Association between gifts from pharmaceutical companies to French general practitioners and their drug prescribing patterns in 2016: retrospective ...
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RESEARCH
Association between gifts from pharmaceutical companies to
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
French general practitioners and their drug prescribing patterns
in 2016: retrospective study using the French Transparency in
Healthcare and National Health Data System databases
Bruno Goupil,1 Frédéric Balusson,2 Florian Naudet,3,4 Maxime Esvan,3 Benjamin Bastian,1,3
Anthony Chapron,1,3 Pierre Frouard1
1
Department of General ABSTRACT the GP groups with at least one gift in 2016 (−€5.33
Medicine, University of Rennes OBJECTIVE (99.9% confidence interval −€6.99 to −€3.66)
1, Rennes, France To evaluate the association between gifts from compared with the GP group with gifts valued at
2
EA 7449 (Pharmaco- pharmaceutical companies to French general €1000 or more reported in 2016) (PRESEARCH
version of the Sunshine Act legislation was implemented database and data from the National Health Data
in 2011, including the introduction of the Transparency System. From the Transparency in Healthcare database
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
in Healthcare database.1 6 (www.data.gouv.fr), we calculated the total monetary
The National Health Data System (Système value of the gifts listed for each French GP in 2016. We
National des Données de Santé) can be used to also included GPs without any gift listed for 2016. For
analyse drug prescribing by French doctors.7 This such GPs, we calculated the total monetary value of
database is used for multiple purposes, including the the gifts received from 2013 to 2015, to differentiate
calculation of drug prescription efficiency indicators between those who did not and those who did receive
for doctors’ performance related financial incentives gifts between 2013 and 2016.
(Rémunération sur Objectif de Santé Publique).8 Under an agreement with the National Health
The Transparency in Healthcare and National Health Insurance (the French system that offers healthcare
Data System databases (box 1) offer an opportunity coverage to all citizens), one of its data officers
to investigate the influence of gift donations on the extracted from the National Health Data System the
prescribing patterns of French general practitioners drug prescription efficiency indicators used for the
(GPs). We evaluated the association between gifts performance related financial incentives, the amount
reported in the Transparency in Healthcare database reimbursed for drug prescriptions per visit (to the practice
and prescribing by French GPs in 2016. As promotional or at home) in 2016, and data on the sociodemographic
activities by pharmaceutical companies are expected characteristics of the GPs and patients. Data in the
to influence the quality, quantity, and cost of drug National Health Data System are anonymised.
prescribing, we hypothesised that an association exists We focused on 2016 data because of the long
between the donations of gifts and poorer quality and administrative procedure to obtain authorisation to
more costly prescribing patterns. access the National Health Data System. Our first
application was submitted on 31 August 2017, and a
Methods protocol detailing the analysis plan was registered on
Data sources 17 January 2018. Ethical approval for the study was
This retrospective study was conducted using data provided on 24 May 2018. Data were available on a
on gifts reported in the Transparency in Healthcare secured remote portal on 21 November 2018.
Box 1: Databases and definitions
Transparency in Healthcare
• This database was created after the introduction of the French “Sunshine Act” in 2011 and is managed by the French
ministry of health
• Since 2013, all data declared by pharmaceutical, medical device, and other health related companies on their
financial links with healthcare professionals and organisations are collected and made accessible
• Companies must complete a declaration
• Data are searchable through a French government public website (transparence.sante.gouv.fr) and can be
downloaded (data.gouv.fr)
Gifts
• One of the information types reported in Transparency in Healthcare
• Any type of present or payment given by a company to a healthcare professional without any counterpart, such as
performing a work or a service
• Gifts include donations of equipment, invitations, catering expenses, travel expenses, and cash payments such as
commissions, rebates, or reimbursement of expenses
• Presents and payments must be declared by companies, starting from €10.00 (£8.60; $11.00) including taxes
(date, amount, type of donation, identity of the receiver, identity of the company)
National Health Data System
• This database was created and is managed by the French National Health Insurance system
• Information is collected on all reimbursement claims from French healthcare insurances
• The database includes, for example, anonymised data on patients, data on prescribers, visits to the practice or at
home, dispensed and reimbursed drugs, chronic medical conditions
• 99% of the French population is covered by the database
• The data are used to calculate the drug prescription efficiency indicators for the French performance related financial
incentives programme
• Anonymous data are accessible for research purposes on a secure portal, after authorisation
French performance related financial incentives programme
• This programme is based on data from the National Health Data System and was launched in 2011
• The aim of the programme for doctors (Rémunération sur Objectifs de Santé Publique) is to encourage more efficient
drug prescription patterns and to control health expenditure
• The programme uses drug prescription indicators to assess GPs’ prescription patterns
• Over-the-counter drugs are not included in the drug prescription indicators
2 doi: 10.1136/bmj.l6015 | BMJ 2019;367:l6015 | the bmjRESEARCH
Study population or of limiting the cost of prescriptions, particularly by
We included GPs who had worked in metropolitan promoting generic drugs.8 We considered these 11
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
France or overseas territories from 1 January 2016 to efficiency indicators (11 variables) and the amount
31 December 2016. To obtain a homogeneous study reimbursed by the National Health Insurance for the drugs
population, we excluded those who were not family prescribed and dispensed per visit in 2016 (one variable)
doctors (eg, allergists, angiologists, geriatricians, as outcomes of interest. Table 1 and supplementary
emergency doctors, and others listed by the National appendix 1 provide details on the indicators.
Health Insurance), did not work exclusively in the
private sector (unlike standard practice in France; that Covariates
is, GPs employed by a public healthcare institution or We adjusted for several covariates in the National Health
who worked in both the private sector and a public Data System that could influence drug prescriptions. The
healthcare institution), worked for part of 2016, and covariates related to the GPs’ characteristics were sex,
had fewer than five registered patients. These exclusion age, size of the city where the practice is located (RESEARCH
Table 1 | Outcomes of interest. Data are for patients registered with each general practitioner (GP) in 2016
Outcomes of interest Calculations What high values indicate
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
Cost of all drugs prescribed by GP, dispensed and reimbursed to patient by the National
Amount reimbursed for drug prescriptions/visit (€) More health expenditures
Health Insurance, divided by number of visits by the GP (€)
11 indicators used for the performance related financial incentives programme
Number of antibiotic prescriptions to 16-65 year old patients without chronic disease
Antibiotics to 16-65 year olds (%)
compared with total number of 16-65 year old patients without chronic disease (%)
Number of patients with a new prescription of benzodiazepines for more than 12 weeks
Benzodiazepines >12 weeks (%)
compared with total number of patients (%)
More side effects or more misuse
Number of patients older than 65 years with one or more prescriptions of long half-life
Benzodiazepines to >65 year olds (%)
benzodiazepines compared with total number of patients older than 65 years (%)
Number of patients older than 65 years with one or more prescriptions of vasodilators
Vasodilators to >65 year olds (%)
compared with total number of patients older than 65 years (%)
Angiotensin converting enzyme (ACE) inhibitors/ Number of ACE inhibitors items prescribed compared with total number of ACE inhibi-
ACE inhibitors+sartans (%) tors and sartans items prescribed (%)
Number of patients with prescriptions for low dose aspirin compared with total number
Antiplatelets (%)
of patients treated with antiplatelet drugs (%)
Number of antibiotic items prescribed as generic drugs compared with total number of
Generic antibiotics (%)
antibiotic items prescribed (%)
Number of antidepressant items prescribed as generic drugs compared with total num-
Generic antidepressants (%) Fewer health expenditures
ber of antidepressant items prescribed (%)
Number of antihypertensive items prescribed as generic drugs compared with total
Generic antihypertensives (%)
number of antihypertensive items prescribed (%)
Number of PPI items prescribed as generic drugs compared with total number of PPI
Generic proton pump inhibitors (PPIs) (%)
items prescribed (%)
Number of statin items prescribed as generic drugs compared with total number of
Generic statins (%)
statin items prescribed (%)
gifts, we performed multivariate analyses by replacing included for analysis. The name and practice postal
the different groups by the median monetary value of code for 3338 listed GPs (6.2% of the sample) could
gifts for each group (the no gift group and the pre-2016 not be matched to data in the National Health Data
gift group (ie, no reported gifts in 2016, but at least one System. These doctors belonged more often to the no
gift between 2013 and 2015) were grouped together as gift group (16.4%) than to the other groups (range 2.5-
having received no gift in 2016). To test the effect of 5.3%). A further 9168 GPs were excluded according to
extreme values on the results we performed the post the exclusion criteria (fig 1). Supplementary appendix
hoc sensitivity analyses after excluding the first and 2 summarises the steps leading to the selection of the
last centiles of each explanatory variable and covariate. GP groups.
Statistical analyses were performed using SAS
software 9.4 (SAS Institute, Cary NC). As we were not Description of study population
allowed to export the National Health Data System The mean age of included GPs was 53.5 (SD 10.2)
data, we analysed the information in the National years, 26 614 (64.5%) were men and 12 857 (31.2%)
Health Data System remote portal. practised in rural areas. In 2016, the GPs carried
out a mean 5359 (SD 2510) visits and had 1177
Changes to the protocol (SD 577) registered patients. Among the 41 257 GPs
We updated the Transparency in Healthcare data included in the study, 27 512 (66.7%) were listed in
on 5 April 2018. This slightly changed the size of the Transparency in Healthcare database as having
the different GP groups. As GPs with fewer than five received gifts in 2016, and 36 232 (87.8%) as having
patients were not eligible for performance related received gifts since the launch of the database in 2013.
incentives, we excluded them from the analysis. In Comparison of the GPs and patients’ characteristics
multivariate analyses we had to split patients in to two (variables used for adjustment) using the analysis
age groups (RESEARCH
53 763
GPs paired in National Council of the College of Physicians list and Transparency in Healthcare database
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
3338
Failed to match name and postal code
with National Health Data System
50 425
GPs paired with National Health Data System
9168
Excluded from analysis
2414 Non-exclusive private sector
220 Particular mode of exercise
1377 Worked part of 2016
3367RESEARCH
Table 2 | Primary analyses. Values are means (standard deviations)
Study groups P values
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
Outcomes All
No gift Pre-2016 gift €10-€69 €70-€239 €240-€999 ≥€1000 Univariate Multivariate
Amount reimbursed for drug prescriptions/
45.8 (40.1) 47.8 (24.4) 48.2 (21.8) 49.4 (21.5) 51.5 (22.0) 53.2 (21.0) 49.1 (25.3)RESEARCH
by pharmaceutical companies.10 Finally, compared solution to health problems.2 In other words, receiving
with the no gift group no difference was found in the gifts from a company might not only be the direct cause
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
percentage of antibiotic prescribed for patients aged of a prescription pattern, but also be a symptom of a
16 to 65 years and of long half-life benzodiazepines for general behaviour.
patients older than 65 years. Our literature search did not find a unique or validated
indicator to evaluate the GPs’ drug prescription quality
Strengths and limitations of this study in a general way.16 Therefore, we used multiple
This study has several strengths. We tried to reduce indicators validated by the French National Health
confounding bias by taking into account the main Insurance to assess prescribing patterns.8 Some of
available confounders in the multivariate analysis.9 them are also used in drug utilisation studies.17 Their
The use of databases is an effective way to explain and validity is, however, questionable.18
highlight differences in prescribing patterns that are Performance related financial incentive indicators
minimised in declarative studies where doctors are were not available for 0.64% to 3.04% of GPs, which
directly interviewed on the influence of promotional roughly corresponds to the 2.8% of refusals from
activities by pharmaceutical companies.2 The external doctors to collaborate in this process.19 Such missing
validity of our results is shown by concordance data may be associated with the gifts perceived and
between the mean values for the indicators in our also with the GP’s pattern of drug prescribing.
population and those of the national averages.11 French GPs may benefit from industry (eg, gifts)
Our study has some limitations. We do not know and from the National Health Insurance through the
whether all gifts were mentioned or the extent of performance related financial incentive programme.
misinformation in the Transparency in Healthcare Gifts from industry and the performance related
database because data are only based on the financial incentives programme cannot be directly
statements made by the pharmaceutical companies linked to each other because no indicator assessed
without effective control.5 The 6.2% of failed matches GPs’ financial links with industry. A GP might receive
for GPs might have introduced some bias, especially the maximum remuneration from the performance
because the matching failure rate was different among related financial incentive programme and
the GP groups. concomitantly many gifts from industry. Nevertheless,
Confounding is a major problem in observational if we assume that the desire of profit is a confounder,
research. Methods, such as computation of E-values our results are not suggesting optimisation trade-offs
(minimum strength of association that an unmeasured by GPs. Indeed, in our study GPs with the best drug
confounder would need to have with both treatment prescription indicator results and therefore the highest
and outcome to fully explain away a specific treatment- National Health Insurance financial incentive for these
outcome association, conditional on the measured indicators seemed to receive fewer gifts from industry.
covariates), have been proposed but have caveats.12 Finally, it is not possible to conclude that the
Despite the adjustment of the analysis to various different drug prescription patterns are the result of the
available factors that might influence prescribing promotional activities by pharmaceutical companies.
patterns, we could not take all of them into account. For An alternative explanation could be that GPs who
example, we did not include type of GP activity (in a group receive gifts may be more targeted or receptive to
or alone), status of university internship supervisor, or pharmaceutical marketing because they have specific
other methods of pharmaceutical promotion. The study prescribing patterns.2 All these possible caveats
is therefore prone to residual confounding. suggest that these findings should be interpreted with
In addition, in the absence of clinical data we caution, and they preclude any definitive conclusion in
could not fully understand the reasoning leading to terms of causality.
each drug prescription.13 Other studies have shown
a link between payments from industry and specific Results consistent with the literature
prescriptions (eg, opioids, gabapentinoids).14 15 As These results are consistent with recent meta-analyses
the Transparency in Healthcare database does not and systematic reviews showing an association
specify the marketed drug or drugs associated with between gifts from pharmaceutical companies and
each listed gift, we could not link a gift to a specific more frequent, lower quality and more costly drug
prescription.5 Our study explores prescription patterns prescriptions.14 20-24 Two recent studies also found a
in a more global way. Indeed, providing gifts is not the lower prescription rate of generic drugs by doctors
only way industry uses to promote drugs. For instance, who benefit from pharmaceutical companies.25 26
sponsored medical press, advertising directed towards According to Health Action International, no study has
doctors, sponsored continuing medical education shown health benefits from promotional activities of
courses (possibly with key opinion leaders), one- pharmaceutical companies.1 2
to-one visits from sales representatives, and sample Our post hoc analyses suggest a possible dose-effect
delivery are many other methods to influence doctors’ association between gifts paid by pharmaceutical
prescribing patterns. Receiving a gift from a company companies and the cost of drug prescriptions per visit
might reflect a higher acceptance, an interest in and drug prescription efficiency indicators. A similar
novelty, a belief in the promotion, a favourable image observation was reported by two large retrospective
of the firms, and a belief in using drugs as a first studies in the United States in 2016.24 27
the bmj | BMJ 2019;367:l6015 | doi: 10.1136/bmj.l6015 7RESEARCH
Our study shows a significant difference between evaluate these features also in specialist doctors and
the group that did not receive gifts and the pre-2016 particularly among the so-called key opinion leaders.2
BMJ: first published as 10.1136/bmj.l6015 on 5 November 2019. Downloaded from http://www.bmj.com/ on 12 March 2020 by guest. Protected by copyright.
gift group for generic drug prescription of antibiotics, Perhaps the time has come for interventional studies
antihypertensive agents, and statins, suggesting that to test the impact of restrictive policies on physicians’
the observed association could also be observed over drug prescription patterns prospectively.
time.
We thank Medhi Gabbas for extracting data from the National Health
Insurance database, Elisabetta Andermarcher for English language
Health and economic impacts editing, and Emmanuel Allory, Irène Frachon, Barbara Mintzes,
The more frequent use of some drugs, such as Emmanuel Oger, Dominique Somme, and Bruno Toussaint for their
help.
benzodiazepines and vasodilators, increases the risk
Contributors: BG and PF initiated and designed the study, searched
of well known adverse effects of these drug classes, the literature, interpreted the results, and wrote the manuscript. FB
with occasional serious or fatal consequences. Our performed the analysis and interpreted results. FN and ME contributed
data suggest that prescription of these drug classes to the study design and interpreted the results. BB contributed to
the study design. AC contributed to the study design and offered
increases slowly but progressively from the no gift institutional support. PF is guarantor. All authors have critically revised
group to the €1000 or more group. Prescriptions of the manuscript for important intellectual content and approved the
brand name drugs instead of generic drugs represent manuscript. The corresponding author attests that all listed authors
meet the authorship criteria and that no others meeting the criteria
an additional cost for the National Health Insurance have been omitted.
with no proved benefit for the patient. In France, the
Funding: None.
price of a generic drug is at least 60% lower than the
Competing interest: All authors have completed the ICMJE uniform
price of the original drug.28 With an additional €1.2 to disclosure form at www.icmje.org/coi_disclosure.pdf and declare:
€5.3 reimbursed per drug prescription, GPs with gifts no financial relationships with any organisations that might have an
reported in the Transparency in Healthcare database interest in the submitted work in the previous three years; AC reports
personal fees and non-financial support from Roche, personal fees
are associated with an important additional charge for and non-financial support from Novartis Pharma, and personal fees
the National Health Insurance compared with GPs who from Congrès colloques conventions, outside the submitted work; no
did not have any gift reported. Notably, among the 12 other relationships or activities that could appear to have influenced
the submitted work.
outcomes we used, the most significant were directly
linked with economic factors: cost of drug prescription Ethical approval: This study was approved by the French Commission
Nationale Informatique et Libertés (authorisation CNIL DR 2018-089).
per visit, and generic drug prescription. This is in line A letter has been delivered to all French URPS (Unions Régionales
with studies showing that pharmaceutical promotion des Professionnels de Santé) to inform general practitioners of the
targets especially market issues.1 2 objective of the research and give them the right to oppose.
In our study, associations were also significant Data sharing: Data from Transparency in Healthcare database are
available on www.data.gouv.fr. We cannot share National Health
for the “€10-€69” group. Differences in prescribing Data System data as they are only available on a secure portal.
behaviours after donation of small gifts have been Authorisation to access this portal needs registration and clearance.
reported by several studies and are based on donation The guarantor (PF) affirms that the manuscript is an honest, accurate,
and counter-donation mechanisms that have been and transparent account of the study being reported; that no
well described by humanities and social science important aspect of the study was omitted; and that any discrepancies
from the study as originally planned have been explained.
studies.29-31 Gifts lead to a sense of accountability and
This is an Open Access article distributed in accordance with the
ultimately negatively influence prescribing habits.32 Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license,
More generally, for most doctors the amount of gifts which permits others to distribute, remix, adapt, build upon this work
reported represents a small part of their annual non-commercially, and license their derivative works on different
terms, provided the original work is properly cited and the use is non-
income, and for pharmaceutical industries a small commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
financial engagement compared with their benefits in
terms of selling drugs.2 1 Health Action International. Fact or Fiction: What Healthcare
Professionals Need to Know about Pharmaceutical Marketing in the
European Union – Health Action International. 2016. https://haiweb.
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prescriptions european-union/
2 World Health Organization, Health Action International.
Before the creation of the Transparency in Healthcare Understanding and responding to pharmaceutical promotion:
database, the scope and frequency of gifts paid by a practical guide. 2009. http://haiweb.org/wp-content/
pharmaceutical companies to French GPs were not uploads/2015/05/Pharma-Promotion-Guide-English.pdf
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