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BioMed Research International
Volume 2015, Article ID 214021, 13 pages
http://dx.doi.org/10.1155/2015/214021
Review Article

Educational Effectiveness, Target, and Content for Prudent Antibiotic Use

1National Leading Research Laboratory of Drug Resistance Proteomics, Department of Biological Sciences, Myongji University, 116 Myongjiro, Yongin, Gyeonggido 449-728, Republic of Korea
2Department of Biological Sciences, Konkuk University, 1 Hwayangdong, Gwangjingu, Seoul 143-701, Republic of Korea

Received 14 November 2014; Accepted 20 March 2015

Academic Editor: Benoît Stijlemans

Copyright © 2015 Chang-Ro Lee et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. A. M. McNulty and N. A. Francis, “Optimizing antibiotic prescribing in primary care settings in the UK: findings of a BSAC multi-disciplinary workshop 2009,” The Journal of Antimicrobial Chemotherapy, vol. 65, no. 11, Article ID dkq361, pp. 2278–2284, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. E. Jawetz, “Antimicrobial chemotherapy,” Annual Review of Microbiology, vol. 10, pp. 85–114, 1956. View at Publisher · View at Google Scholar · View at Scopus
  3. J. H. Lee, S. H. Jeong, S.-S. Cha, and S. H. Lee, “New disturbing trend in antimicrobial resistance of gram-negative pathogens,” PLoS Pathogens, vol. 5, no. 3, Article ID e1000221, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. M. S. Butler and M. A. Cooper, “Screening strategies to identify new antibiotics,” Current Drug Targets, vol. 13, no. 3, pp. 373–387, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. J.-H. Lee, S. H. Jeong, S.-S. Cha, and S. H. Lee, “A lack of drugs for antibiotic-resistant Gram-negative bacteria,” Nature Reviews Drug Discovery, vol. 6, no. 11, pp. 938–939, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. C.-R. Lee, I. H. Cho, B. C. Jeong, and S. H. Lee, “Strategies to minimize antibiotic resistance,” International Journal of Environmental Research and Public Health, vol. 10, no. 9, pp. 4274–4305, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. R. C. Owens Jr., “Antimicrobial stewardship: concepts and strategies in the 21st century,” Diagnostic Microbiology and Infectious Disease, vol. 61, no. 1, pp. 110–128, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. C. A. M. McNulty, D. M. Lecky, D. Farrell et al., “Overview of e-Bug: an antibiotic and hygiene educational resource for schools,” Journal of Antimicrobial Chemotherapy, vol. 66, supplement 5, pp. v3–v12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Davey, C. Pagliari, and A. Hayes, “The patient's role in the spread and control of bacterial resistance to antibiotics,” Clinical Microbiology and Infection, vol. 8, no. supplement 2, pp. 43–68, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. C. C. Butler, S. Rollnick, R. Pill, F. Maggs-Rapport, and N. Stott, “Understanding the culture of prescribing: qualitative study of general practitioners' and patients' perceptions of antibiotics for sore throats,” British Medical Journal, vol. 317, no. 7159, pp. 637–642, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Macfarlane, W. Holmes, R. Macfarlane, and N. Britten, “Influence of patients' expectations on antibiotic management of acute lower respiratory tract illness in general practice: questionnaire study,” British Medical Journal, vol. 315, no. 7117, pp. 1211–1214, 1997. View at Publisher · View at Google Scholar · View at Scopus
  12. D. M. Lecky, C. A. M. McNulty, P. Touboul et al., “Evaluation of e-Bug, an educational pack, teaching about prudent antibiotic use and hygiene, in the Czech Republic, France and England,” The Journal of Antimicrobial Chemotherapy, vol. 65, no. 12, Article ID dkq356, pp. 2674–2684, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Moher, A. Liberati, J. Tetzlaff, D. G. Altman, and The PRISMA Group, “Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement,” PLoS Medicine, vol. 6, no. 7, Article ID e1000097, 2009. View at Publisher · View at Google Scholar
  14. P. Le Corvoisier, V. Renard, F. Roudot-Thoraval et al., “Long-term effects of an educational seminar on antibiotic prescribing by GPs: a randomised controlled trial,” The British Journal of General Practice, vol. 63, no. 612, pp. e455–e464, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. G. de Santis, K. J. Harvey, D. Howard, M. L. Mashford, and R. F. W. Moulds, “Improving the quality of antibiotic prescription patterns in general practice. The role of educational intervention,” Medical Journal of Australia, vol. 160, no. 8, pp. 502–505, 1994. View at Google Scholar · View at Scopus
  16. J. Monette, M. A. Miller, M. Monette et al., “Effect of an educational intervention on optimizing antibiotic prescribing in long-term care facilities,” Journal of the American Geriatrics Society, vol. 55, no. 8, pp. 1231–1235, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. J. W. L. Cals, C. C. Butler, R. M. Hopstaken, K. Hood, and G.-J. Dinant, “Effect of point of care testing for C reactive protein and training in communication skills on antibiotic use in lower respiratory tract infections: cluster randomised trial,” British Medical Journal, vol. 338, Article ID b1374, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. Finkelstein, R. L. Davis, S. F. Dowell et al., “Reducing antibiotic use in children: a randomized trial in 12 practices,” Pediatrics, vol. 108, no. 1, pp. 1–7, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Welschen, M. M. Kuyvenhoven, A. W. Hoes, and T. J. M. Verheij, “Effectiveness of a multiple intervention to reduce antibiotic prescribing for respiratory tract symptoms in primary care: randomised controlled trial,” British Medical Journal, vol. 329, no. 7463, pp. 431–433, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Altiner, S. Brockmann, M. Sielk, S. Wilm, K. Wegscheider, and H.-H. Abholz, “Reducing antibiotic prescriptions for acute cough by motivating GPs to change their attitudes to communication and empowering patients: a cluster-randomized intervention study,” Journal of Antimicrobial Chemotherapy, vol. 60, no. 3, pp. 638–644, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Avorn and S. B. Soumerai, “Improving drug-therapy decisions through educational outreach. A randomized controlled trial of academically based ‘detailing’,” The New England Journal of Medicine, vol. 308, no. 24, pp. 1457–1463, 1983. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Enriquez-Puga, R. Baker, S. Paul, and R. Villoro-Valdes, “Effect of educational outreach on general practice prescribing of antibiotics and antidepressants: a two-year randomised controlled trialal,” Scandinavian Journal of Primary Health Care, vol. 27, no. 4, pp. 195–201, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. J. M. Seager, R. S. Howell-Jones, F. D. Dunstan, M. A. O. Lewis, S. Richmond, and D. W. Thomas, “A randomised controlled trial of clinical outreach education to rationalise antibiotic prescribing for acute dental pain in the primary care setting,” British Dental Journal, vol. 201, no. 4, pp. 217–222, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. D. H. Solomon, L. Van Houten, R. J. Glynn et al., “Academic detailing to improve use of broad-spectrum antibiotics at an academic medical center,” Archives of Internal Medicine, vol. 161, no. 15, pp. 1897–1902, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. E. O. Doyne, M. P. Alfaro, R. M. Siegel et al., “A randomized controlled trial to change antibiotic prescribing patterns in a community,” Archives of Pediatrics & Adolescent Medicine, vol. 158, no. 6, pp. 577–583, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. N. A. Francis, C. C. Butler, K. Hood, S. Simpson, F. Wood, and J. Nuttall, “Effect of using an interactive booklet about childhood respiratory tract infections in primary care consultations on reconsulting and antibiotic prescribing: a cluster randomised controlled trial,” The British Medical Journal, vol. 339, no. 7717, Article ID b2885, pp. 374–376, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. J. T. Macfarlane, W. F. Holmes, and R. M. Macfarlane, “Reducing reconsultations for acute lower respiratory tract illness with an information leaflet: a randomized controlled study of patients in primary care,” The British Journal of General Practice, vol. 47, no. 424, pp. 719–722, 1997. View at Google Scholar · View at Scopus
  28. J. D. Martens, R. A. G. Winkens, T. Van Der Weijden, D. De Bruyn, and J. L. Severens, “Does a joint development and dissemination of multidisciplinary guidelines improve prescribing behaviour: a pre/post study with concurrent control group and a randomised trial,” BMC Health Services Research, vol. 6, article 145, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Naughton, J. Feely, and K. Bennett, “A RCT evaluating the effectiveness and cost-effectiveness of academic detailing versus postal prescribing feedback in changing GP antibiotic prescribing,” Journal of Evaluation in Clinical Practice, vol. 15, no. 5, pp. 807–812, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Briel, W. Langewitz, P. Tschudi, J. Young, C. Hugenschmidt, and H. C. Bucher, “Communication training and antibiotic use in acute respiratory tract infections. A cluster randomised controlled trial in general practice,” Swiss Medical Weekly, vol. 136, no. 15-16, pp. 241–247, 2006. View at Google Scholar · View at Scopus
  31. S. Gjelstad, S. Hoye, J. Straand, M. Brekke, I. Dalen, and M. Lindbaek, “mproving antibiotic prescribing in acute respiratory tract infections: cluster randomised trial from Norwegian general practice (prescription peer academic detailing (Rx-PAD) study),” The British Medical Journal, vol. 347, article f4403, 2013. View at Publisher · View at Google Scholar
  32. N. Zwar, J. Wolk, J. Gordon, R. Sanson-Fisher, and L. Kehoe, “Influencing antibiotic prescribing in general practice: a trial of prescriber feedback and management guidelines,” Family Practice, vol. 16, no. 5, pp. 495–500, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. R. M. Poses, R. D. Cebul, and R. S. Wigton, “You can lead a horse to water—improving physicians' knowledge of probabilities may not affect their decisions,” Medical Decision Making, vol. 15, no. 1, pp. 65–75, 1995. View at Publisher · View at Google Scholar · View at Scopus
  34. A. W. van der Velden, E. J. Pijpers, M. M. Kuyvenhoven, S. K. G. Tonkin-Crine, P. Little, and T. J. M. Verheij, “Effectiveness of physician-targeted interventions to improve antibiotic use for respiratory tract infections,” The British Journal of General Practice, vol. 62, no. 605, pp. e801–e807, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. J. P. Metlay, C. A. Camargo Jr., T. MacKenzie et al., “Cluster-randomized trial to improve antibiotic use for adults with acute respiratory infections treated in emergency departments,” Annals of Emergency Medicine, vol. 50, no. 3, pp. 221–230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Gonzales, T. Anderer, C. E. McCulloch et al., “A cluster randomized trial of decision support strategies for reducing antibiotic use in acute bronchitis,” JAMA Internal Medicine, vol. 173, no. 4, pp. 267–273, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Høye, S. Gjelstad, and M. Lindbæk, “Effects on antibiotic dispensing rates of interventions to promote delayed prescribing for respiratory tract infections in primary care,” The British Journal of General Practice, vol. 63, no. 616, pp. e777–e786, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. A. I. Awad, I. B. Eltayeb, and O. Z. Baraka, “Changing antibiotics prescribing practices in health centers of Khartoum State, Sudan,” European Journal of Clinical Pharmacology, vol. 62, no. 2, pp. 135–142, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Ayieko, S. Ntoburi, J. Wagai et al., “A multifaceted intervention to implement guidelines and improve admission paediatric care in Kenyan district hospitals: a cluster randomised trial,” PLoS medicine, vol. 8, no. 4, Article ID e1001018, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. J. A. Finkelstein, S. S. Huang, K. Kleinman et al., “Impact of a 16-community trial to promote judicious antibiotic use in Massachusetts,” Pediatrics, vol. 121, no. 1, pp. e15–e23, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. J. S. Gerber, P. A. Prasad, A. G. Fiks et al., “Effect of an outpatient antimicrobial stewardship intervention on broad-spectrum antibiotic prescribing by primary care pediatricians a randomized trial,” The Journal of the American Medical Association, vol. 309, no. 22, pp. 2345–2352, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. A. G. Mainous III, W. J. Hueston, M. M. Love, M. E. Evans, and R. Finger, “An evaluation of statewide strategies to reduce antibiotic overuse,” Family Medicine, vol. 32, no. 1, pp. 22–29, 2000. View at Google Scholar · View at Scopus
  43. S. E. Wutzke, M. A. Artist, L. A. Kehoe, M. Fletcher, J. M. Mackson, and L. M. Weekes, “Evaluation of a national programme to reduce inappropriate use of antibiotics for upper respiratory tract infections: effects on consumer awareness, beliefs, attitudes and behaviour in Australia,” Health Promotion International, vol. 22, no. 1, pp. 53–64, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. W. B. Dollman, V. T. LeBlanc, L. Stevens, P. J. O'Connor, and J. D. Turnidge, “A community-based intervention to reduce antibiotic use for upper respiratory tract infections in regional South Australia,” Medical Journal of Australia, vol. 182, no. 12, pp. 617–620, 2005. View at Google Scholar · View at Scopus
  45. R. Gonzales, K. K. Corbett, S. Wong et al., “‘Get smart Colorado’: impact of a mass media campaign to improve community antibiotic use,” Medical Care, vol. 46, no. 6, pp. 597–605, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J. F. Perz, A. S. Craig, C. S. Coffey et al., “Changes in antibiotic prescribing for children after a community-wide campaign,” The Journal of the American Medical Association, vol. 287, no. 23, pp. 3103–3109, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Hemo, N. H. Shamir-Shtein, B. G. Silverman et al., “Can a nationwide media campaign affect antibiotic use?” The American Journal of Managed Care, vol. 15, no. 8, pp. 529–534, 2009. View at Google Scholar · View at Scopus
  48. E. Sabuncu, J. David, C. Bernède-Bauduin et al., “Significant reduction of antibiotic use in the community after a nationwide campaign in France, 2002–2007,” PLoS Medicine, vol. 6, no. 6, Article ID e1000084, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. I. Bauraind, J.-M. Lopez-Lozano, A. Beyaert et al., “Association between antibiotic sales and public campaigns for their appropriate use,” The Journal of the American Medical Association, vol. 292, no. 20, pp. 2468–2470, 2004. View at Google Scholar · View at Scopus
  50. M. F. Lambert, G. A. Masters, and S. L. Brent, “Can mass media campaigns change antimicrobial prescribing? A regional evaluation study,” Journal of Antimicrobial Chemotherapy, vol. 59, no. 3, pp. 537–543, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. LOCAAL Study Group, “Doctors and local media: a synergy for public health information? A controlled trial to evaluate the effects of a multifaceted campaign on antibiotic prescribing (protocol),” BMC Public Health, vol. 11, p. 816, 2011. View at Google Scholar
  52. C. A. M. McNulty, T. Nichols, P. J. Boyle, M. Woodhead, and P. Davey, “The English antibiotic awareness campaigns: did they change the public's knowledge of and attitudes to antibiotic use?” Journal of Antimicrobial Chemotherapy, vol. 65, no. 7, pp. 1526–1533, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. S. R. Arnold and S. E. Straus, “Interventions to improve antibiotic prescribing practices in ambulatory care,” The Cochrane Database of Systematic Reviews, no. 4, Article ID CD003539, 2005. View at Google Scholar
  54. S. R. Ranji, M. A. Steinman, K. G. Shojania, and R. Gonzales, “Interventions to reduce unnecessary antibiotic prescribing: a systematic review and quantitative analysis,” Medical Care, vol. 46, no. 8, pp. 847–862, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. E. A. Belongia and B. Schwartz, “Strategies for promoting judicious use of antibiotics by doctors and patients,” British Medical Journal, vol. 317, no. 7159, pp. 668–671, 1998. View at Publisher · View at Google Scholar · View at Scopus
  56. M. M. Azevedo, C. Pinheiro, J. Yaphe, and F. Baltazar, “Assessing the impact of a school intervention to promote students' knowledge and practices on correct antibiotic use,” International Journal of Environmental Research and Public Health, vol. 10, no. 7, pp. 2920–2931, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. M. J. Fonseca, C. L. Santos, P. Costa, L. Lencastre, and F. Tavares, “Increasing awareness about antibiotic use and resistance: a hands-on project for high school students,” PLoS ONE, vol. 7, no. 9, Article ID e44699, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. M. S. Dryden, J. Cooke, and P. Davey, “Antibiotic stewardship—more education and regulation not more availability?” The Journal of Antimicrobial Chemotherapy, vol. 64, no. 5, Article ID dkp305, pp. 885–888, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. World Health Organization, The Evolving Threat of Antimicrobial Resistance: Options for Action, 2014, http://whqlibdoc.who.int/publications/2012/9789241503181_eng.pdf.
  60. P. Davey and S. Garner, “Professional education on antimicrobial prescribing: a report from the Specialist Advisory Committee on Antimicrobial Resistance (SACAR) Professional Education Subgroup,” The Journal of Antimicrobial Chemotherapy, vol. 60, supplement 1, pp. i27–i32, 2007. View at Google Scholar
  61. C. Pulcini and I. C. Gyssens, “How to educate prescribers in antimicrobial stewardship practices,” Virulence, vol. 4, no. 2, pp. 192–202, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. L. Cantas, S. Q. A. Shah, L. M. Cavaco et al., “A brief multi-disciplinary review on antimicrobial resistance in medicine and its linkage to the global environmental microbiota,” Frontiers in Microbiology, vol. 4, article 96, Article ID Article 96, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Fischer, I. Rodrìguez, S. Schmoger et al., “Salmonella enterica subsp. enterica producing VIM-1 carbapenemase isolated from livestock farms,” The Journal of Antimicrobial Chemotherapy, vol. 68, no. 2, pp. 478–480, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. R. A. Horton, L. P. Randall, E. L. Snary et al., “Fecal carriage and shedding density of CTX-M extended-spectrum β-lactamase-producing Escherichia coli in cattle, chickens, and pigs: implications for environmental contamination and food production,” Applied and Environmental Microbiology, vol. 77, no. 11, pp. 3715–3719, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. N. Britten and O. Ukoumunne, “The influence of patients' hopes of receiving a prescription on doctors' perceptions and the decision to prescribe: a questionnaire survey,” British Medical Journal, vol. 315, no. 7121, pp. 1506–1510, 1997. View at Publisher · View at Google Scholar · View at Scopus
  66. J. Cockburn and S. Pit, “Prescribing behaviour in clinical practice: patients' expectations and doctors' perceptions of patients' expectations—a questionnaire study,” British Medical Journal, vol. 315, no. 7107, pp. 520–523, 1997. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Grigoryan, J. G. M. Burgerhof, J. E. Degener et al., “Attitudes, beliefs and knowledge concerning antibiotic use and self-medication: a comparative European Study,” Pharmacoepidemiology and Drug Safety, vol. 16, no. 11, pp. 1234–1243, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. C. A. M. McNulty, P. Boyle, T. Nichols, P. Clappison, and P. Davey, “The public's attitudes to and compliance with antibiotics,” The Journal of Antimicrobial Chemotherapy, vol. 60, supplement 1, pp. i63–i68, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Davey, E. Brown, L. Fenelon et al., “Interventions to improve antibiotic prescribing practices for hospital inpatients,” The Cochrane Database of Systematic Reviews, no. 4, Article ID CD003543, 2005. View at Google Scholar · View at Scopus
  70. R. G. Finch, F. B. Blasi, T. J. M. Verheij et al., “GRACE and the development of an education and training curriculum,” Clinical Microbiology and Infection, vol. 18, no. 9, pp. E308–E313, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. M. A. Thomson O'Brien, A. D. Oxman, D. A. Davis, R. B. Haynes, N. Freemantle, and E. L. Harvey, “Educational outreach visits: effects on professional practice and health care outcomes,” The Cochrane Database of Systematic Reviews, no. 2, Article ID CD000409, 2000. View at Google Scholar · View at Scopus
  72. S. B. Soumerai and J. Avorn, “Principles of educational outreach (‘academic detailing’) to improve clinical decision making,” The Journal of the American Medical Association, vol. 263, no. 4, pp. 549–556, 1990. View at Publisher · View at Google Scholar · View at Scopus
  73. L. M. Abbo, S. E. Cosgrove, P. S. Pottinger et al., “Medical students' perceptions and knowledge about antimicrobial stewardship: how are we educating our future prescribers?” Clinical Infectious Diseases, vol. 57, no. 5, pp. 631–638, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Heaton, D. J. Webb, and S. R. J. Maxwell, “Undergraduate preparation for prescribing: the views of 2413 UK medical students and recent graduates,” British Journal of Clinical Pharmacology, vol. 66, no. 1, pp. 128–134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. M. J. N. Gordoncillo, J. Bender, J. Noffsinger, and P. C. Bartlett, “Developing an open-access antimicrobial resistance learning site for veterinary medical students,” Journal of Veterinary Medical Education, vol. 38, no. 4, pp. 404–407, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. M. André, A. Vernby, J. Berg, and C. S. Lundborg, “A survey of public knowledge and awareness related to antibiotic use and resistance in Sweden,” The Journal of Antimicrobial Chemotherapy, vol. 65, no. 6, pp. 1292–1296, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. Y.-H. Chan, M. M. Fan, C.-M. Fok et al., “Antibiotics nonadherence and knowledge in a community with the world's leading prevalence of antibiotics resistance: implications for public health intervention,” American Journal of Infection Control, vol. 40, no. 2, pp. 113–117, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. C. A. M. McNulty, P. Boyle, T. Nichols, P. Clappison, and P. Davey, “Don't wear me out—the public's knowledge of and attitudes to antibiotic use,” Journal of Antimicrobial Chemotherapy, vol. 59, no. 4, pp. 727–738, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. F. Napolitano, M. T. Izzo, G. Di Giuseppe, and I. F. Angelillo, “Public knowledge, attitudes, and experience regarding the use of antibiotics in Italy,” PLoS ONE, vol. 8, no. 12, Article ID e84177, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Ferech, S. Coenen, S. Malhotra-Kumar et al., “European Surveillance of Antimicrobial Consumption (ESAC): outpatient antibiotic use in Europe,” Journal of Antimicrobial Chemotherapy, vol. 58, no. 2, pp. 401–407, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. D. M. Lecky and C. A. M. McNulty, “e-Bug implementation in England,” The Journal of Antimicrobial Chemotherapy, vol. 66, supplement 5, pp. v63–v66, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. B. Huttner, H. Goossens, T. Verheij, and S. Harbarth, “Characteristics and outcomes of public campaigns aimed at improving the use of antibiotics in outpatients in high-income countries,” The Lancet Infectious Diseases, vol. 10, no. 1, pp. 17–31, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Majeed and K. Moser, “Age- and sex-specific antibiotic prescribing patterns in general practice in England and Wales in 1996,” The British Journal of General Practice, vol. 49, no. 446, pp. 735–736, 1999. View at Google Scholar · View at Scopus
  84. A. Harnden, R. Perera, A. B. Brueggemann et al., “Respiratory infections for which general practitioners consider prescribing an antibiotic: a prospective study,” Archives of Disease in Childhood, vol. 92, no. 7, pp. 594–597, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. T. J. Sandora, M.-C. Shih, and D. A. Goldmann, “Reducing absenteeism from gastrointestinal and respiratory illness in elementary school students: a randomized, controlled trial of an infection-control intervention,” Pediatrics, vol. 121, no. 6, pp. e1555–e1562, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. D. M. Lecky, C. A. M. McNulty, N. Adriaenssens et al., “What are school children in Europe being taught about hygiene and antibiotic use?” The Journal of Antimicrobial Chemotherapy, vol. 66, no. supplement 5, Article ID dkr120, pp. v13–v21, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. E. de Quincey, P. Kostkova, G. Jawaheer, D. Farrell, C. A. M. McNulty, and J. Weinberg, “Evaluating the online activity of users of the e-Bug web site,” Journal of Antimicrobial Chemotherapy, vol. 66, supplement 5, Article ID dkr123, pp. v45–v49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. D. M. Lecky and C. A. M. McNulty, “Current initiatives to improve prudent antibiotic use amongst school-aged children,” The Journal of Antimicrobial Chemotherapy, vol. 68, no. 11, pp. 2428–2430, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. D. Farrell, P. Kostkova, L. Lazareck et al., “Developing e-Bug web games to teach microbiology,” The Journal of Antimicrobial Chemotherapy, vol. 66, no. 5, Article ID dkr121, pp. v33–v38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. K. Milburn, “A critical review of peer education with young people with special reference to sexual health,” Health Education Research, vol. 10, no. 4, pp. 407–420, 1995. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Maticka-Tyndale and J. P. Barnett, “Peer-led interventions to reduce HIV risk of youth: a review,” Evaluation and Program Planning, vol. 33, no. 2, pp. 98–112, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. P. J. Bush and A. P. Hardon, “Towards rational medicine use: is there a role for children?” Social Science & Medicine, vol. 31, no. 9, pp. 1043–1050, 1990. View at Publisher · View at Google Scholar · View at Scopus
  93. C. R. Lee, J. H. Lee, and S. H. Lee, “Comment on: current initiatives to improve prudent antibiotic use amongst school-aged children,” The Journal of Antimicrobial Chemotherapy, vol. 69, no. 6, pp. 1726–1727, 2014. View at Publisher · View at Google Scholar
  94. F. Allerberger, A. Lechner, A. Wechsler-Fördös, and R. Gareis, “Optimization of antibiotic use in hospitals—antimicrobial stewardship and the EU Project ABS International,” Chemotherapy, vol. 54, no. 4, pp. 260–267, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. L. Pagani, I. C. Gyssens, B. Huttner, D. Nathwani, and S. Harbarth, “Navigating the web in search of resources on antimicrobial stewardship in health care institutions,” Clinical Infectious Diseases, vol. 48, no. 5, pp. 626–632, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. S. A. Simpson, F. Wood, and C. C. Butler, “General practitioners' perceptions of antimicrobial resistance: a qualitative study,” Journal of Antimicrobial Chemotherapy, vol. 59, no. 2, pp. 292–296, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. O. J. Dyar, C. Pulcini, P. Howard et al., “European medical students: a first multicentre study of knowledge, attitudes and perceptions of antibiotic prescribing and antibiotic resistance,” The Journal of Antimicrobial Chemotherapy, vol. 69, no. 3, pp. 842–846, 2014. View at Publisher · View at Google Scholar · View at Scopus
  98. O. J. Dyar, P. Howard, D. Nathwani, and C. Pulcini, “Knowledge, attitudes, and beliefs of French medical students about antibiotic prescribing and resistance,” Medecine et Maladies Infectieuses, vol. 43, no. 10, pp. 423–430, 2013. View at Publisher · View at Google Scholar · View at Scopus
  99. L. A. Paterson Davenport, P. G. Davey, J. S. Ker et al., “An outcome-based approach for teaching prudent antimicrobial prescribing to undergraduate medical students: report of a Working Party of the British Society for Antimicrobial Chemotherapy,” The Journal of Antimicrobial Chemotherapy, vol. 56, no. 1, pp. 196–203, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Ross and S. Maxwell, “Prescribing and the core curriculum for tomorrow's doctors: BPS curriculum in clinical pharmacology and prescribing for medical students,” British Journal of Clinical Pharmacology, vol. 74, no. 4, pp. 644–661, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. D. Nathwani, J. Sneddon, W. Malcolm et al., “Scottish Antimicrobial Prescribing Group (SAPG): development and impact of the Scottish National Antimicrobial Stewardship Programme,” International Journal of Antimicrobial Agents, vol. 38, no. 1, pp. 16–26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. V. P. Luther, C. A. Ohl, and L. A. Hicks, “Antimicrobial stewardship education for medical students,” Clinical Infectious Diseases, vol. 57, no. 9, pp. 1366–1367, 2013. View at Publisher · View at Google Scholar · View at Scopus