Editorial Commentary

Variability in Antibiotic Prescribing: An Inconvenient Truth Lauri A. Hicks1 and Martin J. Blaser2 1

Division of Bacterial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; and 2Departments of Medicine and Microbiology, New York University Langone Medical Center Corresponding Author: Lauri A. Hicks, DO, Centers for Diseases Control and Prevention, 1600 Clifton Road, Mailstop C-25, Atlanta, GA 30329. E-mail: [email protected]. Received September 16, 2014; accepted September 30, 2014; electronically published October 30, 2014.

(See the Original Article by Gerber et al on pages 297–304.) Key words.

antimicrobials; medical practice; microbiome; outpatient.

The rising tide of antibiotic-resistant infections has led to calls to action by public health professionals, professional medical organizations, scientists, and policy makers. Most of us working on the front lines to address this problem agree that we must stop the rampant misuse of antibiotics to preserve antibiotic resources. Understanding variability in the patterns of antibiotic prescribing may help to identify where inappropriate use is most common and inform efforts to improve practices. Antibiotic prescribing rates vary 3-fold among 29 countries in Europe (highest in Greece and lowest in The Netherlands) [1]. In the United States, states in the Appalachian region have antibiotic prescribing rates that more than double those of states in the Pacific Northwest [2]. Ultimately, we need to better understand why providers practice differently, how much variability in prescribing exists at the local level, and whether practice-level data can provide useful information to guide antibiotic stewardship efforts at the health system level. In this issue of the Journal of the Pediatric Infectious Diseases Society, Gerber et al [3] assessed variation in prescribing rates across a pediatric

primary care network that included 25 practices. After adjusting for patient demographics, prior antibiotic use, allergies, and comorbid conditions, antibiotic prescribing for acute respiratory tract infections ranged from 18% to 36% of visits, and variability in using broad-spectrum antibiotics ranged from 15% to 58% of visits during which antibiotics were prescribed [3]. Identifying practice differences may signal the places where inappropriate antibiotic prescribing is most common. Because of their perceived low toxicity, antibiotics are seen as ultrasafe “miracle drugs” by physicians and patients alike. Healthcare providers dispense antibiotics, often reflexively; however, from the earliest days, it became clear that antibiotic use leads to resistance. Because resistance to antibiotics is limiting the treatment options for many infections, including important pathogens such as Staphylococcus aureus, pneumococcus, and enterobacteriaceae, the problem is getting worse. The dilemma is that resistance is a long-term problem, and it affects the community as much as the individual. For both parents and providers, resistance may be a small risk compared with the

potential benefits antibiotics can give to the child in front of them suffering from an infection. The substantial variation identified by Gerber et al [3] indicates that as practitioners weigh risks and benefits, they are drawing their lines in different places; however, parents routinely opt for what they believe is best for their child more than an abstract concern for the community, and it is hard to blame them for this reaction. The game-changer is that it’s increasingly evident that the consequences of antibiotic use are not limited to resistance. For example, there are the immediate complications such as acute toxicity, rashes, and gastrointestinal upset. Fortunately, the most severe complications are uncommon, and the common complications are generally mild. However, antibiotic exposure, especially in early life, may have long-term consequences, including increased risk for obesity, type 1 diabetes, asthma, and inflammatory bowel disease [4–7]. Results from both epidemiologic studies in humans and experimental models in animals [8–9] lead to a similar conclusion: a possible biological cost from early life antibiotic exposures [10]. If these observations are substantiated, then

Journal of the Pediatric Infectious Diseases Society, Vol. 4, No. 4, pp. e136–e138, 2015. DOI:10.1093/jpids/piu106 Published by Oxford University Press on behalf of the Pediatric Infectious Diseases Society 2014. This work is written by (a) US Government employee(s) and is in the public domain in the US.

Editorial Commentary

physicians and parents will be faced with a new dilemma: should the line be redrawn—is the benefit of antibiotic use sufficiently high to be greater than the potential cost? There will always be infections for which children must be treated with antibiotics, because their life and well being are in danger. Fortunately, these are a small subset of cases in which children are seen by a medical professional. Providers will need to take more comprehensive medical history and more carefully examine their patients; they will not be able to rely as fully on the “safety net” of empiric antibiotic use, because the net has health consequences. There must be greater realization at all levels of healthcare, including payers and patients, that the cost of antibiotic use may not be just the price of the drugs but may also include the cost of adverse events and increased risks of chronic diseases. Sadly, the economics of our healthcare delivery systems, which do not factor in the long-term health consequences, conspire against such a rational approach. A corollary issue concerns the optimal duration of therapy. When the perceived cost of antibiotics was limited to the development of resistance, our concerns about efficacy were paramount. This remains a critical point, yet we must now factor in the collateral damage to the microbiome—what is the cost of that? If perturbation of the microbiome during critical developmental windows is deleterious, as animal studies indicate [9], then extended perturbation of the microbiome may lead to more adverse outcomes. Our traditional advice to parents to “take the antibiotic until the course is over, even if your child feels better,” must therefore be reexamined. It is possible that, in some circumstances, we are now doing more harm than good with this practice. A related issue is to examine the biological costs of antibiotic use in

pregnant women in terms of its effects on the intergenerational transfer of microbiota. We have concentrated exclusively on the costs of the infections to thousands of affected women and babies, but we have not come to terms with the costs of treatment and preventive measures to the millions of other exposed patients. How should evidence of short- and long-term consequences strengthen efforts to improve antibiotic use? Through educational efforts, such as the Centers for Disease Control and Prevention’s Get Smart: Know When Antibiotics Work campaign (www. cdc.gov/getsmart), healthcare professionals and patients are informed about the importance of appropriate antibiotic use for reducing resistance. Several state health departments, professional societies, and nonprofit and for-profit organizations have also joined the effort. Improvements in prescribing have been documented, particularly for children, but inappropriate antibiotic use remains common. Although knowledge about antibiotic resistance has grown, the other consequences of antibiotic use are underappreciated. Messages highlighting the potential harms at the patient level are likely to be more powerful than those suggesting a societal risk. Although parents are increasingly receiving information from the internet, providers remain the most trusted source for health information. Educating providers who prescribe the most—family practitioners, pediatricians, and internists—and providing the tools they need to evaluate risk and benefit to draw an appropriate line should be a priority. Changing behavior and the culture of antibiotic use is not easy and will require a sustained effort. Health systems-level changes may speed up changes in practices. Many acute care facilities have introduced, or are in the process of developing, antibiotic stewardship

programs. There is a need to identify how to sustain and scale up stewardship in the ambulatory setting. Gerber et al [3] propose that benchmarking antibiotic prescribing at the practice level could provide the pressure needed for improvements; for practice networks, this may be a great option. Likewise, provider-level audit and feedback (comparing providers to peers or an established standard) is an effective approach to improve prescribing practices [11]. Outpatient antibiotic prescribing quality measures, most of which track provider prescribing practices for specific syndromes, can be used by employers, payers, health systems, and practices as a standard to evaluate provider performance. In conclusion, there is no return to the “good old days” of providing antibiotics for mild infections and not seriously considering the consequences. The role of the physician is to optimize health for the patient and for the community. As shown in the outstanding study of Gerber et al [3], pediatricians are drawing the lines in many different ways. This may not have been of major importance in the past, but the increasing evidence of long-term harm from antibiotic use in childhood necessitates a closer look at our practices and less reliance on the imperfect safety net that antibiotic use represents. Acknowledgments Disclaimer. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. Potential conflicts of interest. All authors: No reported conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest.

References 1. European Centre for Disease Prevention and Control. Surveillance of antimicrobial consumption in Europe 2011. Stockholm: ECDC; 2014.

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2. Hicks LA, Taylor TH Jr, Hunkler RJ. U.S. outpatient antibiotic prescribing, 2010. N Engl J Med 2013; 368: 1461–2. 3. Gerber JS, Prasad PA, Localio AR, et al. Variation in antibiotic prescribing across a pediatric primary care network. J Pediatric Infect Dis Soc 2015; 4:297–304. 4. Azad MB, Bridgman SL, Becker AB, Kozyrskyj AL. Infant antibiotic exposure and the development of childhood overweight and central adiposity. Intern J Obes 2014; 38: 1290–8.

5. Trasande L, Blustein J, Liu M, et al. Infant antibiotic exposures and early life body mass. Int J Obes 2013; 37:16–23. 6. Hviid A, Svanstrom H, Frisch M. Antibiotic use and inflammatory bowel diseases in childhood. Gut 2011; 60: 49–54. 7. Kozyrskyj AL, Ernst P, Becker AB. Increased risk of childhood asthma from antibiotic use in early life. Chest 2007; 131:1753–9. 8. Cho I, Yamanishi S, Cox L, et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 2012; 488:621–6.

9. Cox LM, Yamanishi S, Sohn J, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 2014; 158:705–21. 10. Blaser MJ, Falkow S. What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 2009; 7:887–94. 11. Gerber JS, Prasad PA, Fiks AG, et al. Effect of an outpatient antimicrobial stewardship intervention on broadspectrum antibiotic prescribing by primary care pediatricians: a randomized trial. JAMA 2013; 309:2345–52.

Variability in Antibiotic Prescribing: An Inconvenient Truth.

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