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Regional and statewide antibiograms as targeted interventions against antibiotic resistance

Published online by Cambridge University Press:  25 June 2020

John G Plante
Affiliation:
University of South Carolina School of Medicine, Columbia, South Carolina
Hana R Winders*
Affiliation:
Department of Clinical Pharmacy and Outcomes Sciences, University of South Carolina College of Pharmacy, Columbia, South Carolina
P. Brandon Bookstaver
Affiliation:
Department of Clinical Pharmacy and Outcomes Sciences, University of South Carolina College of Pharmacy, Columbia, South Carolina Department of Pharmacy, Prisma Health Richland, Columbia, South Carolina
Majdi N Al-Hasan
Affiliation:
University of South Carolina School of Medicine, Columbia, South Carolina Department of Medicine, Prisma Health University of South Carolina Medical Group, Columbia, South Carolina
Julie Ann Justo
Affiliation:
Department of Clinical Pharmacy and Outcomes Sciences, University of South Carolina College of Pharmacy, Columbia, South Carolina Department of Pharmacy, Prisma Health Richland, Columbia, South Carolina
Katie S Waites
Affiliation:
South Carolina Department of Health and Environmental Control, Columbia, South Carolina
Sharon Weissman
Affiliation:
University of South Carolina School of Medicine, Columbia, South Carolina Department of Medicine, Prisma Health University of South Carolina Medical Group, Columbia, South Carolina
*
Author for correspondence: Hana R. Winders, Email: hwinders@cop.sc.edu
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Abstract

Type
Letter to the Editor
Copyright
© 2020 by The Society for Healthcare Epidemiology of America. All rights reserved.

To the Editor—Antibiotic resistance is becoming an increasingly heavy burden on our nation, leading to significant patient morbidity, mortality, and healthcare expenditures. 1 Antibiotic misuse may be considered a primary driver of resistance, and recent studies suggest that ~20%–30% of inpatient antibiotics and 30%–40% of ambulatory antibiotics were inappropriately prescribed. Reference Fleming-Dutra, Hersh and Shapiro2,Reference White, Clark, Sellick and Mergenhagen3 According to the Centers for Disease Control and Prevention’s (CDC’s) 2019 Threats Report, 1 >2.8 million resistant infections and 35,000 associated deaths are reported annually in the United States. Although this has been accompanied by a 27% reduction in the number of resistant nosocomial infections, the total number of annual resistant infections has increased, highlighting the need for additional community-focused antimicrobial stewardship interventions. 1

The impact of several statewide and regional antibiograms on clinical management and stewardship efforts has previously been described. Reference Leeman, Zimmermann and Hansen4,Reference Var, Hadi and Khardori5 Here, we discuss regional and statewide antibiograms in South Carolina. The Antimicrobial Stewardship Collaborative of South Carolina (ASC-SC) was established in 2016 with support from the CDC. This organization coordinates a variety of statewide antimicrobial stewardship initiatives, including the statewide antibiogram project presented in this letter. This endeavor represents the continuation of a smaller-scale pilot project conducted from 2007 to 2011 through a collaboration between the South Carolina Department of Health and Environmental Control and the University of South Carolina College of Pharmacy.

From 2007 to 2011 and from 2015 to 2017, hospitals and nursing homes throughout South Carolina were asked to submit their annual facility-specific and ambulatory antibiograms to ASC-SC. Each antibiogram was deconstructed into individual isolates and combined into one statewide and multiple regional antibiograms annually. Most of the data consisted of isolates from acute-care hospitals. The yearly cumulative antibiograms were redistributed for use by healthcare facilities across the state.

The compiled statewide antibiogram contains 2017 isolate data from 49 institutions (Fig. 1). Statewide susceptibility rates for the 2017 year were compared to the 2015 year. We used χ2 analysis to assess significance at an α level of 0.05.

1This figure contains isolate data from 49 institutions across the state of South Carolina. Numbers represent percent susceptibility. Blank cells correspond to insufficient data or lack of antibiotic testing. Not all reported drugs were tested against every available isolate. 2 Enterobacter aerogenes is now Klebsiella aerogenes. 3Differences between the total number of Staphylococcus aureus isolates versus MSSA plus MRSA isolates are due to variations in facility-specific reporting. Note. Trimeth/sulfa, trimethoprim/sulfamethoxazole; # isolates, number of isolates; MSSA, methicillin-sensitive Staphylococcus aureus; MRSA, methicillin-resistant Staphylococcus aureus.

Fig. 1. 2017 South Carolina statewide antibiogram.

Overall, Escherichia coli was the most frequently reported organism (33,848 isolates in 2017). From 2015 to 2017, Acinetobacter baumannii demonstrated increased susceptibility to cefepime (70% vs 83%, P < .001). Susceptibility to ceftazidime and meropenem did not change significantly. Most Enterobacterales exhibited high susceptibility to third- and fourth-generation cephalosporins, and all were highly susceptible to meropenem. Enterobacter spp proved most resistant, but susceptibility significantly improved for ceftriaxone: E. aerogenes: 78% versus 83% (P = .01) and E. cloacae: 72% versus 77% (P = .002). Despite relatively high resistance rates to levofloxacin and trimethoprim-sulfamethoxazole overall, a slight improvement in susceptibility was observed in E. coli isolates for both levofloxacin (73% vs 75%; P < .001) and trimethoprim-sulfamethoxazole (73% vs 74%; P = .01).

The susceptibility of Pseudomonas aeruginosa to meropenem increased slightly (91% vs 92%; P = .03) but did not change significantly to cephalosporins or aminoglycosides. The proportion of methicillin-susceptible Staphylococcus aureus increased slightly (48% vs 50%; P = .009). Nonmeningeal Streptococcus pneumoniae exhibited increased susceptibility to penicillin (73% vs 87%; P < .001) but decreased susceptibility to ceftriaxone (96% vs 93%; P = .03). Susceptibility to erythromycin did not change significantly (49% vs 48%; P = .91).

A statewide antibiogram may serve as a valuable clinical tool for several reasons. First, an understanding of regional variability in resistance rates could encourage more appropriate empiric antibiotic selection. Reference Leeman, Zimmermann and Hansen4,Reference Nodzo and Frisch6 For example, first-line empiric treatment options for acute pyelonephritis include oral fluoroquinolones, unless community resistance is >10%, or oral trimethoprim-sulfamethoxazole, if the isolate is known to be susceptible. Reference Gupta, Hooton and Naber7 Our antibiogram demonstrates E. coli’s poor susceptibility to these agents, and this could guide practitioners, especially in the outpatient setting, to administer a single parenteral dose of a long-acting agent such as ceftriaxone and to more carefully consider patient-specific risk factors for resistance. Reference Gupta, Hooton and Naber7-Reference Shah, Justo, Bookstaver, Kohn, Albrecht and Al-Hasan9 In patients with acute cystitis, empiric prescribing may be improved by observing the increased susceptibility of nitrofurantoin relative to other oral options.

According to recent guidelines, Reference Metlay, Waterer and Long10 macrolides should only be prescribed as empiric monotherapies for community-acquired pneumonia if local resistance to S. pneumoniae is known to be <25%. However, our antibiogram shows minimal organism-specific macrolide susceptibility, thereby encouraging outpatient providers to select a more appropriate empiric treatment (eg, amoxicillin or doxycycline). Reference Metlay, Waterer and Long10

As illustrated herein, evolving trends in resistance patterns may be easily identified, and this may lead to more targeted, robust infection prevention and control responses. Reference Gupta, Hooton and Naber7 Individual facilities may also use these data to compare self-reported resistance rates with those in the region. Finally, institutions without access to local antibiograms, including certain outpatient centers and nursing homes, may find this tool especially beneficial to improve prescribing practices and antibiotic stewardship. Reference Var, Hadi and Khardori5

Regional and statewide antibiograms have several limiations. Most of our data were gathered from hospitals; relatively few ambulatory antibiograms were submitted. Even though inpatient antibiograms include patients admitted with community-acquired infections, community resistance rates are likely underrepresented. These factors may have led to overestimated community rates, a relevant issue considering the growing concern of resistance in this setting. 1,Reference Nodzo and Frisch6

Despite efforts to standardize antibiogram creation procedures, little evidence supports adherence to these guidelines. Reports therefore undoubtedly vary across institutions, limiting the ability to compare interfacility susceptibility rates. Reference Nodzo and Frisch6,Reference Gupta, Hooton and Naber7 Furthermore, although antibiograms may provide general guidance, other patient-specific factors must be considered to make an informed clinical decision, including the type and severity of the current infection and previous antibiotic use. Reference Gupta, Hooton and Naber7

In conclusion, statewide and regional antibiograms may be effective strategies in targeting antibiotic resistance. Even though they must be viewed within the scope of their limitations, they should be considered valuable assets in future antibiotic stewardship endeavors.

Acknowledgments

The authors thank advisory board members of the Antimicrobial Stewardship Collaborative of South Carolina for facilitating this study. The findings of this report are those of the authors and do not necessarily represent the official position of the South Carolina Department of Health and Environmental Control.

Financial support

This work was supported by a federal grant (Epidemiology and Laboratory Capacity Project K2) from the Centers for Disease Control and Prevention awarded to South Carolina DHEC.

Conflicts of interest

P.B.B. served as a research advisory board member of Kedrion Biopharma and on the speaker’s bureau of bioMérieux. He also received a grant from ALK Abello, Inc. H.R.W. and J.J. also served on the speaker’s bureau of bioMérieux. All other authors report no conflicts of interest relevant to this article.

References

US Department of Health and Human Services. Antibiotic resistance threats in the United States, 2019. Centers for Disease Control and Prevention website. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf. Published 2019. Accessed April 18, 2020.Google Scholar
Fleming-Dutra, KE, Hersh, AL, Shapiro, DJ, et al. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010–2011. JAMA 2016;315:18641873.CrossRefGoogle ScholarPubMed
White, AT, Clark, CM, Sellick, JA, Mergenhagen, KA. Antibiotic stewardship targets in the outpatient setting. Am J Infect Control 2019;47:858863.CrossRefGoogle ScholarPubMed
Leeman, H, Zimmermann, C, Hansen, K, et al. 2017 State antibiogram and implications for antibiotic prescribing. New Hampshire Department of Health and Human Services website. https://www.dhhs.nh.gov/dphs/cdcs/hai/documents/antibiogram-sum-2017.pdf. Published 2018. Accessed April 18, 2020.Google Scholar
Var, SK, Hadi, R, Khardori, NM. Evaluation of regional antibiograms to monitor antimicrobial resistance in Hampton Roads, Virginia. Ann Clin Microbiol Antimicrob 2015;14:22.CrossRefGoogle ScholarPubMed
Nodzo, SR, Frisch, NB. The use of antibiograms in orthopedic surgery. Curr Rev Musculoskelet Med 2018;11(3):341346.CrossRefGoogle ScholarPubMed
Gupta, K, Hooton, TM, Naber, KG, et al. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 2011;52(5):e103e120.CrossRefGoogle Scholar
DeMarsh, M, Bookstaver, PB, Gordon, C, et al. Prediction of sulfamethoxazole/trimethoprim resistance in community-onset urinary tract infections. J Glob Antimicrob Resist 2020;21:218222.CrossRefGoogle Scholar
Shah, A, Justo, JA, Bookstaver, PB, Kohn, J, Albrecht, H, Al-Hasan, MN. Application of fluoroquinolone resistance score in management of complicated urinary tract infections. Antimicrob Agents Chemother 2017;61(5):e02313-16.CrossRefGoogle ScholarPubMed
Metlay, JP, Waterer, GW, Long, AC, et al. Diagnosis and treatment of adults with community-acquired pneumonia: an official clinical practice guideline of the American Thoracic Society and Infectious Diseases Society of America. Am J Respir Crit Care Med 2019;200(7):e45e67.CrossRefGoogle ScholarPubMed
Figure 0

Fig. 1. 2017 South Carolina statewide antibiogram.

1This figure contains isolate data from 49 institutions across the state of South Carolina. Numbers represent percent susceptibility. Blank cells correspond to insufficient data or lack of antibiotic testing. Not all reported drugs were tested against every available isolate.2Enterobacter aerogenes is now Klebsiella aerogenes.3Differences between the total number of Staphylococcus aureus isolates versus MSSA plus MRSA isolates are due to variations in facility-specific reporting. Note.Trimeth/sulfa, trimethoprim/sulfamethoxazole; # isolates, number of isolates; MSSA, methicillin-sensitive Staphylococcus aureus; MRSA, methicillin-resistant Staphylococcus aureus.
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