Antimicrobial stewardship programs (ASPs) are integral to addressing antibiotic overuse and resistance. Pediatric ASPs have been shown to decrease inappropriate antimicrobial use, Reference Barlam, Cosgrove and Abbo1,Reference Smith, Gerber and Hersh2 drug costs, and prescription errors, Reference Barlam, Cosgrove and Abbo1,Reference Smith, Gerber and Hersh2 and to increase guideline adherence, Reference Barlam, Cosgrove and Abbo1,Reference Smith, Gerber and Hersh2 without increasing adverse events such as treatment failures and hospital readmissions. Reference Barlam, Cosgrove and Abbo1–Reference McCulloh, Queen and Lee5 Surveys including pediatric prescribers suggest that ASPs are generally viewed favorably. Reference Abbo, Sinkowitz-Cochran and Smith6–Reference Szymczak, Kitt and Hayes9 Data regarding the perceptions of infectious disease (ID) physicians who manage ASPs, and those of ID physicians who are not ASP participants (non-ASP), are limited to a 2008 survey of pediatric ID physicians by the Infectious Diseases Society of America Emerging Infections Network (EIN), though only 33% of respondents reported having an ASP at that time. Reference Hersh, Beekmann, Polgreen, Zaoutis and Newland10 As ASPs have become more prevalent, understanding the perceived differences in ASP and non-ASP physicians is vital because disagreement between ASP and non-ASP physicians could compromise ASP activities. The opportunities for ASP and non-ASP interactions have increased in recent years with the growth of ASP programs; thus, we conducted an EIN survey of pediatric ID physicians, ASP and non-ASP, to understand the difference in perception of ASP procedures and outcomes in their respective facilities.
Methods
In June 2019, a 10-question multiple-choice survey was distributed to pediatric ID physicians who participate in the IDSA EIN. The survey assessed differences in perceptions of ASP interventions and outcomes between ASP and non-ASP ID physicians and the prescribing habits of other clinician groups. A Likert scale was used for most questions. Two weekly reminder e-mails were sent. Only respondents who indicated that their facility had an ASP were allowed to complete the survey. Analyses were restricted to respondents who answered at least 1 question. Mann-Whitney U and χ Reference Smith, Gerber and Hersh2 tests were used for comparisons as appropriate. Statistical analyses were performed using SAS version 9.4 software (SAS Institute, Cary, NC).
Results
Overall, 176 (49%) of 359 pediatric ID physicians surveyed responded. Among them, 161 (91%) worked in a hospital with an ASP and answered at least 1 question; 96 indicated participating as an ASP member. Most (80%) indicated ≥5 years of postfellowship experience. Also, 64% were employed in a university or medical school setting and practiced at a university (66%) or nonuniversity teaching (26%) hospital. All US regions and some Canadian regions were represented.
ASP physicians (94%) and non-ASP physicians (81%) agreed that the ASP at their institution had improved appropriate antibiotic prescribing in the previous 2 years. Most ASP physicians (91%) and non-ASP physicians (84%) disagreed with the statement that ASP had been too focused on reducing antimicrobial costs with resultant compromise of patient care, and a larger proportion of ASP physicians strongly disagreed. Moreover, <50% of both ASP and non-ASP physicians agreed that ASPs should steward their ID colleagues (Table 1).
Table 1. Antimicrobial Stewardship Program (ASP) Participants Versus Non-ASP Infectious Diseases Physician Agreement With Select Statements Regarding ASP Practices in Their Respective Facility
ASP physicians were more likely than non-ASP ID physicians to agree that critical care (49% vs 32%; P = .03) and hospitalists (83% vs 67%; P = .01) adhered to ASP principles. More than 50% of both groups disagreed with the statement that surgeons adhered to ASP principles (Table 1).
Most physicians in both groups were not concerned that ASPs make recommendations without seeing patients. Furthermore, ∼30% of non-ASP and 23% of ASP physicians were at least somewhat concerned about disagreement between ASP and ID physicians (P = .77). Most ASP and non-ASP ID physicians were either neutral or were not concerned about impact on prescriber autonomy, unintended consequences of guidance, decreases in prescriber efficiency, or delays in antibiotic initiation (Table 2).
Table 2. Antimicrobial Stewardship Program (ASP) Participants Versus Non-ASP Infectious Diseases Physician Concern Regarding ASP Practices and Outcomes in their Respective Facility
Discussion
Overall, both ASP and non-ASP physicians viewed ASPs favorably, and concerns about ASP practices and patient outcomes were minimal. Consistent with results from prescriber surveys, Reference Flannery, Swami, Chan and Eppes7–Reference Szymczak, Kitt and Hayes9 physicians in both groups agreed that ASPs had improved appropriate antibiotic prescribing in the prior 2 years. Reduction in unnecessary antibiotic spending should be an ASP goal, Reference Barlam, Cosgrove and Abbo1 and neither group demonstrated concern that their ASP was too focused on cost reduction at the expense of patient care.
ASP physicians were more likely than non-ASP physicians to report that ID and other clinician groups prescribed antibiotics according to ASP principles. The discrepancy may arise as non-ASP physicians observe prescribing practices most often in the context of consultation, whereas ASP physicians regularly review prescribing patterns of other pediatric subspecialties and provide a less biased sample. Furthermore, ASP physicians are more likely to interact with prescribers from other specialties, resulting in an overall more favorable impression of these groups.
Almost 60% of each group disagreed or were unsure whether ASPs should steward their ID colleagues. Furthermore, non-ASP physicians were most concerned with disagreement with the ASP. In a recent survey, Reference Szymczak, Kitt and Hayes9 prescribers expressed similar concerns regarding disagreement between ASP and ID consultants. Although this could pose a significant barrier to effective ASP implementation, data are lacking on how frequently ASPs advise their ID colleagues or give conflicting recommendations. Greater collaboration between ASPs and ID physicians is needed.
Consistent with other research, Reference Smith, Gerber and Hersh2–Reference McCulloh, Queen and Lee5,Reference Flannery, Swami, Chan and Eppes7 <10% of respondents in either group reported concern over unintended consequences of ASP recommendations. In a survey of 153 pediatric providers (93 respondents), 94% reported never having a patient with an adverse event because of an ASP intervention. Reference Flannery, Swami, Chan and Eppes7 In a review of 350 ASP recommendations at a freestanding children’s hospital, there were no differences in 30-day readmission rates or length of stay (LOS) when an ASP recommendation was followed. Reference McCulloh, Queen and Lee5 In a separate study in the same institution, ASP recommendations for medicine patients with complex chronic conditions were associated with a lower 30-day readmission rate (4.2% vs 7.3%; P = .005). Reference Lee, Goldman and Yu4 In a third study in the same institution among patients in hematology-oncology, neonatal intensive care, and pediatric intensive care units, a 28% decrease in the odds of death (95% CI, 0.54–0.96) was observed when a recommendation was made with no increase in readmissions or hospital-acquired Clostridioides difficile infection rates. Reference Goldman, Newland, Price, Yu and Lee3 Although larger, multicenter studies of patient outcomes are needed, the results of this study and others show that concern about the negative consequences of ignoring ASP recommendations is limited.
Prescriber surveys suggest differing views on how ASPs impact efficiency. Only 3.2% of ASP physicians and 6.3% of non-ASP physicians were concerned about decreasing prescriber efficiency. However, a larger proportion of both, 12% and 13%, respectively, were concerned about delays in antibiotic initiation. In a recent, single-institution survey, Reference Szymczak, Kitt and Hayes9 140 (95%) of 145 respondents indicated that their ASP facilitated appropriate antimicrobial use, and 133 (92%) of 144 indicated that their ASP improved quality of patient care. However, 38 (26%) of 146 respondents indicated that the ASP reduced their efficiency and some expressed concerns over delays in antibiotic administration in free-text responses. Notably, the ASP at the institution in that study required prior authorization for >50 antimicrobials. However, institutions with ASPs that primarily audit antimicrobial use prospectively and provide feedback may have a different experience.
This study had several limitations. With a response rate of <50%, results may not be representative of all North American pediatric ID physicians. A larger proportion of respondents were ASP-affiliated; thus, motivation to complete the survey likely differed between the 2 groups, possibly limiting our ability to detect differences. Lastly, these data precede the SARS-CoV-2 pandemic, so results might differ were the survey conducted now.
In this survey of ASP and non-ASP pediatric ID physicians, both groups reported improvement in appropriate antibiotic prescribing and minimal negative consequences. Some differences existed over perception of other subspecialty prescribing practices and ASP outcomes, though responses were overall similar between groups. Studies to better characterize ASP practices, evaluate outcomes, and improve ASP collaborations with ID physicians are needed.
Acknowledgments
Financial support
This work was supported by the Centers for Disease Control and Prevention (cooperative agreement No. 1 U50 CK000477). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the Centers for Disease Control and Prevention or the Department of Health and Human Services.
Conflicts of interest
All authors report no conflicts of interest relevant to this article.
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