104 RESEARCH Amy Patrick and Thayalan Kandiah DOI: /rcsfdj

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1 104 RESEARCH Amy Patrick and Thayalan Kandiah DOI: /rcsfdj

2 RESEARCH 105 Resistance to change: how much longer will our antibiotics work? by Amy Patrick and Thayalan Kandiah Antimicrobial resistance (AMR) is the ability of bacteria to change, rendering antimicrobials (such as antibiotics, antivirals and antimalarials) ineffective in treating common infections, or as prophylaxis after major surgery or cancer treatment. The World Health Organization (WHO) predicts that these superbugs will become a major threat to public health. 1 Authors: Amy Patrick*, Registrar in Oral and Maxillofacial Surgery and Paediatric Dentistry, East Surrey Hospital; and Thayalan Kandiah, Consultant in Paediatric Dentistry, East Surrey Hospital *Corresponding author: E: amy.patrick@nhs.net Keywords: Antibiotic, antimicrobial, dental prescribing guidelines

3 106 RESEARCH Amy Patrick and Thayalan Kandiah The threat is no longer a prediction for the future but a current finding in every region of the world, claiming 700,000 lives each year, a figure that could rise to 10 million by The Department of Health (DH) published a report in 2013 on antimicrobial prescribing and stewardship competencies, 3 for which there is a fiveyear action plan, and in 2017 the National Institute for Health and Care Excellence (NICE) produced similar guidelines. 4 The WHO has also mirrored the DH recommendations and has outlined a global plan. 1,5 The causes of AMR include prescribing unnecessary antibiotics, unsuitable use of broad spectrum antibiotics, wrong selection of drug and incorrect dose or duration. Patients also contribute by not taking antibiotics as prescribed, such as skipping doses or stopping earlier than recommended. 6 This is resulting in a higher demand for healthcare and longer stays in hospital requiring more intensive treatment, which increases the overall cost of healthcare. The National Health Service (NHS) will no longer be able to sustain this demand, and in April 2016 it launched a new programme aimed at hospitals and general practitioners supporting a national effort to improve prescribing practices. 7 Dentists prescribe 9% of antibiotics in primary care in the NHS and 5% overall so their involvement in these programmes is essential. 8 Several studies have investigated the contribution of dentists prescribing practices to AMR. In 2000 Palmer et al demonstrated in a study of 17,007 prescriptions that most were given against the published guidance on drug choice, dose and duration, 9 and their review in 2001 regarding the knowledge of general dental practitioners (GDPs) on antibiotic guidance recognised that postgraduate education had a significant impact on the protocols used. 10 In the same year, a study in Glasgow produced similar results. 11 Although Sweeney et al focused primarily on the impact of antibiotics on oral flora in their 2004 paper, they came to the same conclusion, namely that regular training alongside audit tools would be the best method of change management. 12 It is essential that national standards are being met to ensure patients receive the best possible management, both now and in the future. Contemporaneous, complete and accurate patient records are essential, as described in the General Dental Council s Standards for the Dental Team. 13 The aim of this pilot study was to carry out a retrospective audit of prescribing practices of the East Surrey Hospital (ESH) dental and maxillofacial team. It was also hoped that the audit would encourage good record keeping. Methods Three audit cycles were carried out to measure awareness of good prescribing practices such as when to prescribe and what to prescribe, according to guidelines. Standards for which compliance was measured comprised those in guidelines and recommendations by Public Health England, 7 the Faculty of General Dental Table 1 Summary of guidelines for prescribing antibiotics in a dental setting 3,8, Local measures to treat initial infection o Pulp extirpation o Extraction o Incision for soft-tissue lesion Antibiotics for spreading infection/systemic involvement o Cellulitis o Lymph node involvement o Pyrexia and malaise o Acute ulcerative gingivitis, sinusitis and pericoronitis with systemic features are indications for antibiotics Always use antibiotics in conjunction with local measures Use British National Formulary each time o New dose regimens including double dosage for infections causing eye closure, extraoral swelling or trismus Follow-up review is crucial must be documented Record of temperature is important Duration should be five days unless severe (clinician s judgement) Amoxicillin is the first choice as effective as penicillin V but better absorbed Metronidazole should be an adjunct in severe cases or if allergic to penicillin (exception: first choice for acute ulcerative gingivitis/pericoronitis) Erythromycin is another alternative if allergic to penicillin Pulpitis and dry socket are not indications for antibiotics unless patient is immunocompromised Second-line antibiotics only when first-line antibiotics have been ineffective o Clindamycin is effective against Gram-positive cocci but causes severe side effects o Co-amoxiclav is effective against beta-lactamase producing bacteria and is good in cases of spreading infection o Clarithromycin is marginally more effective than erythromycin o The above antibiotics are broad spectrum and will contribute to the development of antibiotic resistance

4 RESEARCH 107 Practice (UK), 8 the National Institute for Health and Care Excellence (NICE), 14,15 and the Scottish Dental Clinical Effectiveness Programme. 16 Cycle 1 ran from January to May 2014, using 100 random sets of notes from emergency dental service (EDS) patients. Cycle 2 ran from October 2014 to March 2015, with 100 random sets of notes from a mix of EDS and outpatients. The final cycle ran from January to June 2017, also with 100 random sets of notes from an EDS/outpatient mix. A proforma was used for data collection for each of the cycles. Data collected included age, sex, diagnosis, temperature record and appropriateness of prescription with complete details. Appropriateness was measured against the guidelines; for example, antibiotics are indicated in the presence of severe pain, swelling or pyrexia. This had to be evident in the clinical notes for it to be accepted as correct. Changes in practice between cycles 1 and 2 of the audit included addition of a prescription logbook to record details of any prescription issued, modification of the EDS template to include diagnosis and temperature, provision of a thermometer and departmental training regarding antimicrobial stewardship. Changes between the second and third cycles included further departmental training. Summary of guidelines Prescribing of antibiotics must be kept to a minimum and only used when there is a clear need. The use of broad spectrum antibiotics has been associated with a rise of Clostridium difficile in both primary and secondary care, and caution should be exercised when prescribing these to vulnerable groups such as the elderly or those with gastrointestinal disease. 17 The guidelines are summarised in Table 1. Standards to aim for at ESH include that 100% of patients should be prescribed the appropriate drug according to their dental condition and age. Furthermore, 100% of prescribed medicines should be recorded correctly in the patient s notes and prescription logbook. Results Table 2 and Figure 1 summarise the results for the different audit cycles. Prescriptions were documented in the clinical notes in the vast majority of cases in all three audits. Figure 1 Proportion of notes compliant with different standards... Proportion of notes compliant (%) Table 2 Compliance with standards in all three audit cycles showing changes between the cycles. Green indicates a positive change and red indicates a negative change.... Prescription documented in clinical notes Cycle 1 Cycle 2 Change Cycle 3 Change 100% 94% 6pp 91% 3pp Diagnosis documented 28% 87% 59pp 67% 20pp Correct drug and dose prescribed Prescription indicated (based on clinical notes) Patient had treatment and antibiotics Follow-up advice documented Prescription documented Diagnosis documented Prescription recorded correctly Prescription indicated Local measures used Follow-up advice recorded Temperature recorded Logbook used 94% 94% 91% 3pp 38% 61% 23pp 84% 23pp 22% 75% 53pp 68% 7pp 74% 53% 21pp 86% 33pp Temperature documented 0% 64% 64pp 63% 1pp Prescription logbook used 0% 98% 98pp 100% 2pp Cycle 1 Cycle 2 Cycle 3 The diagnosis was recorded in only 28% of cases in cycle 1. This figure rose to 87% in cycle 2 but decreased to 67% in the final audit cycle. The use of local measures followed a similar pattern: 22%, 75% and 68% respectively. The number of prescriptions not indicated decreased in each audit cycle (from 62% of cases in the first audit to 16% in the final audit). During the first audit, 69%

5 108 RESEARCH Amy Patrick and Thayalan Kandiah Figure 2 Proportions of different antibiotics used... Cycle 1 Amoxicillin Metronidazole Cephalosporin of the EDS patients were issued a prescription. This decreased to 47% of EDS patients by the end of the study. As a thermometer was only introduced after the first audit cycle, the patient s temperature was not recorded in any of the clinical notes in the first audit. Once it was introduced, compliance with this standard remained stable at 64% and 63% in the second and third cycles respectively. Co-amoxiclav Erythromycin Clindamycin Similarly, the prescription logbook was not used at all in the first audit period as this was another addition to the protocol after the first audit cycle. In cycle 2, the logbook was used in 98% of cases and this increased to 100% for cycle 3. Cycle 2 The wrong drug or dose was prescribed in 6% of the clinical notes for both the first and second audit cycles. This increased to 9% in the final cycle. Cycle 3 Amoxicillin Metronidazole Cephalosporin Co-amoxiclav Erythromycin Clindamycin Amoxicillin Metronidazole Cephalosporin Co-amoxiclav Erythromycin There was an improvement in terms of the type of antibiotics prescribed. The use of second-line antibiotics (cephalosporins, co-amoxiclav and clindamycin) decreased from 19% in cycle 1 to 6% in cycles 2 and 3 (Figure 2). Overall compliance with national guidelines increased from 22% to 75%. (In 9% of the clinical notes, compliance was non-verifiable as there was no mention of the relevant details.) Discussion Our study used clinical notes to assess whether antibiotics were indicated for each particular case. This may create its own bias. The first audit cycle only included EDS patients whereas outpatients were added for the latter two cycles. EDS appointments are notoriously short and notes may be brief. A clinician might simply write pain and correctly prescribe much needed antibiotics even though only severe pain indicates compliance with guidelines; without mention of swelling or pyrexia, these notes would give a false-negative result. Nevertheless, compliance in this area improved for each cycle, showing that either the notes became more specific (and therefore better justified the prescription) or that training was effective and clinicians became more aware of the stewardship programme. Cope et al found similar results, with 65.6% of antibiotics not being clinically indicated. 18 They felt that time pressures, patient expectation and refusal of operative treatment were the primary reasons for this. It is unlikely that primary care dental practices routinely take temperatures. On the other hand, the equipment for this does not have to be expensive; a simple disposable temperature strip would suffice. Furthermore, not only would it contribute to the evidence for indication for antibiotics but it would also add valuable information for the clinical picture and medical records should the patient return with no improvement or worsening symptoms.

6 RESEARCH 109 Use of a prescription logbook has enabled outpatient prescribing to be monitored. All clinical notes that did not include any details of the prescription (even though a prescription was recorded in the logbook) were for outpatients rather than EDS patients. Full details of the prescription were always provided in EDS notes although in some cases, notes were completely missing. Often, temporary notes are used and it is important that these are merged with the main medical records when the latter become available. Documenting a diagnosis as part of the clinical notes is essential; you cannot treat an individual unless a diagnosis has been reached. For the first audit cycle, 28% of patients had a documented diagnosis and this rose to 87% once the template was modified to include a diagnosis prompt. The third cycle did show a decrease to 67% despite further training but this may be because the training was given at departmental meetings and as EDS staff (who are responsible for most of the prescribing) are hired separately and are therefore not technically part of the department, they generally miss the training. Some notes were illegible and brief; a tick-box template would possibly save time in a pressured environment although it would not necessarily be possible to have an exhaustive list of diagnoses. Despite this, it could be a useful tool to show patients that the guidelines do not recommend antibiotics, perhaps changing their expectations. Prescribing practice became more compliant in terms of the types of drugs being prescribed. In the first audit cycle, second-line antibiotics were used in 19% of cases with no justification for the choice. Following training, this reduced to 6%. Nevertheless, amoxicillin is a broad spectrum antibiotic and will eventually become less effective as AMR predominates. The British National Formulary updated the paediatric dosage for amoxicillin in Previously, young children would be given 250mg courses. Now, anyone aged 5 years and above is prescribed 500mg whereas only children of 1 4 years of age are prescribed 250mg and those under 1 year are given 125mg (taking weight into consideration). 19 In addition, the recommended dose for metronidazole changed in 2016; for patients aged 12 years and above, 400mg courses are now advised. The main reason for non-compliant results in our audits was that old dosage recommendations were being followed, which is a clear indication that regular training and updates are needed. Even in the study by Palmer et al in 2000, looking at 17,007 antibiotic prescriptions from GDPs, the results were very similar. 9 The recommendation for dental infections in the Dental Practitioners Formulary at that time was phenoxymethylpenicillin or metronidazole and yet 78% of prescriptions were for amoxicillin or metronidazole. The ESH study demonstrates the progress made since then; no prescriptions were for Local measures are key in emergency dental treatment and antibiotics should be used as an adjunct phenoxymethylpenicillin. On the other hand, it should be expected that any change in guidance is put into effect immediately as these amendments are readily available in the British National Formulary and is easy to display as a quick reference poster to ensure the correct drug and course are being prescribed. Local measures are key in emergency dental treatment and antibiotics should be used as an adjunct. Cope et al found that only 29.5% of patients received operative treatment. 18 At ESH, use of local measures improved dramatically from 22% initially to 67% in the third audit cycle. Patient autonomy gives them the right to make decisions about their healthcare without the influence of a healthcare practitioner. This does not mean it is their right to have antibiotics if they so choose; if an antibiotic is not clinically indicated, it should not be prescribed but patients can refuse local measures. Nevertheless, this is an opportunity for patient education, which is important when considering how to manage and treat patients. With more than two-thirds of patients now receiving active treatment, it is no wonder the number of prescriptions overall has reduced. Ensuring the patient is followed up is difficult, especially given that many attendees at an emergency clinic are not registered with a GDP. Most dental infections need active treatment (whether extraction, root canal treatment or debridement) and, if this is not completed, the source of bacteria remains present and the patient will likely require another course of antibiotics, with multiple episodes once again contributing to the problem of AMR. Follow-up advice was reported in 86% of cases in the final audit cycle compared with 53%

7 110 RESEARCH Amy Patrick and Thayalan Kandiah Table 3 Summary of our recommendations for prescribing antibiotics... Regular training for all prescribing practitioners, particularly when changes to guidance are put into effect Use of audit tools (eg from FGDP[UK]) 22 for all primary and secondary care facilities Following current guidelines: o Documenting extent of swelling, severity of pain and diagnosis in clinical notes o Pyrexia the temperature should be recorded of any patient being treated for infection o Local measures treat the source of bacteria o Prescribing the correct drug, dose and duration o Correct protocol for prophylactic antibiotics Implementing templates or tick-box proformas in clinical notes (digital or paper) to encourage compliance with guidelines Quick reference guides or posters for general dental practitioners displayed wherever prescriptions are written in cycle 2. Overall, the interventions after each audit (particularly involving staff training in the department) appear to have been successful. Managed clinical networks under NHS England are groups that support local dental networks; each specialty (eg paediatric or special care dentistry) has its own group that can discuss current issues including funding and public health. The local dental networks have a responsibility to involve patients and the public alongside working with local authorities, Health and Wellbeing Boards, and clinical commissioning groups to provide local needs. 20 This is an excellent opportunity to empower GDPs and those who run emergency services should be a priority. These clinics can be sporadic and often have transient staff, there is no opportunity to follow up patients and it is often felt that there is insufficient time for operating. Providing them with courses and lectures as well as audit tools for AMR will give reliable data This is an excellent opportunity to empower GDPs and those who run emergency services should be a priority on a more comprehensive scale, enabling the managed clinical network to create models bespoke to any GDP s deficiencies regarding emergency treatment or prescribing practices. When looking at the benefits of further education on reviewing the knowledge of prescribing practices, Palmer et al found that those who had received training in the previous two years had a more sound understanding of the up-to-date guidance and protocols for antibiotics. 10 Targeting undergraduate and postgraduate students with stewardship programmes would therefore be beneficial. Teaching evidence-based medicine is particularly effective when integrated with clinical activity but can be even more so as spiral learning, where concepts increase in complexity and are reinforced throughout the years of learning within the infrastructure of the curriculum. 21 Our recommendations for prescribing antibiotics are summarised in Table 3. Conclusions AMR is a current issue that requires intervention on a global level. At a local level, departmental training has shown to be effective year on year at improving compliance with national guidelines on prescribing practices. Introducing accessible measures (eg a thermometer and well-designed templates) also aids in keeping comprehensive records. Providing stewardship programmes incorporating audit tools for undergraduate and postgraduate students as well as GDPs would capture a wider community. Alongside good prescribing practices, using local measures is also important as this can eliminate the need for antibiotics completely since the source of the infection will have been removed. Perhaps the drive to inform patients about AMR and the reasons behind it will make them more agreeable either to immediate treatment or to pursuing the follow-up advice given. Overall, efforts have to come from each individual, whether a clinician or a patient, in order to help reduce the occurrence of AMR, preventing common infections becoming death sentences. Clinicians should prescribe correctly, keep up to date and not buckle under pressure.

8 111 References 1. World Health Organization. Antimicrobial resistance. who.int/news-room/fact-sheets/detail/antimicrobial-resistance (cited May 2018). 2. O Neill J. Tackling Drug-resistant Infections Globally. London: HM Government; Public Health England. Antimicrobial Prescribing and Stewardship Competencies. London: PHE; National Institute for Health and Care Excellence. Antimicrobial Stewardship: Changing Risk-related Behaviours in the General Population. London: NICE; World Health Organization. Global Action Plan on Antimicrobial Resistance. Geneva: WHO; NHS Choices. The Antibiotic Awareness Campaign. uk/nhsengland/arc/ (cited May 2018). 7. NHS England. NHS England Launches national programme to combat antibiotic overuse (2016). antibiotic-overusage (cited May 2018). 8. Faculty of General Dental Practice (UK). Antimicrobial Prescribing for General Dental Practitioners. London: FGDP(UK); Palmer NO, Martin MV, Pealing R, Ireland RS. An analysis of antibiotic prescriptions from general dental practitioners in England. J Antimicrob Chemother 2000; 46: 1,033 1, Palmer NO, Martin MV, Pealing R et al. Antibiotic prescribing knowledge of National Health Service general dental practitioners in England and Scotland. J Antimicrob Chemother 2001; 47: Roy KM, Bagg J. Antibiotic prescribing by general dental practitioners in the Greater Glasgow Health Board, Scotland. Br Dent J 2000; 188: Sweeney LC, Dave J, Chambers PA, Heritage J. Antibiotic resistance in general dental practice a cause for concern? J Antimicrob Chemother 2004; 53: General Dental Council. Standards for the Dental Team. London: GDC; National Institute for Health and Care Excellence. Infection Prevention and Control. London: NICE; National Institute for Health and Care Excellence. Prophylaxis against Infective Endocarditis: Antimicrobial Prophylaxis against Infective Endocarditis in Adults and Children Undergoing Interventional Procedures. London: NICE; Scottish Dental Clinical Effectiveness Programme. Drug Prescribing for Dentistry. 3rd edn. Dundee: SDCEP: National Institute for Health and Care Excellence. Clostridium Difficile Infection: Risk with Broad-spectrum Antibiotics. London: NICE; Cope AL, Francis NA, Wood F, Chestnutt IG. Antibiotic prescribing in UK general dental practice: a cross-sectional study. Community Dent Oral Epidemiol 2016; 44: National Institute for Health and Care Excellence. Browse drugs. (cited May 2018). 20. NHS Commissioning Board. Securing Excellence in Commissioning NHS Dental Services. Leeds: NHS Commissioning Board; Ilic D, Maloney S. Methods of teaching medical trainees evidencebased medicine: a systematic review. Med Educ 2014; 48: Faculty of General Dental Practice (UK). Antimicrobial Prescribing for GDPs. antimicrobial-prescribing-gdps (cited May 2018).

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