Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Endophthalmitis Associated With Intravitreal Injections of Anti-VEGF Agents at a Tertiary Referral Center: In-House and Referred Cases

Nicolas A. Yannuzzi, MD; Ninel Z. Gregori, MD; Philip J. Rosenfeld, MD; Nidhi Relhan, MD; Nimesh A. Patel, MD; Nancy Si, BS; Darlene Miller, CIC, DHSc; Sander R. Dubovy, MD; William E. Smiddy, MD; Stephen G. Schwartz, MD, MBA; Harry W. Flynn, MD

Abstract

BACKGROUND AND OBJECTIVE:

To report the incidence rates, causative organisms, and visual acuity (VA) outcomes in patients with endophthalmitis associated with intravitreal injection of anti-vascular endothelial growth factor inhibitors.

PATIENTS AND METHODS:

Retrospective case series between 2005 and 2017.

RESULTS:

The study included 39 eyes of 39 patients, including 27 (69%) referred and 12 (31%) institutional patients. The use of topical antibiotics after an injection was gradually phased out at the authors' institution, where the preinjection rate of all clinically suspected endophthalmitis was 0.013% (24 of 183,898). The most common isolates were coagulase-negative Staphylococcus and Streptococcus. A VA of 5/200 or better was achieved in 21 of 39 eyes (54%) overall and in two of 15 eyes (13%) infected with Streptococcus.

CONCLUSIONS:

The rate of post-intravitreal injection endophthalmitis is low. Outcomes were generally poor, and the worst were associated with Streptococcus.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:313–319.]

Abstract

BACKGROUND AND OBJECTIVE:

To report the incidence rates, causative organisms, and visual acuity (VA) outcomes in patients with endophthalmitis associated with intravitreal injection of anti-vascular endothelial growth factor inhibitors.

PATIENTS AND METHODS:

Retrospective case series between 2005 and 2017.

RESULTS:

The study included 39 eyes of 39 patients, including 27 (69%) referred and 12 (31%) institutional patients. The use of topical antibiotics after an injection was gradually phased out at the authors' institution, where the preinjection rate of all clinically suspected endophthalmitis was 0.013% (24 of 183,898). The most common isolates were coagulase-negative Staphylococcus and Streptococcus. A VA of 5/200 or better was achieved in 21 of 39 eyes (54%) overall and in two of 15 eyes (13%) infected with Streptococcus.

CONCLUSIONS:

The rate of post-intravitreal injection endophthalmitis is low. Outcomes were generally poor, and the worst were associated with Streptococcus.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:313–319.]

Introduction

Intravitreal anti-vascular endothelial growth factor (VEGF) therapy has altered the treatment of age-related macular degeneration (AMD), diabetic macular edema (DME), and other retinal vascular diseases. Though rare, the most concerning complication from an intravitreal injection is endophthalmitis. Retrospective reviews of endophthalmitis following intravitreal injection have reported an incidence of approximately 0.02%,1,2 and population-based studies have estimated it at 0.05%.2 In spite of prompt and appropriate treatment, visual outcomes are frequently poor. The purpose of this study is to report the incidence rates, medications utilized, causative organisms, and visual acuity (VA) outcomes due to infectious endophthalmitis following intravitreal injection at a tertiary referral center.

Patients and Methods

The current study is a non-comparative consecutive case series. Data were gathered by a retrospective review of medical records and from records from the Infection Control Committee of our institution. This study included patients who had received intravitreal injections at our institution. The study also included those who had been treated with intravitreal anti-VEGF therapy at outside practices and were later referred with the diagnosis of clinically suspected endophthalmitis. Approval for this review was obtained by the institutional review board of the University of Miami School of Medicine.

Clinical and microbiology records were reviewed for all patients who presented to Bascom Palmer Eye Institute between January 1, 2005, and December 31, 2017, with clinically diagnosed, culture-positive endophthalmitis occurring after intravitreal injections. However, all cases of clinically suspected endophthalmitis receiving intravitreal antibiotics were included when calculating the rate of endophthalmitis following intravitreal injection at our center for comparative purposes. Clinically suspected endophthalmitis was defined as a clinical diagnosis to warrant administration of intravitreal antibiotics. One patient with late-onset endophthalmitis after intravitreal injection, occurring greater than 6 weeks after injection, was excluded because of an unclear causative relationship. Management of endophthalmitis at the time of diagnosis was at the discretion of the treating physician regarding the use of pars plana vitrectomy (PPV) or vitreous tap and inject.

Anti-VEGF injections at our center were performed with nursing personnel who prepared the eye with topical anesthesia and antisepsis according to a standard protocol.2 Povidone-iodine 5% and lidocaine 4% drops, 10% povidone-iodine swab to the lids and lashes, and sterile calipers were used. For bevacizumab (Avastin; Genentech, South San Francisco, CA) injections performed at our hospital-based practices in Miami and Plantation, the drug was prepared by the hospital's pharmacy. Bevacizumab syringes were released for clinical use only after the microbiology laboratory reported negative cultures from 10% of aliquots held for 14 days. The prepared syringes were then refrigerated and used in the clinics within 3 months of the repackaging date. For bevacizumab injections performed at our non-hospital-based satellites during the period from 2005 to 2016, there was a transition from using the hospital-prepared bevacizumab to using bevacizumab procured from an outside compounding pharmacy.

Starting in 2008, topical antibiotics used prophylactically before, during, or after intravitreal injections were gradually phased out. By 2009, the majority of physicians at our institution were not using topical antibiotics, and by 2012, the entire faculty had ceased using them. The use of a mask (by patient, nurse, or physician) and a (sterile) lid speculum were at the discretion of the treating physician.

Of note, the majority of virulent cases in the current study were referred from the community at the time of an outbreak of Streptococcus endophthalmitis stemming from contaminated bevacizumab prepared at an outside compounding pharmacy supplying community practices.3 Injection protocols and the sources of bevacizumab used by community ophthalmologists who had referred post-injection endophthalmitis were not available for this report.

Vitreous fluid cultures were obtained by direct vitreous aspiration with a needle with size chosen by the treating physician. Direct vitreous samples were inoculated onto chocolate, 5% sheep blood agar (anaerobic), sabouraud dextrose agar and thioglycollate broth in the clinic or delivered to the laboratory in a syringe for direct plating. Chocolate and blood agar plates were kept for 7 days. Thioglycollate broth and sabouraud dextrose agar were kept for 14 days. Chocolate agar, 5% sheep blood, and thioglycollate broth were incubated at 35° Celsius in carbon dioxide. Sabouraud dextrose agar plates were incubated at 35° Celsius without carbon dioxide.

The current report includes some data that were previously published.1,2 However, it also includes referred cases that have not been previously reported, as well as more recent cases from 2015 to 2017 treated after the aforementioned studies were concluded. In total, the prior manuscript included nine of the current 39 cases described in this report. Furthermore, the current report focuses more deeply on the microbiological features and compares the characteristics of the institutional and referred cases. All statistical comparisons between categorical variables were conducted by using a Fisher's exact or Pearson's test and were performed in SPSS version 22 (SPSS, Chicago, IL).

Results

In total, there were 39 culture positive eyes of 39 patients. Eighteen (46%) of the 39 eyes were right eyes. Eighteen (46%) of the 39 patients were male. The average age at diagnosis was 79 years (range: 44 years to 94 years). Twelve (31%) of 39 eyes received the inciting intravitreal injection at our institution, whereas the remaining 27 (69%) were referred. Of the 27 referred cases, nine (33%) were associated with an outbreak of Streptococcus endophthalmitis from contaminated bevacizumab in the community. The average length of follow-up after diagnosis of endophthalmitis was 12.5 months (median: 5.2 months; range: 3 days to 53.4 months). Baseline clinical features are summarized in Table 1, including a breakdown of institutional and referred cases.

Clinical Characteristics in Patients With Culture-Positive Endophthalmitis After Intravitreal Injection With Anti-VEGF Agents

Table 1:

Clinical Characteristics in Patients With Culture-Positive Endophthalmitis After Intravitreal Injection With Anti-VEGF Agents

Among intravitreal injections administered at our center, there were no statistically significant differences between the anti-VEGF drugs in the rates of endophthalmitis. The rate of clinically suspected endophthalmitis at our institution was 0.011% (10 of 87,883) with bevacizumab, 0.016% (six of 37,916) with ranibizumab (Lucentis; Genentech, South San Francisco, CA), and 0.016% (eight of 56,094) with aflibercept (Eylea; Regeneron, Tarrytown, NY) (Table 2). From 2005 to 2011, the rate of endophthalmitis was 14 of 75,579 (0.019%); after complete cessation of prophylactic antibiotic use, the rate of endophthalmitis from 2012 to 2017 was 10 of 108,319 (0.009%; P = .09). During the past 2 years, there was an increasing trend toward the use of aflibercept and a decreasing trend toward the use of ranibizumab (Figure).

Clinically Suspected Endophthalmitis Rates for Each Anti-VEGF Medication Administered at Bascom Palmer Eye Institute From 2005–20171

Table 2:

Clinically Suspected Endophthalmitis Rates for Each Anti-VEGF Medication Administered at Bascom Palmer Eye Institute From 2005–2017

Intravitreal anti-vascular endothelial growth factor utilization at Bascom Palmer Eye Institute, 2005–2017.

Figure.

Intravitreal anti-vascular endothelial growth factor utilization at Bascom Palmer Eye Institute, 2005–2017.

The most common preinjection diagnosis overall was AMD, which was present in 33 (85%) of 39 eyes. Other diagnoses included cystoid macular edema (n = 2; 5%), diabetic macular edema (n = 1; 3%), branch retinal vein occlusion (n = 1; 3%), central retinal vein occlusion (n = 1; 3%), and idiopathic choroidal neovascularization (n = 1; 3%). Overall, among institutional and referred culture-positive cases, the most common medication injected was bevacizumab in 23 (59%) of 39 eyes. Ranibizumab had been injected in eight (21%) of 39 eyes, aflibercept in six (15%), pegaptanib (Macugen; Bausch + Lomb, Rochester, NY) in one (3%), and an unspecified anti-VEGF drug in one eye (3%).

Based on the information recorded in the medical records, hypopyon was present in 26 (67%) of 39 eyes. Fibrin was present in 20 (51%) of 39 eyes. The average and median times from intravitreal injection to presentation with endophthalmitis were 3 days (range: 1 day to 8 days). In the 39 eyes, 24 (62%) presented in 3 days or less, 13 (33%) presented between 4 days and 7 days, and two (5%) presented in more than 7 days. VA at initial presentation was 5/200 or better in four (10%) of 39 eyes and light perception in 11 eyes (28%).

Intravitreal vancomycin (1 mg/0.1 mL) and ceftazidime (2.25 mg/0.1 mL) were used for the initial treatment in 38 (97%) of 39 eyes. One (3%) of 39 eyes was treated with intravitreal vancomycin and amikacin (0.4 mg/0.1 mL). Twenty-eight (72%) of 39 eyes also received intravitreal dexamethasone (Ozurdex; Allergan, Inc., Irvine, CA) (0.4 mg/0.1 mL). All patients were treated with initial vitreous tap and injection of intravitreal antibiotics. Seven (18%) of 39 eyes received a PPV for a clinically worsening status after tap and inject, but not as the initial treatment.

Overall, the most common isolates were coagulase-negative Staphylococcus (18 eyes, 46%), Streptococcus species (15 eyes, 38%), and Staphylococcus warneri (three eyes, 8%) (Table 3). Other isolates included S. aureus (one eye, 3%), Bacillus (one eye, 3%), and Haemophilus influenza (one eye, 3%). There were no cases caused by multiple organisms. A larger proportion of referred cases were caused by Streptococcus species than institutional cases (11 of 27 eyes [41%] versus four of 12 eyes [33%]), and nine of these cases stemmed from an outbreak of contaminated bevacizumab compounded at a facility in the community.

Distribution of Isolates in Patients With Endophthalmitis After Intravitreal Injection of Anti-VEGF Agents

Table 3:

Distribution of Isolates in Patients With Endophthalmitis After Intravitreal Injection of Anti-VEGF Agents

All 38 gram-positive isolates were sensitive to vancomycin (Vancocin; Pfizer, New York City, NY). Thirteen of 23 (57%) isolates tested were sensitive to ceftazidime. Eleven of 20 (55%) isolates tested were sensitive to cefazolin, cephalothin, and cefuroxime. Sensitivity to fluoroquinolones included 21 of 32 (66%) to levofloxacin, eight of 21 (38%) to ciprofloxacin, seven of 19 (37%) to moxifloxacin, and zero of five (0%) to gatifloxacin among tested isolates. All 38 eyes were sensitive to at least one of the initially chosen antibiotics.

VA outcomes at last examination are summarized in Table 4 and are divided by institutional and referred cases. VA outcomes were most favorable with Staphylococcus species with 18 (82%) of 22 eyes achieving 5/200 or better in comparison to two (13%) of 15 eyes with Streptococcus species (P < .001). Five (13%) of 39 eyes had VA better than or equal to 20/40 at last follow-up, and 21 (54%) eyes had VA of 5/200 or better. Eleven of 39 (28%) eyes were no light perception at last follow-up, all of which had Streptococcus species, and eight of which were referred. Of these eight eyes, seven were linked to the outbreak of contaminated bevacizumab in the community. Eyes presenting in 3 days or less achieved 5/200 or better in nine (38%) of 24 eyes in comparison to 12 (80%) of 15 eyes presenting in 4 days or later (P = .01). Eyes treated with bevacizumab achieved 5/200 in 10 (43%) of 23 eyes in comparison to 11 (69%) of 16 eyes treated with ranibizumab, aflibercept, or pegaptanib (P = .12). Of the eyes where preinjection VA had been recorded, four of 16 (25%) attained preinjection VA by last follow-up. Eyes presenting with VA of count fingers or better at presentation achieved 5/200 or better in 11 (79%) of 14 eyes in comparison to 10 (45%) of 25 eyes in patients presenting with hand motion vision or worse (P = .02). Of those eyes treated concurrently with steroids and antibiotics, 14 of 28 (50%) achieved 5/200 or better in comparison to seven of 11 eyes (64%) treated with antibiotics alone (P = .44).

VA Outcomes by Causative Organism in Patients With Endophthalmitis After Intravitreal Injection With Anti-VEGF Agents

Table 4:

VA Outcomes by Causative Organism in Patients With Endophthalmitis After Intravitreal Injection With Anti-VEGF Agents

Discussion

This study demonstrates that patients with post-intravitreal injection endophthalmitis had variable visual outcomes, with the least favorable results occurring in eyes infected with Streptococcus. Patients presenting within 3 days also had less favorable visual outcomes compared with those presenting after 3 days. This observation may be a reflection of higher virulence organisms having an earlier onset of clinical symptoms. The average time of onset of 3 days reported in this series is consistent with prior studies.1,4

A meta-analysis showed that the most common isolates in endophthalmitis associated with intravitreal injection of anti-VEGF agents are Staphylococcus and Streptococcus species.5 The current study found a similar distribution of cases caused by Staphylococcus and Streptococcus species, with comparatively less favorable visual outcomes in eyes infected with Streptococcus. Streptococcal isolates are at least three-times more common after intravitreal injection than intraocular surgery, and this difference is believed to be secondary to increased oropharyngeal contamination.6–8 Of note, the large proportion of Streptococcus cases in this series is influenced by the patients who presented to the emergency room for treatment following an outbreak of Streptococcus endophthalmitis caused by contaminated compounded bevacizumab in the community.3

The rate of clinically suspected endophthalmitis occurring after intravitreal injection at a tertiary care referral center over the past decade was 0.013% or approximately one in 7,000 and did not differ between anti-VEGF agents. Data recently presented from the Intelligent Research in Sight Registry disclosed a post-injection rate of endophthalmitis with aflibercept, bevacizumab, and ranibizumab of 0.0059% (one of 17,000), 0.0071% (one of 14,000), and 0.0052% (one of 19,000), respectively.9 These rates were not statistically different between drugs and are similar to the rates at our institution during the past 2 years (one of 21,000 in 2016 and one of 22,000 in 2017). During the past 2 years, at our institution, there has also been a steady increase in the utilization of aflibercept and bevaizumab, albeit to a lesser degree, with decreased utilization of ranibizumab.

Similarly, in a 2015 report of nosocomial acquired endophthalmitis after anti-VEGF intravitreal injections, there was no difference in the rate of endophthalmitis following intravitreal bevacizumab and non-compounded ranibizumab and aflibercept.2 A meta-analysis of 445,503 intravitreal injections reported an infectious endophthalmitis rate of 0.58% with bevacizumab versus 0.029% with ranibizumab, though the difference was secondary to a larger number of culture-negative cases in the bevacizumab group and culture-positive cases were not statistically different.10 Another large population-based retrospective cohort study using medical claims data for more than 500,000 injections found no difference in the rate of endophthalmitis after injection with compounded bevacizumab or ranibizumab while controlling for other clinical characteristics.11

The current study corroborates previous reports that establish a consistently low rate of infection after intravitreal injection. The favorable safety profile of intravitreal injection also does not appear to differ between anti-VEGF agents including compounded bevacizumab. Furthermore, prophylactic antibiotics do not appear necessary to maintain a low incidence of infection. Indeed, current evidence suggests that the rate of endophthalmitis with antibiotic prophylaxis may even be higher.12 Endophthalmitis is a serious complication with a poor visual prognosis, and treatment with vancomycin and ceftazidime is currently recommended to maximize visual acuity outcomes.

References

  1. Moshfeghi AA, Rosenfeld PJ, Flynn HW Jr., et al. Endophthalmitis after intravitreal vascular [corrected] endothelial growth factor antagonists: A six-year experience at a university referral center. Retina. 2011;31(4):662–668. doi:10.1097/IAE.0b013e31821067c4 [CrossRef]
  2. Gregori NZ, Flynn HW Jr., Schwartz SG, et al. Current infectious endophthalmitis rates after intravitreal injections of anti-vascular endothelial growth factor agents and outcomes of treatment. Ophthalmic Surg Lasers Imaging Retina. 2015;46(6):643–648. doi:10.3928/23258160-20150610-08 [CrossRef]
  3. Goldberg RA, Flynn HW Jr., Isom RF, Miller D, Gonzalez S. An outbreak of streptococcus endophthalmitis after intravitreal injection of bevacizumab. Am J Ophthalmol. 2012;153(2):204–208.e1. doi:10.1016/j.ajo.2011.11.035 [CrossRef]
  4. Shah CP, Garg SJ, Vander JF, Brown GC, Kaiser RS, Haller JA. Outcomes and risk factors associated with endophthalmitis after intravitreal injection of anti-vascular endothelial growth factor agents. Ophthalmology. 2011;118(10):2028–2034. doi:10.1016/j.ophtha.2011.02.034 [CrossRef]
  5. Fileta JB, Scott IU, Flynn HW Jr, . Meta-analysis of infectious endophthalmitis after intravitreal injection of anti-vascular endothelial growth factor agents. Ophthalmic Surg Lasers Imaging Retina. 2014;45(2):143–149. doi:10.3928/23258160-20140306-08 [CrossRef]
  6. McCannel CA. Meta-analysis of endophthalmitis after intravitreal injection of anti-vascular endothelial growth factor agents: Causative organisms and possible prevention strategies. Retina. 2011;31(4):654–661. doi:10.1097/IAE.0b013e31820a67e4 [CrossRef]
  7. Chen E, Lin MY, Cox J, Brown DM. Endophthalmitis after intravitreal injection: The importance of viridans streptococci. Retina. 2011;31(8):1525–1533. doi:10.1097/IAE.0b013e318221594a [CrossRef]
  8. Simunovic MP, Rush RB, Hunyor AP, Chang AA. Endophthalmitis following intravitreal injection versus endophthalmitis following cataract surgery: Clinical features, causative organisms and post-treatment outcomes. Br J Ophthalmol. 2012;96(6):862–866. doi:10.1136/bjophthalmol-2011-301439 [CrossRef]
  9. Parke DW 2nd, . Introduction of the IRIS Registry. Paper presented at: the Retina Society Annual Meeting. ; October 5–8, 2017. ; Boston, MA. .
  10. Sigford DK, Reddy S, Mollineaux C, Schaal S. Global reported endophthalmitis risk following intravitreal injections of anti-VEGF: A literature review and analysis. Clin Ophthalmol. 2015;9:773–781.
  11. VanderBeek BL, Bonaffini SG, Ma L. Association of compounded bevacizumab with postinjection endophthalmitis. JAMA Ophthalmol. 2015;133(10):1159–1164. doi:10.1001/jamaophthalmol.2015.2556 [CrossRef]
  12. Reibaldi M, Pulvirenti A, Avitabile T, et al. Pooled estimates of incidence of endophthalmitis after intravitreal injection of anti-vascular endothelial growth factor agents with and without topical antibiotic prophylaxis. Retina. 2018;38(1):1–11. doi:10.1097/IAE.0000000000001583 [CrossRef]

Clinical Characteristics in Patients With Culture-Positive Endophthalmitis After Intravitreal Injection With Anti-VEGF Agents

n (%)

Institutional CasesReferred CasesTotal
12 (31%)27 (69%)39 (100%)

Preinjection Diagnosis
  Age-related macular degeneration10 (83%)23 (85%)33 (85%)
  Not specified choroidal neovascular membrane-1 (4%)1 (3%)
  Not specified-2 (7%)2 (5%)
  Diabetic macular edema-1 (4%)1 (3%)
  Branch retinal vein occlusion1 (8%)-1 (3%)
  Central retinal vein occlusion1 (8%)-1 (3%)

Intravitreal Agent
  Bevacizumab6 (50%)17 (63%)23 (59%)
  Ranibizumab4 (33%)4 (15%)8 (21%)
  Aflibercept2 (17%)4 (15%)6 (15%)
  Pegaptanib-1 (4%)1 (3%)
  Unspecified anti-VEGF agent-1 (4%)1 (3%)

Presenting VA ≥ 5/2002 (17%)2 (7%)4 (10%)

Mean Time to Presentation (days)333

Presence of Hypopyon4 (33%)22 (81%)26 (67%)

Presence of Fibrin7 (58%)13 (48%)19 (51%)

Clinically Suspected Endophthalmitis Rates for Each Anti-VEGF Medication Administered at Bascom Palmer Eye Institute From 2005–20171

YearBevacizumabRanibizumabAfliberceptPegaptanibTotal
20050/998000/1,3130/2,311 (0%)
20060/3,1391/,252300/6721/6,443 (0.016%)
20071/6,1982/4,31700/83/10,523 (0.029%)
20083/9,3451/3,399004/12,744 (0.031%)
20093/10,6801/3,630004/14,310 (0.028%)
20100/9,3400/4,738000/14,078 (0%)
20112/9,6410/5,4340/1920/122/15,279 (0.013%)
20120/6,8850/3,4442/4,36802/14,697 (0.014%)
20130/5,0361/2,8824/6,64805/14,566 (0.034%)
20140/5,7810/2,7670/7,89500/16,443 (0%)
20151/5,8460/2,1800/10,68201/18,708 (0.005%)
20160/7,2140/1,4771/12,69301/21,384 (0.005%)
20170/7,7800/1,1250/13,61601/22,521 (0.004%)
Total Culture-Positive6/87,883 (0.007%)4/37,916 (0.011%)2/56,094 (0.004%)0/2,005 (0%)12/183,898 (0.007%)
Total Culture-Negative4/87,883 (0.005%)2/37,916 (0.005%)6/56,094 (0.011%)0/2,005 (0%)12/183,898 (0.007%)
Total Culture-Positive and Culture-Negative10/87,883 (0.011%)6/37,916 (0.016%)8/56,094 (0.014%)0/2,005 (0%)24/183,898 (0.013%)

Distribution of Isolates in Patients With Endophthalmitis After Intravitreal Injection of Anti-VEGF Agents

n (%)
Institutional Cases12 (31%)Referred Cases27 (69%)Total39 (100%)
Coagulase-Negative Staphylococcus5 (42%)13 (48%)18 (46%)
Streptococcus Species4 (33%)11 (41%)15 (38%)
Staphylococcus warneri2 (17%)1 (4%)3 (8%)
Staphylococcus aureus-1 (4%)1 (3%)
Bacillus1 (8%)-1 (3%)
Haemophilus influenzae-1 (4%)1 (3%)
Gram-Positive Species12 (100%)26 (96%)38 (97%)
Gram-Negative Species-1 (4%)1 (3%)
Related to Outbreak3-9 (33%)9 (23%)

VA Outcomes by Causative Organism in Patients With Endophthalmitis After Intravitreal Injection With Anti-VEGF Agents

Isolates (n)≥ 20/40≥ 20/100≥ 5/200LPNLP
Institutional Cases (12)1 (8%)4 (33%)7 (58%)1 (8%)3 (25%)
  Coagulase-negative Staphylococcus (5)1 (20%)3 (60%)4 (80%)--
   Streptococcus species (3)---1 (25%)3 (75%)
   Staphylococcus warneri (2)--2 (100%)--
  Other gram-positive species (1)-1 (100%)1 (100%)--
  Gram-negative species-----
Referred Cases (27)4 (15%)10 (37%)14 (52%)1 (4%)8 (30%)
  Coagulase-negative   Staphylococcus (13)3 (23%)7 (54%)10 (77%)--
   Streptococcus species(11)1 (9%)2 (18%)2 (18%)-8 (73%)
   Staphylococcus warneri (1)--1 (100%)--
  Other gram-positive species (1)-1 (100%)1 (100%)--
  Gram-negative species (1)---1 (100%)-
Total Cases (38)5 (13%)14 (36%)21 (54%)2 (5%)11 (28%)
  Coagulase-negative Staphylococcus (18)4 (24%)10 (59%)14 (82%)--
   Streptococcus speciesa (14)1 (7%)2 (13%)2 (13%)1 (7%)11 (73%)
   Staphylococcus warneri (3)--3 (100%)--
  Other gram-positive speciesb (2)-2 (100%)2 (100%)--
  Gram-negative speciesc (1)---1 (100%)-
Authors

From the Department of Ophthalmology, Bascom Palmer Eye Institute, University of Miami Miller School of Medicine, Miami.

This study is supported in part by NIH Center Core Grant P30EY014801 and Research to Prevent Blindness Unrestricted Grant. The funding organizations had no role in the design or conduct of this research.

Dr. Schwartz has received personal fees from Alimera, Bausch + Lomb, and Welch Allyn outside the submitted work and is partially supported by NIH Center Core Grant P30EY014801 and an Unrestricted Grant from Research to Prevent Blindness. Drs. Flynn and Relhan are supported in part by NIH Center Core Grant P30EY014801 and Research to Prevent Blindness Unrestricted Grant. The remaining authors report no relevant financial disclosures.

Address correspondence to Harry W. Flynn Jr., MD, Department of Ophthalmology, Bascom Palmer Eye Institute, University of Miami, Miller School of Medicine, 900 NW 17th Street, Miami, FL 33136; email: hflynn@med.miami.edu.

Received: June 17, 2017
Accepted: November 01, 2017

10.3928/23258160-20180501-04

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