The literature shows that the prescription of antibiotics in dental care is often unnecessary or inappropriate. Indicators estimating the appropriateness of antibiotics prescribed by dentists based on routine databases are, however, not available in the literature.
KEYWORDS: antimicrobial stewardship, appropriateness, dentists, proxy indicators, quality of care
ABSTRACT
The literature shows that the prescription of antibiotics in dental care is often unnecessary or inappropriate. Indicators estimating the appropriateness of antibiotics prescribed by dentists based on routine databases are, however, not available in the literature. Our objectives were to (i) design proxy indicators estimating the appropriateness of antibiotics prescribed by dentists, (ii) evaluate their clinimetric properties, and (iii) provide results for these proxy indicators for dentists located in a northeastern French region. We selected and adapted proxy indicators from the literature. Using 2019 Regional Health Insurance data, we evaluated the proxy indicators’ clinimetric properties (measurability, applicability, and potential room for improvement), their results with performance scores (percentage of dentists who reached the target value), and the case-mix stability. We included 3,014 general dental practitioners, who prescribed a total of 373,975 antibiotics to 308,123 patients in 2019. We identified four proxy indicators estimating antibiotic prescribing appropriateness in dental care. All proxy indicators had good clinimetric properties. Performance scores were generally low (10.5 to 73.0%, depending on the indicator), suggesting important room for improvement. These results showed large variations between dentists (large interquartile ranges) and according to the patients’ characteristics (case-mix stability). These four proxy indicators might be used to guide antibiotic stewardship interventions in dental care.
INTRODUCTION
Antimicrobial resistance is considered one of the 10 threats to global public health (https://www.who.int/vietnam/news/feature-stories/detail/ten-threats-to-global-health-in-2019), and the misuse and overuse of antimicrobials is accelerating this process (https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance). In France, around 125,000 persons were infected by multidrug-resistant bacteria in 2015, and more than 5,500 of them died because of it (https://www.santepubliquefrance.fr/maladies-et-traumatismes/infections-associees-aux-soins-et-resistance-aux-antibiotiques/resistance-aux-antibiotiques). Overall, 78% of antibiotics are prescribed in primary care in France (https://www.santepubliquefrance.fr/les-actualites/2019/consommation-d-antibiotiques-et-antibioresistance-en-france-en-2018), of which 10% are prescribed by dentists. In dental care, antibiotics are recommended in a few indications, either as a curative treatment, ideally in association with a source control procedure, or as a prophylactic treatment for very specific situations (1–3). The literature shows that the use of antibiotics in dental care is often unnecessary or inappropriate (1, 4–7), highlighting the urgent need for antibiotic stewardship programs in dentistry (3, 5, 6). The FDI World Dental Federation recently published a White Paper advocating for this (https://www.fdiworlddental.org/resource/fdi-white-paper-essential-role-dental-team-reducing-antibiotic-resistance).
Antimicrobial stewardship (AMS) has been defined by Dyar et al. as a “coherent set of actions which promote a responsible use of antimicrobials” (8). A systematic review published in 2017 assessed the effectiveness of interventions aiming at optimizing the prescription of antibiotics in dental care (9). The most frequent interventions were audit and feedback, education, and guidelines. All interventions led to a decrease in antibiotic prescribing. Few studies, however, looked at the appropriateness of antibiotic prescriptions.
Evaluating the quality or appropriateness of antibiotic prescriptions is essential to guide AMS interventions. Calculating quality indicators requires information on the clinical indication/diagnosis, but computerized national systems linking drug prescriptions to clinical diagnosis are not available in most European countries (10). The evaluation of the appropriateness of antibiotic prescriptions can be done at the prescriber or facility level, but manual data collection is time-consuming. Therefore, it is usually not possible to monitor quality indicators on a large scale (regional or national) and for prolonged periods of time. To overcome this issue, Thilly et al. used routine databases from the National Health Insurance to design proxy indicators (PIs) estimating the appropriateness of antibiotic prescriptions by general practitioners (GPs) (11). PIs share characteristics of both quantity metrics and quality indicators. They are derived from quantity metrics and have the advantage of not requiring clinical data to be calculated. PIs are associated with a quantitative target that reflects the appropriateness of prescription practices: depending on whether the defined target is reached or not, the antibiotic use at the prescriber level is appropriate or not. To the best of our knowledge, indicators estimating the appropriateness of antibiotics prescribed by dentists based on routine databases are not available in the literature.
In the present study, we used a large regional routine reimbursement database to (i) design PIs estimating the appropriateness of antibiotics prescribed by dentists, (ii) evaluate PIs’ clinimetric properties, and (iii) provide performance results of these PIs for dentists located in a northeastern French region to illustrate the potential practical use of these indicators.
RESULTS
Dentist and patient characteristics.
Out of the 3,372 general dental practitioners practicing in the Grand Est region, we included 3,014 (89.4%) who met the inclusion criteria. Their mean age was 47.5 ± 12.6 years, 56.9% were men, and, on average, they were practicing for 17.7 ± 12.6 years. On average, they took care of 804 ± 391 different patients in 2019, with a mean number of 1,678 ± 802 consultations. The 3,014 included dentists prescribed a total of 373,975 antibiotics in 2019, dispensed to 308,123 patients. Regarding their patients’ characteristics, 16.7% were aged <16 years, 17.3% were aged >65 years, 0.3% lived in a nursing home, 11.8% had a chronic disease, and 7% had a low income.
Selection and operationalization of proxy indicators.
Four PIs were selected from the literature and adapted to the dental care context (11, 12). Table 1 presents the four PIs, with their numerator, denominator, and targets. PI 1 focuses on preferred prescribing of amoxicillin rather than amoxicillin-clavulanate, amoxicillin being the first-line antibiotic in most indications in dental care (2, 3). PI 2 refers to the antibiotic treatment duration, which should rarely exceed 1 week (3 days for azithromycin) (https://www.ansm.sante.fr/Dossiers/Antibiotiques/Odonto-Stomatologie/(offset)/5). PI 3 and 4 focus on antibiotics that should not be used in routine dental practice (PI 3) or should be reserved for very specific cases (PI 4), according to national guidelines (https://www.ansm.sante.fr/Dossiers/Antibiotiques/Odonto-Stomatologie/(offset)/5).
TABLE 1.
Description of the four proxy indicators estimating the appropriateness of antibiotics prescribed by dentistsa
| PI | Numerator description | Denominator description | Target value |
|---|---|---|---|
| 1, amoxicillin/amoxicillin-clavulanate (ratio) | No. of prescriptions of amoxicillin (J01CA04) | No. of prescriptions of amoxicillin-clavulanate (J01CR02) | >10 |
| 2, estimated duration of antibiotic prescriptions (%) | No. of prescriptions of >8 days for amoxicillin (J01CA04), amoxicillin-clavulanate (J01CR02), clindamycin (J01FF01), and pristinamycin (J01FG01) and >4 days for azithromycin (J01FA10) | Total no. of prescriptions for these five antibiotics | Optimal, <5%; acceptable, <10% |
| 3, prescriptions of not indicated antibiotics (%) | No. of prescriptions of lymecycline (J01AA04), minocycline (J01AA08), pivmecillinam (J01CA08), phenoxymethylpenicillin (J01CE02), cloxacillin (J01CF02), cefadroxil (J01DB05), cefuroxime (J01DC02), cefaclor (J01DC04), cefotiam (J01DC07), ceftriaxone (J01DD04), cefixime (J01DD08), cefpodoxime (J01DD13), trimethoprim-sulfamethoxazole (J01EE01), erythromycin (J01FA01), midecamycin (J01FA03), roxithromycin (J01FA06), josamycin (J01FA07), telithromycin (J01FA15), tobramycin (J01GB01), gentamicin (J01GB03), ofloxacin (J01MA01), ciprofloxacin (J01MA02), norfloxacin (J01MA06), lomefloxacin (J01MA07), levofloxacin (J01MA12), moxifloxacin (J01MA14), flumequine (J01MB07), fusidic acid (J01XC01), nitrofurantoin (J01XE01), and fosfomycin (J01XX01) | Total no. of antibiotic prescriptions | <1% |
| 4, prescriptions of rarely indicated antibiotics (%) | No. of prescriptions of pristinamycin (J01FG01), spiramycin-metronidazole (J01RA04), and doxycycline (J01AA02) | Total no. of antibiotic prescriptions | <5% |
The ATC (anatomical, therapeutic, chemical) denomination of the drugs mentioned here is presented in parentheses (https://www.whocc.no/).
For PI 1, a high fraction indicates high quality of care, while for the other PIs, a low fraction indicates high quality of care.
The scientific evidence base for the four PIs is presented in Tables S1 and S2 in the supplemental material.
Clinimetric properties of the proxy indicators.
The clinimetric properties are presented in Table 2.
TABLE 2.
Clinimetric properties of the four proxy indicators and case-mix stability (n = 3,014)
| PI | Measurability of missing data (%) | Applicability, n (%) | Improvement potentiala (%) | Case-mix stability of improvement potential for specific populations (%) |
|---|---|---|---|---|
| 1, amoxicillin/amoxicillin-clavulanate (ratio) | 0 | 2,822 (93.6) | 60.4 | Chronic disease, 80.2; low income, 89.4; nursing home, 100.0; age >65 yr, 71.8 |
| 2, estimated duration of antibiotic prescriptions (%) | 0 | 3,007 (99.8) | 37.2 | Chronic disease, 36.4; low income, 29.9; nursing home, 14.8; age >65 yr, 35.8 |
| 3, prescriptions of not indicated antibiotics (%) | 0 | 3,014 (100.0) | 27.0 | Chronic disease, 7.4; low income, 5.3; nursing home, 0.8; age >65 yr, 8.4 |
| 4, prescriptions of rarely indicated antibiotics (%) | 0 | 3,014 (100.0) | 89.5 | Chronic disease, 65.3; low income, 48.7; nursing home, 18.3; age >65 yr, 69.5 |
Improvement potential is determined as 100 – acceptable performance.
(i) Measurability.
As data required to calculate the PIs were collected from the outpatient reimbursement database of the Regional Health Insurance Fund and all antibiotics are reimbursed, we had no missing data and all the PIs were 100% measurable.
(ii) Applicability.
All PIs were applicable, i.e., scores could be calculated from at least ten clinical situations for more than 75% of dentists.
(iii) Potential room for improvement.
Improvement potential was greater than 15% for all PIs and varied between 27.0% (for PI 3) and 89.5% (for PI 4).
Overall, all four PIs had good clinimetric properties.
Appropriateness of dentists’ antibiotic prescriptions and variability.
Table 3 presents results for the four PIs. Antibiotic prescription practices were not optimal, and wide variations between dentists were observed. Performances ranged between 10.5% for antibiotics rarely indicated (PI 4) and 73.0% for antibiotics not indicated (PI 3).
TABLE 3.
Results for the four proxy indicators, calculated at the dentist level (n = 3,014)
| PI | Median | IQR (lower quartile; upper quartile) | Range (minimum; maximum) | Performance (% of dentists who reached the target) |
|---|---|---|---|---|
| 1, amoxicillin/amoxicillin-clavulanate (ratio) | 7.0 | 2.5; 17.6 | 0.0; 444.0 | 39.6 |
| 2, estimated duration of antibiotic prescriptions (%) | 5.1 | 1.1; 19.5 | 0.0; 96.9 | Optimal, 48.7; acceptable, 62.8 |
| 3, prescriptions of not indicated antibiotics (%) | 0.0 | 0.0; 1.1 | 0.0; 88.2 | 73.0 |
| 4, prescriptions of rarely indicated antibiotics (%) | 14.2 | 5.3; 37.3 | 0.0; 100.0 | 10.5 |
The results for the case-mix stability are presented in Table 2. The performance scores were influenced by the patient populations for all PIs. For PIs 2, 3, and 4, improvement potentials were lower in the specific populations (i.e., the elderly, patients with chronic diseases, patients with low income, and residents of nursing homes) compared to the general population, highlighting better prescription practices for these specific populations. In contrast, the improvement potential for PI 1 (amoxicillin/amoxicillin-clavulanate ratio) was higher for these specific populations, especially for nursing home residents.
DISCUSSION
Four proxy indicators were defined from the literature, estimating the appropriateness of antibiotics prescribed by dentists, using routine reimbursement databases, and based on national guidelines. These PIs encompass the most common clinical situations encountered in dental care and address the most frequent causes of inappropriate prescribing (6), i.e., the overuse of second-line antibiotics when guidelines recommend amoxicillin as the first-line treatment for most indications, the excessive durations of treatment, and the overuse of nonindicated or rarely indicated antibiotics, such as the spiramycin-metronidazole fixed-dose combination that is frequently prescribed in France but is not recommended in national or international guidelines (https://www.ansm.sante.fr/Dossiers/Antibiotiques/Odonto-Stomatologie/(offset)/5) (13). All four PIs showed good clinimetric properties.
We decided to focus on prescriptions by general dental practitioners. The clinical practice of oral surgeons and orthodontists and, therefore, the indications to prescribe antibiotics are very different from those of general dental practitioners. However, even when focusing on the homogeneous group of general dental practitioners, we noticed a huge variability between dentists in antibiotic prescription practices for the four PIs. The room for improvement was significant for all PIs, being particularly high for rarely indicated antibiotics (89.5%).
The evaluation of case-mix stability showed that performance scores were different depending on the characteristics of the patient population (elderly people, patients with chronic diseases, residents in nursing homes, and patients with low income), while recommendations used to define PIs and their targets are applicable for these specific populations. These results can help dentists identify, for each PI, the patient populations for whom they need most to improve their prescription practices.
To the best of our knowledge, there is only one published article dealing with quality indicators of antibiotic prescriptions in dental care. Hussein et al. designed three quality indicators of antibiotic prescriptions by German dentists in 2013, with the aim of reducing both unnecessary and inappropriate prescriptions (14). These quality indicators were developed through a literature review, an analysis of the claims data of the statutory health insurance, and a panel process with dental experts and patient representatives. The three final selected indicators were usage of systemic antibiotics in dental treatments without indication for antibiotics, the percentage of penicillin prescriptions (first-line treatment) in dental treatments, and the percentage of clindamycin prescriptions (second-line treatment) in dental treatments. The first indicator needs a specific diagnosis/clinical indication to be calculated. Moreover, a clear target is missing for all three indicators, making it difficult to truly assess the quality of care. As a consequence, our proxy indicators are innovative, as, by providing targets, they allow for an estimation of the appropriateness of prescriptions at the prescriber level.
Our PIs may be useful tools for estimating the appropriateness of antibiotic prescriptions by dentists, as they present targets reflecting the appropriateness of prescription practices. They are easily calculable from routine databases and can be used by different stakeholders to help improve antibiotic prescribing practices of dentists (e.g., by health authorities, professional organizations, AMS teams, and regional antibiotic stewardship networks), as already described in detail previously (11). These PIs may also be used in different countries by adapting their definition and target to the national prescribing guidelines, following a validation process similar to the one we used.
Contrary to GPs, who have been the target of many government-led AMS interventions over the last 20 years in France, dentists have not been targeted by such national multifaceted AMS interventions so far. Based on our results, we suggest different priorities to guide future AMS interventions among dentists. First, the PIs are useful to prioritize improvement interventions. For example, in our sample of dentists, prescriptions of nonindicated antibiotics do not seem a priority compared to the other three PIs. Second, PIs can be included in personalized audit and feedback programs and can help monitor the impact of AMS interventions. The Grand Est region in northeastern France is currently implementing a multifaceted AMS intervention called DentibioResist. This stepwise intervention, led by the Regional Health Insurance and targeting all general dental practitioners in the region, includes an information website (http://dentibioresist.online.fr/), annual audit and feedback using personalized prescription profiles, including the PIs described in the manuscript, academic detailing targeting low-performing dentists, and an e-learning training program. The literature suggests that such multifaceted AMS interventions can have a significant impact both on unnecessary and inappropriate prescribing (9, 15).
Our study is innovative but has some limitations. First, dispensations were used as a proxy for prescriptions. This can underestimate the quantity of antibiotics really prescribed if some patients do not collect their treatment from the pharmacy. Second, while being set by a multidisciplinary group of experts, the target values we selected are debatable, and a consensus procedure with a large group of stakeholders and experts might be useful to further validate these targets before using these PIs on a large scale.
To conclude, AMS interventions should urgently be implemented in dental care. Our easily calculable four PIs, showing good clinimetric properties and estimating the appropriateness of antibiotic prescriptions by dentists, could be a useful AMS tool.
MATERIALS AND METHODS
Study setting and population.
Our study focused on primary care dentists of the Grand Est region of northeastern France, with 5,550,000 inhabitants according to the 2017 census (https://www.insee.fr/fr/statistiques). In France, primary care dentists can belong to three groups: general dental practitioners (who represent 95% of dentists), oral surgeons, and orthodontists. We included in the present study the general dental practitioners who had at least 100 patients in 2019 and prescribed at least 10 antibiotics during the year.
Data source and study design.
In France, all antibiotics are prescribed and reimbursed. The National and Regional Health Insurance databases identify antibiotics dispensed by community pharmacies, prescriber specialty, and patient characteristics (e.g., age, gender, certain costly chronic diseases, and place of residence) from the prescriber and the patient identification numbers. As information on the prescription is not available, dispensation was used as a proxy for prescription. Clinical indications or diagnoses related to a prescription are not available in these databases.
We conducted a cross-sectional observational study to analyze the antibiotics prescribed by eligible dentists and dispensed by a community pharmacy during the year 2019. Data were collected from the Regional Health Insurance Fund databases (DRSM Grand Est/National Health Data System), covering 95% of the population.
Selection of proxy indicators based on the literature.
The European project DRIVE-AB used a systematic literature review and a structured international multidisciplinary consensus procedure to identify quality indicators and quantity metrics on antibiotic use. Based on the DRIVE-AB quality indicators in the outpatient setting (12) and the PIs developed previously by our team for GPs (11), a group of experts (including dentists, pharmacists, and public health and infectious disease specialists) designed PIs adapted to the dental care context.
Proxy indicators estimating the appropriateness of antibiotic prescriptions by dentists and its variability.
As detailed in our previous work (11), PIs calculated at the prescriber level could estimate the appropriateness of antibiotic prescriptions by French dentists and the variability (i.e., variation in PI scores between dentists). For each PI, target values were defined to indicate a high quality of care. The optimal target reflected 100% compliance with national guidelines, while the acceptable target reflected acceptable practices and was less restrictive, as it was considered that recommendations do not cover some specific cases. The unit of measurement at the patient level was the antibiotic treatment, i.e., the antibiotic prescribed by a dentist and dispensed by a community pharmacy on a given day in 2019. As exact days of therapy are not available in health insurance databases, the procedure for the calculation of an estimated treatment duration is presented in Tables S1 and S2 in the supplemental material and was detailed in our previous work (11).
The case-mix stability was assessed through a subgroup analysis to look at the PI scores across different patient populations. The following patient characteristics were studied: age of >65 years, presence of a chronic disease (https://www.ameli.fr/medecin/exercice-liberal/presciption-prise-charge/situation-patient-ald-affection-longue-duree/definition-ald), living in a nursing home, and presence of low income (https://www.ameli.fr/assure/droits-demarches/difficultes-acces-droits-soins/complementaire-sante/complementaire-sante-solidaire-qui-peut-en-beneficier-et-comment).
Clinimetric properties of the proxy indicators.
Three clinimetric properties were evaluated for each PI (11): measurability, applicability, and potential room for improvement.
(i) Measurability.
Measurability represents the availability of data required to calculate the PI. A PI was considered measurable if data necessary for its calculation were available for more than 75% of prescriptions.
(ii) Applicability.
A PI was applicable if the score was meaningful for the dentists, i.e., calculated from at least ten clinical situations. A PI was considered applicable if this was the case for more than 75% of dentists.
(iii) Potential room for improvement.
Potential room for improvement represents the sensitivity of a PI to detect variations in appropriateness of prescriptions between dentists and over time. It is calculated as 100% minus the performance score (i.e., the percentage of dentists who reached the PI target). A low room for improvement corresponds to a less sensitive indicator, which is less useful in routine practice. The improvement potential was considered low when it was less than 15%.
Overall, a PI with good clinimetric properties had to meet all three of the following criteria: measurability of >75%, applicability of >75%, and potential room for improvement of ≥15%.
Statistical analyses.
PI results are presented using medians, interquartile ranges (IQRs), and performance scores, i.e., the percentage of dentists who reached the optimal or acceptable targets. Measurability, applicability, and improvement potential are presented as percentages and case-mix stability as potential room for improvement for the above-mentioned specific patient populations. All analyses were performed with SAS Enterprise Guide, version 7.1 (SAS Institute Inc., Cary, NC).
Ethics statement.
The present study was observational (i.e., did not modify the medical care of patients), and complete anonymity was preserved for both patients and dentists. Therefore, an ethical committee was not required, in accordance with French law.
Supplementary Material
ACKNOWLEDGMENTS
We thank Odile Blanchard, director of the DRSM Grand Est, for her support.
Conceptualization, C.P. and N.T.; methodology, O.P., M.E.H., C.P., and N.T.; software and formal analysis, O.P.; writing–original draft, M.S.; writing–review and editing, N.T., C.P., O.P., J.G.T., M.E.H.
We have no conflicts of interest to declare.
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Footnotes
Supplemental material is available online only.
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