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REVIEW ARTICLE Antibiotic Stewardship Using Clinical Guidelines to Control Antibiotic Overuse and Deter Microbial Adaptation Clifford G. Wlodaver, MD*Þ and Christopher May, PharmDþ Abstract: The multidrug-resistant organism and Clostridium difficile epidemics, which are adverse consequences of antibiotic use, continue to grow. Antibiotic stewardshipVa program aimed at the judicious use of antibioticsVis a deterrent. Yet, its implementation, whether through prospective audit with intervention and feedback or by formulary restriction and preauthorization, experiences the underuse of clinical guidelines for when antibiotics should be withheld and withdrawn. This article is the first to catalog and summarize the guidelines for controlling antibiotic overuse to facilitate their implementation. Conditions for which antibiotics are not justified include nonbacterial respiratory syndromes, asymptomatic bacteriuria, colonization and culture contamination, selected cases of acute otitis media and skin and soft tissue infections, and ‘‘low-grade’’ fever. Traditionally accepted durations should be shortened for acute exacerbations of chronic bronchitis, pneumonias, urinary tract infections, intra-abdominal infections, Staphylococcus aureus bacteremia, and surgical prophylaxis. Studies demonstrate that guideline implementation through antibiotic stewardship can enhance outcomes and decrease resistance. Unfamiliarity with the guidelines should be addressed by their more widespread dissemination. Their imperfections should be addressed by more placebo-controlled trials. Concerns of undertreatment need to be counterbalanced by the adverse consequences of overtreatment. We believe that regulatory agencies should consider promoting antibiotic stewardship. Key Words: antibiotic stewardship, antibiotic overuse, multidrug-resistant organisms, Clostridium difficile (Infect Dis Clin Pract 2012;20: 12Y17) T hat antibiotics perform countless benefits is uncontroversial. Yet, their use and misuse are the root cause for microbial adaptation resulting in the multidrug-resistant organism (MDRO) and Clostridium difficile (CDI) epidemics.1,2 This natural selection was predicted by Fleming3 in his Nobel Prize lecture on discovering penicillin. Because antibiotics are relatively so effective, safe, and inexpensive, these are used liberally and are prone to overuse. Too little attention has been paid to when not to use antibiotics. Prescribing these is often more comfortable than practicing the necessary restraint. Antibiotic stewardship (ABS)V a program aimed at the judicious use of antibioticsVhas evolved to address this problem.4 The process involves reviewing patients who are receiving antibiotics and then making recommendations for change, when indicated, using guidelines to adjust the delicate balance between use and misuse. Whether ABS takes the strategy of ‘‘prospective audit with intervention and feedback’’ or ‘‘formulary restriction and preauthorization’’4 and whether it uses clinical pathways, educational programs, and/or computerized systems, the clinical challenge is in distinguishing when a patient in fact has a bacterial infection meriting antibiotics and, if so, when these can be safely discontinued. The current trend is to give antibiotics freely, sometimes injudiciously, out of concern for mistakenly omitting treatment, that is, the ‘‘just-in-case’’ approach. Concerns about relapse often result in unnecessary prolongation. Antibiotic duration is in fact based more on tradition than on scientific evidence.5 Although the concept of ABS is not new, its literature has been relatively vague on translating the guidelines into specific interventions, and these are used irregularly. To facilitate their implementation, we have collected and summarized the guidelines. Their implementation should reduce the incidence of MDRO and CDI.6Y9 We need a paradigm shift. WHEN TO WITHHOLD AND WHEN TO WITHDRAW ANTIBIOTICS Respiratory Tract Syndromes Acute Pharyngitis Most cases of acute pharyngitis are viral and should not be treated with antibiotics.10 The Centers for Disease Control promote antibiotic restraint through their ‘‘Get Smart’’ campaign.11 However, 15% to 30% of pediatric cases and 5% to 10% of adult cases are caused by group A streptococcus. This is the only common bacterial cause of pharyngitis meriting antibiotics, the other bacteria being very rare. Yet, Linder and Stafford12 reported that three fourths of adults who consulted their physician for a sore throat received antibiotics. It is therefore important to exclude streptococcal pharyngitis to avoid unnecessary antibiotics. Because distinguishing it from a respiratory virus is difficult on clinical grounds alone, the use of rapid antigen detection testing reflexed to culture is recommended before starting antibiotics.13 Acute Rhinosinusitis Most cases of acute rhinosinusitis are also viral.10 To decrease the use of unnecessary antibiotics, waiting 10 days is recommended if the clinical severity is mild and is stable or improving.14 This is because most viruses and even some bacterial infections resolve spontaneously within this period. Acute Bronchitis From the *Midwest Regional Medical Center, Midwest City; †College of Medicine, The University of Oklahoma Health Sciences Center, Oklahoma City; and ‡Department of Pharmacy, Midwest Regional Medical Center, Midwest City, OK. Correspondence to: Clifford G. Wlodaver, MD, 8121 National Ave, Suite 310, Midwest City, OK 73110. E-mail: [email protected]. The authors have no funding or conflicts of interest to disclose. Copyright * 2012 by Lippincott Williams & Wilkins ISSN: 1056-9103 12 www.infectdis.com Although most cases of acute bronchitis are viral in origin,10 acute exacerbations of chronic bronchitis may have a bacterial component.15 Criteria for when to use antibiotics are proposed in the Global Initiative for Chronic Obstructive Lung Disease (GOLD) report, namely, dyspnea, increased sputum volume and purulence, and systemic symptoms and signs of infection.16 If antibiotics are decided upon, an abbreviated course may suffice. Infectious Diseases in Clinical Practice & Volume 20, Number 1, January 2012 Copyright © 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Infectious Diseases in Clinical Practice & Volume 20, Number 1, January 2012 For example, a 3-day course of amoxicillin-clavulanate was as effective as a 10-day course in microbiological success, symptom recovery, use of corticosteroids, duration of oxygen therapy, and length of hospital stay.17 Community-Acquired Pneumonia Community-acquired pneumonia (CAP) merits antibiotics, and the time to first antibiotic dose has become a core measure of a hospital’s quality of care by the Centers for Medicare and Medicaid Services (CMS) Hospital Quality Alliance and Joint Commission. The present cutoff is 6 hours.18 Feeling the pressure of time constraints, especially in emergency departments, and confronted with diagnostic uncertainty, physicians often prescribe antibiotics prematurely. Congestive heart failure and other cardiopulmonary disorders may be mistakenly diagnosed as CAP. When the time to first antibiotic dose was shorter (G4 hours) compared with longer (98 hours), Welker et al19 found that the final diagnosis at dischargeVCAP versus other cardiopulmonary disordersVdid not meet predefined criteria for CAP 39% of the time. Chest x-ray reports that read ‘‘probable vascular congestion, cannot rule out pneumonia,’’ appear frequently and invite prescriptions for antibiotics. Careful review of the patient’s history and physical examination along with the white blood cell count, sputum examination, urine antigen tests, and B-type natriuretic peptide can help to distinguish between congestive heart failure and CAP. Ultimately, when pneumonia seems unlikely, antibiotics should be discontinued. Recent studies suggest that a shorter (5 days) rather than longer course of antibiotics is sufficient for CAP, and this has received recognition from the Infectious Diseases Society of America (IDSA) and American Thoracic Society (ATS).20 These societies also remind us not to base duration on chest radiograph normalization because infiltrate resolution may lag clinical recovery. Health CareYAssociated Pneumonia Similar to CAP, health careYassociated pneumonia requires a shorter duration of antibiotics than previously believed. Eight days of therapy is adequate for patients who are not infected with nonfermenting gram-negative bacilli.21 Acute Otitis Media in Children According to the American Academy of Pediatrics and American Academy of Family Physicians Clinical Practice Guideline, ‘‘Observation without use of antibacterial agents in a child with uncomplicated AOM is an option for selected children based on diagnostic certainty, age, illness severity, and assurance of follow-up. (This option is based on randomized, controlled trials with limitations and a relative balance of benefit and risk.)’’22 Although concerns that antibiotic restraint may result in an increased incidence of mastoiditis have been raised, this has not been the case. ‘‘Placebo-controlled trials of AOM over the past 30 years have shown consistently that most children do well, without adverse sequelae, even without antibiotic therapy.’’22 Since these guidelines were written, 2 placebo-controlled trials that support early antibiotic treatment of acute otitis media (AOM) have been published. Tähtinen et al23 showed a 62% reduction in treatment failure and an 81% reduction for rescue therapy, and Hoberman et al24 showed earlier and more sustained resolution of symptoms with therapy. As pointed out in an accompanying editorial, diagnostic accuracy is the key to management.25 If the child in fact has a bacterial infection, early initiation of antibiotics is beneficial. * 2012 Lippincott Williams & Wilkins Antibiotic Stewardship Skin and Soft Tissue Infections Cutaneous Abscesses Cutaneous abscesses respond to incision and drainage alone and do not require antibiotics, with the following exceptions: ‘‘severe or extensive disease (eg, involving multiple sites of infection) or rapid progression in presence of associated cellulitis, signs and symptoms of systemic illness, associated comorbidities or immunosuppression, extremes of age, abscess in area difficult to drain (eg, face, hand, and genitalia), associated septic phlebitis, and lack of response to I & D alone.’’26 Cellulitis For cellulitis, it is important to distinguish whether it is purulent or not. Purulence is more often associated with methicillin-resistant Staphylococcus aureaus, whereas the absence of purulence suggests A-hemolytic streptococcus. Empirical antibiotics need to be selected accordingly.26 When antibiotics are used for skin and soft tissue infections (SSTIs), Jenkins et al27 noted their inappropriately long duration. They found that the median duration was nearly 13 days and cited evidence that 5 days should suffice.28 Lower Extremity Venous InsufficiencyYAssociated Stasis Dermatitis Lower extremity venous insufficiencyYassociated stasis dermatitis, a locus minoris resistancia, may become acutely infected, thus meriting antibiotics. However, the stable, chronic bilateral inflammation that typifies stasis dermatitis should not be treated with antibiotics.29 Urinary Tract Infections Asymptomatic Bacteriuria and Pyuria in Adults Asymptomatic bacteriuria and pyuria in adults do not merit treatment (except in pregnancy and when associated with a urologic procedure). Abundant literature indicates the absence of any treatment benefit.30 It does not lead to hypertension, chronic kidney disease, genitourinary cancer, or decreased survival. Antibiotics do not decrease the incidence of symptomatic infection. The IDSA Guidelines conclude that ‘‘Itreatment of asymptomatic bacteriuria does not decrease the frequency of symptomatic infection or improve other outcomes. Thus, in populations other than those for whom treatment has been documented to be beneficial [pregnancy and urologic procedures], screening for or treatment of asymptomatic bacteriuria is not appropriate and should be discouraged.’’30 A urine culture should not be done unless a patient has a syndrome compatible with a urinary tract infection (UTI). However, recent movements to report hospital-acquired infections and the CMS’ new regulations that deny reimbursement for hospital-acquired UTIs have led some hospitals to routinely culture urine upon admission and to document bacteriuria (if present), to avoid subsequent accusations of hospital-acquired infections and reimbursement-denial issues, respectively.31 Furthermore, intuition argues to treat, and practitioners often do not feel comfortable disregarding bacteriuria and pyuria once they learn of its presence. Not only does screening not improve outcomes, but it may also lead to the unnecessary use of antibiotics and their unintended consequences, as reaffirmed by the US Preventive Services Task Force.32 To deal with the dilemma, there is a burgeoning movement to increase adherence to nontreatment guidelines. Gross and Patel33 have proposed a national performance measure for not treating asymptomatic bacteriuria. For patients with indwelling urinary catheters, it is likewise important to distinguish asymptomatic from www.infectdis.com Copyright © 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 13 Wlodaver and May Infectious Diseases in Clinical Practice symptomatic bacteriuria. Similar to asymptomatic bacteriuria in noncatheterized patients, evidence-based guidelines proscribe culturing for and treating asymptomatic bacteriuria (except in pregnancy and when associated with a urologic procedure).34 The IDSA Guidelines for treating symptomatic UTIs are type (cystitis or pyelonephritis), pathogen, and drug specific.35 In essence, they recommend nitrofurantoin monohydrate/ macrocrystals for 5 days or trimethoprim-sulfamethoxazole for 3 days (if local resistance G20%) for acute cystitis. In some instances, trimethoprim alone is used. The guidelines also discuss other choices based on availability outside North America. Although efficacious, the fluoroquinolones should be reserved for resistant organisms because of their potential for ‘‘collateral damage.’’ Because of inferior efficacy and more adverse effects, A-lactam agents, in general, ‘‘should be used with caution,’’ and ampicillin and amoxicillin should not be used for empirical treatment because of the high prevalence of resistance. For acute pyelonephritis, the guidelines recommend ciprofloxacin when the community prevalence of resistance is less than 10%, considering the initial dose given intravenously (IV), or using an initial IV dose of ceftriaxone or an aminoglycoside if the community resistance to quinolones is more than 10%. In patients not requiring hospitalization, provided that the pathogen is susceptible, oral levofloxacin for 5 days, ciprofloxacin for 7 days, or trimethoprim-sulfamethoxazole for 14 days is an appropriate choice. A-lactams are relatively less effective than other agents. If used, the recommended duration is 10 to 14 days. For catheterassociated UTIs, 7 days is recommended, prolonged to 10 to 14 days for a delayed response.35 The antibiotic regimen should always be tailored to the susceptibility results. Bacteremia Cultures of blood that grow coagulase-negative staphylococci and other normal skin flora often represent contamination and do not merit antibiotics, although these need to be considered carefully when associated with intravascular catheters and bioprostheses. Multiple samples and quantitative cultures help distinguish contamination from true infection.36 The duration of antibiotics for Staphylococcus aureus bacteremia has been addressed by Fowler et al,37 with a risk score for estimating the likelihood of developing complications. Four factors were noted to be related to the development of complications: community-acquired skin findings suggestive of acute systemic infection, fever for more than 3 days, and positive follow-up blood cultures at 48 to 96 hours. One point is given to each of the first 3 factors, and 2 points are given to the last. The risk of developing complications was 16% for no factors and rose steadily to 90% for all factors. Accordingly, a shorter course (eg, 2 weeks) of antibiotics may suffice in the absence of risk factors, whereas 4 to 6 weeks is indicated when there are more risk factors. Intra-Abdominal Infections Guidelines for the duration of antibiotics for complicated intra-abdominal infections by the Surgical Infection Society and IDSA state that it should be limited to 4 to 7 days, as long as there is adequate source control.38 A longer duration has not been shown to improve outcomes. Surgical Prophylaxis Antibiotics for surgical prophylaxis decrease the risk of surgical site infection.39,40 Although these are traditionally prolonged in the perioperative period, evidence shows no benefit beyond the immediate preoperative dose. The first dose should be given within 60 minutes of the surgical incision (120 minutes for vancomycin or fluoroquinolones). For prolonged procedures 14 www.infectdis.com & Volume 20, Number 1, January 2012 or when there has been a significant delay in starting the operation, a second dose at 1 to 2 half-lives is recommended. Prophylactic antibiotics should not be continued beyond 24 hours after the end of surgery, without exception.40 Continuing them until the surgical drains are removed is of unproven benefit. For dirty/ contaminated surgery, antibiotics should be continued beyond 24 hours. ‘‘Low-Grade’’ Fever Elevated temperature is the hallmark of infection and drives consideration for antibiotic use. A temperature of 98.6-F (37.0-C) has been the time-honored maximum normal body temperature. However, Mackowiak et al41 demonstrated that 99.9-F (37.7-C) is the true normal maximum temperature by measuring the temperatures of 148 healthy men and women aged 18 to 40 years using an oral electronic digital thermometer. Lowgrade fever, that is, with a temperature less than 99.9-F, should not be treated with antibiotics or used as a reason to continue these unless there are other signs or symptoms of infection. OUTCOMES Several studies have demonstrated that ABS can increase the appropriateness of antibiotics. This translates into decreased use, decreased resistance, and decreased CDI. Gross et al6 compared usual practice to a university hospital program and noted a statistically significant increase in appropriate antibiotic use from 32% to 90% and in cure from 55% to 91% and a decrease in resistance from 9% to 1%. Methicillin-resistant S. aureus and C. difficile rates decreased significantly after implementation of a stewardship program reported by Fowler et al,8 and the rate of resistant Enterobacter decreased significantly on a stewardship program reported by Carling et al.7 A nationwide campaign in France to reduce antibiotic use entitled ‘‘Antibiotics Are Not Automatic’’ decreased the mean number of prescriptions from 72.4 to 56.6 per 100 people from 2000Y2001 to 2006Y2007.9 DISCUSSION The MDRO and CDI epidemics are progressing rapidly. Their significance, association with antibiotic use, and the limitations these place on antibiotic therapy are discussed in detail elsewhere.1,2 Antibiotic stewardship offers a deterrent.6Y9 However, translating its concepts into practice is inconsistent (whether ABS takes the strategy of ‘‘prospective audit with intervention and feedback’’ or ‘‘formulary restriction and preauthorization’’4) as evidenced by these uncontrolled epidemics and is the focus of this article. We decided to divide our perspectives into 2 broad categories: when not to use antibiotics in the first place (Table 1) and when to discontinue these once in use (Table 2). For support, we decided to focus on published clinical guideline recommendations, when available, rather than citing the primary studies upon which these are based. Limiting antibiotic exposure is applicable in academic and nonacademic situations to both adult and pediatric infections and in inpatient and outpatient settings, as noted in the broad scope of the recommendations that we have listed. Guidelines also exist for ABS in febrile neutropenic patients,42 and the concepts apply to intensive care unit patients as well.43 Although the intent of our article is to catalog when to judiciously withhold and withdraw antibiotics, in these complex and critically ill patients, multiple antibiotics for prolonged duration may be required. These patients may be more appropriately addressed by a face-to-face infectious diseases consultation. The decision whether to use antibiotics is based on clinical judgment. For a septic patient, timely, appropriate empirical treatment can be lifesaving. Then, once a pathogen has been * 2012 Lippincott Williams & Wilkins Copyright © 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Infectious Diseases in Clinical Practice & Volume 20, Number 1, January 2012 TABLE 1. Specific Situations Where Antibiotics Should Be Withheld Respiratory tract syndromes Viral pharyngitis10 Viral rhinosinusitis10 Viral bronchitis10 Noninfectious cardiopulmonary disorders misdiagnosed as pneumonia AOM (for selected cases, refer to article)22 SSTIs Subcutaneous abscesses (for selected cases, refer to article)26 Lower extremity stasis dermatitis29 Asymptomatic bacteriuria and pyuria, including catheterized patients30,34 Microbial colonization and culture contamination36 Low-grade fever41 identified or at least suspected, the regimen should be deescalated.4 On the other hand, although the presence of bacteria may, of course, signal infection and merit antibiotics, colonization is natural and should not be treated. The problem is distinguishing one from the other. Cultures need to be evaluated in their clinical setting. For example, bacteriuria in a patient who is asymptomatic represents colonization and should not be treated.30,34 There are few studies examining the duration of antibiotic therapy. With the exception of streptococcal pharyngitis (10 days of penicillin V) and prolonged courses for infectious endocarditis and osteomyelitis, for example, duration is remarkably arbitrary.5 Yet, it is not without staunch proponents. Observational studies, expert opinion, conventional wisdom, and round numbers such as 5, 7, 10, and 14 days are often proposed dogmatically, albeit without evidence or physiologic rationale. Duration of therapy should be individualized. Serial measurements of inflammation markers such as the erythrocyte sedimentation rate and C-reactive protein and procalcitonin levels have some value in helping decide when an infection has resolved and antibiotics can be discontinued, although these lack complete specificity and sensitivity.44 Normalization of a patient’s temperature and white blood cell count remain the standard and most physiologic indicators to discontinue antibiotics, although their predictive value is also imperfect. Difficult clinical decisions must not be oversimplified. When uncertain, for patients initially treated with IV antibiotics, a compromise in duration is a po substitution.4 It is predicated on a patient’s clinical improvement, an acceptable po alternative, and a functioning gastrointestinal tract. However, if the patient is doing well clinically, we believe that consideration should be given to discontinuing antibiotics altogether. Shorter durations may be as effective as longer ones and may lead to less MDRO and CDI. Although the ideal duration of antibiotics remains uncertain in most cases and needs more study, practice guidelines for several infections are progressing and are summarized in this article. There are several obstacles confronting the implementation of ABS. First, there is apparent unfamiliarity with the specific clinical guidelines to control antibiotic overuse. The Centers for Disease Control address this with their programs.11 Furthermore, the goal of this article is to facilitate implementation by cataloging and summarizing these guidelines. Second, even when recognized, there is incomplete acceptance of the guideline recommendations. Khan et al45 and Lee et al46 have pointed out that * 2012 Lippincott Williams & Wilkins Antibiotic Stewardship many of the recommendations are based on low-quality evidence. In their reviews, only 16% and 14%, respectively, are based on randomized clinical trials. A recently published study on hospitalacquired, ventilator-associated, and health careYassociated pneumonia reported that compliance with the IDSA/ATS Guidelines resulted in increased mortality.47 However, as noted in the accompanying editorial,48 ‘‘the validity of [the] analysis is subject to controversy.’’ The comparison groups were not equal in regards to the risk for mortality. In particular, the guideline-compliant group had a statistically higher incidence of sepsis (91% vs 76%), had previously received antibiotics more frequently (75% vs 56%), and had lower antibiotic coverage of certain multidrugresistant pathogens (59% vs 94%). Furthermore, up to one half of the guideline-compliant group failed to undergo appropriate deescalation of antibiotics based on the microbial results (ie, they were actually in the nonYguideline-compliant group). In addition, the comparison groups were not analyzed in regards to the timing of antibiotics, a critical issue for sepsis. Clearly, the guidelines are imperfect. In acknowledging their imperfection, the IDSA/ATS CAP Guidelines, for example, make the following statement: ‘‘Although these guidelines are evidence based, the committee strongly urges that deviation from them not necessarily be considered substandard care, unless they are accompanied by evidence for worse outcomes in a studied population.’’20 We need to be wary of unintended consequences. We need more and better studies. Third, there is fear, by both physicians and patients, that undertreatment, that is, withholding or prematurely discontinuing antibiotics, will result in harm. Litigation may fuel these concerns. Intuition suggests that more is better, but the correct balance remains uncertain. Indeed, clinical medicine remains more of an art than a science in many situations, and clinical uncertainty is common. Although using the recommendations summarized in this article should give physicians confidence in their antibiotic restraint decisions, ABS needs to be practiced with a healthy skepticism and conservatism. The principles and practice of ABS should not be overstated, and indiscriminate application of the guideline recommendations must be avoided. Cases for interventions need to be selected carefully. To counterbalance patients’ concerns, the negative consequences of antibiotic overuse appear regularly in the press and are even satirized.49,50 The medical establishment needs to continue to popularize the drawbacks of antibiotic overuse. Furthermore, litigation based on adverse reactions to antibiotic misuse is evolving and acts as an additional counterbalance. Lastly, there is no clear TABLE 2. Practice Guideline Recommendations Regarding Duration of Therapy CAP, 5 d20 Health careYacquired pneumonia, 8 d21 SSTI, 5 d28 UTI Cystitis, 3-5d (depending on antibiotic)35 Pyelonephritis, 5Y14 d (depending on antibiotic)35 Catheter associated, 7 d (prolonged to 10Y14 d for delayed response)34 S. aureus bacteremia Low risk of complications, 2 wk37 High risk of complications, 4Y6 wk37 Intra-abdominal infection, 4Y7 d38 Surgical antibiotic prophylaxis, 1 dose (up to 24 h, without exception)39,40 www.infectdis.com Copyright © 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 15 Infectious Diseases in Clinical Practice Wlodaver and May & Volume 20, Number 1, January 2012 mandate to enforce the ABS guidelines. This said, the Joint Commission and CMS have made the surgical antibiotic prophylaxis recommendations mandatory.51 We believe that regulatory agencies should similarly promote antibiotic restraint. Gross and Patel’s33 ‘‘call for a national performance measure for not treating asymptomatic bacteriuria’’ is an excellent example of how to proceed. Not interveningVallowing antibiotic overuse to continue uncheckedVunnecessarily promotes the MDRO and CDI epidemics. 13. Bisno AL, Gerber MA, Gwaltney JM Jr, et al. Practice guidelines for the diagnosis and management of group A streptococcal pharyngitis. Clin Infect Dis. 2002;35(2):113Y125. CONCLUSIONS 16. Global strategy for the diagnosis, management, and prevention of chronic lung disease [Global Initiative for Chronic Obstructive Lung Disease Web site]. Available at: http://www.goldcopd.com/ Guidelineitem.asp?l1=2&l2=1&intId=2003. Accessed January 31, 2011. Although the concept of ABS is not new, precisely when to withhold and withdraw antibiotics from the practical point of view has received relatively little attention. Its importance is punctuated by the MDRO and CDI epidemics. Implementing ABS by using the clinical practice guidelines summarized in this article should be promoted to quell the MDRO and CDI epidemics. ACKNOWLEDGMENT The authors thank Alice Engelbrecht, PharmD, clinical pharmacist, Department of Pharmacy, Oklahoma University Medical Center, Oklahoma City, OK. REFERENCES 14. Rosenfeld RM, Andes D, Bhattacharyya N, et al. Clinical practice guideline: adult sinusitis. Otolaryngol Head Neck Surg. 2007;137(suppl 3):S1YS31. 15. Sethi S, Murphy TF. Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N Engl J Med. 2008;359(22):2355Y2365. 17. Roede BM, Bresser P, El Moussaoui R, et al. Three vs. 10 days of amoxicillin-clavulanic acid for type 1 acute exacerbations of chronic obstructive pulmonary disease: a randomized, double-blind study. Clin Microbiol Infect. 2007;13(3):284Y290. 18. National summary statistics for RHQDAPU clinical process measures on hospital compare [Centers for Medicare and Medicaid Services Web site]. Available at: http://www.cms.gov/HospitalQualityInits/downloads/ HospitalNationalLevelPerformance.pdf. Accessed April 11, 2011. 19. Welker JA, Huston M, McCue JD. Antibiotic timing and errors in diagnosing pneumonia. Arch Intern Med. 2008;168(4):351Y356. 1. Spellberg B, Guidos R, Gilbert D, et al. The epidemic of antibiotic-resistant infections: a call to action for the medical community from the Infectious Diseases Society of America. Clin Infect Dis. 2008;46(2):155Y164. 20. Mandell LA, Wunderink RG, Anzueto A, et al. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis. 2007;44(suppl 2):S27YS72. 2. McDonald LC, Owings M, Jernigan DB. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996Y2003. Emerg Infect Dis. 2006;12(3):409Y415. 21. American Thoracic Society and Infectious Diseases Society of America. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med. 2005;171(4):388Y416. 3. Sir Alexander FlemingVNobel Lecture [Nobel Prize Web site]. Available at: http://nobelprize.org/nobel_prizes/medicine/laureates/ 1945/fleming-lecture.html. Accessed January 31, 2011. 4. Dellit TH, Owens RC, McGowan JE Jr, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis. 2007;44(2):159Y177. 22. American Academy of Pediatrics and American Academy of Family Physicians. Clinical practice guideline on the diagnosis and management of acute otitis media. Pediatrics. 2004;113(5):1451Y1465. 23. Tähtinen PA, Laine MK, Houvinen, P, et al. A placebo-controlled trial of antimicrobial treatment for acute otitis media. N Engl J Med. 2011;364(2):116Y126. 5. Rice LB. The Maxwell Finland Lecture: for the duration-rational antibiotic administration in an era of antimicrobial resistance and Clostridium difficile. Clin Infect Dis. 2008;46(4):491Y496. 24. Hoberman A, Paradise JL, Rockette HE, et al. Treatment of acute otitis media in children under 2 years of age. N Engl J Med. 2011;364(2):105Y115. 6. Gross R, Morgan AS, Kinky DE, et al. Impact of a hospital-based antimicrobial management program on clinical and economic outcomes. Clin Infect Dis. 2001;33(3):289Y295. 25. Klein JO. Is acute otitis media a treatable disease? N Engl J Med. 2011;364(2):168Y169. 7. Carling P, Fung T, Killion A, et al. Favorable impact of a multidisciplinary antibiotic management program conducted during 7 years. Infect Control Hosp Epidemiol. 2003;24(9):699Y706. 26. Liu C, Bayer A, Cosgrove SE, et al. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis. 2011;52(3):1Y38. 8. Fowler S, Webber A, Cooper BS, et al. Successful use of feedback to improve antibiotic prescribing and reduce Clostridium difficile infection: a controlled interrupted time series. J Antimicrob Chemother. 2007;59(5):990Y995. 27. Jenkins TC, Sabel AL, Sarcone EE, et al. Skin and soft-tissue infections requiring hospitalization at an academic medical center: opportunities for antimicrobial stewardship. Clin Infect Dis. 2010;51(8):895Y903. 9. Huttner B, Harbarth S. ‘‘Antibiotics are not automatic anymore’’Vthe French national campaign to cut antibiotic overuse. PLoS Med. 2009;6(6):e1000080. 28. Hepburn MJ, Dooley DP, Skidmore PJ, et al. Comparison of short-course (5 days) and standard (10 days) treatment for uncomplicated cellulitis. Arch Intern Med. 2004;164(15):1669Y1674. 10. Mandell GL, Bennett JE, Dolin R, eds. Principles and Practice of Infectious Diseases. 7th ed. Philadelphia, PA: Elsevier Inc; 2010. 29. Weingarten MS. State-of-the-art treatment of chronic venous disease. Clin Infect Dis. 2001;32(6):949Y954. 11. Get smart: know when antibiotics work [Centers for Disease Control and Prevention Web site]. Available at: http://www.cdc.gov/getsmart/ campaign-materials/info-sheets/adult-approp-summary.html. Accessed January 31, 2011. 30. Nicolle LE, Bradley S, Colgan R, et al. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis. 2005;40(5):643Y654. 12. Linder JA, Stafford RS. Antibiotic treatment of adults with sore throat by community primary care physicians: a national survey, 1989Y1999. JAMA. 2001;286(10):1181Y1186. 16 www.infectdis.com 31. Hospital-acquired conditions [Centers for Medicare and Medicaid Services Web site]. 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