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Communicationtrainingandtheprescribingpatternofantibioticprescriptioninprimaryhealthcare.pdf

RESEARCH ARTICLE

Communication training and the prescribing

pattern of antibiotic prescription in primary

health care

Christoph StrumannID 1*, Jost Steinhaeuser1, Timo Emcke2, Andreas Sönnichsen3,

Katja Goetz 1

1 Institute of Family Medicine, University Hospital Schleswig-Holstein, Luebeck, Germany, 2 Association of

Statutory Health Insurance Physicians of the Federal State of Schleswig-Holstein, Bad Segeberg, Germany,

3 Department of General Practice and Family Medicine, Medical University of Vienna, Center for Public

Health, Vienna, Austria

* [email protected]

Abstract

Background

The treatment of upper respiratory tract infections (URTIs) accounts for the majority of anti-

biotic prescriptions in primary care, although an antibiotic therapy is rarely indicated. Non-

clinical factors, such as time pressure and the perceived patient expectations are consid-

ered to be reasons for prescribing antibiotics in cases where they are not indicated. The

improper use of antibiotics, however, can promote resistance and cause serious side

effects. The aim of the study was to clarify whether the antibiotic prescription rate for infec-

tions of the upper respiratory tract can be lowered by means of a short (2 x 2.25h) communi-

cation training based on the MAAS-Global-D for primary care physicians.

Methods

In total, 1554 primary care physicians were invited to participate in the study. The control

group was formed from observational data. To estimate intervention effects we applied a

combination of difference-in-difference (DiD) and statistical matching based on entropy bal-

ancing. We estimated a corresponding multi-level logistic regression model for the antibiotic

prescribing decision of German primary care physicians for URTIs.

Results

Univariate estimates detected an 11-percentage-point reduction of prescriptions for the

intervention group after the training. For the control group, a reduction of 4.7% was

detected. The difference between both groups in the difference between the periods was

-6.5% and statistically significant. The estimated effects were nearly identical to the effects

estimated for the multi-level logistic regression model with applied matching. Furthermore,

for the treatment of young women, the impact of the training on the reduction of antibiotic

prescription was significantly stronger.

PLOS ONE

PLOS ONE | https://doi.org/10.1371/journal.pone.0233345 May 19, 2020 1 / 19

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OPEN ACCESS

Citation: Strumann C, Steinhaeuser J, Emcke T,

Sönnichsen A, Goetz K (2020) Communication

training and the prescribing pattern of antibiotic

prescription in primary health care. PLoS ONE 15

(5): e0233345. https://doi.org/10.1371/journal.

pone.0233345

Editor: Martin Chalumeau, Universite Paris

Descartes, FRANCE

Received: December 20, 2019

Accepted: May 3, 2020

Published: May 19, 2020

Peer Review History: PLOS recognizes the

benefits of transparency in the peer review

process; therefore, we enable the publication of

all of the content of peer review and author

responses alongside final, published articles. The

editorial history of this article is available here:

https://doi.org/10.1371/journal.pone.0233345

Copyright: © 2020 Strumann et al. This is an open access article distributed under the terms of the

Creative Commons Attribution License, which

permits unrestricted use, distribution, and

reproduction in any medium, provided the original

author and source are credited.

Data Availability Statement: The dataset used and

analyzed during the current study is extracted from

administrative data and provided by the

Association of Statutory Health Insurance

Conclusions

Our results suggest that communication skills, implemented through a short communication

training with the MAAS-Global-D-training, lead to a more prudent prescribing behavior of

antibiotics for URTIs. Thereby, the MAAS-Global-D-training could not only avoid unneces-

sary side effects but could also help reducing the emergence of drug resistant bacteria. As a

consequence of our study we suggest that communication training based on the MAAS-

Global-D should be applied in the postgraduate training scheme of primary care physicians.

Introduction

The widespread use of antibiotics and the lack of new drug development serve as the main

causes for the emergence of drug resistant bacteria [1], limiting the effectiveness of antimicro-

bial therapy [2]. The rapid increase of resistant bacteria is regarded as one of the greatest

threats to global health [3]. Infections with antibiotic-resistant bacteria may cause higher

severity of illness, mortality rates, risk of complications, admissions to hospital, hospital length

of stay and health care costs [2, 4–7].

Especially, not indicated antibiotic use is considered to be a primary cause of increasing

risk of bacterial resistance [8]. Therefore, several initiatives address the improvement of pre-

scribing practices of antibiotics worldwide [9–11]. A prominent example for an irrational use

of antibiotics can be found in primary care, where primary care physicians (PCPs) often treat

upper respiratory tract infections (URTIs) with antibiotics [12]. URTIs are one of the most

common reasons for encounter in primary care and are mostly caused by viral infections,

making antibiotic-therapy appropriate for only a small number of high risk patients [13].

However, the treatment of URTIs accounts for the majority of antibiotic prescriptions in pri-

mary care [12, 14, 15], although there is very limited evidence for their benefits [16–18].

Besides characteristics of the physicians (e.g., specialty, training, experience), patients (e.g.,

sex, age, insurance status, comorbidities) and environmental factors (e.g. access to and quality

of care), patient knowledge and expectations, as well as the physicians’ assumptions regarding

these expectations play a crucial role in the prescribing process [19–21]. Furthermore, evi-

dence strongly suggests that antibiotic prescriptions are associated with a communication

problem. Most patients seem to possess insufficient knowledge about the difference between

viral and bacterial infections [22]. Due to the patients’ belief that a previously received antibi-

otic drug cured their infection, their expectations to receive antibiotic therapy when next pre-

senting with URTI symptoms will increase [23]. Additionally, physicians may wrongly assume

that the patient will demand antibiotics and preemptively prescribe the medicine [24–26].

Moreover, due to an overload of patients, physicians might not take the time to change the

patient’s expectations by explaining the differences between viruses and bacteria in an under-

standable and effective way [27–29]. Therefore, patient expectations could strongly influence

physicians, who are willing to prescribe an antibiotic to maintain a good relationship and to

save time [20, 30, 31].

Communication trainings have been found to be effective in decreasing the antibiotic pre-

scription rate [32–37]. Although the benefits of adequate communication skills are well

known, they are not part of the postgraduate training scheme of any medical specialty in Ger-

many [38]. In the Netherlands, a mandatory instrument for training and measuring physi-

cians’ communication and medical skills is widely used in under- and postgraduate training

[39]. This instrument, named Maastricht history taking and advice scoring list (MAAS-Glo-

bal), has been recently translated and adapted for use in Germany (MAAS-Global-D) [40].

PLOS ONE Communication training and the prescribing pattern of antibiotic prescription in primary health care

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Physicians of the Federal State of Schleswig-

Holstein. The data are secured by strict German

data protection regulation and we are not allowed

to share the data with other researchers. However,

a request to ac-cess the data for scientific

purposes and to replicate the findings can be made

to the Associa-tion of Statutory Health Insurance

Physicians (ASHIP) in official writing at Dr. Monika

Schliffke, [email protected], ASHIP, Bismarckallee

1-6, 23795 Bad Segeberg. The relevant software

codes and technical support to replicate the

findings are stored in the Supporting Information

files.

Funding: The study was funded by the German

Federal Ministry of Health (grant-number: ZMVI1-

2515NIK002). The funder of the study had no role

in study design, data collection, data analysis, data

interpretation, or writing of the report.

Competing interests: CS, KG, TE and JS: the

authors declare that they have no competing

interests. I have read the journal’s policy and the

author AS of this manuscript have the following

competing interests: AS is an editor of the German

version of EbMG. The online access is provided

free of charge to the study PCPs by Verlagshaus

der Aerzte, Vienna. This does not alter our

adherence to PLOS ONE policies on sharing data

and materials.

The aim of this study was to investigate whether a communication training based on the

MAAS-Global-D can reduce the rate of antibiotic prescribing for URTIs. Since the expecta-

tions of the patients and their perceptions of the physicians are subjective and might differ

between patients, we additionally evaluate the intervention effect by the patient’s age and sex

to increase the insights of the communication effect.

Materials and methods

Data source

This study was based on the analysis of routine data of the years 2013 to 2016 from the Associ-

ation of Statutory Health Insurance Physicians (ASHIP) of the federal state Schleswig-Hol-

stein, located in Northern Germany. The ASHIP is in charge for the reimbursement of services

that are provided to patients within the statutory health insurance system. The dataset covers

85% of the population and 83% of the PCPs of Schleswig-Holstein [41, 42]. The URTI cases

were identified by the target-diagnoses of acute bronchitis, sinusitis and pharyngitis (classified

by the International Classification of Diseases, version 10 (ICD-10) codes: J01.-; J02.-; J20.-

[43]). We concentrate the analysis to these diagnoses, since only in some cases the use of anti-

biotics is suggested by respective guidelines within these diagnoses. For cases of acute bronchi-

tis (J20) an antibiotic prescription is indicated for elderly patients as well as for those with a

severe cardiac or respiratory disease or a congenital or acquired immunodeficiency [44]. In

the case of acute pharyngitis (J02), the indications for an antibiotic therapy are: pharyngitis

due to group A streptococcus bacterial infections (GAS pharyngitis), scarlet fever, peritonsillar

abscess, a suspected serious illness or clinical worsening as well as consumptive diseases,

immunosuppression and acute rheumatic fever in the personal or family history [45]. For

acute sinusitis (J01), an antibiotic therapy should be considered for patients with specific risk

factors, as well as complications such as severe headache, facial swelling, lethargy and acute

exacerbation of recurrent sinusitis. Moreover, severe pain and an increased inflammation

score complaints in the course of the disease and with fever above 38.5˚C [46].

Since the antibiotic prescriptions have been inferred based on the visit diagnoses, we

excluded cases with additional diagnoses. This includes the presence of diagnoses regarding

puerperium/pregnancy (O00-O99), further (bacterial) infections (A00 to A37, A39 to A79,

J15, J17, J18) or chronic diseases (I50, J44, J45, C00 to C75). If the diagnosis had been made

several times or more than one diagnosis had been made from the three groups (J01, J02, J20),

the corresponding cases were also excluded. To increase the comparability of the included

cases and, thus, minimize a potential estimation bias of the communication training effect,

only cases of patients that were older than 18 years are included in the analysis.

Recruitment and inclusion criteria

All primary care physicians in private practices, working in a contract with statutory public

health insurance and with a work experience of at least five years, who have patients with at

least one of the target-diagnoses between 2013 and 2015 were considered for the intervention.

In total, 1554 (76%) primary care physicians of Schleswig-Holstein have been invited by letter

to participate in a study named “Effects of communication training with the MAAS-Global-D

on the prescription of antibiotics for respiratory infections”.

Study design and estimation strategy

The intervention and the previously planned randomized controlled trial (RCT) has been

described by Hammersen et al. [47] (Trial registration: DRKS00009566). The study was

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originally designed to consist of two interventional study arms. In addition to the communica-

tion training, the second intervention group received an educational introduction into the

use of and online-access to EbMG online (Evidence–based Medicine Guidelines) [48]. This point-of-care online tool provides further information material on the prescribing of antibiot-

ics for uncomplicated respiratory infections. Since the inclusion rate was lower than initially

expected, both intervention groups have been consolidated. Furthermore, a comparison

between the pooled intervention group and the control group did not yield significant results

due to a lack of power because of the small sample size. Instead, we formed a control group

from observational data and applied a combination of difference-in-difference (DiD) estima-

tion and matching approach that is considered to reproduce the results of RCTs very well

under certain assumptions [49]. For instance, under the assumption that the average outcomes

for the intervention and control group would have followed parallel trends over time before

intervention, the DiD estimator identifies causal effects by contrasting the change for the inter-

vention and control groups in pre- and post-intervention outcomes [50]. However, the

assumption of parallel trends might be implausible in our setting. For instance, if physicians

recognized a too high antibiotic prescription rate for URTIs, they presumably tried reducing

it. Therefore, they might have been more likely to respond to the training offer that advertised

a reduction of the prescription rate through improved communication skills. Consequently,

the evolutions of the prescription rates were suspected to differ between the intervention and

control group if the control group, as in this case, had not been built upon a controlled ran-

domization. An alternative identifying assumption is that the potential outcomes are indepen-

dent of intervention status, conditional on past outcomes and covariates [51]. By means of

balancing the intervention and control group according to pre-intervention outcomes and

covariates all potential outcome trends are perfectly aligned and the DiD estimates can be

interpreted as causal effects [49, 52]. However, recent studies showed that the combination of

DiD and matching might also deliver biased estimates [53]. In order to enhance the robustness

of our findings and minimize the risk of estimation bias we compared DiD estimates from

both unmatched and matched (on pre- intervention outcomes) data [54].

In the search for relevant variables determining the decision to prescribe an antibiotic for a

specific URTI case (our dependent variable) we first estimated a multi-level random effects

logistic regression model based on case-, patient- and physician-level data of the pre-interven-

tion period. A logistic regression model was chosen to account for the binary nature of the

dependent variable. Moreover, the logit model showed computational merits and, unlike the

probit model, it did not suffer from any convergence failures. Random effects were specified

on the physician level to account for intra-physician variability [55]. In a second step, we

aggregated the data on the physician level and matched the intervention and control groups

according to aggregated pre- intervention outcomes and covariates by means of entropy bal-

ancing [56]. Based on the balanced data, in the third step, we estimated a multi-level random

effects logistic DiD regression model using the weights of the physician-level from entropy bal-

ancing. Alternatively, we also specified fixed physician effects in the pre-intervention analysis

and the DiD regression models. For all models the results between fixed and random effects

models are very similar and we conclude there is no correlation between the explanatory vari-

ables and the individual effects. The physicians, who had previously been selected to the con-

trol group were excluded from the third step of the analysis, since we could not rule out that

their prescribing behavior might have been affected by the cancellation of participation in the

communication training.

The study was approved by the ethics committee of Luebeck University before the recruit-

ment of participants on 9 June 2015 (number of approval: 15–139). Statistical analyses were

performed with STATA 15 (StataCorp LLC, College Station, TX, USA).

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Intervention

The intervention group received a communication training with an interactive workshop

character (two times 2.25 hours), which was held at the Institute of Family Medicine in Febru-

ary and March of 2016. It was delivered face-to-face by members of the research team, includ-

ing an expert in physician-patient communication. The curriculum of the training was derived

from the German version (MAAS-Global-D [40]) of the Dutch instrument MAAS-Global

[39]. After establishing the relevance and success of physician-patient communication, the

participant were provided with information concerning the associated evidence base regarding

treatment of URTIs. Furthermore, they learned about the different communicative phases of a

consultation, corresponding communication skills as well as general communication skills for

the whole consultation (e.g. adequate provision of information, structuring and empathy,

shared decision-making).

Measurements

As the outcome variable we considered the binary choice whether an antibiotic was prescribed

for a URTI case. The selection of potential determinants serving as control variables in both

the pre- intervention and the DiD regression analyses was based on related previous literature

[25, 57]. They can be classified into three categories: (i) case related (year, quarter, diagnosis and its certainty, emergency service), (ii) patient specific (insurance status, age, sex) and (iii) physician characteristics (age, sex, number of URTI-patients in that quarter). Seasonal effects and a general trend in the prescribing pattern were considered by respective dummy variables

identifying the quarter and the year of the consultation, respectively. As the prescription rate

might differ between the considered diagnoses, we introduced dummy variables for sinusitis and pharyngitis with bronchitis serving as reference. According to the German coding policy, primary care physicians are required to designate their diagnoses as validated (certain) or sus-

pected (cases without an established definite diagnosis). We controlled for the cases with a cer- tain diagnosis by including a respective dummy variable. Further, we distinguish whether the patient visited an emergency care center during the out-of-hours care (emergency service). Demographic variables of the patient were comprised of the sex (sex = 1: female), the age and the insurance status (normal, family or retired). The age was grouped by respective dummy variables for patients aged <35, 35–65, 65+ to allow for nonlinear age effects. In Germany, the

insurance status signifies whether the patient is ordinary insured, retired or coinsured. Chil-

dren and grandchildren aged below 25 as well as spouses that are unemployed, not self-

employed and are not exceeding an income of EUR 450 per month are coinsured with an ordi-

nary insurance member. The considered age and insurance status based clusters reflect differ-

ent stages of life that might go along with different expectations about the treatment. At the

physician level, we controlled for the specialty, since primary care physician workforce in Ger-

many consists of general practitioners, physicians in general internal medicine and a declining

number of practitioners without special training in primary care (12%). Previous studies have

shown substantial differences in prescribing behavior between general internists and general

practitioners [58]. Further, we considered the age and the sex of the physician. Finally, to approximate the workload of the physician’s practice we included the number of total URTI

patients in the respective quarter. The logarithmic function to this variable accounts for

unequal variation.

In the intervention analysis, the DiD dummy variable identifies observations of the inter- vention group for the post-intervention period. To control for any other time-invariant differ-

ences between both groups a dummy variable trained is additionally included.

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Results

In the first part of the analysis (pre-intervention), the sample of the pre-intervention analysis

(2013 to 2015) consisted of 315,752 adult patients with 476,260 cases from 2,189 PCPs. For the

second part of the study, we invited 1,554 PCPs in SH to participate in the training. The group

of interested participants has been divided randomly in a control and an intervention group

with each 17 PCPs. Due to a lack of power, we alternatively form the control group from obser-

vational data. Do to so, we excluded the prior control group physicians (n = 17) and practition- ers without special training in primary care, since they are lacking in the intervention group

(n = 198). Moreover, 492 PCPs are not considered because they are not treating URTIs in each of the considered years, for instance since they are entering or leaving the ASHIP payment sys-

tem during the study period. Finally, the intervention/control group in the intervention analy-

sis consisted of 17/1,460 PCPs with 1,807/170,683 patients with 2,284/235,355 cases in the pre-

intervention period (2013:q1 to 2015:q4) and 585/61,755 patients with 698/75,167 cases after

the intervention (2016:q2 to 2016:q4) (Fig 1).

Pre-intervention analysis

The mean values of the considered variables in the pre-intervention analysis and the regression

results are shown in Table 1. An antibiotic was prescribed in half of the considered cases

(49%).

Fig 1. Flow chart.

https://doi.org/10.1371/journal.pone.0233345.g001

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Table 1. Multilevel logistic regression analysis of the pre-intervention period of prescribing an antibiotic.

Variable means (1) (2) Dependent variable

antibiotic prescription (= 1) 0.49 Case characteristics

quarter

2 nd

quarter 0.21 -0.01 -0.01 3

rd quarter 0.17 -0.07�� -0.07��

4 th

quarter 0.26 -0.08�� -0.08��

(Reference: 1 st

quarter)

year

2014 0.32 -0.03�� -0.03��

2015 0.33 -0.14�� -0.14��

(Reference: 2013)

diagnosis

sinusitis (J01) 0.21 -0.19�� -0.19��

pharyngitis (J02) 0.29 -0.18�� -0.18��

(Reference: bronchitis (J20))

certainty

certain diagnosis 0.99 0.38�� 0.38��

type of service

emergency service 0.03 0.40�� 0.40��

Patient characteristics Insurance status

Family insured 0.12 0.11�� 0.11��

Pensioners insured 0.16 0.16�� 0.17��

(Reference: ordinary insured)

Patient demographics

Patient aged 35–65 0.52 0.33�� 0.45��

Patient aged 65+ 0.14 0.28�� 0.39��

(Reference: < 35)

Female patient 0.59 0.09��

(Reference: male)

sex-age interactions

Female patient aged <35 0.19 0.22��

(Reference: male<35)

Female patient aged 35–65 0.31 0.02 (Reference: male aged 35–65)

Female patient aged 65+ 0.09 0.04 (Reference: male aged 65+)

Physician characteristics PCP specialty

PCP without special training 0.13 0.16 0.16 General Internist 0.18 0.00 0.00

(Reference: GP)

PCP demographics

Physician age 55.11 0.00 0.00 Female physician 0.31 -0.04 -0.04 (Reference: male)

(Continued )

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The results of two logistic regression models with specified random effects on the physician

level are shown in the third and fourth column of Table 1. In both models, the estimated intra-

class coefficients (21.6%) suggest that conditional on the covariates, almost one quarter of total

variation in antibiotic prescription could be explained by the individual physician’s practice

style. The estimated regression coefficients indicated that patients aged over 35 years were sig-

nificantly more likely to receive an antibiotic prescription than younger patients. The strongest

effect was achieved for patients aged between 35–65 years. Female patients were also more likely

to receive an antibiotic. The interaction effects between the patients’ gender and age groups in

Model (2) signified that the gender difference only exists for patients younger than 35 years. As

indicated by the smaller Akaike Information Criterion (AIC), the fit of the model was signifi-

cantly improved, leading to our final model that was considered for the intervention analysis.

Matching

The entropy balancing was applied to match physicians of the intervention group with physi-

cians of the control group in the pre-intervention period. In addition to the control variables,

the pre-intervention prescription rates served as conditional variables used in the matching.

Case- and patient-level variables were aggregated on the physician level. Table 2 shows the

means of the variables for the intervention as well as the matched and non-matched control

group. Further, the differences between intervention group and unmatched controls as well as

the share of missing observations are shown for each variable.

The intervention group is characterized by higher average prescriptions per physician in

comparison with the control group. This hints for a selection of the participants in the interven-

tion group due to their pre-intervention outcome. Furthermore, the change over time differed

between both groups, underlining that the assumption of parallel trends might not hold. The

average number of patients was higher in the control group. However, none of the differences

were significant, except for the fraction of patients with a certain diagnosis and family insur-

ance. This might have been due to the low number of observations at the physician level in the

intervention group (n = 17). Nevertheless, after applying the reweighting approach based on entropy balancing the means in the control group equaled the means in the intervention group.

Univariate DiD analysis

To assess the sensitivity of the DiD analysis due to model specifications and the balancing we

started presenting univariate DiD estimates (simple mean comparison) based on unmatched

Table 1. (Continued )

Variable means (1) (2) PCP workload

log(#URTI-patients) 3.60 0.15�� 0.15��

intercept -1.19�� -1.27��

s2RE (Variance of random effects on physician level) 0.90 �� 0.91��

Intra-class correlation (in %) 21.57 21.58

Log-Like -288,587 -288,480

Akaike Info Criterion (AIC) 577,216 577,006

R 2 -MacFadden (in %) 12.56 12.60

The first column presents sample means. The other columns display the estimated regression coefficients. Based on 476,260 observations (315,752 patients from 2,189

primary care physicians). Estimated by means of Maximum Likelihood. Significance levels: � 5%, �� 1%.

https://doi.org/10.1371/journal.pone.0233345.t001

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Table 2. Means of aggregated variables before intervention.

variables Intervention group Control group Difference between (a) and (b) Share of missing observations (in %) Un matched matched

(a) (b) (c)

Outcome: Prescription rate (in %)

2013 51.5 46.5 51.5 5.0 3.74

2014 48.3 44.7 48.3 3.6 2.01

2015 47.6 43.2 47.6 4.4 2.64

Number of URTI-patients 2013 66.5 88.4 66.4 -21.9 3.74

2014 65.1 79.0 65.0 -13.9 2.01

2015 69.3 82.3 69.3 -13.0 2.64

Share of cases (in %) quarter

2 nd

quarter 22.3 21.8 22.3 0.5 0

3 rd

quarter 18.6 18.1 18.6 0.5 0

4 th

quarter 27.6 26.2 27.6 1.4 0

(Reference: 1 st

quarter)

diagnosis

sinusitis (J01) 14.8 19.7 14.8 -4.9 0

pharyngitis (J02) 47.2 41.3 47.2 5.9 0

(Reference: bronchitis (J20))

certainty

certain diagnosis 99.3 97.9 99.3 1.4�� 0

service-type

Emergency services 6.6 5.5 6.6 1.1 0

Patient demographics

Patients aged 35–65 55.0 51.5 55.0 3.5 0

Patients aged >65 13.6 14.0 13.6 -0.4 0

Female patients 59.4 60.6 59.4 -1.2 0.02

sex-age interactions

Female patients aged 35–65 32.9 31.3 32.9 1.6 0.02

Female patients aged >65 7.9 8.5 7.9 -0.6 0.02

Insurance status

Patients family insurance 8.7 12.4 8.7 -3.7� 0

Patients pensioners insurance 15.6 16.1 15.6 -0.5 0

Physician characteristics PCP specialty

General Internists (in %) 23.5 26.4 23.5 -2.9 0

(Reference: GP)

Female physician (in %) 23.5 37.9 23.5 -14.4 0

(Reference: male)

Physician age 54.3 53.6 54.3 0.7 0.00

Number of PCPs 17 1,460 17

The first three columns present means of selected variables used for the matching before intervention for trained controls and matched controls, respectively. The last

column displays the differences between intervention and control group before matching. Significance levels: � 5%, �� 1%. Patient variables are aggregated on physician

level by summing up (Number of URTI-patients) or computing as shares of cases.

https://doi.org/10.1371/journal.pone.0233345.t002

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and matched sample data in Table 3. Neglecting physician-specific effects and other covariates,

the reduction in the overall prescription rate of the intervention group between the pre-inter-

vention and post-intervention period was 11.2%. For the control group a reduction of 4.7%

could be detected. The difference between both groups in the difference between the periods is

the DiD estimator, which is -6.5% [95% CI: (-10.7%; -2.3%)], and significant. Reweighting the

observations of the case-level by the entropy weights on the physician-level increased the pre-

scription rate of the matched control group to 52.9%. This was also slightly smaller than the

rate of the intervention group (55.4%), which might be, because the matching was done at the

physician level and not at the case level. However, the DiD estimate for the matched sample

was rather similar (-6.1% [95% CI: (-12.0%; -0.2%)],) and also significant. Concluding, both

univariate DiD estimates suggest a significant reduction of antibiotic prescriptions after the

communication training.

Multilevel DiD regression analysis

To take into account the control variables and the random effects on the physician-level, we

estimated the specification of Model (2) based on the extended data set, as well as the DiD and training dummy variable. Table 4 shows the estimated DiD effects and the moderation effects. To ease the interpretation of the estimated DiD coefficient, the marginal effect on the prescrip-

tion rate was also shown for the direct effects.

All specifications obtained a significant reduction of the prescription rate due to the inter-

vention. There were no substantial differences between the estimates of the matched and

unmatched sample. The marginal effects were close to the estimated univariate DiD effects.

The results of a moderation effect of the DiD effect by the age and sex of the patients are

also shown in Table 4. They suggest that the intervention had a significantly stronger effect on

the treatment of female patients aged below 35.

Discussion

In this study, we estimated the effect and its moderations of a communication training based

on the MAAS-Global-D instrument on the antibiotic prescription rate of primary care physi-

cians for the treatment of upper respiratory tract infections. Since the control group was

formed from observational data, we applied a combination of difference-in-difference estima-

tion and statistical matching based on entropy balancing to estimate the intervention effect.

Relevant variables for the matching were selected after estimating a multi-level logistic regres-

sion model for the antibiotic prescribing decision, based on case-, patient- and physician-level

Table 3. Univariate difference-in-difference analysis of the communication training on the antibiotic prescribing behavior.

Prescribing rate (in %)

Intervention Group Control Group Difference-in-Difference

unmatched matched unmatched matched

Before 55.43 47.27 52.86

(2014–2015) (n = 2284) (n = 235355) (∑wi�2282) After 44.27 42.61 47.80

(2016) (n = 698) (n = 75167) (∑wi�736) Difference -11.16�� -4.65�� -5.07� -6.51�� -6.10�

p-value <0.001 <0.001 0.017 0.003 0.043

313,504 observations (234,723 patients from 1,477 general practitioners). Significance levels: � 5%, �� 1%. Matching is based on Entropy balancing using the variables

listed in Table 2 and wi denotes the Entropy balancing weights.

https://doi.org/10.1371/journal.pone.0233345.t003

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data of the pre-intervention period in the first stage. In the second stage, the same model was

estimated, based on matched data and extended by the intervention period and DiD

specification.

Pre-intervention analysis

During the pre-intervention period, an antibiotic was prescribed in almost half of the consid-

ered cases. This relatively high number of antibiotic prescriptions is also observed in related

studies [57, 59]. In both groups (intervention and control), the prescription rate slightly

decreased over time. This is similar to the declining trend of general antibiotic use in other

countries [60] and might be explained by an increased awareness of antimicrobial resistance

[61], e.g. due to successful antibiotic stewardship programs as the German Strategy against Antibiotics Resistance [62]. The estimated intra-class coefficient of the multilevel regression model shows that the individual physician’s practice style explains about 22% of the total vari-

ance in antibiotic prescription and is similar to the results of related studies [25, 35, 63]. It sug-

gests the prospect of a successful reduction in the prescription rate by changing the individual

physician’s prescribing behavior. Most of the observable characteristics of the physician do not

explain the variance in prescribing behavior. Only the number of URTI patients (serving as a

proxy of the physician’s workload) increases the probability of antibiotic prescription. This

effect underlines the hypothesis that insufficient communication determines the antibiotic

prescription. It is more complicated for physicians lacking sufficient time for the consultation

due to an overload of patients, to change the patients’ expectations [28, 64]. A similar mecha-

nism might explain the positive association of emergency service and the antibiotic prescrip-

tion probability. In Germany, PCPs face an overload of patients, especially when providing

out-of-hours care in emergency service [65]. Patients visiting the emergency service for respi-

ratory complaints might be more severe and therefore might have a strong expectation of

receiving an antibiotic [66]. The expectations might also differ between patients, as suggested

by the estimated effects of the patient characteristics.

Table 4. Multilevel logistic regression analysis of the difference-in-difference effect of the communication training on prescribing an antibiotic.

(3) (4) (5) (6)

matching no yes no yes

trained 0.15 -0.08 0.14 -0.08

DiD -0.31�� -0.28� 0.19 0.14

95%-CIa of DiD [-0.50, -0.12] [-0.50, -0.05] ME

b of DiD (in %) -6.34�� -6.44�

95%-CIa of ME (in %) [-10.31–2.37] [-11.67, -1.22] Odds Ratio DiD 0.73�� 0.76�

95%-CI of OR [0.61, 0.89] [0.60, 0.95] Interaction effects DiD�Pat age (35–65) -0.52 -0.49�

DiD�Pat age (65+) -0.33 -0.26

DiD�Fem pat (<35) -0.73� -0.65��

DiD�Fem pat (35–65) -0.13 -0.03

DiD�Fem pat (65+) -0.00 0.07

313,504 observations (234,723 patients from 1,477 general practitioners). Significance levels: �� 5%, ��� 1%. a

Confidence interval b

Marginal Effect. Estimated coefficients of the control variables and the variance of the random effects are not shown. Matching is based on Entropy balancing using the

variables listed in Table 2.

https://doi.org/10.1371/journal.pone.0233345.t004

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Patients above the age of 35 years receive a significantly higher number of antibiotic pre-

scriptions than younger patients do. For patients belonging to a higher-risk group (e.g., elderly

patients) respective guidelines suggest the use of antibiotics in some cases [44–46]. Therefore,

the application of guidelines cannot explain the lower prescription rates for patients aged

above 65 in comparison with patients aged between 35 and 65 (Model (1): 0.28 vs. 0.33). Dif-

ferences between the patients’ expectations in the age-groups below and above 35 respectively,

might be more likely to serve as an explanation. Work pressure and other related stress cause

patients to desire rapid relieve from symptoms and cure of their sickness [67]. The perceived

importance of the patient’s job promotes the decision to prescribe an antibiotic [30, 68]. This

might explain that the antibiotic prescription rate considerably exceeds the clinically justified

amount for young and middle-aged adults with respiratory infections in the UK [69].

Our results further suggest that women receive more frequent an antibiotic prescription.

Women are more likely to visit a physician for URTI than men [57] and are found to be more

skeptical towards the physician’s suggestions [70]. This patient group might combine higher

expectations and wariness that might lead to additional communication requirements. This

hypothesis is in line with the higher antibiotic prescription rate that is observed for female

patients in our data. However, the underlying mechanisms were not aim of our research focus

and is, therefore, subjected to future research. Similar to other studies, the gender gap vanishes

with the increasing patient-age [71]. Only female patients below the age of 35 receive a signifi-

cantly higher number of antibiotic prescriptions. This result might indicate that the communi-

cation problem is mostly pronounced for the treatment of this group of patients. In the

following, we discuss the effects of the communication training on the antibiotic prescription

probability.

Intervention analysis

We applied different approaches and specifications to robustly estimate the effect of the com-

munication training on the antibiotic prescribing behavior. The univariate approach estimates

an 11-percentage-point reduction of prescriptions for the intervention group after the training.

This result is very similar to a related study [72]. All our approaches (univariate and multivari-

ate) estimate a decrease of around 6.5 percentage-points in the prescription probability of the

trained physicians. These robust estimates are in line with the findings of other related studies

applying RCT methodology [32, 35, 73]. The moderation analysis confirms that the effect of

the communication training is stronger for the treatment of patients marked by a larger com-

munication problem. The impact of the training on the reduction of antibiotic prescription is

significantly stronger for the treatment of young women. Thus, physicians with improved

communication skills might be able to better address the potentially higher expectations of

young female patients to receive an antibiotic therapy and their wariness towards the physi-

cian’s suggestions [70].

As argued by Fritz and Holton [74], the lack of trust in the patient-doctor relationship

enhances the likelihood of overprescribing. A patient trusting in the physician’s clinical judg-

ment, can be reassured to accept non-prescribing [75]. Furthermore, secured trust between

the patient and physician could reduce the probability of the physician to misperceive the

patient’s expectation to receive antibiotic treatment. To establish a trustful relationship it is

important for the patient to recognize the physician’s trust in them and believe that the physi-

cian acts in their best interest [76]. Signals of trustworthiness are given by verbal and nonver-

bal communication and serve to establish patients’ trust, and, thus, influence the doctor-

patient relationship [77]. For this purpose, the MAAS-Global-D might be a promising tool to

improve effective communication since both verbal and nonverbal communication skills are

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part of the training. To comprehend emotions as well as feelings and to react adequately, the

MAAS-global-D-manual proposes the physician to render the feelings expressed by the patient

during the consultation either in words or nonverbally [39]. Trust is considered for most

patients to be an integral part of an ongoing relationship with a physician [78]. An increased

continuity of care enables, on the one hand, physicians to better evaluate the patient’s expecta-

tions of receiving an antibiotic by the more intimate knowledge of their living conditions. On

the other hand, patients can build up a deep understanding of appropriate antibiotic use and

will change their expectations permanently. The findings of Robert et al. [79] suggest that

receiving information about antibiotics from family physicians is usually not associated with

an increased knowledge of the patients. A trustful and continued relationship might be helpful

for physicians to provide information about the use of antibiotics, and to improve knowledge

about antibiotics especially among target groups [79, 80]. As we found in our pre-intervention

data analysis, one specific target group consists of young female patients.

Limitations and strengths

The study estimated the effects of a communication training for primary care physicians on

the antibiotic prescription rate for infections of the upper respiratory tract and its moderation

by age and gender of the patients.

The study has strengths as well as limitations. In contrast to the previously planned ran-

domized controlled trial [47], in this study we formed a control group from observational

data. In contrast to the control group physicians the members of the intervention group did

know that their prescription data would be analyzed for the periods before and after the train-

ing. Therefore, we cannot exclude that behavior change in the intervention group is due to the

physicians’ awareness of being under observation rather than solely due to the intervention

(Hawthorne effect) [81]. However, since we considered the data of the physicians up to one

year after the training, we do not believe that this effect is responsible for persistent behavior

changes. Further, the approach that has been applied to estimate the intervention effect is

more sophisticated and is, thus, more susceptible to misspecification than an RCT [82]. To

minimize the risk of biased estimates we applied several alternative approaches (univariate,

multivariate, matching, no-matching) and specifications (fixed and random effects) as robust-

ness checks. All estimated effects of the intervention are very similar. Therefore, we believe

that misspecification is not a big issue here.

A strength of this study is that it relies on routine data collected from all primary care physi-

cians in a specific region of Germany. The relatively large number of physicians of the

(matched) control group (n = 1,460) might ensure a higher external validity of our findings

than the rather small sample sizes of other related studies applying an RCT [32, 33, 35, 36].

However, the small number of the intervention group highlights the problem to convince

PCPs to participate in intervention studies [83, 84]. Another reason for the low response rate

might have been rooted in the PCPs’ (who already faced an overload of patients) concerns that

improved communication skills would prolong the consultation, although so far, there is no

evidence to support this claim [85].

While on the one hand, the focus on the federal state of Schleswig-Holstein constrained the

representativeness of the findings, it on the other hand also reduced practice variations based

on regional differences and state-specific regulations [86]. The analyzed moderation of the

patient’s age and gender on the communication training effect further increased the insights of

antibiotic prescribing behavior. In line with the findings of our pre-intervention data analysis,

our results suggest that improved communication skills are mostly effective in cases where the

underlying communication problem is particularly pronounced due to high expectations of

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the patient to receive an antibiotic or due to the physicians’ perceptions. To clarify the moder-

ating role of expectation and its perception for the communication training effect on antibiotic

usage future research should include direct measures of these variables [25].

Conclusion

In this study, we estimated the effect and its moderations of a communication training on the

antibiotic prescription rate of primary care physicians for the treatment of upper respiratory

tract infections, i.e. acute bronchitis, sinusitis and pharyngitis. The short communication

training has been based on the MAAS-Global-D [40], the German version of the Dutch instru-

ment MAAS-Global [39]. Since the control group has been formed from observational data, a

combination of difference-in-difference (DiD) and matching has been applied to estimate the

intervention effect. To minimize the risk of biased estimates we applied several alternative

approaches and specifications as robustness checks that all reveal similar intervention effects.

The results show that the communication training decreases the prescribing probability by

around 6.5-percentage-points for the physicians of the intervention group. For the treatment

of female patients aged below 35, the intervention has a stronger impact.

Our results suggest that communication skills implemented via MAAS-Global-D-training

lead to more prudent prescribing of antibiotics for URTIs. Therefore, the MAAS-Global-D-

training could not only avoid unnecessary side effects but could also help to reduce the emer-

gence of drug resistant bacteria. The instrument MAAS-Global-D has been proven to provide

a valid tool for a training of physicians that encourages an effective communication with the

patient. In the Netherlands, communication training is an integral part in the postgraduate-

training program of general practitioners. A similar communication training based on the

MAAS-Global-D could also be applied in Germany, as well as in other countries, where post-

graduate training schemes of PCPs lack in training of communication skills. The instrument

and the explanatory manual in German language are available for free download [87].

Trial registration

The intervention and the previously planned randomized controlled trial (RCT) has been reg-

istered in the German Clinical Trial Register (DRKS00009566).

Supporting information

S1 Checklist. STROBE statement—checklist of items that should be included in reports of

observational studies.

(DOCX)

S1 Data. STATA software codes.

(ZIP)

Author Contributions

Conceptualization: Christoph Strumann, Jost Steinhaeuser, Andreas Sönnichsen, Katja

Goetz.

Data curation: Timo Emcke.

Formal analysis: Christoph Strumann.

Funding acquisition: Jost Steinhaeuser, Andreas Sönnichsen.

Investigation: Christoph Strumann, Jost Steinhaeuser, Katja Goetz.

PLOS ONE Communication training and the prescribing pattern of antibiotic prescription in primary health care

PLOS ONE | https://doi.org/10.1371/journal.pone.0233345 May 19, 2020 14 / 19

Methodology: Christoph Strumann, Katja Goetz.

Project administration: Katja Goetz.

Resources: Jost Steinhaeuser, Katja Goetz.

Software: Christoph Strumann.

Supervision: Katja Goetz.

Validation: Christoph Strumann, Jost Steinhaeuser, Timo Emcke, Andreas Sönnichsen, Katja

Goetz.

Writing – original draft: Christoph Strumann.

Writing – review & editing: Christoph Strumann, Jost Steinhaeuser, Timo Emcke, Andreas

Sönnichsen, Katja Goetz.

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