Audit of Antibiotic Dispensing in Community Pharmacy (Happy Patient Project)

INTRODUCTION

The discovery of penicillin by Alexander Fleming at the start of the 20th century (1) led to the development of antibiotics. This transformed pharmacotherapy and saves many lives. However, the use of antibiotics has entailed the phenomenon of antibiotic microbial resistance (2).

The World Health Organization (WHO) as part of the antibiotics resistance containment strategy spurs on community pharmacists to notify patients of the correct way to use antibiotherapy and the importance of completing the treatments prescribed (3). When patients visit the CP to pick up medication prescribed by the doctor, the community pharmacist, by means of community pharmacy services (CPS) for dispensing, should perform the process according to a protocol.

The Pharmaceutical Care Forum in Community Pharmacy defines the dispensing of medicines and medical devices as “the CPS aimed to guarantee that the recipients of medicines and medical devices, after an initial evaluation, receive and use the medicines in accordance with their medical needs, at the doses prescribed according to their individual requirements, for the right amount of time, with the information to correctly process their use and in accordance with prevailing legislation” (4).

The dispensing and prescription of antibiotics may not be the most suitable in many European Union countries including Spain (5). This threatens the health of the population. So much so that incorrect use of antibiotics leads to death associated with more than 30,000 people a year in Europe, a figure that rises associated with the number of antibiotic-resistant infections from 2016 to 2020.

The Happy Patient project (www.happypatient.eu) (7) aims to reduce antibiotic resistance especially for the pathologies most commonly acquired in the community: infections of the respiratory, urinary and dental tract.

The actions performed in the Community Pharmacy are based on current scientific evidence and centred on the patient. This kind of strategy entails all the usual health professionals within the community setting. “Happy Patient” includes healthcare professionals accessible to patients in accident and emergency, health centres, socio-health centres, dental clinics and community pharmacies. The project is carried out in four countries with a high prescription of broad spectrum antibiotics (France, Poland, Greece and Spain) and a low prescription country (Lithuania) (8).

“Happy Patient” (9) is the acronym for “Health Alliance for Prudent Prescription and Yield of Antibiotics in a Patient-centred Perspective”. This is a consortium of research bodies, universities, scientific societies, foundations and a governmental entity ( see Appendix 1). The Spanish Society for Clinical, Family and Community Pharmacy (SEFAC) takes part in this project as a scientific society representing Spanish community pharmacists.

The community pharmacy project (CP) consists of an initial audit in which it is sought to tackle the intervention in regard to antibiotics from the point of view of the pharmacist. The aim is to analyze the characteristics and possible areas of improvement. Subsequently, training and specific materials are received targeted both at community pharmacists and patients to encourage a rational use of antibiotics. Consequently, the quality of the pharmaceutical intervention during community pharmacy services (CPS) for dispensing this group of medicines.

A second audit will be performed to ascertain the impact of the training received ( see Appendix 2) and to evaluate whether the intervention performed by community pharmacists taking part in the project has progressed.

This paper briefly reports the global results of the initial audit of the project “Happy Patient” in CP in Spain. Its aims were:

• To ascertain the antibiotherapy dispensing characteristics in Spanish community pharmacies.
• To compare the variability among the different Spanish community pharmacies whilst antibiotics are dispensed.

 

MATERIAL AND METHODS

To see the situation of different Spanish community pharmacies for dispensing antibiotics the “Audit Project Odense” (APO) method was used (10). Pharmacies taking part were asked to fill in a registration form for each orally administered antibiotic prescription received for at least five days. All pharmacies taking part had to record at least 25 antibiotic dispensing records (Figure 1). All pharmacists taking part, in addition to other health professionals (pharmacy technicians, assistants) who might take part in the dispensing procedure, also had an instructions sheet available to correctly fill out these registration forms (Figure 2).

The study was performed in Spain in 20 CP between February and April 2022. Only oral antibiotics for human use and treatment of acute infections were included. No antibiotics for veterinary or prophylactic use were recorded.

The registration sheets filled in were scanned and sent to the principal investigators of the “Happy Patient” project who statistically processed the data. Computerized data processing was performed with the programme Microsoft Excel® version 2021 .

The study was approved by IDIAPJGol Research Ethics Committee for Medicines (RECm) with code 21/120-P.

Figure 1 Antibiotic prescriptions record sheet

Figure 2 Instructions to correctly fill in the antibiotic prescriptions record sheet

RESULTS

A total of 573 antibiotic prescription users were interviewed. The estimated time to fill in the information for each patient was under one minute.

Filling in the registration sheets among Spanish CP taking part was highly variable (14 to 53 records, with a median of 28 records). A total of 59.9% of users (n=343) were women mainly belonging to the age group 40 to 49; 12.6% (n=72) of total users in the age group 0 to 19. The predominant user in this group was a man. A total of 78.4% (n=449) of records were filled in by pharmacists. Figure 3 reports the kinds of antibiotics prescribed. A total of 83.6% (n=479) of users knew about the kind of infection for which they had been prescribed an antibiotic. The most commonly prescribed antibiotic was amoxicillin (n=148), followed by amoxicillin with clavulanic acid (n=129) and macrolides or clindamycin (n=86).

To avoid possible negative outcomes associated with medicines (NOM), safety verifications on using prescribed medicines prior to dispensing, were 30.2% (n=173), 23.7% (n=136) and 48.5% (n=278) drug interactions, contraindications and allergies, respectively. No verification was made in 39.1% (n=224) of cases of dispensing.

Table 1 reports the personalized information for the medicine provided to users in regard to the use of prescribed antibiotics.

The pharmacist and technician agreed in 80.1% (n=459) of cases with the treatment prescribed by the doctor. However, not having sufficient information to decide was manifested in 17.6% of total cases and the prescriber was only contacted to request clarifications in four cases of dispensing (0.7%).

In regard to the personalized information for the medicine supplied to patients by pharmacies, 30% (n=6) of the 20 pharmacies taking part offered personalized information for the medicine about how long treatment lasts in at least nine out of every ten cases of dispensing. A total of 25% (n=5) of CP notified at least one in two times about the risk of antimicrobial resistance, whilst in 30% of CP (n=6) this warning did not occur under any circumstances.

Table 1 Personalized medicine information given to users

Figure 3 Types of antibiotics recorded

A total of 20% (n=4) of CP notified adverse effects in over 70% of the dispensing performed and in 95% (n=19) of pharmacies at least one safety verification was made.

DISCUSSION

To reduce antibiotic resistance, it may be suitable to ascertain the quality of dispensing in the CP. The purpose is to guarantee the efficacy and safety of the antimicrobial treatments prescribed. Obtaining a starting point such as the “Happy Patient” Audit is essential to help optimize the use of antibiotics, because analysis of the data obtained would enable making improvements and ensuring correct clinical practice, as has been carried out in other countries (11,12).

Although many pharmacists are aware of antibiotic resistance and agree that incorrect use is one of the main reasons for resistance, antibiotics are not correctly dispensed in all cases (13). They are sometimes dispensed without a medical prescription both in Spain (14) and in our close setting (15,16) or in the rest of Europe (17).

Antibiotic dispensing during the “Happy Patient” audit in Spanish CP was mainly to women (59.9%). This data is in accordance with the results of the systematic review by Schröder et al. in 2016. This concludes that more antibiotics were dispensed to women (18), which could be accounted for by more visits by women to health centres. We must also highlight that, during the “Happy Patient” audit and at earlier ages (0-10 years), males are prescribed more antibiotics than women; and that similar values are revealed in the studies published using meta-analysis techniques.

In the study by Bianco et al in 2021 (16) performed on 415 community pharmacists in Italy, 95.5%, 66.2% and 55.0% of pharmacists ask about allergies to antibiotics, notify patients about adverse effects and inform about the duration of the treatment, respectively. If we compare this to our study in regard to safety warnings we see that recommendations on allergies to antibiotics are almost half in our study (95.5% vs 48.5%), approximately 20% less in terms of warning about adverse effects (66.2% vs 39.4%); whilst there is slightly more information in our study (62.3% vs 55%) about the duration of treatment.

One of the possible roles of the community pharmacist in managing antibiotherapy, according to Liaskou et al. in 2018 (19), may be health education in patients. Despite this our results in the medicine’s personalized information to patients reveal low percentages of information on bacterial resistance (25.8%); return of excess medicine (5.4%); what to do if symptoms worsen (9.8%) and even in 14% of dispensing no personalized information on the medicine was issued. The latest Eurobarometer results (17) published by the European Commission, suggest that 85% of Spaniards surveyed believe that unnecessary use of antibiotics renders them ineffective, which could account for this little information on bacterial resistance. It is also true that those who believe that antibiotics are effective to cure colds (36%) and those who do not know whether or not they are effective for this pathology (9%) include almost half of those surveyed; whereby patient health education over a rational use of antibiotics is necessary, especially for common pathologies such as the common cold or symptoms such as a cough, which do not usually require antibiotics to be cured.

One of the measures generally recommended to prevent resistance is reducing the prescription of broad spectrum antibiotics (20). However, we observe that in our study only 16.1% of dispensing is broad spectrum antibiotics (penicillin V and macrolides). These data may help, together with those obtained by prescribers, to improve the quality of prescription of antimicrobials, as recommended by the European Union (20).

After the analysis of the audit, a subsequent educational intervention with the pharmacist might improve clinical practice and rational use of antibiotics, as has occurred in successful interventions focused on the community pharmacist in arterial hypertension, diabetes or dyslipidaemia (21). Furthermore, when a multidisciplinary approach is applied to management of antibiotics a significant reduction in unnecessary consumption is revealed (22). If the community pharmacist performs tests such as streptotest A in upper respiratory tract (23) or lower respiratory tract infections such as C reactive protein (24), may also mean a fall in unnecessary prescription of antibiotics.

However, an intervention by the pharmacist on the rational use of the medicine may lead to dissatisfaction in patients; in thinking that if their pathology actually requires an antibiotic (positive test) it is a waste of time having to go to the doctor to get a prescription from her (25).

The interventions a posteriori, have revealed, in different studies, the increased quality of dispensing, which improves patient safety and information on necessary aspects of pharmacotherapy (26–28). Moreover, it is related to a better adherence to antibiotics (29,30), improved perception of the information received by the patient and an increased knowledge on antibiotic resistance (29,31,32). These educational interventions may be: follow up and adherence to pharmacotherapeutic guidelines, tackling infections, training on requests for antibiotics in the CP without a prescription and good dispensing practices, and healthcare education for patients (33).

However, in the study by Saleh et al. in 2021 (34), after an educational intervention, 19% of community pharmacists still thought they should use broad spectrum antibiotics to try and reduce resistance or 18% thought that the most expensive antibiotic was related to better efficacy and lower resistance.

Beaucage et al. in 2006 (35) compared the effect of a phone call from the community pharmacist three days after routine dispensing with no phone call. In a subsequent contact after completing the treatment in the control group (without a call) a lower number of NOM were identified, mainly adverse reactions.

A total of 80.1% agreed with the antibiotic prescribed by the doctor and on very few occasions, was it deemed that based on its specifications the treatment was not the most suitable (0.3%). Bearing in mind that an incorrect diagnosis is related to antibiotic resistance (36), there was a critical lack of adapting pharmacotherapy to the patient’s health problem and a minimal communication among professionals. However, it must be highlighted that the four times the pharmacist contacted the doctor, the latter was receptive to the switch in prescription. The pharmacist should be more proactive in his actions, because being a specialist in the medicine he could train other health professionals in the pharmacology of antibiotics and collaborate on the correct choice of antibiotherapy (19,37); as the levels of antibiotic prescription vary locally, according to the individual practice of doctors or antibiotic class prescribed (38).

However, in 101 (17.1%) cases of dispensing, the pharmacist stated she did not have sufficient information to deem whether this antibiotherapy prescription was the most suitable. In these cases, without the necessary information, it is impossible for the community pharmacist to use the antibiotic rationally. This therefore facilitates adherence to clinical practice guidelines (37).

Moreover, despite the low frequency of contact with the prescriber (0.7%) in our study, all health professionals, the administration and patients should work together to carry out strategies with the aim of using antibiotics rationally; given that the multidisciplinary work on antibiotic resistance has proven its benefits in different studies (39–41).

Study weaknesses

The study was performed over a short timeframe, with a limited number of records and in only 20 community pharmacies. Moreover, the interventions were recorded by the members of the community pharmacies themselves. This may lead to bias in the results.

CONCLUSIONS

This audit enables ascertaining the routine practice of CP during antibiotic dispensing. It may also serve as a starting point to improve clinical practice, which improves the information to users and therapeutic adherence. This in turn would doubtless lead to a reduction in antibiotic resistance.

An intervention in antibiotic dispensing is needed in terms of safety verifications (interactions, allergies and contraindications), personalized information on the medicine (how long treatment lasts, dose, correct administration, adverse effects) and healthcare education (antibiotic resistance, recycling of medicines).

Subsequently, the variation in dispensing in each CP should be verified to correct possible deviations that may endanger the safety and efficacy of antibiotherapy.

ACKNOWLEDGMENTS

We are grateful to all Spanish community pharmacists who collated data. For reasons of study protocol they cannot be identified.

REFERENCES

1. Bentley R. The Development of Penicillin: Genesis of a Famous Antibiotic. Perspectives in Biology and Medicine. 2005;48(3):444-52. doi:10.1353/pbm.2005.0068

2. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022 Feb 12;399(10325):629-55. doi:10.1016/S0140-6736(21)027 24-0

3. Burroughs T, Najafi M, Lemon SM, Knobler SL. The resistance phenomenon in microbes and infectious disease vectors: implications for human health and strategies for containment: workshop summary. Appendix D, WHO Global Strategy for Containment of Antimicrobial Resistance: Executive Summary [Internet]. Washington: National Academies Press; 2003. Available at: https://www.ncbi.nlm.nih.gov/books/NBK97127/

4. Foro de Atención Farmacéutica-Farmacia Comunitaria (Foro AF-FC). Guía práctica para los Servicios Profesionales Farmacéuticos Asistenciales en la Farmacia Comunitaria. Madrid: Consejo General de Colegios Oficiales de Farmacéuticos; 2019. Available at: https://www.farmaceuticos.com/wp-content/uploads/2021/02/2021-guia-practica-spfa.pdf

5. Carbajal de Lara JA, Cantalapiedra Fernández F, Eguilleor Villena A, Gutiérrez Ríos P, Amador Fernández N, Molinero A. Perfil de las solicitudes de antibióticos en farmacia comunitaria con receta privada y prescripción irregular. Medicina de Familia SEMERGEN. 2020 Apr;46(3):194-201. doi:10.1016/j.semerg.2019.10.003

6. European Centre for Disease Prevention and Control. Assessing the health burden of infections with antibiotic-resistant bacteria in the EU/EEA, 2016-2020. [Internet]. LU: Publications Office; 2022 [cited 2022 Dec 27]. Available at: https://data.europa.eu/doi/10.2900/73460

7. Bjerrum A, García-Sangenís A, Modena D, Córdoba G, Bjerrum L, Chalkidou A, et al. Health alliance for prudent prescribing and yield of antibiotics in a patient-centred perspective (HAPPY PATIENT): a before-and-after intervention and implementation study protocol. BMC Prim Care. 2022 Dec;23(1):102. doi:10.1186/s12875-022-01710-1

8. European Centre for Disease Prevention and Control. Antimicrobial consumption in the EU/EEA (ESAC-Net) - Annual Epidemiological Report 2020. Stockholm; 2021. Available at: https://www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-consumption-europe-2021

9. Happy Patient [Internet]. 2019 [cited 2023 Mar 23]. Third European Union Health Programme [Internet]. Available at: ­https://­happypatient.eu/

10. Lambert M, Benko´´ R, Chalkidou A, Lykkegaard J, Hansen MP, Llor C, et al. Developing a Tool for Auditing the Quality of Antibiotic Dispensing in Community Pharmacies: A Pilot Study. Antibiotics. 2022 Nov 1;11(11):1529. doi:10.3390/antibiotics11111529

11. Ashiru-Oredope D, Susan Hopkins on behalf of the English Surveillance Programme for Antimicrobial Utilization and Resistance Oversight Group, Kessel A, Hopkins S, Ashiru-Oredope D, Brown B, et al. Antimicrobial stewardship: English Surveillance Programme for Antimicrobial Utilization and Resistance (ESPAUR). Journal of Antimicrobial Chemotherapy. 2013 Nov 1;68(11):2421-3. doi:10.1093/jac/dkt363

12. Nathwani D, Sneddon J, Malcolm W, Wiuff C, Patton A, Hurding S, et al. Scottish Antimicrobial Prescribing Group (SAPG): development and impact of the Scottish National Antimicrobial Stewardship Programme. International Journal of Antimicrobial Agents. 2011 Jul;38(1):16-26. doi:10.1016/j.ijantimicag.2011.02.005

13. Jamshed S, Padzil F, Shamsudin S, Bux S, Jamaluddin A, Bhagavathula A, et al. Antibiotic Stewardship in Community Pharmacies: A Scoping Review. Pharmacy. 2018 Aug 23;6(3):92. doi:10.3390/pharmacy6030092

14. Molinero A, Carbajal de Lara JA, Cantalapiedra Fernández F, Eguilleor Villena A, Gutiérrez Ríos P, Amador-Fernández N. Demanda de antibióticos sin prescripción en la farmacia comunitaria. Descripción de la intervención del farmacéutico. Medicina de Familia SEMERGEN. 2020 Nov;46(8):545-52. doi:10.1016/j.semerg.2020.06.025

15. Carbajal De Lara JA, Cantalapiedra Fernández F, Eguilleor Villena A, Gutiérrez Ríos P, Amador Fernández N, Molinero A. Perfil de las solicitudes de antibióticos en farmacia comunitaria con receta privada y prescripción irregular. Medicina de Familia SEMERGEN. 2020 Apr;46(3):194-201. doi:10.1016/j.semerg.2019.10.003

16. Bianco A, Licata F, Trovato A, Napolitano F, Pavia M. Antibiotic-Dispensing Practice in Community Pharmacies: Results of a Cross-Sectional Study in Italy. Antimicrob Agents Chemother. 2021 May 18;65(6):e02729-20. doi:10.1128/AAC.02729-20

17. European Commission. Directorate General for Health and Food Safety., Kantar Public. Antimicrobial resistance: report. [Internet]. LU: Publications Office; 2022 [cited 2023 Apr 4]. Available at: https://data.europa.eu/doi/10.2875/16102

18. Schröder W, Sommer H, Gladstone BP, Foschi F, Hellman J, Evengard B, et al. Gender differences in antibiotic prescribing in the community: a systematic review and meta-analysis. J Antimicrob Chemother. 2016 Jul;71(7):1800-6. doi:10.1093/jac/dkw054

19. Liaskou M, Duggan C, Joynes R, Rosado H. Pharmacy’s role in antimicrobial resistance and stewardship. Pharmaceutical Journal [Internet]. 2018 [cited 2023 Jan 11]. Available at: ­https://pharmaceutical-journal.com/article/research/pharmacys-role-in-antimicrobial-resistance-and-stewardship

20. European Commision. European Union Guidelines for the prudent use of antimicrobials in human health. Official Journal of the European Union. 2017;212:1-12. Available at: https://health.ec.europa.eu/latest-updates/eu-guidelines-prudent-use-antimicrobials-human-health-published-23-languages-2017-07-06_en

21. Bishop C, Yacoob Z, Knobloch MJ, Safdar N. Community pharmacy interventions to improve antibiotic stewardship and implications for pharmacy education: A narrative overview. Research in Social and Administrative Pharmacy. 2019 Jun;15(6):627-31. doi:10.1016/j.sapharm.2018.09.017

22. Roque F, Teixeira-Rodrigues A, Breitenfeld L, Piñeiro-Lamas M, Figueiras A, Herdeiro MT. Decreasing antibiotic use through a joint intervention targeting physicians and pharmacists. Future Microbiology. 2016 Jul;11(7):877-86. doi:10.2217/fmb-2016-0010

23. Bonafonte Jimeno MÁ, Boleda Relats X, Ricote Belinchón M. Utilidad del Streptotest en la farmacia comunitaria para la discriminación rápida de faringitis bacteriana y vírica en pacientes adultos. Farm Comunitarios. 2013;5(2):59-63. Available at: https://www.farmaceuticoscomunitarios.org/es/journal-article/utilidad-streptotest-farmacia-comunitaria-discriminacion-rapida-faringitis

24. Huddy JR, Ni MZ, Barlow J, Majeed A, Hanna GB. Point-of-care C reactive protein for the diagnosis of lower respiratory tract infection in NHS primary care: a qualitative study of barriers and facilita­tors to adoption. BMJ Open. 2016 Mar;6(3):e009959. doi:10.1136/bmjopen-2015-009959

25. Ashworth M, White P, Jongsma H, Schofield P, Armstrong D. Antibiotic prescribing and patient satisfaction in primary care in England: cross-sectional analysis of national patient survey data and prescribing data. Br J Gen Pract. 2016 Jan;66(642):e40-6. doi:10.3399/bjgp15X688105

26. Chalker J, Chuc NTK, Falkenberg T, Tomson G. Private pharmacies in Hanoi, Vietnam: a randomized trial of a 2-year multi-component intervention on knowledge and stated practice regarding ARI, STD and antibiotic/steroid requests. Trop Med Int Health. 2002 Sep;7(9):803-10. doi:10.1046/j.1365-3156.2002.00934.x

27. Tumwikirize WA, Ekwaru PJ, Mohammed K, Ogwal-Okeng JW, Aupont O. Impact of a face-to-face educational intervention on improving the management of acute respiratory infections in private pharmacies and drug shops in Uganda. East Afr Med J. 2004 Feb;Suppl: S25-32. Available at: https://pubmed.ncbi.nlm.nih.gov/ 15125113/

28. Chalker J, Ratanawijitrasin S, Chuc NTK, Petzold M, Tomson G. Effectiveness of a multi-component intervention on dispensing practices at private pharmacies in Vietnam and Thailand—a randomized controlled trial. Social Science & Medicine. 2005 Jan;60(1):131-41. doi:10.1016/j.socscimed.2004.04.019

29. West LM, Cordina M. Educational intervention to enhance adherence to short-term use of antibiotics. Research in Social and Administrative Pharmacy. 2019 Feb;15(2):193-201. doi:10.1016/j.sapharm. 2018.04.011

30. Muñoz EB, Dorado MF, Guerrero JE, Martínez FM. The effect of an educational intervention to improve patient antibiotic adherence during dispensing in a community pharmacy. Atención Primaria. 2014 Aug;46(7):367-75. doi:10.1016/j.aprim.2013.12.003

31. Merks P, S´ wieczkowski D, Balcerzak M, Drelich E, Białoszewska K, Cwalina N, et al. Patients’ Perspective And Usefulness Of Pictograms In Short-Term Antibiotic Therapy – Multicenter, Randomized Trial. PPA. 2019 Oct;13:1667-76. doi:10.2147/PPA.S214419

32. Gotsch AR, Liguori S. Knowledge, Attitude, and Compliance Dimensions of Antibiotic Therapy With PPIs: A Community Pharmacy-Based Study. Medical Care. 1982 Jun;20(6):581-95. doi:10. 1097/00005650-198206000-00004

33. Harris DJ. Initiatives to improve appropriate antibiotic prescribing in primary care. Journal of Antimicrobial Chemotherapy. 2013 Nov 1;68(11):2424-7. doi:10.1093/jac/dkt360

34. Saleh D, Abu Farha R, Alefishat E. Impact of Educational Intervention to Promote Jordanian Community Pharmacists’ Knowledge and Perception Towards Antimicrobial Stewardship: Pre-Post Interventional Study. IDR. 2021 Aug;14:3019-27. doi:10.2147/IDR.S324865

35. Beaucage K, Lachance-Demers H, Ngo TTT, Vachon C, Lamarre D, Guévin JF, et al. Telephone follow-up of patients receiving antibiotic prescriptions from community pharmacies. American Journal of Health-System Pharmacy. 2006 Mar;63(6):557-63. doi: 10.2146/ajhp050177

36. Chokshi A, Sifri Z, Cennimo D, Horng H. Global contributors to antibiotic resistance. J Global Infect Dis. 2019;11(1):36. doi:10.4103/jgid.jgid_110_18

37. Saha SK, Hawes L, Mazza D. Effectiveness of interventions involving pharmacists on antibiotic prescribing by general practitioners: a systematic review and meta-analysis. Journal of Antimicrobial Chemotherapy. 2019 May 1;74(5):1173-81. doi:10.1093/jac/dky572

38. Ashiru-Oredope D, Sharland M, Charani E, McNulty C, Cooke J, on behalf of ARHAI Antimicrobial Stewardship Group. Improving the quality of antibiotic prescribing in the NHS by developing a new ­Antimicrobial Stewardship Programme: Start Smart-Then Focus. Journal of Antimicrobial Chemotherapy. 2012 Jul 1;67(suppl 1):i51-63. doi:10.1093/jac/dks202

39. The Lancet. NICE antimicrobial stewardship: right drug, dose, and time? The Lancet. 2015 Aug;386(9995):717. doi:10.1016/S0140-6736(15)61522-7

40. Ashiru-Oredope D, Budd EL, Bhattacharya A, Din N, McNulty CAM, Micallef C, et al. Implementation of antimicrobial stewardship ­interventions recommended by national toolkits in primary and secondary healthcare sectors in England: TARGET and Start Smart Then Focus. J Antimicrob Chemother. 2016 May;71(5):1408-14. doi:10. 1093/jac/dkv492

41. Colligan C, Sneddon J, Bayne G, Malcolm W, Walker G, Nathwani D, et al. Six years of a national antimicrobial stewardship programme in Scotland: where are we now? Antimicrob Resist Infect Control. 2015 Dec;4(1):28. doi:10.1186/s13756-015-0068-1