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  1. 1. BSG Guidelines in Gastroenterology 2007ANTIBIOTIC PROPHYLAXIS IN GASTROINTESTINAL ENDOSCOPYMC Allison, JAT Sandoe, R Tighe, IA Simpson, RJ Hall, TSJ Elliott1.0 EXECUTIVE SUMMARY1.1 Infective endocarditis is an extremely rare complication following endoscopy.Because its sequelae can be devastating, it is recommended that antibiotics are givenbefore endoscopy in certain circumstances even though there is no good evidence thatantibiotics can prevent this complication.1.2 Antibiotic prophylaxis is recommended for all endoscopic procedures in patients athigh cardiac risk for endocarditis. Evidence Grade III, Recommendation Grade B.1.3 Antibiotic prophylaxis should also be given to patients at moderate risk ofendocarditis, or those with a history of recent vascular grafting or stenting, undergoing aprocedure with a high risk of bacteraemia. Procedures with high risk of bacteraemia areoesophageal dilatation, variceal injection, and thermal procedures such as laser or argonbeam ablation of a tumour. Oesophageal stenting and interventional procedures doneunder endoscopic ultrasound guidance are included in this category even though studieson associated bacteraemia are lacking. Evidence Grade IV, Recommendation Grade C.1.4 The recommended regime for adults is a single slow intravenous injection ofamoxicillin (1g for adults), followed by a single slow intravenous injection of gentamicin(1.5mg/kg). The post-procedure dose of amoxicillin has been abandoned. Teicoplaninshould be given instead of amoxicillin if there is a history of penicillin allergy. EvidenceGrade IV, Recommendation Grade C.1.5 Antibiotic prophylaxis is also recommended in circumstances whereimmunosuppression and/or neutropenia might cause symptomatic bacteraemia tobecome a potentially life-threatening event. Evidence Grade IV, Recommendation GradeC.1.6 Microbiological advice based on any recent positive cultures should be taken into 1
  2. 2. account when deciding on antibiotic prophylaxis regimens. Evidence Grade IV,Recommendation Grade C.1.7 Patients having a percutaneous endoscopic gastrostomy (PEG) should normallyreceive a single dose of intravenous cefuroxime or co-amoxiclav during the hour beforethe procedure. Evidence Grade Ia, Recommendation Grade A.1.8 Those already receiving broad spectrum antibiotics do not require additionalprophylaxis for PEG unless endocarditis cover is indicated. Evidence Grade III,Recommendation Grade B. The choice of antibiotic for patients having PEG with a historyof serious penicillin sensitivity has not been established, but clindamycin can be given.1.9 Antibiotic prophylaxis is recommended for all patients with pancreatic pseudocystundergoing ERCP. Patients with ongoing cholangitis should have already beenestablished on antibiotics. Routine prophylaxis for ERCP is not necessary in most othercircumstances provided that adequate biliary decompression can be achieved. EvidenceGrade III, Recommendation Grade B.1.9 There are specific circumstances where antibiotic prophylaxis should be givenroutinely to cover ERCP. These include patients with immunosuppression (e.g. followingliver transplant), and those biliary disorders, such as primary sclerosing cholangitis orhilar cholangiocarcinoma in whom it can be anticipated that complete biliary drainagewill be difficult or impossible to achieve during one procedure. Evidence Grade III,Recommendation Grade B.1.10 When prophylaxis for ERCP is given, oral ciprofloxacin or parenteral gentamicin isrecommended. A combination of parenteral amoxicillin and gentamicin should normallybe used to cover patients with endocarditis risk factors and evidence of biliaryobstruction. Evidence Grade IIa, Recommendation Grade B.1.11 The recommended antibiotic regimen for ERCP prophylaxis and persisting biliaryobstruction post-ERCP may need to be altered locally in the light of epidemiologicalpatterns in isolates of microorganisms resistant to these agents. Evidence Grade IV,Recommendation Grade C.1.12 Patients with suspected variceal bleeding, or patients with decompensataed liver 2
  3. 3. disease who develop acute gastrointestinal bleeding, should have already been establishedon intravenous antibiotics before undergoing endoscopy. The choice of antibiotics willnormally be guided by regional liver unit practice. Evidence Grade Ia, RecommendationGrade A.1.13 Units should ensure that there is a routine method (such as a check list) for drawingthe attention of the endoscopist to the patients to whom antibiotics should be given. Aspecimen pre-assessment proforma is attached.2.0 PREAMBLE2.1 AimThese guidelines aim to help clinicians in deciding which patients undergoing gastrointestinalendoscopy should receive antibiotic prophylaxis. They apply to the prevention of infectiveendocarditis in patients with cardiac risk factors, and also to patients at low risk of endocarditisundergoing procedures that are associated with a high risk of bacteraemia.2.2 DevelopmentThe British Society of Gastroenterology (BSG) first published guidelines on the use ofprophylactic antibiotics in 1996, and these were revised by Professor Mike Bramble in 2001.The British Cardiac Society (BCS) updated its guidelines on the prophylaxis and treatment ofinfecitive endocarditis in 2004. This prompted the Endoscopy Committee of the BSG toconvene a further Working Party, which met in March 2006. This was chaired by Dr RobinTeague, and, in addition to members of the Endoscopy Committee, incorporated representationfrom the BCS and the British Society for Antimicrobial Chemotherapy (BSAC). Dr MilesAllison researched the current literature, prepared the briefing documentation, and, after theWorking Party met, set about revising the previous version of the guidelines and preparing thefirst draft of the current guidelines. Further changes have been made in the light of commentsfrom members of the Endoscopy Committee and the Working Party.The members of the Working Party were not unanimous in their opinions concerning the riskof endocarditis following endoscopy. The recommendations are therefore based on a majority 3
  4. 4. consensus and are in concordance with the recently published guidelines for the prevention ofendocarditis published by BSAC (1).The guidelines conform to the North of England evidence based guidelines developmentProject. The grading of each recommendation is dependant on the category of evidencesupporting it. Recommendations based on the level of evidence are presented and graded as:A: requires at least one randomised controlled trial of good quality addressing the topic ofrecommendation (evidence categories Ia and Ib);B: requires the availability of clinical studies without randomisation on the topic ofrecommendation (evidence categories IIa, IIb and III);C: requires evidence from expert committee reports or opinions or clinical experience ofrespected authorities in the absence of directly applicable clinical studies of good quality(evidence category IV).2.3 Scheduled reviewThe content and evidence base for these guidelines should be reviewed within five years ofpublication.3. INTRODUCTIONBacteraemia is common following some forms of gastrointestinal endoscopic therapy, such asdilatation or submucosal injection, and can occur with diagnostic endoscopy alone.Fortunately complications resulting from dissemination of endogenous bacteria are uncommon,and infective endocarditis is a very rare complication. The evidence to support the view thatantibiotic prophylaxis can reduce the incidence of infective complications is somewhat limited.The area that has attracted the most controversy in recent years has been the use of antibioticprophylaxis in the prevention of infective endocarditis. The recommendations by the AmericanHeart Association (2: but see Footnote 14 below) have guided the advice of the national bodies 4
  5. 5. representing endoscopic practice (3,4), including the BSG (5). The traditionalrecommendation has been that patients at high risk of endocarditis, such as those with aprosthetic (i.e. tissue or artificial metal) valve and/or a past history of endocarditis shouldreceive antibiotics for all endoscopic procedures. More recently the European Society ofCardiology has recommended antibiotic prophylaxis to cover therapeutic endoscopy in patientswith acquired valvular heart disease (moderate endocarditis risk) (6) and the British CardiacSociety has gone even further, advising antibiotic prophylaxis for patients at moderate risk ofendocarditis undergoing any endoscopic procedure (7).The fact that current guidance is conflicting has been recognised by the British Society forAntimicrobial Chemotherapy, which at the time of writing has produced the most recentguidelines (1). The Endoscopy Committee of the BSG recognised the need for consensus onthis issue, and to this end convened a Working Party in the spring of 2006. The membership,comprised physicians with a special interest in gastroenterology, gastroenterologists,cardiologists and microbiologists. The gastroenterologists and microbiologists from thisWorking Party also took the opportunity to review the evidence underpinning the use ofantibiotic prophylaxis in other areas of endoscopic practice, in particular EndoscopicRetrograde Cholangiopancreatography (ERCP) and Percutaneous Endoscopic Gastrostomy(PEG).4. GENERAL CONSIDERATIONS4.1. The aims of antimicrobial prophylaxis in gastrointestinal endoscopy are to prevent:•Infective endocarditis.•Symptomatic bacteraemia.•Colonisation of vascular grafts and endovascular stents, orthopaedic and other non- cardiac prosthetic implants.•Pancreatico-biliary infection following ERCP.•Wound infection and peritonitis following percutaneous procedures. 5
  6. 6. 4.2. The potential benefits of antibiotic prophylaxis should be weighed up against:• The potential contribution to the selection of resistant bacteria, such as MRSA• The knowledge that antibiotics may fail to prevent infective endocarditis or other infective complications• The small risk of adverse events, including anaphylaxis• The practical difficulties and costs of antibiotic administration, especially in patients who are allergic to penicillin 4.3 Endocarditis risk following endoscopy Prospective studies to determine the value of antibiotic prophylaxis of endocarditis during gastrointestinal endoscopy are not available. Such research is unlikely to be done for two reasons. Firstly there is a natural reluctance to include patients at high risk of endocarditis into a placebo group, and secondly endocarditis complicating endoscopy is extremely rare, so prospective studies would need to recruit very large numbers of subjects. Thus, although recommendations can be based on an understanding of the pathology of infective endocarditis, they are of necessity pragmatic. 4.4. Identification of at-risk patients Units should ensure that there is a routine method (such as a check list) for drawing the attention of the endoscopist to the patients to whom antibiotics should be given. The conditions which render the patient at high risk of developing endocarditis are listed later. 5. BACTERAEMIA 5.1. Evidence for bacteraemia in gastrointestinal endoscopy The existence of bacteraemia during upper and lower gastrointestinal endoscopy has been well established in numerous series over decades (Table 1). These studies were reviewed in the previous edition of these guidelines (5) and more recently by Nelson (8). Some published papers overestimate the rates of potentially significant bacteraemia because microorganisms which are frequent contaminants (with little or no pathogenic potential) have been included. Other series, particularly some of the older studies, give misleadingly low rates because of deficiencies in culture techniques, especially those for anaerobic bacteria. 6
  7. 7. One study of bacteraemia associated with upper gastrointestinal endoscopy inimmunosuppressed patients (in whom intravascular destruction of bacteria is minimised)reported a high rate of clinically significant bacteraemia (9/47, 19%) (9).Bacteraemia during ERCP is considered to result mainly from contrast injection andmanipulation around endogenous bacteria in bile and/or pancreatic tissue of patients with pre-existing pathology such as biliary obstruction or pseudocyst. Bacteraemia during ERCP isinfrequent among patients without evidence of biliary or pancreatic ductal obstruction (8).5.2. Clinical importance of bacteraemiaRecent evidence confirms that everyday activities such as chewing or tooth brushing produce abacteraemia of dental flora (10,11). The incidence of bacteraemia during endoscopy has beenextensively studied but the incidence of symptomatic bacteraemia is less well understood. Inthe great majority of cases endoscopy-related bacteraemia is not associated with anyrecognisable symptoms.Thus, in most instances, there would seem to be little reason to attempt to reduce the rate ofendoscopy associated asymptomatic bacteraemia in the absence of delayed clinical sequelae.The most serious potential sequelae of bacteraemia include infective endocarditis, meningitis,cerebral abscess, and infected ascites (bacterial peritonitis) in patients with cirrhosis (8). Thesecomplications, whilst rare, are more likely to follow procedures associated with the highest riskof bacteraemia, namely oesophageal dilatation or injection sclerotherapy of varices.5.3 Prevention of bacteraemiaOne study has assessed prospectively (but in an open study design) the efficacyof antibiotic treatment in reducing bacteraemia rates during endoscopy (12). Alternatepatients aged 60 years and over undergoing gastroscopy were given antibiotics. Bloodcultures were negative in all 130 patients receiving antibiotics but positive in 13/132controls (9.8%, p<0.001). However, the microorganisms isolated could all have been skin 7
  8. 8. contaminants, and neither the patients who received antibiotics nor the controls experiencedany symptoms likely to have been associated with bacteraemia.6. INFECTIVE ENDOCARDITIS6.1. Background and literature surveyOver recent decades the numbers of gastrointestinal endoscopic procedures have been carriedout worldwide has risen exponentially. It is therefore reassuring that there is no evidence ofany concomitant increase in the incidence of endocarditis. Reports of endocarditis associatedwith endoscopic procedures have occurred less than once per year (Table 2) and it is not cleareven in this small number of cases whether the association was always causal. On the otherhand not all cases of infective endocarditis following endoscopy are reported, and theassociation may not always be recognised.A UK collaborative survey of 582 patients with infective endocarditis identified three patientsin whom there was a history of recent gastroscopy (13). The significance of these findings hasbeen questioned because there was no control group. The other case reports linking infectiveendocarditis to recent endoscopic procedures (14-30) are summarised in Table 2. Someimportant points arise from these cases:• High risk patients such as those with tissue or mechanical prosthetic valves are included (17,19)• There is an example of failure of antibiotic prophylaxis (17)• There are examples of patients with no prior history of cardiac disease (16,23)• Other clinical factors may have influenced the endocarditis risk (18,19)• Marked variation in time interval between endoscopy and onset of symptoms6.2. Does antibiotic prophylaxis prevent endocarditis?There is only limited evidence that antibiotic administration during dental or surgical 8
  9. 9. procedures reduces the risk of endocarditis (31). Failures of antibiotic prophylaxis to preventendocarditis are well recognised (32), and include an example of failure of prophylaxisduring a gastrointestinal endoscopic procedure (17). In the rabbit model, antibiotic prophylaxishas been shown to reduce the risk of infection in damaged valves following high bacterialchallenge (33). A retrospective case control study of patients at risk suggested that antibioticprophylaxis might be effective in preventing endocarditis in dental practice (34), but a recentCochrane review has come out against the routine use of prophylactic penicillin for invasivedental procedures (35).Many patients with cardiac pathology are unaware that they have any abnormality. Thusascertainment of at-risk patients will always be incomplete. One member of our Working Partybelieves that “the presence of moderate or high risk cardiac conditions should be excluded by acareful history and physical examination before performing any invasive investigationincluding endoscopy” (36). There are real practical difficulties inherent in putting such adviceinto practice:6.2.1. Many patients referred for endoscopy could harbour previously unknown valvular disease. Over half of males aged over 65 years have systolic murmurs (37). It has been suggested that one in six patients attending for diagnostic endoscopy has a clinically detectable valvular lesion (38).6.2.2. Not all patients with documented acquired valvular disease will carry an antibiotic card or be aware of the findings from previous echocardiography.6.2.3. Tens of thousands of patients per year in the UK undergo direct access endoscopy under the care of a nurse endoscopist.6.2.4. Even if guidelines are established, many patients may be given the wrong antibiotic or none at all.6.3. Risk factors for endocarditisThe risk of endocarditis varies according to the nature of the underlying cardiac condition. Forthe large majority of patients there is worldwide consensus on the classification of endocarditis 9
  10. 10. risk (2, 39-41). Nonetheless there are some differences of opinion in this area. Europeancardiology working parties have classified complex and/or cyanotic congenital heart diseasewithin the high risk bracket (6,7). One of these groups also regards mitral valve prolapse to bea high risk cardiac lesion in circumstances where there is marked valve thickening and/orregurgitation (7). Given the recent advice to dentists by the British Society for AntimicrobialChemotherapy (1) that routine antibiotic prophylaxis should be restricted to those with ahistory of previous endocarditis, prosthetic heart valves and surgically constructed intra-thoracic vascular conduits, the majority of the BSG Working Group agree that the high riskgroup should comprise the above three conditions (Table 3). This is in keeping with Americanguidelines, which encompass also the rare scenario of endoscopy in patients with complexcyanotic congenital heart disease (e.g. single ventricle states, transposition of the great arteries,tetralogy of Fallot ) (2,4).The risk of endocarditis is probably influenced by the incidence (Table 2) and intensity ofbacteraemia associated with the endoscopic procedure and on the potential virulence of themicro-organism(s). Indeed bacteria vary greatly in their propensity to infect damaged heartvalves.6.4. Recommendations for endocarditis prophylaxis during endoscopy (Tables 4 and 5)Previously healthy patients not known to have cardiac lesions who undergo proceduresassociated with a low incidence of bacteraemia have an extremely low risk of endocarditis.Antibiotic prophylaxis is therefore not justified in these circumstances.Patients with cardiac lesions associated with a high risk of endocarditis should be givenantibiotic prophylaxis for all endoscopic procedures. Those with a moderate risk ofendocarditis who undergo gastrointestinal endoscopic procedures with a known high risk ofbacteraemia (42-48) have an increased risk of endocarditis and should also receive antibioticprophylaxis. It is recognised that the American Heart Association, over a year after themeeting of our Working Party and at the time of submission of the guidelines herein, haveconcluded that there is no evidence to support the administration of antibiotics with the sole 10
  11. 11. aim of preventing endocarditis after gastrointestinal and genitourinary procedures (seeFootnote 14 below).Recommendations for endocarditis prophylaxis are set out according to cardiac and procedure-associated risk factors in Table 4. Recommendations on the type of antibiotics, doses andtiming of administration are given in Table 5. Teicoplanin has replaced vancomycin in patientswho are allergic to penicllin. There are two reasons for this: firstly teicoplanin is easier andquicker to administer, and secondly there is some evidence that teicoplanin has a longerduration of action following a single dose (49).7. ENDOSCOPIC RETROGRADE CHOLANGIOPANCREATOGRAPHY (ERCP)7.1 Bacteraemia is well recognised during ERCP (45-48). Pancreato-biliary infection occursafter 0.4-0.8% of endoscopic biliary procedures. These episodes must always be takenseriously because fatality may occur in 8-20% of such cases (50)..7.2 It was initially believed that the failure of early studies of antibiotic prophylaxis to showbenefit was because the case mix included both diagnostic and therapeutic procedures.Infection is rare after diagnostic ERCP in the absence of stones or pancreatic or biliaryobstruction. In patients with obstructed bile ducts with features of previous infection, orpancreatic pseudocyst, the available data suggests a reduction in clinically significant infectivecomplications when prophylactic antibiotics are used (47,51,52). On closer scrutiny of thesepapers, however, the examples of procedure-related cholangitis were almost all in patients forwhom adequate biliary drainage had not been achieved during ERCP. The contention thatrelief of obstruction is more important than antibiotic prophylaxis is reinforced by the findingthat the chief predictor of infective complications after therapeutic ERCP is incomplete bileduct drainage (53).Although not all authorities are in agreement (54-57), the case has been made for prophylacticadministration of antibiotics for patients likely to undergo a therapeutic procedure in thecontext of ongoing biliary obstruction and/or infection and/or pancreatic pseudocyst (58,59). 11
  12. 12. There is also a suggestion that antibiotic prophylaxis is cost-effective in these circumstances(58). This begs the question as to what constitutes “biliary obstruction”. Patients presentingwith bacterial cholangitis should already be established on antibiotics at the time of ERCP.Patients with jaundice secondary to obstructing common duct stones or strictures may notnecessarily require antibiotics provided that the obstruction can be properly relieved at ERCP(54). Similarly non-jaundiced patients with common duct stones may not need antibiotic coverprovided that the stones can be removed or drainage can be secured by means of stenting (withor without biliary sphincterotomy). These arguments have led Subhani and colleagues topropose that antibiotics can be administered immediately after ERCP if it has not been possibleto decompress the biliary tree (56). This approach has not been tested in clinical practice anddeserves further study.Other factors that are important in reducing the risk of infection include (i) the optimalcleansing and disinfection of the endoscope; (ii) the employment of single use accessoriesdown the working channel of the duodenoscope; and (iii) the use of sterile contrast mediumand careful control of the volume of contrast used. Some experts advocate that the endoscopistshould aspirate bile from the biliary tree in order to attenuate the rise in intrabiliary pressurefollowing contrast injection. Some authorities add antibiotics to the contrast media prior toinjection. Neither of these two strategies, however, has been shown to reduce the risk ofbacteraemia or cholangitis.The choice of antibiotic depends on the clinical context. Common causative micro-organismsin ascending cholangitis are Escherichia coli, Pseudomonas aeruginosa, Klebsiella spp.,enterococci, coagulase negative staphylococci and Bacteroides spp, but many infections arepolymicrobial (56).Our recommendations are summarised in Table 5. There are several scenarios to consider:7.2.1 Patients with cardiac pathology at moderate or high risk of endocarditis. Those with moderate endocarditis risk should receive endocarditis prophylaxis if biliary obstruction and/or pancreatic pseudocyst are suspected. All patients at high risk of endocarditis should receive prophylaxis as discussed in Section 4, and Tables 4 and 5. 12
  13. 13. 7.2.2 Patients with ongoing pancreatic or biliary sepsis. The choice of antibiotic prophylaxis is best guided by the results of recent microbiological cultures. These patients will normally already be receiving appropriate antibiotics, and the need for additional cover should be discussed with a clinical microbiologist.7.2.3. Patients with first ERCP for biliary obstruction, no clinical evidence of infection and low endocarditis risk. In these circumstances it is reasonable for the endoscopist to elect not to give antibiotics pre-procedure provided that their administration is ensured as soon as possible post-procedure if adequate decompression of the biliary tree has not been achieved. The course of antibiotics should continue whilst arrangements are being made to relieve biliary obstruction as soon as possible (either by repeat ERCP or by some other means) and should last at least until this endpoint has been achieved. The choice of antibiotics has been debated and reviewed in depth (56-58) and the role of specific antibiotics is discussed in Section 12. Most authorities recommend either oral ciprofloxacin taken 90 minutes before the procedure, or intravenous gentamicin at the time of sedation. Both ciprofloxacin and gentamicin have gaps in the cover they provide. Both have generally good activity against Gram-negative aerobic bacteria but are much less active against many Gram-positive species, including enterococci. Increasing ciprofloxacin resistance among coliforms (Enterobacteriaceae) has also been reported (60). Therefore the choice between ciprofloxacin and gentamicin may be influenced by local epidemiology in microbial resistance. Oral ciprofloxacin is less expensive than the intravenous formulation and results in satisfactory blood concentrations. Although gentamicin does not penetrate into bile very well, and has limited activity against enterococci, it probably has broader Gram-negative activity than ciprofloxacin. Neither regimen provides particularly good cover for an obstructed biliary system where enterococci are implicated in up to 40% of infections (55). Therefore the combination of amoxicillin with continued treatment with the antibiotic chosen for prophylaxis should be considered in a patient who became febrile 13
  14. 14. post-procedure.7.2.4 Patients with a history of prior biliary manipulations: Bile within the biliary tree is normally sterile. ERCP with sphincterotomy and/or stenting disrupts the normal ampullary barrier to the gut, and is associated with long term bacterobilia (61,62). It is therefore logical to infer that patients needing repeat biliary intervention at ERCP are at increased risk of bacteraemia and cholangitis. In a large prospective series (as yet unpublished) cholangitis complicating ERCP was more likely to occur in patients with a history of prior ERCP (with sphincterotomy and/or stenting) (P Cotton: personal communication). Patients who have been receiving continuous antibiotic prophylaxis for the prevention of recurrent symptomatic bacteraemia following biliary stenting may have acquired resistant bacterial flora, and should be given a different antibiotic to cover further biliary endoscopic procedures such as stent changes. Because of the lack of an evidence base, we believe that the decision as to whether to use prophylactic antibiotics in immunocompetent patients undergoing repeat ERCP rests with the endoscopist, the local clinical microbiologist and the clinical team caring for the patient. When ERCP is performed in patients who have previously received full treatment courses of one antibiotic, consideration should be given to the use of an alternative antibiotic (or combination of antibiotics) to cover the procedure. For example, if a patient has been exposed to prolonged and/or frequent ciprofloxacin, a combination of amoxicillin and gentamicin, or monotherapy with a wider spectrum penicillin such as piperacillin with tazobactam, could be given.7.2.5 Other settings in which prophylaxis for ERCP should be given include (i) immunosuppressed patients including those undergoing biliary intervention post liver transplant, and those with neutropenia; (ii) patients with known Caroli’s disease or primary sclerosing cholangitis, not only because bacterial cholangitis is common following biliary manipulation (63) but also because complete relief of biliary obstruction is unlikely to be achieved at ERCP; (iii) patients with Bismuth type III or type IV cholangiocarcinoma, for whom it may likewise be difficult or impossible to secure drainage of all liver segments; (iv) patients with pancreatic pseudocysts; and (v) 14
  15. 15. those with a history of recent vascular graft insertion.8. COLONISATION OF VASCULAR GRAFTS/STENTS AND ORTHOPAEDIC,NEUROSURGICAL AND OTHER NON-CARDIAC PROSTHESES8.1 It has been suggested that some delayed infections of orthopaedic, neurosurgical andother prostheses may be due to haematogenous spread of bacteria following endoscopy orsurgery. If so, the incidence of such infections might be reduced by more widespread use ofantibiotic prophylaxis in both dentistry and endoscopy. As bacteraemia occurs during activitiesas trivial and as frequent as tooth brushing (10,11), there appears to be minimal benefit fromsuch treatment. Lifelong antibiotic prophylaxis for all patients with orthopaedic, neurosurgicaland other implanted prosthetic materials would be more logical but adverse effects wouldalmost certainly outweigh any potential benefit.8.2 We are in agreement with the American Society of Colon and Rectal Surgeons in theirview that the risk following colonic and rectal endoscopy is low for patients with orthopaedicprostheses, central nervous system vascular shunts, penile prostheses, intra ocular lenses,pacemakers and local tissue augmentation materials (64). We do not recommend the useof prophylactic antibiotics in this setting.8.3 Expert opinion has suggested that patients who have undergone vascular grafting and/orendovascular stenting within the preceding 3 months should be treated in the same manner aspatients at moderate endocarditis risk. Selective antibiotic prophylaxis should be administeredto cover the endoscopic procedures commonly associated with bacteraemia (Table 4).9. PERCUTANEOUS ENDOSCOPIC GASTROTOMY (PEG)Early evaluations of single-dose intravenous cephalosporins failed to demonstrate efficacy inthe prevention of peristomal infections (65,66). The last ten years have witnessed a wealth of 15
  16. 16. controlled trials in this area. The evidence from these is consistent and indicates that antibioticprophylaxis is effective at reducing wound infection rates using a single dose of an appropriateantibiotic (67-74). A meta-analysis also comes out in favour of antibiotic prophylaxis,suggesting a number needed to treat of 5.7 to prevent one peristomal infection (75). A secondor third generation cephalosporin or co-amoxiclav given intravenously are both effective, andthere is also some evidence that antibiotic prophylaxis is cost-effective (76). Many patientswho claim to be allergic to penicillin will have previously received a cephalosporin withoutincident, and, cefuroxime can be used in this setting. Cefuroxime can be given safely to mostpatients who have a history of penicillin allergy (77), but should be avoided in people whohave a clear history of anaphylaxis with penicillin and/or cephalosporins. In suchcircumstances an infusion of clindamycin (300mg in adults) will cover staphylococci and moststreptococci excluding enterococci.Three areas of uncertainty remain on this topic. Firstly many patients undergoing PEG arealready receiving courses of broad-spectrum antibiotics, and there is some evidence that woundinfections are less common in this group (65, 67, 73). Such patients may not need furtherprophylaxis, and the use of additional antibiotics could predispose to methicillin-resistantStaphylococcus aureus (MRSA) colonisation. Secondly, the most common end-point inclinical trials of antibiotic prophylaxis is the development of peristomal wound infections,many of which are of doubtful clinical importance. Notwithstanding this caveat, there is someevidence that single-dose intravenous antibiotic may help in preventing more serious infectionssuch as aspiration pneumonia (68, 71, 74). Thirdly, a significant proportion of peristomalinfections are MRSA-related, particularly in patients with nasopharyngeal colonisation (78.79).It has recently been suggested that MRSA decolonisation using oral and nasally deliveredpreparations might reduce the risk of MRSA-related peristomal infection in such patients (80).The possible role of prophylaxis with vancomycin in patients with MRSA colonisationrequiring PEG remains to be determined.10. ANTIBIOTICS IN VARICEAL BLEEDING 16
  17. 17. Bacterial infections occur within 48 hours of admission in about 20% of patients with cirrhosis withupper gastrointestinal bleeding (81). Variceal sclerotherapy in the emergency setting commonlycauses bacteraemia (43). Prognosis in terms of rebleeding, failure to control bleeding, and in-hospitaloutcome is worsened in patients with associated bacterial infection. (82,83). In a meta-analysis offive controlled trials of antibiotic prophylaxis in patients with variceal bleeding, their use wasassociated with significantly improved short term survival (84). A Cochrane review also suggeststhat patients with cirrhosis and upper gastrointestinal bleeding should receive antibiotic prophylaxis(85). Patients with suspected variceal bleeding should already have been commenced on antibioticsbefore endoscopy. There is limited evidence to suggest superiority of any particular regimen in thissetting (86) but a combination of cefuroxime and metronidazole, or co-amoxiclav alone, arereasonable choices. Intravenous ceftriaxone has been shown to reduce infection risk moreeffectively than oral norfloxacin in one study (87). Third or fourth-generation cephalosporins (or co-amoxyclav) should be employed in patients with co-existing spontaneous bacterial peritonitis (88).11. ENDOSCOPIC ULTRASOUNDAlthough bacteraemia following endoscopic ultrasound (EUS) with fine needle aspiration (FNA) isuncommon (89-91), infective complications can occur following aspiration of pancreatic cysticlesions (92-96). It is therefore recommended that endocarditis prophylaxis is given to patients atmoderate or high cardiac risk undergoing EUS-guided therapeutic endoscopy. Patients at low riskmay require antibiotic cover for therapy, especially if there is a possibility of pre-existing infectionwithin a cyst or cavity being treated. Endoscopic ultrasound guided FNA does not require antibioticprophylaxis unless the patient is at high endocarditis risk (97).12. ANTIBIOTIC RECOMMENDATIONS12.1 Ampicillin and amoxicillinGram-positive bacteria, especially streptococci and enterococci, cause most infectiveendocarditis. Because of the possibility sequelae from enterococcal bacteraemia, particularlyafter instrumentation of the lower gastrointestinal tract, ampicillin or amoxicillin 17
  18. 18. are preferred to penicillin for prophylaxis. All three are effective in killing most oralstreptococci.12.2 AminoglycosidesThe use of an aminoglycoside such as gentamicin increases the bactericidal power ofampicillin or amoxicillin against streptococci and enterococci. Although the use of one or twodoses only of gentamicin confers negligible risk of nephro-or ototoxicity, care must be taken inpatients with a history of pre-existing renal impairment and/or a history of gentamicinnephrotoxicity. Gentamicin is also active against most aerobic coliforms (and mostPseudomonas sp.) and is also suitable for use in neutropaenic patients.12.3 CiprofloxacinCiprofloxacin has good antimicrobial activity against aerobic gram-negative bacteria but ismuch less active against many gram-positive species, including enterococci. It is therefore notsuitable for prevention of endocarditis but is widely used for the prevention of gram-negativesepsis after ERCP (98-101). Oral ciprofloxacin is considerably cheaper than the intravenouspreparation and results in adequate blood concentrations.12.4 GlycopeptidesGlycopeptides such as vancomycin or teicoplanin, with a very broad spectrum of activityagainst gram-positive bacteria, have a role when the patient has been exposed in the recent pastto penicillin, ampicillin or amoxicillin, and in patients who are allergic to penicillins.However, though still uncommon in the UK, vancomycin resistant enterococci (VRE) arebeing encountered with increasing frequency in some hospitals. Teicoplanin is recommendedin preference to vancomycin for two reasons; firstly it is simpler and quicker to administer, andsecondly more sustained blood levels occur following a single dose (49).12.5 Other beta lactam agentsThe incidence of enterococcal infections is increasing rapidly in some countries at present,often associated with heavy use of cephalosporins. Cephalosporins have no activity against 18
  19. 19. enterococci and are therefore inappropriate for endocarditis prophylaxis. As they have anoverall broad spectrum of activity (particularly against coliforms) and are present in bowelcontents, extensive use of cephalosporins has been associated with outbreaks ofClostridium difficile enterocolitis. Ureidopenicillins, for example piperacillin, are also broadspectrum agents but with limited activity against most strains of staphylococci. Likecephalosporins, they may provoke Clostridium difficile enterocolitis.12.6 Immunocompromised patientsNeutropenia predisposes to septicaemia after endoscopy (9), though the magnitude of theincreased risk is not clear. Patients with severe neutropenia (<0.5 x109 /litre) who are febrileshould have already been established on empirical antibiotic therapy according to localhaematology protocols. Afebrile patients with a neutrophil count below 0.5 x109 /litre shouldbe offered antibiotic prophylaxis for those gastrointestinal endoscopic procedures which areknown to be associated with a high risk of bacteraemia (Table 1). Gram-negative aerobic (andless frequently anaerobic) bacteria including Escherichia coli are the most likely pathogens inthese conditions and the choice of prophylactic antibiotics should reflect the local sensitivitiesof organisms.There are no data to establish whether patients with a normal neutrophil count but who arenevertheless immunocompromised (e.g. through drug treatment following organtransplantation) are at an increased risk of infective complications following endoscopy. Untilsuch time as data become available we do not recommend antibiotic prophylaxis routinely forthis group. Routine antibiotic prophylaxis is not recommended in patients with HIV infection.13. CONCLUSIONS AND SUGGESTED TOPICS FOR FURTHER RESEARCH13.1. Endocarditis is an illness that can be associated with devastating and/or life-threateningcomplications. While the evidence favouring antibiotic prophylaxis is limited, there isincreasing consensus among cardiology, microbiology and gastroenterology specialty groupsthat the spectrum of cover should be extended to encompass patients at moderate cardiac risk 19
  20. 20. undergoing therapeutic procedures associated with a high risk of bacteraemia. In order tobetter understand the true risk of post-procedure endocarditis it would be useful if specialistsocieties could gather a database of endocarditis following endoscopy.13.2. Percutaneous endoscopic gastrostomy: There is good evidence favouring antibioticprophylaxis in the prevention of PEG-associated wound infection, but there is uncertaintyregarding its value in the prevention of more serious infections such as peritonitis or aspirationpneumonia. MRSA, and its importance in such wound infections, is worthy of further study.The report that the risk may be reduced by local measures, such as oral disinfection, requiresconfirmation.13.3. ERCP: The strategy of selective administration of prophylactic antibiotics to patientswith biliary obstruction (according to the criteria set out in 7.2.4 and 7.2.5), with immediateantibiotic commencement in patients for whom suboptimal drainage is achieved, deservesprospective evaluation. There should be better understanding of the frequency with whichquinolone-resistant gram negative bacteria complicate therapeutic ERCP. Ciprofloxacinresistance is becoming increasingly common, and for patients undergoing ERCP would beexpected to be more of a problem in patients with a history of prior biliary manipulations, suchas sphincterotomy and/or stent insertion for stones, primary sclerosing cholangitis or malignantdisease. There is a need to perform multicentre studies of cholangitis and bacteraemiafollowing repeat ERCP in patients with a history of prior therapeutic ERCP.13.4. Immunosuppressed patients. Antibiotic prophylaxis for therapeutic endoscopy is recommended for patients with neutropaenia, advanced haematological malignancy and a history of liver transplantation. It remains unclear whether patients on immunosuppressive agents are at increased risk of infective complications following therapeutic endoscopy, and prophylaxis is not recommended for such patients. It is likely that a large multicentre collaboration would be required in order to address this topic.14. FOOTNOTE 20
  21. 21. At the time of our completing the final draft of these guidelines, the American HeartAssociation published their 2007 advice that antibiotics need not be administered to patientssolely for the indication of preventing endocarditis following gastrointestinal or genitourinaryprocedures (102). For the time being we continue to recommend endocarditis prophylaxis inselected circumstances until further information is available.15. ACKNOWLEDGMENTSProfessor Mike Bramble was the author of the preceding version of these guidelines. Somechanges to this version were made on advice from Prof Peter Cotton. Dr Norman Simmonsand Dr David Durack commented helpfully on earlier versions of this report. The WorkingParty was chaired by Robin H Teague, Torbay Hospital, and valuable advice and assistancewas given by Suzannah J Eykyn, Emeritus Professor of Microbiology, Guys and St Thomas’sHospitals.16. AUTHORSHIPThis guideline was prepared by members of the Endoscopy Committee of the British Societyof Gastroenterology, with valuable assistance from members of the British Cardiac Society andBritish Society for Antimicrobial Chemotherapy.Miles C Allison, Royal Gwent Hospital, NewportJonathan AT Sandoe, Leeds Teaching Hospitals NHS TrustRichard Tighe, Norwich and Norfolk University HospitalIain A Simpson, Southampton University Hospitals NHS TrustRoger J Hall, Norwich and Norfolk University HospitalThomas SJ Elliott, University Hospital Birmingham NHS Foundation TrustCorrespondence should be sent to Chris Romaya, British Society of Gastroenterology, 3 StAndrews Place, Regents Park, London NW1 4LB. c.romaya@mailbox.ulcc.ac.ukREFERENCES 1. Gould FK, Elliott TSJ, Foweraker J et al. Guidelines for the prevention of endocarditis: report of the Working Party of the British Society for Antimicrobial Chemotherapy. J Antimicrob Chemother 2006; 57;1035-42. 21
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  33. 33. Table 1: Approximate incidence of bacteraemia in immunocompetent individuals undergoinggastrointestinal endoscopy. Comparable figures for barium enema and dental manipulation are givenfor comparison.Bacteremia: BSG review (5) Nelson et al (8)Rectal digital examination 4%Rigid proctosigmoidoscopy 5-9% 7.6%Barium enema 11%Tooth brushing 25%Dental extraction 30-60%Colonoscopy 2-4% 4.4%Diagnostic OGD +/- biopsy 4% 4.1%Flexible sigmoidoscopy 0.5%ERCP (no duct occlusion) 6% 6.4%ERCP (duct occluded) 11% 18%Variceal band ligation 6% 8.8%Sclerotherapy 10-50% 14.6%Oesophagealdilatation/prosthesis 34-54%Oesophageal laser therapy 35%EUS + FNA 0-6% (Refs 89-91) 0% 33
  34. 34. Table 2. Case reports of infective endocarditis occurring within weeks after endoscopicproceduresType of endoscopy Author Reference Patient detailsOesophageal Yin et al 14 Known mitral regurgitationbougienage Niv et al 15 Known MV prolapse Breuer et al 16 No known prior valve diseaseVariceal Baskin et al 17 Prosthetic valve (failure ofsclerotherapy prophylaxis) Wong et al 18 Native valveDiagnostic OGD +/- Pritchard et al 19 Prosthetic aortic valve replacementbiopsy Logan et al 20 Known MV prolapse Rumfeld et al 21 MV stenosis ( patient also had RIH repair) Montalko et al 22 MV prolapse (symptoms predated OGD in patient on steroids) Pentimone et al 23 Young man; no known cardiac disease Cho et al 24 Valvular heart diseaseLower GI Rodriguez et al 25 Rheumatic mixed valve disease following flexible sigmoidoscopy Rigilano et al 26 MV prolapse, rigid sigmoidoscopy Watanakunakorn et al 27 Known aortic stenosis, following polypectomy Greco et al 28 Polypectomy Norfleet 29 Aortic regurgitation: flexible sigmoidoscopy for polyp follow up Giusti de Marle et al 30 Mixed AVD, colonoscopy 34
  35. 35. Table 3. Endocarditis risk stratification according to cardiac pathology (1,2,6)High riskPrevious endocarditisProsthetic heart valves (tissue or mechanical)Surgically constructed systemic pulmonary shunts or intra-thoracic vascular conduitsComplex cyanotic congenital heart disease (see Section 6.3)).Moderate riskPreviously diagnosed acquired valvular heart disease with echocardiographic demonstrationof substantial regurgitationMitral valve prolapse with mitral regurgitation and/or thickened valve leafletsNon-cyanotic ongenital cardiac defects, e.g. patent ductus arteriosus, coarctation of aorta,ventricular septal defect, primum atrial septal defect, bicuspid aortic valveOther structural cardiac abnormalities, eg hypertrophic obstructive cardiomyopathy, aorticroot replacementLow riskAll other patients 35
  36. 36. Table 4. Recommendations for antibiotic prophylaxis in gastrointestinal endoscopic practice(+ = antibiotic cover is indicated)Procedure High risk patient Moderate risk patient Low risk (prosthetic valve, (e.g. mitral valve prolapse patient previous IE, surgical with Echocardiographic thoracic vascular demonstration of substantial conduit, complex leaflet pathology and congential heart regurgitation: See Table 3) disease: See Table 3)OGD (+/- biopsy, banding) + - -Colonoscopy (+/- polyp) + - -Flexible sigmoidoscopy + - -Oesophageal dilatation and/or + + -stentingVariceal Sclerotherapy + + -ERCP (straightforward) + - -ERCP (obstructed system or + if unable to + +pseudocyst) decompressPEG + + +Thermal procedure(e.g. laser, heater probe, argon + + -plasma coagulation)Endoscopic ultrasound + - -for diagnosis/staging/FNAEndoscopic ultrasound guided Case by + +therapy Case basisColonic stenting + + - 36
  37. 37. Table 5. Summary of recommended prophylactic antibiotic regimens for gastrointestinalendoscopy.Scenario Antibiotics Dose/route Comment1) Endocarditis risk Ampicillin or 1 gram Single i.v. dose justAll patients at high risk of amoxicillin (for those aged <5yr before procedure or atendocarditis (Table 3), plus give 250mg, for those time of administeringall patients at moderate risk PLUS aged 5-10 years give sedationof endocarditis undergoing 500mg)certain therapeutic procedures(Table 4) Gentamicin 1.5mg/kg iv Give over 2-3 minutes2) Patients as (1) above who Teicoplanin 400mg iv i.v over half an hourare allergic to Penicillin (6mg/kg for children. just before procedure PLUS Seek specialist advice for neonates) Gentamicin 1.5mg/kg iv Give over 2-3 minutesProcedures3) ERCP for followingpatient groups: As abovea) endocarditis riskb) ongoing cholangitis or Be guided by Seek advice fromsepsis elsewhere recent culture clinical microbiologist resultsc) obstructed biliary tree and/ Ciprofloxacin 750mg orally 60-90 minutes beforeor pancreatic pseudocyst procedure[NOTE this is only routinely OR Not recommended inrecommended for patients childrenwith pancreatic pseudocyst,or those for whom completedrainage is unlikely to beachieved at a single ERCP – Gentamicin 1.5mg/kg i.v. Administer over 2-3(see section 7.2.5) BUT a full minutescourse of antibiotics becomesmandatory if adequate biliarydecompression is notachieved during theprocedure. For antibiotics tocover a repeat ERCP see7.2.4]d) Immunosuppressed As (c) PLUS 1gram i.v. Amoxicillin given as(including post liver Amoxicillin single i.v. dosetransplant, and neutropaenia OR Vancomycin infused(<0.5x109/l) Vancomycin 20mg/kg i.v. over at least one hour4) PERCUTANEOUS Co-amoxiclav 1.2g i.v. Slow iv injection orENDOSCOPIC OR infusion just beforeGASTROSTOMY (PEG) Cefuroxime procedure. Clindamycin 750mg i.v. 300mg i.v. can be used if past anaphylaxis with penicillin/cephalosporin5) VARICEAL BLEEDING Be guided by Cefotaxime is used in local liver unit preference to practice cefuroxime in patients with SBP 37
  38. 38. St Elsewhere’s NHS Trust Integrated Care Pathway for Endoscopy Unit ProceduresName: …………………………………………………………………Hospital Number: …………………………………………………….Date of Admission: …………………………………………………..Consultant: …………………………………………………………...Named Nurse: ……………………………………………………….. OGD Flexi Sig Colon ERCP Bronch Other 38
  39. 39. Care Pathway for : Pt detailsAppointment date and time: Arrival time:Next of Kin: Name: Address:Telephone No: Manual Handling AssessmentIndependent: Assistance: Aids: 1 person walking stick 2 people zimmer Other (please state) hoist WheelchairWeight <7 stone 7-12 stone 12-14 stone 14-16 stone >16 stone 44.5kgs 44.5-76.2kgs 76.2-88.7kgs 88.7-101kgs >101.6kgsScore 1 2 3 4 5Medical History History of falls History of vertigo Low haemoglobin Spasm Other within last 48hrs Faintness,dizziness Epilepsy 5 3 7 2 points perScore Before 48hrs symptom 3Resident Gallery Independent Low Assistance Moderate High Bed-ridden Assistance Assistance Unconscious/ (A) (B) (C) (D) comatose (E)Score 0 2 4 7 10Mental State/ Fully co- Tranquilisers Confused, poor Agitated AggressiveMedication operative Hypnotics comprehension Anxious Resistive Other medication Lack of special Apprehensive Depression 39
  40. 40. affecting mobility Awareness, poor Psychotic manual handling co-ordinationScore 0 3 5 5 2 points per symptomEnvironment No attachments Attachments eg IV etc Space Other constraints (cannot clear area)Score 0 1 point per attachment 3 3 Unsedated Sedated Low Risk 0 – 8 Requires assistance 0 – 1 staff members Moderate Risk 9 – 15 Score: Requires assistance of 1 – 2 staff members plus may require handling aids eg handling belt, sliding sheets High Risk 16+ Signature: Requires assistance of 2 or more staff members plus Handling aids eg hoist, pat slide, sliding sheets etc Date: Patient Assessment 40
  41. 41. Discharge Arrangements:Name of person collecting: Type of transport:Telephone Number: Responsible adult at home for 12 hrs? Yes/No1. Please list any medications you are presently taking: …………………………………………………………………………………………………… …………………………………………………………………………………………………… …………………………………………………………………………………………………… …………………………………………………………………………………………………… ……………………………………………………………………………………………………2. Do you have any allergies or sensitivities to any medication, food or latex? Yes/No (if yes, what?) ……………………………………………………………………………………………………3. Relevant Past Medical History: 41
  42. 42. …………………………………………………………………………………………………………….…………………………………………………………………………………………………………….Any history of diabetes: Insulin/Tablets/Diet aloneAny history of cardiomyopathy, heart valve disease, valve replacement…………………………….Any history of internal prosthesis, grafting or stent…………………………………………………..Any history of unexplained neurological illness……………………………………………………….Any history of receipt of multiple blood products (e.g. haemophilia)………………………………………………………………………………………………………………………………………………..Any history of being on variant CJD at risk register…………………………………………………..Indication for Investigation:……………………………………………………………………………………………………………. 42
  43. 43. Nursing Admission PlanProcedure explained Yes/No Explanation understood Yes/NoTime fasted from food ………. Time fasted from fluids ……….Bowel prep, type ………….. Result of Prep: Good/Fair/PoorAnti-coagulant therapy Yes/No Result/date last INR/appt: ……….………..Prophylactic antibiotics Yes/No Chance of pregnancy: Yes/No/NADentures Yes/No Hearing aid: Yes/No(Caps,crowns,loose teeth) Top/bottom Left/right/bothGlasses/contact lenses Yes/No Internal prosthesis, graft or stent: Yes/No TypeIdentity band/notes/x-rays Checked and correct: Yes/NoWeight BMI BP Temp Pulse SpO2 BM Moving & HandlingHeight Resps Assessment completed Yes/No 43
  44. 44. Care Plan:……………………………………………………………………………………………..……………………………………………………………………………………………..……………………………………………………………………………………………..……………………………………………………………………………………………..……………………………………………………………………………………………..……………………………………………………………………………………………..Nurse’s Signature: ………………………………. Patient’s Signature: ………………………………….Nursing Record for: ………………………………………………Endoscopist_________________________ Assistant______________________Consent obtained Yes/NoCannula site/type____________________________Throat spray: Time:Sedation given: Type/Amount …………………………… Time…………Opiates given: Type/Amount: ………………………….. Time…………Antibiotics given: Type/amount:…………………………… Time…………Other medication: Type/Amount: ………………………….. Time…………No sedation: ________________________________ 44
  45. 45. Record observations as individually needed:Peri procedure: Pulse:Oxygen given: Tolerated well? Yes/No (if no, why)Sp02: Time into Recovery: …………………am/pm Post Procedure Recovery Time R P BP SPO2 OtherSedation ScoreEyes open: Spontaneously 4 To speech 3 To gentle stimuli 2 To painful stimuli 1Conscious level: Awake communicates spontaneously 4 Sleeping at times 3 45
  46. 46. Sleeping for long periods but rousable by command 2 Sleeping but arousable with intense stimuli 1Airway Awake maintaining airway 4 Sleeping quietly 3 Sleeping but breathing stertorous 2 Labour and irregular breathing 1Oxygen status No oxygen required 4 Oxygen in progress but to be discontinued after 30 minutes 3 Oxygen needed for greater than 1 hour 2 Needs medical intervention 1 Adding up these scores will give you one of these categories Awake 16 - 18 Asleep 14 - 16 Light Sedation 12 – 14 Deep Sedation 5- 7Complications/Comments:…………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………………Nursing Discharge RecordAbsence of pain Yes/No Absence of bleeding Yes/NoTolerating Fluids/Food 46
  47. 47. Further investigations:Dentures/glasses/ Yes/NoOPD Follow up (Date & Time) Yes/NoTTHs Yes/NoAdvice Leaflets/Literature Yes/NoInformation given (verbal) Yes/NoAccompanied Yes/NoCannula Removed Yes/NoAny other comments:…………………………………………………………………………………………………………………..……………………………………………………………………………………………………Nurse Signature: ……………………………………………..Time of Discharge: ……………………… 47
  48. 48. 48

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