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Trends in Antibiotic Resistance Among Ocular Microorganisms in the United States From 2009 to 2018

Educational Objective
To assess overall antibiotic resistance profiles and trends among bacterial isolates from ocular sources collected during 10 years.
1 Credit CME
Key Points

Question  What are the antibiotic resistance profiles and trends among common ocular pathogens across the United States?

Findings  In this cross-sectional study of more than 6000 ocular isolates of Staphylococcus aureus, coagulase-negative staphylococci, Streptococcus pneumoniae, Pseudomonas aeruginosa, and Haemophilus influenzae collected between 2009 and 2018, methicillin resistance and multidrug resistance were prevalent among staphylococci. Antibiotic resistance profiles were mostly unchanged during 10 years.

Meaning  These in vitro antibiotic resistance data may assist clinicians in selecting appropriate antibiotics for treatment of ocular infections.

Abstract

Importance  Antibiotic resistance in ocular infections can affect treatment outcomes. Surveillance data on evolving antibacterial susceptibility patterns inform the treatment of such infections.

Objective  To assess overall antibiotic resistance profiles and trends among bacterial isolates from ocular sources collected during 10 years.

Design, Setting, and Participants  This cross-sectional study of longitudinal data from the ongoing, nationwide, prospective, laboratory-based surveillance study, the Antibiotic Resistance Monitoring in Ocular Microorganisms (ARMOR) study, included clinically relevant isolates of Staphylococcus aureus, coagulase-negative staphylococci (CoNS), Streptococcus pneumoniae, Pseudomonas aeruginosa, and Haemophilus influenzae cultured from patients with ocular infections at US centers from January 1, 2009, to December 31, 2018.

Main Outcomes and Measures  Minimum inhibitory concentrations were determined for various combinations of antibiotics and species. Odds ratios (ORs) were determined for concurrent antibiotic resistance; analysis of variance and χ2 tests were used to evaluate resistance rates by patient age and geographic region; Cochran-Armitage tests identified changing antibiotic susceptibility trends over time.

Results  A total of 6091 isolates (2189 S aureus, 1765 CoNS, 590 S pneumoniae, 767 P aeruginosa, and 780 H influenzae) from 6091 patients were submitted by 88 sites. Overall, 765 S aureus (34.9%) and 871 CoNS (49.3%) isolates were methicillin resistant and more likely to be concurrently resistant to macrolides (azithromycin: S aureus: OR, 18.34 [95% CI, 13.64-24.67]; CoNS: OR, 4.59 [95% CI, 3.72-5.66]), fluoroquinolones (ciprofloxacin: S aureus: OR, 22.61 [95% CI, 17.96-28.47]; CoNS: OR, 9.73 [95% CI, 7.63-12.40]), and aminoglycosides (tobramycin: S aureus: OR, 18.29 [95% CI, 13.21-25.32]; CoNS: OR, 6.28 [95% CI, 4.61-8.56]) compared with methicillin-susceptible isolates (P < .001 for all). Multidrug resistance was observed among methicillin-resistant S aureus (577 [75.4%]) and CoNS (642 [73.7%]) isolates. Antibiotic resistance among S pneumoniae isolates was highest for azithromycin (214 [36.3%]), whereas P aeruginosa and H influenzae isolates showed low resistance overall. Differences in antibiotic resistance were found among isolates by patient age (S aureus: F = 28.07, P < .001; CoNS: F = 11.46, P < .001) and geographic region (S aureus: F = 8.03, P < .001; CoNS: F = 4.79, P = .003; S pneumoniae: F = 8.14, P < .001; P aeruginosa: F = 4.32, P = .005). Small changes in antibiotic resistance were noted over time (≤2.5% per year), with decreases in resistance to oxacillin/methicillin (oxacillin: −2.16%; 95% CI, −3.91% to −0.41%; P < .001) and other antibiotics among S aureus isolates, a decrease in ciprofloxacin resistance among CoNS (−1.38%; 95% CI, −2.24% to −0.52%; P < .001), and an increase in tobramycin resistance among CoNS (0.71%; 95% CI, –0.29% to 1.71%; P = .03). Besifloxacin retained consistently low minimum inhibitory concentrations.

Conclusions and Relevance  Antibiotic resistance may be prevalent among staphylococcal isolates, particularly among older patients. In this study, a few small differences in antibiotic resistance were observed by geographic region or longitudinally.

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Article Information

Accepted for Publication: December 24, 2019.

Published Online: April 9, 2020. doi:10.1001/jamaophthalmol.2020.0155

Open Access: This is an open access article distributed under the terms of the CC-BY-NC-ND License. © 2020 Asbell PA et al. JAMA Ophthalmology.

Corresponding Author: Penny A. Asbell, MD, MBA, Department of Ophthalmology, The University of Tennessee Health Science Center, 930 Madison Ave, Ste 100, Memphis, TN 38163 (pasbell@uthsc.edu).

Author Contributions: Drs Sanfilippo and DeCory had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: All authors.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Sanfilippo, DeCory.

Critical revision of the manuscript for important intellectual content: All authors.

Administrative, technical, or material support: Sanfilippo, Sahm, DeCory.

Supervision: Asbell, Sanfilippo, DeCory.

Conflict of Interest Disclosures: Dr Asbell reported serving as a consultant and receiving personal fees from Alcon, Kao, Medscape, Perrigo, Santen, ScientiaCME, Senju, and Shire and serving on advisory boards for Allakos, Allergan, Bausch + Lomb (a division of Bausch Health US, LLC), Dompé, Kala, Novaliq, Novartis, Regeneron Pharmaceuticals, and Sun Pharmaceuticals outside the submitted work. Dr Sanfilippo reported being an employee of Bausch + Lomb (a division of Bausch Health US, LLC). Dr Sahm reported being an employee of International Health Management Associates Inc. Dr DeCory reported being an employee of Bausch + Lomb (a division of Bausch Health US, LLC).

Funding/Support: The Antibiotic Resistance Monitoring in Ocular Microorganisms (ARMOR) study was funded by Bausch + Lomb (a division of Bausch Health US, LLC).

Role of the Funder/Sponsor: The funding source was responsible for the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Meeting Presentation: This paper was presented in part at the annual meeting of the American Academy of Ophthalmology; October 12-15, 2019; San Francisco, California; and the annual meeting of the American Academy of Optometry; October 24, 2019; Orlando, Florida.

Additional Contributions: Medical writing assistance and statistical assistance was provided by Churchill Communications in Maplewood, New Jersey, and funded by Bausch + Lomb (a division of Bausch Health US, LLC).

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