A Systematic Review of Multi-decade Antibiotic Resistance Data for Ocular Bacterial Pathogens in the United States

Abstract

Introduction: Since 2009, the Antibiotic Resistance Monitoring in Ocular Microorganisms (ARMOR) surveillance study has been assessing in vitro antibiotic resistance for bacterial isolates sourced from ocular infections in the US. The main goal of this systematic review was to compare in vitro resistance data for ocular pathogens from published US studies with the most recently published data from the ARMOR study (2009-2018) and, where possible, to evaluate trends in bacterial resistance over time over all studies.

Methods: A literature search was conducted using MEDLINE®, BIOSIS Previews®, and EMBASE^® databases (1/1/1995-6/30/2021). Data were extracted from relevant studies and antibiotic susceptibility rates for common ocular pathogens (Staphylococcus aureus, coagulase-negative staphylococci [CoNS], Streptococcus pneumoniae, Pseudomonas aeruginosa, and Haemophilus influenzae), longitudinal changes in susceptibility, and multidrug resistance (MDR) were compared descriptively.

Results: Thirty-two relevant studies were identified. High in vitro resistance was found among S. aureus and CoNS to fluoroquinolones, macrolides, and methicillin/oxacillin across studies, with high rates of MDR noted, specifically among methicillin-resistant staphylococci. Data from studies pre-dating or overlapping the early years of ARMOR reflected increasing rates of S. aureus resistance to fluoroquinolones, macrolides, methicillin/oxacillin, and aminoglycosides, while the ARMOR data suggested slight decreases in resistance to these classes between 2009 and 2018. Overall, methicillin-resistant S. aureus (MRSA) prevalence peaked from 2005 to 2015 with a possible decreasing trend in more recent years.

Discussion and conclusions: Data from local and regional US datasets were generally consistent with data from the national ARMOR surveillance study. Continued surveillance of ocular bacterial pathogens is needed to track trends such as methicillin resistance and MDR prevalence and any new emerging antibiotic resistance phenotypes. Susceptibility data from ARMOR can inform initial choice of therapy, especially in practice areas where local antibiograms are unavailable.

Keywords: Antibiotic resistance; Conjunctivitis; Endophthalmitis; Keratitis; MRSA; Multidrug resistance; Ocular; Surveillance.

Fig. 1

Antibiotic class in vitro susceptibility of common ocular bacterial pathogens (US studies). Data points represent the percentages of pathogens susceptible to the antibiotic classes indicated along the bottom of the figure. Where reported as such, data are presented by ocular diagnosis/tissue source (top labels C, K, E; see explanatory legend below panel A). Data without a known ocular diagnosis/tissue source and/or data inclusive of multiple diagnoses/tissue sources are depicted by horizontal lines spanning the antibiotic category. Red squares/lines represent ARMOR data^a; black circles/lines represent other published data with time frames at least partially contemporary with ARMOR (2009–2018); gray circles/lines represent other published data with time frames exclusively older than ARMOR (pre-2009). For studies reporting resistance rates by individual year only, most recent year data are reflected. Only studies with pathogen samples consisting of ≥  20 isolates per species are included. Source data can be viewed in Table S1 of the Supplemental Material. AG aminoglycosides, CHL chloramphenicol, CoNS coagulase-negative staphylococci, FQ fluoroquinolones, MET methicillin/oxacillin, ML macrolides, MRSA methicillin-resistant Staphylococcus aureus, MSSA methicillin-susceptible Staphylococcus aureus, PEN penicillin, TET tetracycline, VAN vancomycin. ^aNote: For the ARMOR study, the horizontal data lines reflect all ARMOR data for that pathogen/antibiotic class combination and include the tissue source-specific data represented by the red square plot points in the same categories. Tissue source was unknown for about half (49%) of all isolates collected in ARMOR. A S. aureus. B MSSA. Note: Markers labeled “X2” indicate the presence of 2 data points with identical values at the indicated plot point. C MRSA. Note: Markers labeled “X2” indicate the presence of 2 data points with identical values at the indicated plot point. D CoNS. S. epi = Staphylococcus epidermidis. E S. pneumoniae. F P. aeruginosa. Note: Markers labeled “X2” or “X3” denote the presence of 2 or 3 data points, respectively, with identical values at the indicated plot point. G H.  influenzae

Fig. 2

Published data on prevalence of MRSA among S. aureus isolates by year (US studies) [–27, 29, 32, 40, 46]. Points connected by lines reflect a single percentage reported for a range of years