Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Culture-Proven Endophthalmitis After Intravitreal Injection: A 10-Year Analysis

Joseph M. Simonett, MD; Austin Igelman, BS; Stanford C. Taylor, MD; J. Peter Campbell, MD, MPH; Thomas S. Hwang, MD; Phoebe Lin, MD, PhD; Andreas K. Lauer, MD; Christina J. Flaxel, MD

Abstract

BACKGROUND AND OBJECTIVE:

To report on the microbiology, management, and visual outcomes of intravitreal injection (IVI)-associated, culture-proven endophthalmitis.

PATIENTS AND METHODS:

All patients seen at a tertiary referral center with culture-proven endophthalmitis associated with an IVI between June 2007 and July 2017 were included in this retrospective analysis.

RESULTS:

Thirty-five patients with culture-positive endophthalmitis following IVI were identified. All gram-positive organisms (34 of 35) were susceptible to vancomycin. Cases due to pathogens associated with oral or respiratory flora were common (31.4%, n = 11), presented earlier (2.0 days vs. 4.6 days, P < .001), were more likely to undergo pars plana vitrectomy (81.8% vs. 25.0%, P = .002) and had worse visual acuity outcomes.

CONCLUSION:

IVI-associated endophthalmitis pathogens and anti-microbial susceptibilities in the Pacific Northwest are similar to those reported from other geographic locations. Bacteria associated with the oral and respiratory flora are common isolates that result in a more aggressive course and worse visual outcomes.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:33–38.]

Abstract

BACKGROUND AND OBJECTIVE:

To report on the microbiology, management, and visual outcomes of intravitreal injection (IVI)-associated, culture-proven endophthalmitis.

PATIENTS AND METHODS:

All patients seen at a tertiary referral center with culture-proven endophthalmitis associated with an IVI between June 2007 and July 2017 were included in this retrospective analysis.

RESULTS:

Thirty-five patients with culture-positive endophthalmitis following IVI were identified. All gram-positive organisms (34 of 35) were susceptible to vancomycin. Cases due to pathogens associated with oral or respiratory flora were common (31.4%, n = 11), presented earlier (2.0 days vs. 4.6 days, P < .001), were more likely to undergo pars plana vitrectomy (81.8% vs. 25.0%, P = .002) and had worse visual acuity outcomes.

CONCLUSION:

IVI-associated endophthalmitis pathogens and anti-microbial susceptibilities in the Pacific Northwest are similar to those reported from other geographic locations. Bacteria associated with the oral and respiratory flora are common isolates that result in a more aggressive course and worse visual outcomes.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:33–38.]

Introduction

The widespread adoption of pharmacotherapy delivered by intravitreal injection (IVI) has transformed the management of many ocular diseases. Every injection, however, carries a small risk of endophthalmitis. Published rates of endophthalmitis following IVI range from 0.016% to 0.056%.1–9 Although the overall risk of a single injection is low, many patients with chronic retinal diseases require long term, if not indefinite, treatment and are exposed to a progressively higher cumulative risk over their lifetime.

According to Medicare records, fewer than 5,000 intravitreal injections of a pharmacologic compound were performed annually prior to 2001.10 Since then, there has been rapid growth in the use of intravitreal injections, with more than 2.5 million performed in the US in 2014.11 Compared to postoperative endophthalmitis following cataract surgery, which has been studied for decades, information regarding the clinical course, microbial etiology, and treatment outcomes in endophthalmitis following IVI has been emerging in only the last decade. Analysis of microbial data from culture-proven post-IVI endophthalmitis is even more limited, with the total number of culture positive cases ranging from 26 to 68 in the largest meta-analyses.4,5,12,13 Coagulase-negative Staphylococcus is the most common isolated pathogen in both processes, but Streptococcus species and other organisms associated with the oral and respiratory flora have been found more commonly in post-IVI endophthalmitis than postoperative cases.12,14,15 The clinical follow-up after intraocular surgery, for which patients are routinely seen on multiple postoperative visits, may allow for closer monitoring for infection and is different than the follow-up commonly applied after IVI. Furthermore, intraocular and topical antibiotics are routinely used during and after intraocular surgery; although similar prophylactic antibiotics following IVI have been shown to be ineffective in the prevention of endophthalmitis, their absence may contribute to differences in microbial etiology and treatment response between post-IVI and postoperative infections.16–18 The purpose of this study is to describe the microbial etiology and clinical outcomes of culture-positive endophthalmitis associated with IVI in the Pacific Northwest.

Patients and Methods

This retrospective study conducted at a single, tertiary referral center was approved by the institutional review board of Oregon Health & Science University and adhered to the tenets of the Declaration of Helsinki. The electronic medical records of all patients treated at the Casey Eye Institute of Oregon Health & Science University from June 1, 2007, to June 31, 2017, were queried for a relevant International Classification of Disease (ICD) Ninth Revision diagnosis code (360.00, purulent endophthalmitis, unspecified; 360.01, acute endophthalmitis; 360.03, chronic endophthalmitis; 360.19, other endophthalmitis) or ICD Tenth Revision diagnosis code (H44.001, unspecified purulent endophthalmitis, right eye; H44.002, unspecified purulent endophthalmitis, left eye; H44.003 unspecified purulent endophthalmitis, bilateral; H44.009, unspecified purulent endophthalmitis, unspecified eye; H44.19, other endophthalmitis) and the presence of a positive culture from an intraocular sample. The electronic medical record of cases meeting the ICD and culture inclusion criteria were reviewed to determine whether the patient had received an intravitreal injection in the infected eye within the 15 days preceding presentation. Cases involving the injection of a drug suspension, such as an anti-vascular endothelial growth factor (VEGF) agent, or drug releasing implant were included. Cases were included regardless of whether the preceding IVI was performed in house or by a referring physician.

Following identification of culture-positive, post-IVI endophthalmitis cases, type of pharmacotherapy injected, patient age, presenting visual acuity (VA), time between injection and presentation of endophthalmitis, pathogen species, antimicrobial susceptibilities, method of endophthalmitis treatment, and VAs from the exam closest to the one month and 3-month follow-up date were recorded.

Quantitative variables are reported as mean ± standard deviation and qualitative variables are reported as percentages. A Chi-squared test was used to assess the statistical significance of cohort differences. Due to the poor VA frequently associated with endophthalmitis and the problematic conversion of the associated non-numerical VAs to quantitative numerical values, such as logMAR acuities, VAs were binned based on median presenting VA into hand motion (HM) or worse and count fingers (CF) or better for statistical analysis.

Results

Presenting Clinical Features

Thirty-five cases of culture-positive, post-IVI endophthalmitis were identified. Twenty-one cases (60.0%) were referred from physicians outside of the academic tertiary referral center. Thirty-four cases (97.1%) were associated with injection of a VEGF antagonist (10 bevacizumab [Avastin; Genentech, South San Francisco, CA], five ranibizumab [Lucentis; Genentech, South San Francisco, CA], 11 aflibercept [Eylea; Regeneron, Tarrytown, NY], and eight recorded as an unspecified anti-VEGF agent from a referring provider), whereas one occurred after injection of a dexamethasone embedded intravitreal implant (Ozurdex; Allergan, Dublin, Ireland). Mean patient age was 73.8 years ± 14.2 years, and mean time from IVI to presentation was 3.8 days ± 2.4 days. Presenting VA was available in 33 of 35 cases and ranged from 20/60 to no light perception (NLP), with 63.6% (n = 21) of patients presenting with HM vision or worse and 21.2% (n = 7) of patients presenting with light perception (LP) vision or worse.

Microbial Etiology and Susceptibilities

Thirty-four of 35 isolates (97.1%) were gram-positive bacteria. Coagulase-negative Staphylococcus was the most common isolate (57.1%, n = 20) (Table 1). Bacteria associated with the oral or respiratory flora made up 31.4% (n = 11) of isolates and included nine cases (25.7%) of Streptococcus species and two cases (5.7%) of Enterococcus faecalis. Finally, there were three cases of Staphylococcus aureus (8.6%) and one case of Haemophilus influenza (2.9%). There were no fungal isolates.

Bacterial Isolates From Culture-Positive Endophthalmitis Following Intravitreal Injection

Table 1:

Bacterial Isolates From Culture-Positive Endophthalmitis Following Intravitreal Injection

All isolated gram-positive bacteria (n = 34) were susceptible to vancomycin (Vancocin; Pfizer, New York, NY). Of tested organisms, 100% (18 of 18) were susceptible to amikacin, 88.2% (15 of 17) were susceptible to ceftazidime, 93.8% (30 of 32) were susceptible to clindamycin, 92.9% (26 of 28) were susceptible to ofloxacin, and 56.3% (18 of 32) were susceptible to erythromycin.

Treatment and Outcomes

All patients were treated with immediate intravitreal antibiotics. In addition to antibiotic therapy, 11 cases (31.4%) underwent pars plana vitrectomy (PPV) within 48 hours of presentation; four of these cases were due to Streptococcus species: four Staphylococcus, two Enterococcus, and one Haemophilus. An additional four cases (11.4%) underwent PPV after 48 hours due to persistent infection or vitreous inflammation, three of which were due to infection with a Streptococcus species. One-month follow-up data (average 31.9 days from initial presentation) were available in 77.1% (n = 27) of cases and 3-month follow-up data (average 93.8 days from initial presentation) were available in 60.0% (n = 21) of cases. There were no enucleations within the first 3 months of follow-up.

At 1-month follow-up, 66.7% (18 of 27) of cases had a VA of CF or better and 44.4% (n = 12 of 27) had 20/200 or better. At 3-month follow-up, 66.7% (14 of 21) of cases had a VA of CF or better and 47.6% (10 of 21) had 20/200 or better. Patients with endophthalmitis due to organisms associated with oral or respiratory flora presented sooner after injection (2.0 days ± 0.6 days vs. 4.61 days ± 4.6 days; P < .001) (Table 2), were more likely to have a presenting VA of HM or worse (90.0% vs. 59.1%; P = .038), and were more likely to have undergone PPV (81.8% vs. 25.0%; P < .001) than cases caused by other bacteria. Cases due to organisms associated with oral or respiratory flora were more likely to have HM or worse VA at 1-month follow-up (66.7%, n = 6) compared to cases due to other organisms (16.7%, n = 3; P = .009). There was no significant difference in days from presentation to the approximate 1-month follow-up visit (30.6 days ± 4.6 days vs. 32.6 days ± 13.7 days; P = .582) between these two cohorts.

Comparison of Clinical Data Between Cases of Endophthalmitis Following IVI Due to Pathogens Associated With the Oral or Respiratory Flora (Streptococcus and Enterococcus Species) and Other Bacteria

Table 2:

Comparison of Clinical Data Between Cases of Endophthalmitis Following IVI Due to Pathogens Associated With the Oral or Respiratory Flora (Streptococcus and Enterococcus Species) and Other Bacteria

Discussion

Although the risk of endophthalmitis following a single IVI is low, the growing number of indications for intravitreal pharmacotherapy, cumulative risk acquired with long term treatment, and associated visual morbidity makes post-IVI endophthalmitis a major concern for patients and their treating physicians. In this 10-year retrospective analysis, we report 35 cases of culture proven endophthalmitis following IVI, of whom 21 were referred from outside providers. Similar to prior studies, we found a wide spectrum of disease severity at the time of presentation and variable clinical outcomes.

All but one case in our series were due to gram-positive organisms. Coagulase-negative Staphylococcus, which is commonly found on the ocular surface and routinely the most commonly implicated organism in endophthalmitis following IVI or intraocular surgery,12,14,15,19–23 was cultured in 57.1% (n = 20) of cases. All gram-positive isolates in this study were susceptible to vancomycin, consistent with prior studies that have reported very low rates of vancomycin-resistant, gram-positive bacteria in endophthalmitis following IVI or intraocular surgery.24

Several studies have demonstrated that organisms associated with the normal oral or respiratory flora are seen more frequently in post-IVI endophthalmitis than in endophthalmitis following intraocular surgery.12,14,15,25 In line with these prior results, nearly one-third of cases (11 of 35) in this study were due to bacteria associated with the oral or respiratory flora, with the majority being Streptococcal species. These patients presented sooner and with more severe vision loss, were more likely to have undergone PPV, and had worse visual outcomes compared to cases caused by other organisms. Chen et al. reported similar findings in which cases of endophthalmitis due to Streptococcal species, an important part of the normal oral flora, presented sooner and had worse VA outcomes.14 In another large study, 44.2% of eyes with Streptococcal endophthalmitis had no remaining vision at the last follow-up visit and early PPV, defined as surgery within 48 hours of presentation, did not influence visual outcomes.26 Two cases of endophthalmitis in our study due to E. faecalis, a virulent organism formerly classified as group D Streptococcus, for which the oral cavity is a significant reservoir.27 These cases had particularly aggressive clinical courses, with one case ending in LP and the other in NLP vision. It remains unclear why these organisms have increased virulence in endophthalmitis; proposed mechanisms include the production of various toxins, including pneumolysin, hemolysin, and bacterial capsule components that may trigger an early and uncontrolled release of inflammatory mediators or induce direct host cell lysis.28–32

Specific strategies for reducing infection have been investigated since the recognition that oral and respiratory flora are common causes of post-IVI endophthalmitis. Wearing facemasks and maintaining physician and patient silence during the procedure have been shown to decrease dispersion of bacteria.33,34 Although these precautions have been advanced as recommendations, their rate of implementation and effectiveness in preventing endophthalmitis is unknown. Additional strategies for reducing oral and respiratory flora infections are warranted and might include improved adherence to masking and silence while drawing up medications and ensuring that the needle remains capped whenever possible. These potential strategies are in addition to the standard of care: pre-injection application of povidone-iodine, which decreases conjunctival bacteria counts and is likely the single most effective antimicrobial for ophthalmic procedures.35 Prophylactic topical antibiotics at the time of injection have been found to increase rates of endophthalmitis and the risk of infection with drug-resistant bacteria.8,16–18

One case in our series was due to Haemophilus influenza, a gram-negative organism that has been associated with delayed onset post-surgical endophthalmitis, poor visual outcomes and a high rate of evisceration or enucleation.36,37 Interestingly, our case presented acutely 1 day after intravitreal injection and had an excellent VA outcome, with improvement from CF vision at the time of presentation to 20/40 at 3-month follow-up.

The present study was not designed to assess the role of early PPV in post-IVI endophthalmitis. Although some prior retrospective studies have found no association between early PPV and improved visual outcomes in post-IVI or Streptococcal endophthalmitis,4,6,26,38 these findings must be interpreted cautiously. Many of these studies were not powered to investigate the effect of PPV on the subgroup of patients presenting with LP or worse VA, a group identified by the Endophthalmitis Vitrectomy Study as having a substantial benefit from immediate surgical intervention.39 Additionally, the decision to proceed with surgery was made by the treating surgeon and may be affected by clinical features not captured in a retrospective analysis. As an example, there was no difference in VA at 6-month follow-up between patients with IVI-associated endophthalmitis who underwent PPV versus tap and injection of intravitreal antibiotics in a large retrospective analysis by Xu et al.; however, the PPV cohort had a higher proportion of culture positive vitreous samples (91% vs. 48%), suggesting a possible selection bias for more severe cases with a higher bacterial load going for initial PPV.9

A limitation of this study is the variability in available follow-up data due to the retrospective design. To manage this variability, only patients who had 1 month or greater follow-up data were included in the analysis of VA outcomes, but a potential lost-to-follow-up bias cannot be fully excluded. This variability also resulted in a non-standardized number of days from presentation to the approximate 1-month follow-up date; however, there was no significant difference in this length of time between compared subgroups. Future investigations utilizing nationwide databases, including the Intelligent Research in Sight (IRIS) registry that already contains data from more than 2.4 million intravitreal injections, promise to provide data on larger patient cohorts with longer follow-up.40

In summary, culture-positive endophthalmitis following IVI remains a difficult entity to manage and frequently has long-term visual consequences. In this study, the vast majority of cases were due to gram-positive organisms, all of which were susceptible to vancomycin. Commonly implicated bacteria and anti-microbial susceptibilities were consistent with studies from outside of the Pacific Northwest. Bacteria associated with the oral or respiratory flora, such as Streptococcus and Enterococcus species, are common pathogens in post-IVI endophthalmitis and are associated with higher virulence, a more aggressive clinical course and worse visual outcomes.

References

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Bacterial Isolates From Culture-Positive Endophthalmitis Following Intravitreal Injection

Bacterial IsolateN (% Total)
Coagulase-negative Staphylococcus20 (57.1)
   S. epidermidis8 (22.9)
   S. lugdunensis2 (5.7)
  Unspecified species10 (28.6)
Staphylococcus aureus3 (8.6)
Streptococcus species9 (25.7)
   S. mitis6 (17.1)
   S. pneumoniae1 (2.9)
   S. salivarius1 (2.9)
  Unspecified species1 (2.9)
Enterococcus faecalis2 (5.7)
Haemophilus influenza1 (2.9)

Comparison of Clinical Data Between Cases of Endophthalmitis Following IVI Due to Pathogens Associated With the Oral or Respiratory Flora (Streptococcus and Enterococcus Species) and Other Bacteria

Bacteria Associated With Oral or Respiratory FloraOther BacteriaP Value
Days From IVI to Presentation2.0 ± 0.64.61 ± 4.6< .001
Presenting VA of HM or Worse90.0% (9)59.1% (12).038
Underwent PPV81.8% (9)25.0% (6).002
VA of HM or Worse at 1 Month66.7% (6)16.7% (3).009
Authors

From Casey Eye Institute, Oregon Health & Science University, Portland, Oregon.

This project was supported by core grant P30 EY010572 (Casey Eye Institute) from the National Institutes of Health (Bethesda, MD) and an unrestricted grant to the Casey Eye Institute from Research to Prevent Blindness (New York, NY).

Dr. Campbell has received personal fees from Allergan outside the submitted work. The remaining authors report no relevant financial disclosures.

Address correspondence to Christina J. Flaxel, MD, Casey Eye Institute, Oregon Health & Science University, 3303 SW Bond Ave., Center for Health and Healing Building 1, 11th Floor, Portland, OR 97239; email: flaxelc@ohsu.edu.

Received: May 25, 2018
Accepted: November 02, 2018

10.3928/23258160-20181212-05

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