 5 days
If the treatment cannot be delayed
  • Nitrofurantoin, 7 days
  • Fosfomycin trometamol 3 g, three doses each administered 48 h apart (D1-D3-D5)
Prophylactic treatment (>1 episode per month)
-
Trimethoprim 150 mg, once daily
-
Trimethoprim-sulfamethoxazole 80/400 mg, once daily
-
Fosfomycin trometamol 3 g, once weekly
* Recommendations used as a reference; published by the French Infectious Diseases Society in 2018 [10].
Table
Table 2. Patients’ characteristics (n = 303).
Table 2. Patients’ characteristics (n = 303).
Patients’ CharacteristicsNumber of Patients (%)
Age18–2454 (17.8)
25–3560 (19.8)
36–4536 (11.9)
46–5561 (20.1)
56–6592 (30.4)
Type of cystitisUncomplicated240 (79.2)
Recurrent36 (11.9)
At risk of complication27 (8.9)
Risk factorAbnormalities of the urinary tract 18 (5.9)
Severe immunodeficiency 9 (3.0)
No276 (91.1)
First infectionYes68 (22.4)
No235 (77.6)
Last infection<15 days13 (4.3)
<1 month26 (8.6)
<3 months57 (18.8)
<12 months70 (23.1)
>12 months58 (19.1)
Do not know11 (3.6)
NA68 (22.4)
Episode frequency in the last 12 months0128 (42.2)
155 (18.2)
247 (15.5)
337 (12.2)
418 (5.9)
>418 (5.9)
Quinolones in the last 6 monthsYes15 (5.0)
No287 (94.7)
Do not know1 (0.3)
Supplementary boxYes36 (11.9)
No267 (88.1)
Urine dipstick realizedYes44 (14.5)
No259 (85.5)
Urine culture realizedYes108 (35.6)
No195 (64.4)
Hygienic and dietary rules explainedYes171 (56.4)
No132 (43.6)
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Piraux, A.; Hammoud, R.; Riou, J.; Lebdai, S.; Faure, S. Assessment of the Compliance of Cystitis Management According to French Recommendations through the Analysis of Prescriptions Collected in Community Pharmacies. Antibiotics 2022, 11, 976. https://doi.org/10.3390/antibiotics11070976

AMA Style

Piraux A, Hammoud R, Riou J, Lebdai S, Faure S. Assessment of the Compliance of Cystitis Management According to French Recommendations through the Analysis of Prescriptions Collected in Community Pharmacies. Antibiotics. 2022; 11(7):976. https://doi.org/10.3390/antibiotics11070976

Chicago/Turabian Style

Piraux, Arthur, Ramy Hammoud, Jérémie Riou, Souhil Lebdai, and Sébastien Faure. 2022. "Assessment of the Compliance of Cystitis Management According to French Recommendations through the Analysis of Prescriptions Collected in Community Pharmacies" Antibiotics 11, no. 7: 976. https://doi.org/10.3390/antibiotics11070976

APA Style

Piraux, A., Hammoud, R., Riou, J., Lebdai, S., & Faure, S. (2022). Assessment of the Compliance of Cystitis Management According to French Recommendations through the Analysis of Prescriptions Collected in Community Pharmacies. Antibiotics, 11(7), 976. https://doi.org/10.3390/antibiotics11070976

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