Volume 121, Issue 3, March 2017, Pages 250–256
Open Access
Highlights
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- Quality of government is associated with consumption of antibiotics in European regions.
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- The association is persistent when controlling for socioeconomic development and health system quality.
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- Dysfunctional public institutions partly accounts for between-region variation in antibiotic consumption.
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- Policy-makers interested in prudent use of antibiotics should pay attention to governance.
Abstract
The
aim of this article is to investigate the association between
corruption and antibiotic use at sub-national level. We explore the
correlation between, on the one hand, two measures of corruption
(prevalence of corruption in the health sector and prevalence of bribes
in the society) at regional level from the European Quality of
Government Index; and, on the other, the consumption of antibiotics in
those European regions from a 2009 Special Euro Barometer. In a
multivariate regression model, we control for potential confounders:
purchasing power of standardized regional gross domestic product,
inhabitants per medical doctor and age-standardized all-cause mortality
rates. We find that there is a strong positive association between both
measures of corruption (i.e. in the health sector, and in the society at
large) and antibiotics use; and that this association is robust to the
introduction of the control variables. These results support previous
findings in the literature linking corruption to higher antibiotic use
at cross-national level. We show that corruption does seem to account
for some of the remarkable between-region variation in antibiotic
consumption in Europe.
Keywords
- Antibiotic use;
- Corruption;
- Bribery;
- Europe;
- Regions
1. Background
Antibiotic
resistance – an unavoidable side effect of the consumption of
antibiotics – is one of the greatest global challenges to public health.
Increasing bacterial resistance to existing antibiotics causes
substantial morbidity and mortality and increases health care and
societal costs. As the World Health Organization (WHO) points out, “a
post-antibiotic era—in which common infections and minor injuries can
kill—far from being an apocalyptic fantasy, is instead a very real
possibility for the 21 st century” [1].
In Europe alone, antimicrobial resistance is estimated to cause 25,000
deaths each year and result in related costs of over €1.5 billion in
healthcare expenses and reduced productivity [2] while, in the US, it is estimated to cause 2 million illnesses and 23,000 deaths per year [3].
If resistance is left unchecked, a conservative estimate is that by
2050 an additional 10 million people are expected to die every year and
the cumulative cost − among other, increased complications, waste,
lengthier hospital stays and the development of more expensive drugs −
will be more than one and a half times annual world Gross Domestic
Product today (GDP) [4]. In other words, “rarely has modern medicine faced such a grave threat” [5].
There
is a recognition that limiting antibacterial resistance is far from
just a medical concern but rather a behavioural and social problem.
Since consumption of antibiotics is considered to be the main driver of
the development of antibacterial resistance [6], large-scale behavioural change in relation to antibiotic consumption is urgently called upon.
In
a European perspective, there is a huge variation in outpatient
antibiotic consumption, variation in the class of antibiotics, dosage
and treatment duration, and variation in the quality of outpatient
antibiotic consumption between European countries [6]; [7]; [8]; [9]; [10] ; [11]. This variation is unlikely to be the result of differences in the frequency of bacterial infections [6].
Take for instance Belgium and the Netherlands, which exhibit remarkable
differences in antibiotic use, with the former using them to a much
larger extent than the latter.
What
could possibly account for this heterogeneity? Some researchers
emphasize differences in regulatory practices and healthcare systems [6]; [7] ; [12]
while for others it is ineffective healthcare systems and poor
enforcement of regulations what might explain the widespread
non-prescription sales of antibiotics that are prevalent in many
European countries [6]. There is also a growing literature exploring the effects of corruption on health care [13] ; [14].
A pioneering analysis of a panel data set including 28 European
countries found that “corruption is the main socioeconomic factor that
explains antibiotics resistance” [15],
leading the authors to conclude that addressing corruption and
improving governance will lead to a reduction in resistance to
antibiotics. Moreover, a report from the European Commission (2013, p.
146) explicitly brings up increased antimicrobial resistance as possibly
being the result of improper market relations, since promotion of
pharmaceutical products create loyalty and may trigger
over-medicalization [16].
However,
the literature linking corruption and antibiotics abuse has not taken
into consideration sub-national differences. And we know from other
studies that there are both very large within-state variations in levels
of corruption [17] and consumption of antibiotics [11] ; [18].
For example, there are pronounced differences across regions within the
same country, such as the very high levels of antibiotic consumption in
Spain’s Catalonia (or Italy’s Lazio) and the moderate levels in Spain’s
Basque Country (or Italy’s Tuscany). The picture emerging from these
findings is thus more nuanced than the conventional view that the rates
of antibiotic use and resistance “remain low in northern European
countries” while “reaching alarming levels in Southern and Central
Europe” [6].
In
general, the aim of this paper is to provide a more detailed map of the
relationship between corruption and antibiotic consumption—by examining
over 100 European regions instead of countries. Despite causality
cannot be established in a cross-sectional study like the one presented
here, our findings do indeed question the validity of national-level
explanations of both corruption and antibiotics use, either
institutional (e.g. the national health care system) or cultural (e.g.
the national language).
In
particular, the goal of this paper is to investigate the association
between two regional measures of corruption – prevalence of corruption
in the health sector and prevalence of bribes in the society – and
consumptions of antibiotics in the European regions. This paper uses
novel data from the European Quality of Government Index [17]
that collect perceptions of the prevalence of bribes in the public
sector in general and the prevalence of corruption in the health sector
in regions of Europe. The data shows a strong bivariate association
between these measures of corruption at the regional level and
consumption of antibiotics in European regions—with data from a special
2009 Euro-Barometer survey on antibiotic consumption. When controlling
in multivariate regression models for multiple confounders – e.g.
purchasing-power standardized regional GDP per capita, inhabitants per
medical doctor, age-standardized mortality rates – the associations
between regional corruption and antibiotic consumption remain persistent
and strong.
2. Methods
2.1. Independent variables
We
test proxies for both indicators of corruption: the perception of
corruption in the healthcare sector; and citizens’ reported experience
of bribery. Data come from a survey data of about 85,000 EU citizens
distributed in all the 206 NUTS-1 and NUTS-2 (Nomenclature des Unités
Territoriales Statistiques) regions in Europe. Making use of telephone
interviews in the local language of each region, randomly drawn
respondents 18 years of age or older were asked questions relating to
Quality of Government on the one hand and questions about demographics
on the other. The survey was administered beginning in February 2013 and
sampled 400 or more respondents in each region. The robustness and
external validity of the data have been verified thoroughly [17].
To
measure the perception of corruption in the healthcare sector,
respondents were asked to rate on a 10-point scale the extent to which
they agreed or disagreed with the following statement: ‘Corruption is
prevalent in the public healthcare system in my area’ (agree/disagree
0–10). In the empirical analysis, higher scores indicate lower levels of
healthcare sector corruption. To measure citizens’ reported experience
with bribery, the following question was asked: ‘In your opinion, how
often do you think other citizens in your area use bribery to obtain
public services?’ Respondents were asked to answer on a 10-point scale
(never/often 0–10). In the empirical analysis, higher scores indicate
higher levels of bribery. The indicators of perceptions of corruption in
the healthcare sector and perceptions of the prevalence of bribes in
the society were aggregated from the individual level to the regional
level as the mean score. The indicators are highly but far from
perfectly correlated (Pearson's R 0.7430). This signifies that, although
related, the indicators seem to measure different aspects of
corruption. To increase comparability, the measures were also
standardized so that the mean is 0 and the standard deviation is 1.
The
measure of corruption in the healthcare sector ranges from the
Hovedstaden region in Denmark (1.825, very low levels of healthcare
sector corruption) to the region of Yugozapaden in Bulgaria (−2.268,
very high levels of healthcare sector corruption). The measure of
bribery in society ranges from the region of Midtylland in Denmark
(0.926, very low levels of bribery) to the region of Bucuresti-Ilfov in
Romania (4.624, very high levels of bribery).
2.2. Dependent variable
The
Special Eurobarometer 338 was in field between 13 November and 9
December 2009 and included residents aged 15 years or above in all the
27 EU member states. The survey concerned the use of antibiotics by
Europeans, public knowledge and perceptions about antibiotics, and the
impact of antibiotic awareness campaigns on the knowledge and practices
of Europeans related to antibiotics. To measure antibiotic consumption,
the following question was asked in the survey: ‘Have you taken any
antibiotics orally such as tablets, powder or syrup in the last 12
months?’ In total, about 40% of all respondents answered that they had
taken antibiotics during the past year. The answers to the question were
aggregated to the regional level by means of the survey question
regarding respondents’ region of residence.
2.3. Confounders
In
the multivariate analysis, the confounders of purchasing power
standardized regional gross domestic product (GDP), inhabitants per
medical doctor and age-standardized all case mortality rates were
included in the model because they are likely to be correlated with both
the main independent variable, corruption, and the main dependent
variable, antibiotic consumption [14] ; [19].
The
data on purchasing power standardized regional GDP 2011, inhabitants
per medical doctor and age-standardized all case mortality rates
2008–2011 were obtained from Eurostat’s statistical depository.
2.4. Statistics
In
the bivariate analysis, scatter plots were constructed to illustrate
the association between the two dependent variables, prevalence of
corruption in the health care sector and prevalence of bribes, and
antibiotic consumption in the European regions.
Pearson's
R was calculated to investigate the correlation between these
variables. Ordinary least square (OLS) regression models were used in
the multivariate analysis, so as to investigate the link between the
independent variables and antibiotic consumption, while controlling for
the regional measures of purchasing power standardized regional GDP,
inhabitants per medical doctor and age-standardized all case mortality
rates.
The
correlations between the independent variables were generally low or
moderate in strength. The correlation between regional GDP and mortality
rates turned out to be the strongest (0.692). However,
multicollinearity diagnostics show that all Variance Inflation Factors
(VIFs) were below 2.5.
In
total, indicators for both corruption/bribery and antibiotic
consumption were available for 172 regions. However, to limit the
residual from biased estimations of antibiotic consumption from regions
with few respondents in the Eurobarometer survey, regions in which there
were fewer than 50 answers were excluded from the analysis. The
bivariate analysis consists of 117 regions, and 88 in the multivariate
analysis. However, all analyses were also carried out including regions
with few Eurobarometer respondents, and the difference between the
restricted sample and the full sample is limited.
3. Results
3.1. Bivariate analysis
Fig. 1
shows the bivariate correlation between the prevalence of corruption in
the health sector and antibiotic use in the European regions. Low
values in the X-axis indicate that individuals perceive that there is a
great deal of corruption in their region (e.g. Campania, Vest), and high
values correspond to perceptions of low corruption (e.g. Hovedstaden,
Sjaelland). The correlation between these variables is −0.422 and
significant at the 0.001 level. Individuals living in regions with high
corruption in the health sector report consuming more antibiotics than
individuals in regions with lower levels of corruption.
- Fig. 1.Corruption in in the health sector and antibiotic use in the European regions, N = 117.Regions with fewer than 50 respondents were excluded.Source: European Quality of Government Index 2013 and Special Eurobarometer 338.
Fig. 2
displays the bivariate correlation between prevalence of bribery and
antibiotic use in the European regions. Low values in the X-axis
indicate high levels of bribery in the region (e.g. Bucuresti-Ilfov,
Yugozapaden), and high values correspond to low levels of bribery (e.g.
Mecklenburg-Vorpommen, Ita-Suomi). The correlation is −0.435 and is
significant at the 0.001 level. Individuals experiencing that bribery is
common in their region report consuming more antibiotics than
individuals in regions where bribery is less prevalent.
- Fig. 2.Bribery and antibiotic use in the European regions, N = 117.Regions with fewer than 50 respondents were excluded.Source: European Quality of Government Index 2013 and Special Eurobarometer 338.
3.2. Multivariate analysis
In
order to check whether the bivariate correlation between corruption (or
bribery) and antibiotic consumption is spurious, we perform a
multivariate analysis where we control for alternative factors that
could explain divergences in antibiotic consumption, according to the
literature [24]. Table 1
shows that the negative association between corruption in the
healthcare sector and antibiotic consumption is highly significant even
when we control for the level of regional economic development (per
capita GDP in the regions) and measures of the quantity (inhabitants per medical doctor) and the quality (age-adjusted all case mortality rates)
of the healthcare system. It is noteworthy that there was no
significant association between medical doctors per capita and
antibiotic consumption. Yet there was a significant negative association
between age-adjusted all case mortality rates and antibiotic
consumption. Moreover, there was no significant association between the
regional per capita GDP and antibiotic consumption.
- Table 1. Multivariate regression coefficients and standard errors of antibiotic consumption in the regions according to corruption in the healthcare sector, purchasing power standardized regional gross domestic product (GDP), inhabitants per medical doctor and age-standardized all case mortality rates.
Variable Beta S.E. 95% conf. int. Corruption in the healthcare sector −10.314*** 1.491 −13.280 to 7.348 GDP in the regions (in €1000) −0.075 0.162 −0.398 to 0.247 Inhabitants per medical doctor 0.021 0.117 -0.002 to 0.443 Age-adjusted all case mortality rates −0.026*** 0.006 −0.004 to 0.002 Constant 61.065*** 9.409 42.351–79.779 N 88 R2 0.398 - Levels of significance *P < 0.05; **P < 0.005; ***P < 0.001. Regions with fewer than 50 respondents were excluded.
- Source: European Quality of Government Index 2012, Special Eurobarometer 338, and Eurostat.
Table 2 is a copy of Table 1
except that, this time, the measure of bribery is used as an
independent variable. The results are similar. There is a highly
significant and strong negative association between bribery and
antibiotic consumption, even when controlling it for the prevailing
confounders in the literature for which we have data at the regional
level. In this case, antibiotic consumption is not only significantly
and negatively associated with the quality of the health at the regional
level (age-adjusted all case mortality rates) and with the level of economic development (per capita GDP in the regions), although the level of significance is lower. No significant association was found between inhabitants per medical doctor and antibiotic consumption.
- Table 2. Multivariate regression coefficients and standard errors of antibiotic consumption in the regions according to bribery, purchasing power standardized regional gross domestic product (GDP), inhabitants per medical doctor and age-standardized all case mortality rates.
Variable Beta S.E. 95% conf. int. Bribery −7.125*** 1.089 −9.29 to −4.960 GDP in the regions (In €1000) −0.375* 0.158 −0.690 to −0.060 Inhabitants per medical doctor 0.001 0.011 -0.221 to 0.234 Age-adjusted all case mortality rates −0.026*** 0.006 −0.038 to −0.014 Constant 75.915*** 9.990 56.045–95.784 N 88 R2 0.374 - Levels of significance *P < 0.05; **P < 0.005; ***P < 0.001. Regions with fewer than 50 respondents were excluded.
- Source: European Quality of Government Index 2012, Special Eurobarometer 338, and Eurostat.
4. Discussion
If a great variation in antibiotic use across European countries has been found in numerous previous studies [6]; [7]; [8]; [9]; [10] ; [11], our analysis corroborates others that also noted a great variation at the sub-national level [11] ; [18].
Similarly to these studies, this variation is unlikely to be explained
by differences in the frequency of bacterial infections. Take, for
instance, the remarkable divergences between the neighbouring regions of
Lazio and Toscana, or between Wallonie/Brussels and Flanders. Their
pronounced differences in antibiotics consumption cannot either be
accounted for by national cultural factors. Neighbouring regions within
the same country behave very differently, and the question is why.
In
order to address this puzzle, we have followed a growing interest among
health researchers and policymakers in how corruption affects health
outcomes [20]. Corruption has been found to be negatively associated with a large variety of healthcare outputs and outcomes [14]; [20]; [21]; [22]; [23]; [24] ; [25].
The effects of corruption may matter as much as – or even more than –
traditionally explored factors such as health-spending measures [14] or the level of democratization [26].
Corruption is not only confined to developing countries; “corrupt
practices in the health-care plague many developed countries” [14].
In
particular, this study has explored the statistical association between
antibiotic consumption and two measures of corruption. The analysis
shows a significant and strong negative association between these
measures of corruption and antibiotic consumption. The percentage of the
population stating that they have consumed antibiotics in the past year
was significantly lower in regions with low levels of corruption, both
when corruption is measured as the perception of corruption in the
health sector and when corruption is measured as a direct experience
with bribes.
To
minimize the possibility of a spurious relationship, we include
multivariate OLS regression models controlling for potential
confounders, such as the level of economic development (measured by the
regional GDP per capita) and the quality of the healthcare in the region
(measured by the number of inhabitants per medical doctor and
age-standardized all case mortality rates). The association between the
two independent variables (corruption in the health sector and bribery)
and the dependent variable (antibiotic consumption) is found to be
persistent and strong when it is also subjected to these controls.
What
are the mechanisms connecting high levels of corruption and high
antibiotic consumption? The data presented here cannot identify the
particular mechanisms, but, unlike previous studies we find an
association between two different proxies for corruption (corruption in
the health sector and bribery), thus indicating that the mechanisms may
be multiple. Those mechanisms have been pointed out in the literature.
In general, several scholars have noted that a characteristic of
healthcare is the prevalence of problems of asymmetric information that
give opportunities for abuse [14].
Different players may take advantage of their privileged position for
personal gain, including the government regulator, the payer (social
security, private or public health insurance), the provider (public or
private), the drug and equipment suppliers, and the patients [27].
In
the first place, researchers have remarked that corruption in the
supply of pharmaceutical could explain the connection between overall
levels of corruption in a country and its health outcomes [25]. The existence of an influential market of vendors and pharmaceutical firms creates a risk of bribery [28],
and the discretion that health professionals have in deciding what
medicines, and in what quantities, are needed increases the opportunity
for abuse [20].
Physicians may become both psychologically and financially dependent on
pharmaceutical firms as a result of gifts, and physicians may
reciprocate by prescribing drugs of those pharmaceuticals [13] ; [29].
These mechanisms may help to explain the link between measures of
corruption in the health sector and antibiotic abuse. In addition,
scholars also note that the relation between patients and health
professionals also presents risks of bribery, as a result of information
asymmetries and a demand for health services, which is largely
inelastic [20].
Consequently, patients can ask, or be asked to, follow inappropriate
procedures (e.g. antibiotics) in exchange for under-the-table payments [30].
These mechanisms may help to explain the link between measures of
patients’ direct experience with corruption (i.e. bribery) and
antibiotic abuse.
4.1. Strengths and limitations
This
study is the first to investigate the link between regional levels of
health system corruption/prevalence of bribery and consumptions of
antibiotics. In the light of large regional variation in both prevalence
of corruption and consumptions of antibiotics in Europe, this study is
an extension of prior findings about the link between corruption and
antimicrobial resistance at the national level [15].
Even so, the study has several limitations. The current study may be
sensitive to ecological fallacy, i.e. to draw inferences about an
individual level relationship based on aggregated data analysis. Future
studies might address the relationship between corruption and individual
consumption-patterns of antibiotics. Moreover, residual confounding
from availability of non-prescription of antibiotics may account for
part of the co-variation between corruption and antibiotic consumption.
Additionally, social desirability might influence on respondents
answering the question about their own consumption of antibiotics.
Lastly, the relationship between corruption and antibiotic consumption
could be spurious to cultural factors, such as cultural dimensions,
that, in cross-country analyses, have been found to affect – or, to be
more precise, to be statistically correlated, since the causation of
culture is inherently difficult to falsify – both for explaining
corruption and quality of governance [31] and antibiotic use [32].
Future research with reliable regional data on cultural dimensions
should help to disentangle the relations, and the direction of the
causal arrow, between corruption, cultural values, and health outcomes
such as antibiotic consumption.
5. Conclusions
Using
novel data from the European Quality of Government Index, the paper
finds that indicators of corruption – the prevalence of corruption in
the health sector and prevalence of bribes in the relations between
citizens and public institutions – are strongly and positively linked to
consumption of antibiotics. The association between corruption in the
health sector (and the extension of bribery in the society) and
antibiotic consumption is found to be persistent and strong also when
controlling for indicators of socioeconomic development as well as the
quality of the healthcare system. This paper thus shows that
dysfunctional public institutions seem to be factors accounting for some
of the notable sub-national variation in antibiotic consumption across
Europe. Consequently, policy-makers interested in promoting a prudent
use of antibiotics should pay attention to the role of governance and
corruption.
Competing interests
There are no competing interests.
Funding
Funding
for this research comes from institutional grant (V. Lapuente) and from
the NORFACE WSF project ‘The Paradox of Health State Futures HEALTHDOX’
funded by the Swedish Research Council (462-14-076) (B. Rönnerstrand).
We would also like to express our appreciation to Gunnar Jacobsson,
Karsten Vrangbæk and two anonymous reviewers for very useful comments
and suggestions.
Appendix A. Supplementary data
The following is Supplementary data to this article:
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© 2017 The Authors. Published by Elsevier Ireland Ltd.
