Perceptions and attitudes regarding antibiotic resistance in Germany: a cross-sectoral survey amongst physicians, veterinarians, farmers and the general public

Perceptions and attitudes regarding antibiotic resistance in Germany: a cross-sectoral survey... Abstract Background Drivers of antibiotic (AB) resistance (ABR) include outpatient treatment, hospital care and animal husbandry. During the first phase of the One Health project RAI (Responsible Antibiotic Use via Information and Communication) surveys were conducted in these sectors. Objectives To compare perceptions and attitudes towards ABR among general practitioners (GPs), hospital physicians, veterinarians, pig farmers and the general public. Methods Cross-sectional questions on AB use and ABR were integrated in group-specific surveys of GPs, hospital physicians, veterinarians, pig farmers and the German general population. Results A total of 1789 participants (340 GPs, 170 hospital physicians, 215 pig farmers, 60 veterinarians and 1004 members of the public) responded. Each group tended to identify drivers of ABR as being from outside its own area of activity. Guidelines were shown to be an important information source for AB therapy for all prescriber groups, but the frequency of routine use differed (39% of GPs, 65% of hospital physicians and 53% of veterinarians). Regarding further information sources, hospital physicians preferred smartphone apps and e-learning, GPs preferred non-sponsored training and veterinarians preferred multidisciplinary networks and e-learning. Farmers were predominantly satisfied with existing solutions. Farmers had three times better basic knowledge of ABR and knew twice as many people with MDR organism problems than the general public. They also received information on ABR more often from their veterinarians than patients did from their doctors. Conclusions This study reveals considerable differences in perceptions and attitudes to ABR among the groups investigated. The results can help to tailor future interventions. Furthermore, they promote mutual understanding and thus support the One Health approach. Introduction The topic of antibiotic (AB) resistance (ABR) concerns professionals and private individuals across sector borders.1,2 Whereas AB stewardship (ABS) measures have successfully addressed hospitals,3 outpatients4 and the animal farming sector5 individually during the last decade, recent action plans demand connected activities to effectively reduce ABR.6 Following this One Health approach, German scientists and practitioners from veterinary and human medicine, together with design and communication experts, have established the network project RAI (Responsible Antibiotic Use via Information and Communication).7 The project aims to develop targeted intervention tools to foster responsible AB use in hospitals, primary care and livestock farming and to enhance mutual understanding. The first project phase explored the perceptions and attitudes concerning AB use and ABR within target groups. This publication aims to illustrate similarities and differences between physicians, veterinarians, farmers and non-professionals. Methods The following target groups were selected with consideration of efficacy and feasibility aspects: general practitioners (GPs), hospital physicians (ICU or surgery), veterinary practitioners and pig farmers (details in Table S1, available as Supplementary data at JAC Online). Cross-sectional questions were integrated into anonymous questionnaires for all target groups (list of questions in Table S2). Wording was identical unless adaptation to specific group characteristics was inevitable. The survey period was May–December 2015. Questionnaire distribution was adapted to group-specific characteristics (details in Table S1). The questionnaires were complemented by a telephone-based survey of the German general population carried out on our behalf by TNS Emnid, a market research and consulting service (details in Table S1 and Schneider et al.8). Some cross-sectional questions were integrated here too (Table S2). Calculations were weighted by a sociodemographic factor provided by TNS Emnid to approximate representativeness. Descriptive statistics and univariate analysis were performed with SPSS (IBM SPSS Statistics, Somer, NY, USA). Multivariate analyses were conducted with SAS 9.4 (SAS Institute, Cary, NC, USA). Statistical significance was defined as P value <0.05. Results Valid responses were obtained from 340 GPs, 170 hospital physicians (109 ICU physicians and 61 surgeons), 215 pig farmers, 60 veterinarians and 1004 members of the general public. Table S3 provides group-specific characteristics. Problem perception Most hospital physicians (85%) believed their AB prescribing behaviour had an impact on ABR development, followed by GPs (70%) and veterinarians (53%). Sixty-four percent of pig farmers but only 37% of the general population believed their AB application behaviour influenced ABR (Table 1, Question 1). Table 1. Perceived self-influence and drivers of ABR GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 Table 1. Perceived self-influence and drivers of ABR GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 When asked about starting points to reduce ABR, each group identified the main topic outside its own sphere of influence (Table 1, Question 2). GPs (81%), farmers (89%) and the general population (66%) most often named hospital hygiene, whereas hospital physicians (89%) and veterinarians (87%) selected ambulatory AB prescriptions as number one. However, doctors of human medicine named their own fields the second most often, whereas veterinarians and farmers selected the three most important topics from the human sector. Figure S1 shows a comparison of veterinarians and farmers versus GPs and hospital physicians. AB(R) in daily life The relevance of ABR to daily work was highest for hospital physicians (high relevance, 82%) corresponding to reported frequent contact with patients with MDR organisms (MDROs). In contrast, only 37% of GPs, 40% of veterinarians and 19% of pig farmers reported high relevance of ABR to their daily work (Figure S2). Twenty percent of the general population but 42% of pig farmers reported personal acquaintance with individuals with MDRO problems. Information sources About 80% of all prescriber groups stated that AB guidelines were an important source of information (Table 2, Question 6). However, application of guidelines for AB therapy differed considerably between groups: 65% of hospital physicians reported frequent routine use of AB guidelines, compared with 39% of GPs. Veterinarians were in-between (53%). Doctors of human medicine expressed a need for better guidelines more frequently than veterinarians (GPs 42%, hospital physicians 42%, veterinarians 15%; Table 2, Question 7). Table 2. Sources of information on ABs % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 NA, not applicable. a GPs, national/international guidelines; hospital physicians, national/international/in-house guidelines; veterinarians, national practice guidelines/manual on oral medication in livestock. b GPs, infectious diseases specialist/microbiologist; hospital physicians, infectious diseases specialist/microbiologist/clinical pharmacist; veterinarians, microbiologist; farmers, consultant veterinarian. Table 2. Sources of information on ABs % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 NA, not applicable. a GPs, national/international guidelines; hospital physicians, national/international/in-house guidelines; veterinarians, national practice guidelines/manual on oral medication in livestock. b GPs, infectious diseases specialist/microbiologist; hospital physicians, infectious diseases specialist/microbiologist/clinical pharmacist; veterinarians, microbiologist; farmers, consultant veterinarian. Other reported information sources differed clearly between groups (Table 2, Question 6). Common information sources for GPs and veterinarians were scientific journals (83% of respondents in each group) and advanced training courses (76% and 92%, respectively). Communication with peers was another important source for veterinarians (80%). Main sources for hospital physicians were direct communication with experts (75%) and with peers (65%). Pig farmers considered their consulting veterinarians as their main information source on ABs (94%). Additionally, many farmers reported scientific journals (80%) and advanced training courses (55%) as information sources. The desire for additional information sources was also more diverse within groups (Table 2, Question 7). Nevertheless, 44% of hospital physicians would welcome an AB training app for smartphones. E-learning-based training and interactive case studies were also of interest to them. Veterinarians requested multidisciplinary networks, interactive case studies and e-learning (35% each). GPs favoured more non-sponsored medical training courses (38%). Knowledge Whereas prescribers were addressed group-specifically concerning AB knowledge, farmers and the public were asked the same basic question (Question 8, Table S2). Interestingly, three times more pig farmers than the public answered correctly (75% versus 24%). Level of education and personal acquaintance with MRDO carriers were independent influencing factors on answering correctly (Table S4). Communication The majority of GPs and veterinarians said they discussed ABR with their patients or farmers. GPs did so less frequently when prescribing AB than when not prescribing AB (68% versus 81%). For veterinarians there was no difference between prescription and non-prescription (67% each). Answering complementary questions, only a fifth of patients reported receiving information on ABR from their doctor whereas nearly half of the farmers did (Table S5). Discussion Perceptions and attitudes concerning ABR have already been investigated in physicians,9,10 veterinarians,11,12 farmers12 and the public.13,14 To our knowledge, this is the first study that addresses these various groups in a joint survey. Our findings have enabled us to tailor interventions for the RAI project,7 but they also provide insights into the field for other One Health projects. Target groups differed considerably in the perception of their own impact on ABR development. Greater awareness among hospital physicians regarding their prescribing behaviour compared with GPs and veterinarians might result from more frequent contact with infections caused by MDROs and more advanced ABS programmes in hospital settings.2,3 When asked about potential starting points for limiting ABR development, all groups favoured external sectors over their own fields of activity. This is not surprising considering the fact that the public debate on ABR is often characterized by mutual blame. However, GPs and hospital physicians named their own area as a close second after their number one selection. Although it is difficult to quantify separate contributions to the ABR situation, it is evident that AB use in humans,15 as well as in food-producing animals,16 is involved. Therefore, it is also important to raise awareness regarding the consequences of AB use within the groups that do not necessarily experience them directly. Clinical practice guidelines were a major information source on AB(R) for all three prescriber groups. However, frequent use in daily routine differed considerably. GPs utilized guidelines the least often. This is in line with previous findings, indicating reservations about clinical guidelines among German GPs.17 Compared with physicians, fewer veterinarians requested better guidelines. A possible explanation could be that veterinarians have a single, recently revised guideline on the prudent use of antimicrobials in animals,18 whereas physicians from human medicine have to search through various disease-specific guidelines. The most important information source for hospital physicians next to guidelines was experts. The frequency of GPs and veterinarians consulting an expert was considerably lower, possibly owing to lower accessibility in the outpatient or veterinary settings. Fewer hospital physicians than GPs and veterinarians used advanced training courses as information sources on AB therapy. In contrast, many could imagine a smartphone app as beneficial. All these differences show the importance of tailoring future interventions differently for the various target groups. Nearly all pig farmers reported their consulting veterinarian as an information source on ABs. However, scientific journals and advanced training courses were also of interest to them. These findings indicate that rather than being regarded as lay people, farmers should be considered at least semi-professionals, when addressed by interventions on the subject of ABR. This is also supported by the finding that pig farmers have much better basic knowledge of ABR than does the general population. About two-thirds of both GPs and veterinarians stated that they discussed ABR with their patients or farmers, respectively, when prescribing an AB. Interestingly, considerably lower numbers of patients than farmers stated that they received information on ABR when they received an AB prescription. Although recall bias might have been stronger in a telephone interview than in a written survey, the data could also reflect the different types of relationship in different settings. Whereas patients contact a GP when they have an acute illness, the veterinarian–farmer relationship is more a continuous consulting situation. Studies indicate that enhanced communication between the GP and patient helps reduce the number of AB prescriptions.19,20 Hence, ABS tools for GPs should support communication about ABR with patients. However, since the consultant veterinarian is the main information source on ABR for more than 90% of the pig farmers, communication should be facilitated here too. Of course, our study has limitations. In order to obtain insights into the very different target groups addressed by our questionnaires, we elected to use specific means and channels to reach the various participants. Thus, findings from the surveys on our target groups do not represent their entire German parent populations. In all probability, respondents were more interested in the subject of ABR and problem awareness was greater than in the non-participating population. A simple transfer of findings to other countries is difficult, too, because of cultural and systemic differences. Larger multinational studies would be of interest in the future. Concerning the general population the survey strategy was different. Telephone interviews are, for example, more vulnerable to recall bias than are written surveys and so comparability is limited. However, computer-assisted telephone interviews are currently the most common method of getting information on so-called public opinion. Except for the core questions, questionnaires were group-specific. Content as well as the number of items differed between groups. This could have influenced response behaviour to the core questions. The groups investigated were rather specific because in the RAI project we decided to start with interventions in manageable target groups. Investigation of additional groups from the various sectors (e.g. pet veterinarians, poultry farmers, paediatricians) could also be interesting. In conclusion, this study confirms the importance of information and education on ABR for all the groups investigated. But it also shows relevant differences in communication behaviour and information sources. It shows gaps between self-perception and external perception concerning the effects of action. Hence, future ABS interventions should address distinct target groups differently and specifically. Yet, the One Health concept should be taken into account when developing information materials for any group. This could help to overcome the search for responsibility outside one’s own sector. Acknowledgements Preliminary data from this study were presented at the Twenty-seventh European Congress of Clinical Microbiology and Infectious Diseases, Vienna, Austria, 2017 (Abstract P1134).  We thank the German Farmers’ Federation (DBV), the Interest Group of German Pig Farmers (ISN) and the Federal Association of Veterinary Practitioners (BPT) for support with the distribution of the pig farmers’ and veterinarians’ questionnaires. We thank Gerald Brennan for proofreading the manuscript prior to submission. Members of the RAI Study Group Muna Abu Sin, Esther-Maria Antão, Michael Behnke, Evgeniya Boklage, Tim Eckmanns, Christina Forstner, Petra Gastmeier, Jochen Gensichen, Alexander Gropmann, Stefan Hagel, Regina Hanke, Wolfgang Hanke, Anke Klingeberg, Lukas Klimmek, Ulrich Kraft, Markus Lehmkuhl, Norman Ludwig, Antina Lübke-Becker, Oliwia Makarewicz, Anne Moeser, Inga Petruschke, Mathias W. Pletz, Florian Salm, Katja Schmücker, Sandra Schneider, Christin Schröder, Frank Schwab, Joachim Trebbe, Szilvia Vincze, Horst Christian Vollmar, Jan Walter, Sebastian Weis, Wibke Wetzker and Lothar H. Wieler. Funding This work was supported by the German Federal Ministry of Education and Research (BMBF) within the consortium InfectControl 2020 (Project RAI, grant ID 03ZZ0804). Transparency declarations None to declare. Supplementary data Tables S1 to S5 and Figures S1 and S2 are available as Supplementary data at JAC Online. References 1 Holmes AH , Moore LS , Sundsfjord A et al. Understanding the mechanisms and drivers of antimicrobial resistance . Lancet 2016 ; 387 : 176 – 87 . Google Scholar CrossRef Search ADS PubMed 2 Baur D , Gladstone BP , Burkert F et al. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis . Lancet Infect Dis 2017 ; 17 : 990 – 1001 . Google Scholar CrossRef Search ADS PubMed 3 Davey P , Marwick CA , Scott CL et al. Interventions to improve antibiotic prescribing practices for hospital inpatients . Cochrane Database Syst Rev 2017 ; 2 : CD003543 . Google Scholar PubMed 4 Drekonja DM , Filice GA , Greer N et al. Antimicrobial stewardship in outpatient settings: a systematic review . Infect Control Hosp Epidemiol 2015 ; 36 : 142 – 52 . Google Scholar CrossRef Search ADS PubMed 5 Bos ME , Mevius DJ , Wagenaar JA et al. Antimicrobial prescription patterns of veterinarians: introduction of a benchmarking approach . J Antimicrob Chemother 2015 ; 70 : 2423 – 5 . Google Scholar CrossRef Search ADS PubMed 6 European Commission . A European One Health Action Plan against Antimicrobial Resistance (AMR). 2017 . https://ec.europa.eu/health/amr/sites/amr/files/amr_action_plan_2017_en.pdf. 7 RAI—Rationaler Antibiotikaeinsatz durch Information und Kommunikation. http://www.rai-projekt.de/rai/startseite/. 8 Schneider S , Salm F , Schröder C et al. [Antibiotic intake and resistance development - Knowledge, experience and behavior among the German general population] . Bundesgesundheitsblatt, Gesundheitsforschung, Gesundheitsschutz 2016 ; 59 : 1162 – 70 . Google Scholar CrossRef Search ADS PubMed 9 Velasco E , Espelage W , Faber M et al. A national cross-sectional study on socio-behavioural factors that influence physicians' decisions to begin antimicrobial therapy . Infection 2011 ; 39 : 289 – 97 . Google Scholar CrossRef Search ADS PubMed 10 Gonzalez-Gonzalez C , Lόpez-Vázquez P , Vázquez-Lago JM et al. Effect of physicians' attitudes and knowledge on the quality of antibiotic prescription: a cohort study . PLoS One 2015 ; 10 : e0141820. Google Scholar CrossRef Search ADS PubMed 11 Postma M , Speksnijder DC , Jaarsma AD et al. Opinions of veterinarians on antimicrobial use in farm animals in Flanders and the Netherlands . Vet Rec 2016 ; 179 : 68 . Google Scholar CrossRef Search ADS PubMed 12 Visschers VH , Backhans A , Collineau L et al. A comparison of pig farmers' and veterinarians' perceptions and intentions to reduce antimicrobial usage in six European countries . Zoonoses Public Health 2016 ; 63 : 534 – 44 . Google Scholar CrossRef Search ADS PubMed 13 European Commission . Special Eurobarometer 445—Antimicrobial Resistance—April 2016. 2016 . https://ec.europa.eu/health/amr/sites/amr/files/eb445_amr_generalreport_en.pdf. 14 McCullough AR , Parekh S , Rathbone J et al. A systematic review of the public's knowledge and beliefs about antibiotic resistance . J Antimicrob Chemother 2016 ; 71 : 27 – 33 . Google Scholar CrossRef Search ADS PubMed 15 Bell BG , Schellevis F , Stobberingh E et al. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance . BMC Infect Dis 2014 ; 14 : 13. Google Scholar CrossRef Search ADS PubMed 16 Tang KL , Caffrey NP , Nόbrega DB et al. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis . Lancet Planet Health 2017 ; 1 : e316 – 27 . Google Scholar CrossRef Search ADS PubMed 17 Butzlaff M , Kempkens D , Schnee M et al. German ambulatory care physicians' perspectives on clinical guidelines—a national survey . BMC Fam Pract 2006 ; 7 : 47. Google Scholar CrossRef Search ADS PubMed 18 Federal Veterinary Surgeons' Association (BTK = Bundestierärztekammer) . Guidelines for the Prudent Use of Veterinary Antimicrobial Drugs—With Notes for Guidance. Addendum to the German Veterinary Gazette 3/2015. 2015. http://www.bundestieraerztekammer.de/downloads/btk/antibiotika/AB_Leitlinien2015_EN.pdf. 19 Altiner A , Brockmann S , Sielk M et al. Reducing antibiotic prescriptions for acute cough by motivating GPs to change their attitudes to communication and empowering patients: a cluster-randomized intervention study . J Antimicrob Chemother 2007 ; 60 : 638 – 44 . Google Scholar CrossRef Search ADS PubMed 20 Butler CC , Simpson SA , Dunstan F et al. Effectiveness of multifaceted educational programme to reduce antibiotic dispensing in primary care: practice based randomised controlled trial . BMJ 2012 ; 344 : d8173. Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Antimicrobial Chemotherapy Oxford University Press

Perceptions and attitudes regarding antibiotic resistance in Germany: a cross-sectoral survey amongst physicians, veterinarians, farmers and the general public

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Abstract

Abstract Background Drivers of antibiotic (AB) resistance (ABR) include outpatient treatment, hospital care and animal husbandry. During the first phase of the One Health project RAI (Responsible Antibiotic Use via Information and Communication) surveys were conducted in these sectors. Objectives To compare perceptions and attitudes towards ABR among general practitioners (GPs), hospital physicians, veterinarians, pig farmers and the general public. Methods Cross-sectional questions on AB use and ABR were integrated in group-specific surveys of GPs, hospital physicians, veterinarians, pig farmers and the German general population. Results A total of 1789 participants (340 GPs, 170 hospital physicians, 215 pig farmers, 60 veterinarians and 1004 members of the public) responded. Each group tended to identify drivers of ABR as being from outside its own area of activity. Guidelines were shown to be an important information source for AB therapy for all prescriber groups, but the frequency of routine use differed (39% of GPs, 65% of hospital physicians and 53% of veterinarians). Regarding further information sources, hospital physicians preferred smartphone apps and e-learning, GPs preferred non-sponsored training and veterinarians preferred multidisciplinary networks and e-learning. Farmers were predominantly satisfied with existing solutions. Farmers had three times better basic knowledge of ABR and knew twice as many people with MDR organism problems than the general public. They also received information on ABR more often from their veterinarians than patients did from their doctors. Conclusions This study reveals considerable differences in perceptions and attitudes to ABR among the groups investigated. The results can help to tailor future interventions. Furthermore, they promote mutual understanding and thus support the One Health approach. Introduction The topic of antibiotic (AB) resistance (ABR) concerns professionals and private individuals across sector borders.1,2 Whereas AB stewardship (ABS) measures have successfully addressed hospitals,3 outpatients4 and the animal farming sector5 individually during the last decade, recent action plans demand connected activities to effectively reduce ABR.6 Following this One Health approach, German scientists and practitioners from veterinary and human medicine, together with design and communication experts, have established the network project RAI (Responsible Antibiotic Use via Information and Communication).7 The project aims to develop targeted intervention tools to foster responsible AB use in hospitals, primary care and livestock farming and to enhance mutual understanding. The first project phase explored the perceptions and attitudes concerning AB use and ABR within target groups. This publication aims to illustrate similarities and differences between physicians, veterinarians, farmers and non-professionals. Methods The following target groups were selected with consideration of efficacy and feasibility aspects: general practitioners (GPs), hospital physicians (ICU or surgery), veterinary practitioners and pig farmers (details in Table S1, available as Supplementary data at JAC Online). Cross-sectional questions were integrated into anonymous questionnaires for all target groups (list of questions in Table S2). Wording was identical unless adaptation to specific group characteristics was inevitable. The survey period was May–December 2015. Questionnaire distribution was adapted to group-specific characteristics (details in Table S1). The questionnaires were complemented by a telephone-based survey of the German general population carried out on our behalf by TNS Emnid, a market research and consulting service (details in Table S1 and Schneider et al.8). Some cross-sectional questions were integrated here too (Table S2). Calculations were weighted by a sociodemographic factor provided by TNS Emnid to approximate representativeness. Descriptive statistics and univariate analysis were performed with SPSS (IBM SPSS Statistics, Somer, NY, USA). Multivariate analyses were conducted with SAS 9.4 (SAS Institute, Cary, NC, USA). Statistical significance was defined as P value <0.05. Results Valid responses were obtained from 340 GPs, 170 hospital physicians (109 ICU physicians and 61 surgeons), 215 pig farmers, 60 veterinarians and 1004 members of the general public. Table S3 provides group-specific characteristics. Problem perception Most hospital physicians (85%) believed their AB prescribing behaviour had an impact on ABR development, followed by GPs (70%) and veterinarians (53%). Sixty-four percent of pig farmers but only 37% of the general population believed their AB application behaviour influenced ABR (Table 1, Question 1). Table 1. Perceived self-influence and drivers of ABR GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 Table 1. Perceived self-influence and drivers of ABR GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 GPs Hospital physicians General population Veterinary practitioners Pig farmers Question 1: ‘Do you think that your antibiotic prescribing/application behaviour influences antibiotic resistance development within your region?’  % yes 70 85 37 53 64 Question 2: ‘In your opinion, which sectors should be targeted to reduce the development of antibiotic resistance?’ (multiple selection)  topic 1 hospital hygiene ambulatory AB prescriptions hospital hygiene ambulatory AB prescriptions hospital hygiene  % 81 89 66 87 89  topic 2 ambulatory AB prescriptions hospital AB prescriptions ambulatory AB prescriptions hospital AB prescriptions patients’ AB use  % 80 79 57 85 83  topic 3 livestock AB use hospital hygiene livestock AB use patients’ AB use ambulatory AB prescriptions  % 79 75 53 77 81 When asked about starting points to reduce ABR, each group identified the main topic outside its own sphere of influence (Table 1, Question 2). GPs (81%), farmers (89%) and the general population (66%) most often named hospital hygiene, whereas hospital physicians (89%) and veterinarians (87%) selected ambulatory AB prescriptions as number one. However, doctors of human medicine named their own fields the second most often, whereas veterinarians and farmers selected the three most important topics from the human sector. Figure S1 shows a comparison of veterinarians and farmers versus GPs and hospital physicians. AB(R) in daily life The relevance of ABR to daily work was highest for hospital physicians (high relevance, 82%) corresponding to reported frequent contact with patients with MDR organisms (MDROs). In contrast, only 37% of GPs, 40% of veterinarians and 19% of pig farmers reported high relevance of ABR to their daily work (Figure S2). Twenty percent of the general population but 42% of pig farmers reported personal acquaintance with individuals with MDRO problems. Information sources About 80% of all prescriber groups stated that AB guidelines were an important source of information (Table 2, Question 6). However, application of guidelines for AB therapy differed considerably between groups: 65% of hospital physicians reported frequent routine use of AB guidelines, compared with 39% of GPs. Veterinarians were in-between (53%). Doctors of human medicine expressed a need for better guidelines more frequently than veterinarians (GPs 42%, hospital physicians 42%, veterinarians 15%; Table 2, Question 7). Table 2. Sources of information on ABs % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 NA, not applicable. a GPs, national/international guidelines; hospital physicians, national/international/in-house guidelines; veterinarians, national practice guidelines/manual on oral medication in livestock. b GPs, infectious diseases specialist/microbiologist; hospital physicians, infectious diseases specialist/microbiologist/clinical pharmacist; veterinarians, microbiologist; farmers, consultant veterinarian. Table 2. Sources of information on ABs % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 % GPs % Hospital physicians % Veterinary practitioners % Pig farmers Question 6: ‘Which are your sources for current information on antibiotic therapy and ABR?’ (multiple selection)  clinical practice guidelinesa 82.9 83.5 81.7 NA  expertsb 35.9 74.7 45.0 94.4  peer colleagues 56.5 64.7 80.0 42.3  scientific journals 82.6 47.6 83.3 79.5  advanced training courses 75.6 36.5 91.7 55.3  textbooks 33.5 32.9 38.3 NA  Internet portals/forums 25.3 20.0 21.7 12.6 Question 7: ‘Which additional information sources would be particularly helpful?’ (multiple selection)  no further 21.2 3.5 30.0 50.7  multidisciplinary networks 11.8 21.2 35.0 NA  better practice guidelines 41.5 41.8 15.0 NA  better access to existing guidelines 31.2 NA 5.0 NA  interactive case studies 17.6 27.1 35.0 NA  smartphone app 14.7 44.1 18.3 9.8  web site 22.1 21.2 30.0 28.4  non-sponsored training 37.9 23.5 NA NA  e-learning 19.1 36.5 35.0 12.6  educational games 9.4 1.9 0.0 1.9 NA, not applicable. a GPs, national/international guidelines; hospital physicians, national/international/in-house guidelines; veterinarians, national practice guidelines/manual on oral medication in livestock. b GPs, infectious diseases specialist/microbiologist; hospital physicians, infectious diseases specialist/microbiologist/clinical pharmacist; veterinarians, microbiologist; farmers, consultant veterinarian. Other reported information sources differed clearly between groups (Table 2, Question 6). Common information sources for GPs and veterinarians were scientific journals (83% of respondents in each group) and advanced training courses (76% and 92%, respectively). Communication with peers was another important source for veterinarians (80%). Main sources for hospital physicians were direct communication with experts (75%) and with peers (65%). Pig farmers considered their consulting veterinarians as their main information source on ABs (94%). Additionally, many farmers reported scientific journals (80%) and advanced training courses (55%) as information sources. The desire for additional information sources was also more diverse within groups (Table 2, Question 7). Nevertheless, 44% of hospital physicians would welcome an AB training app for smartphones. E-learning-based training and interactive case studies were also of interest to them. Veterinarians requested multidisciplinary networks, interactive case studies and e-learning (35% each). GPs favoured more non-sponsored medical training courses (38%). Knowledge Whereas prescribers were addressed group-specifically concerning AB knowledge, farmers and the public were asked the same basic question (Question 8, Table S2). Interestingly, three times more pig farmers than the public answered correctly (75% versus 24%). Level of education and personal acquaintance with MRDO carriers were independent influencing factors on answering correctly (Table S4). Communication The majority of GPs and veterinarians said they discussed ABR with their patients or farmers. GPs did so less frequently when prescribing AB than when not prescribing AB (68% versus 81%). For veterinarians there was no difference between prescription and non-prescription (67% each). Answering complementary questions, only a fifth of patients reported receiving information on ABR from their doctor whereas nearly half of the farmers did (Table S5). Discussion Perceptions and attitudes concerning ABR have already been investigated in physicians,9,10 veterinarians,11,12 farmers12 and the public.13,14 To our knowledge, this is the first study that addresses these various groups in a joint survey. Our findings have enabled us to tailor interventions for the RAI project,7 but they also provide insights into the field for other One Health projects. Target groups differed considerably in the perception of their own impact on ABR development. Greater awareness among hospital physicians regarding their prescribing behaviour compared with GPs and veterinarians might result from more frequent contact with infections caused by MDROs and more advanced ABS programmes in hospital settings.2,3 When asked about potential starting points for limiting ABR development, all groups favoured external sectors over their own fields of activity. This is not surprising considering the fact that the public debate on ABR is often characterized by mutual blame. However, GPs and hospital physicians named their own area as a close second after their number one selection. Although it is difficult to quantify separate contributions to the ABR situation, it is evident that AB use in humans,15 as well as in food-producing animals,16 is involved. Therefore, it is also important to raise awareness regarding the consequences of AB use within the groups that do not necessarily experience them directly. Clinical practice guidelines were a major information source on AB(R) for all three prescriber groups. However, frequent use in daily routine differed considerably. GPs utilized guidelines the least often. This is in line with previous findings, indicating reservations about clinical guidelines among German GPs.17 Compared with physicians, fewer veterinarians requested better guidelines. A possible explanation could be that veterinarians have a single, recently revised guideline on the prudent use of antimicrobials in animals,18 whereas physicians from human medicine have to search through various disease-specific guidelines. The most important information source for hospital physicians next to guidelines was experts. The frequency of GPs and veterinarians consulting an expert was considerably lower, possibly owing to lower accessibility in the outpatient or veterinary settings. Fewer hospital physicians than GPs and veterinarians used advanced training courses as information sources on AB therapy. In contrast, many could imagine a smartphone app as beneficial. All these differences show the importance of tailoring future interventions differently for the various target groups. Nearly all pig farmers reported their consulting veterinarian as an information source on ABs. However, scientific journals and advanced training courses were also of interest to them. These findings indicate that rather than being regarded as lay people, farmers should be considered at least semi-professionals, when addressed by interventions on the subject of ABR. This is also supported by the finding that pig farmers have much better basic knowledge of ABR than does the general population. About two-thirds of both GPs and veterinarians stated that they discussed ABR with their patients or farmers, respectively, when prescribing an AB. Interestingly, considerably lower numbers of patients than farmers stated that they received information on ABR when they received an AB prescription. Although recall bias might have been stronger in a telephone interview than in a written survey, the data could also reflect the different types of relationship in different settings. Whereas patients contact a GP when they have an acute illness, the veterinarian–farmer relationship is more a continuous consulting situation. Studies indicate that enhanced communication between the GP and patient helps reduce the number of AB prescriptions.19,20 Hence, ABS tools for GPs should support communication about ABR with patients. However, since the consultant veterinarian is the main information source on ABR for more than 90% of the pig farmers, communication should be facilitated here too. Of course, our study has limitations. In order to obtain insights into the very different target groups addressed by our questionnaires, we elected to use specific means and channels to reach the various participants. Thus, findings from the surveys on our target groups do not represent their entire German parent populations. In all probability, respondents were more interested in the subject of ABR and problem awareness was greater than in the non-participating population. A simple transfer of findings to other countries is difficult, too, because of cultural and systemic differences. Larger multinational studies would be of interest in the future. Concerning the general population the survey strategy was different. Telephone interviews are, for example, more vulnerable to recall bias than are written surveys and so comparability is limited. However, computer-assisted telephone interviews are currently the most common method of getting information on so-called public opinion. Except for the core questions, questionnaires were group-specific. Content as well as the number of items differed between groups. This could have influenced response behaviour to the core questions. The groups investigated were rather specific because in the RAI project we decided to start with interventions in manageable target groups. Investigation of additional groups from the various sectors (e.g. pet veterinarians, poultry farmers, paediatricians) could also be interesting. In conclusion, this study confirms the importance of information and education on ABR for all the groups investigated. But it also shows relevant differences in communication behaviour and information sources. It shows gaps between self-perception and external perception concerning the effects of action. Hence, future ABS interventions should address distinct target groups differently and specifically. Yet, the One Health concept should be taken into account when developing information materials for any group. This could help to overcome the search for responsibility outside one’s own sector. Acknowledgements Preliminary data from this study were presented at the Twenty-seventh European Congress of Clinical Microbiology and Infectious Diseases, Vienna, Austria, 2017 (Abstract P1134).  We thank the German Farmers’ Federation (DBV), the Interest Group of German Pig Farmers (ISN) and the Federal Association of Veterinary Practitioners (BPT) for support with the distribution of the pig farmers’ and veterinarians’ questionnaires. We thank Gerald Brennan for proofreading the manuscript prior to submission. Members of the RAI Study Group Muna Abu Sin, Esther-Maria Antão, Michael Behnke, Evgeniya Boklage, Tim Eckmanns, Christina Forstner, Petra Gastmeier, Jochen Gensichen, Alexander Gropmann, Stefan Hagel, Regina Hanke, Wolfgang Hanke, Anke Klingeberg, Lukas Klimmek, Ulrich Kraft, Markus Lehmkuhl, Norman Ludwig, Antina Lübke-Becker, Oliwia Makarewicz, Anne Moeser, Inga Petruschke, Mathias W. Pletz, Florian Salm, Katja Schmücker, Sandra Schneider, Christin Schröder, Frank Schwab, Joachim Trebbe, Szilvia Vincze, Horst Christian Vollmar, Jan Walter, Sebastian Weis, Wibke Wetzker and Lothar H. Wieler. Funding This work was supported by the German Federal Ministry of Education and Research (BMBF) within the consortium InfectControl 2020 (Project RAI, grant ID 03ZZ0804). Transparency declarations None to declare. Supplementary data Tables S1 to S5 and Figures S1 and S2 are available as Supplementary data at JAC Online. References 1 Holmes AH , Moore LS , Sundsfjord A et al. Understanding the mechanisms and drivers of antimicrobial resistance . Lancet 2016 ; 387 : 176 – 87 . Google Scholar CrossRef Search ADS PubMed 2 Baur D , Gladstone BP , Burkert F et al. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis . Lancet Infect Dis 2017 ; 17 : 990 – 1001 . Google Scholar CrossRef Search ADS PubMed 3 Davey P , Marwick CA , Scott CL et al. Interventions to improve antibiotic prescribing practices for hospital inpatients . Cochrane Database Syst Rev 2017 ; 2 : CD003543 . Google Scholar PubMed 4 Drekonja DM , Filice GA , Greer N et al. Antimicrobial stewardship in outpatient settings: a systematic review . Infect Control Hosp Epidemiol 2015 ; 36 : 142 – 52 . Google Scholar CrossRef Search ADS PubMed 5 Bos ME , Mevius DJ , Wagenaar JA et al. Antimicrobial prescription patterns of veterinarians: introduction of a benchmarking approach . J Antimicrob Chemother 2015 ; 70 : 2423 – 5 . Google Scholar CrossRef Search ADS PubMed 6 European Commission . A European One Health Action Plan against Antimicrobial Resistance (AMR). 2017 . https://ec.europa.eu/health/amr/sites/amr/files/amr_action_plan_2017_en.pdf. 7 RAI—Rationaler Antibiotikaeinsatz durch Information und Kommunikation. http://www.rai-projekt.de/rai/startseite/. 8 Schneider S , Salm F , Schröder C et al. [Antibiotic intake and resistance development - Knowledge, experience and behavior among the German general population] . Bundesgesundheitsblatt, Gesundheitsforschung, Gesundheitsschutz 2016 ; 59 : 1162 – 70 . Google Scholar CrossRef Search ADS PubMed 9 Velasco E , Espelage W , Faber M et al. A national cross-sectional study on socio-behavioural factors that influence physicians' decisions to begin antimicrobial therapy . Infection 2011 ; 39 : 289 – 97 . Google Scholar CrossRef Search ADS PubMed 10 Gonzalez-Gonzalez C , Lόpez-Vázquez P , Vázquez-Lago JM et al. Effect of physicians' attitudes and knowledge on the quality of antibiotic prescription: a cohort study . PLoS One 2015 ; 10 : e0141820. Google Scholar CrossRef Search ADS PubMed 11 Postma M , Speksnijder DC , Jaarsma AD et al. Opinions of veterinarians on antimicrobial use in farm animals in Flanders and the Netherlands . Vet Rec 2016 ; 179 : 68 . Google Scholar CrossRef Search ADS PubMed 12 Visschers VH , Backhans A , Collineau L et al. A comparison of pig farmers' and veterinarians' perceptions and intentions to reduce antimicrobial usage in six European countries . Zoonoses Public Health 2016 ; 63 : 534 – 44 . Google Scholar CrossRef Search ADS PubMed 13 European Commission . Special Eurobarometer 445—Antimicrobial Resistance—April 2016. 2016 . https://ec.europa.eu/health/amr/sites/amr/files/eb445_amr_generalreport_en.pdf. 14 McCullough AR , Parekh S , Rathbone J et al. A systematic review of the public's knowledge and beliefs about antibiotic resistance . J Antimicrob Chemother 2016 ; 71 : 27 – 33 . Google Scholar CrossRef Search ADS PubMed 15 Bell BG , Schellevis F , Stobberingh E et al. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance . BMC Infect Dis 2014 ; 14 : 13. Google Scholar CrossRef Search ADS PubMed 16 Tang KL , Caffrey NP , Nόbrega DB et al. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis . Lancet Planet Health 2017 ; 1 : e316 – 27 . Google Scholar CrossRef Search ADS PubMed 17 Butzlaff M , Kempkens D , Schnee M et al. German ambulatory care physicians' perspectives on clinical guidelines—a national survey . BMC Fam Pract 2006 ; 7 : 47. Google Scholar CrossRef Search ADS PubMed 18 Federal Veterinary Surgeons' Association (BTK = Bundestierärztekammer) . Guidelines for the Prudent Use of Veterinary Antimicrobial Drugs—With Notes for Guidance. Addendum to the German Veterinary Gazette 3/2015. 2015. http://www.bundestieraerztekammer.de/downloads/btk/antibiotika/AB_Leitlinien2015_EN.pdf. 19 Altiner A , Brockmann S , Sielk M et al. Reducing antibiotic prescriptions for acute cough by motivating GPs to change their attitudes to communication and empowering patients: a cluster-randomized intervention study . J Antimicrob Chemother 2007 ; 60 : 638 – 44 . Google Scholar CrossRef Search ADS PubMed 20 Butler CC , Simpson SA , Dunstan F et al. Effectiveness of multifaceted educational programme to reduce antibiotic dispensing in primary care: practice based randomised controlled trial . BMJ 2012 ; 344 : d8173. Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Journal of Antimicrobial ChemotherapyOxford University Press

Published: Mar 26, 2018

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