American Academy of Ophthalmology

Recommendations on Screening for

Endogenous Candida Endophthalmitis
Mark P. Breazzano, MD,1 John B. Bond III, MD,2 Srilaxmi Bearelly, MD, MHS,3 Donna H. Kim, MD,4
Sean P. Donahue, MD, PhD,2 Flora Lum, MD,5 Timothy W. Olsen, MD,6 for the American Academy of
Ophthalmology

The American Academy of Ophthalmology evaluated the practice of routine screening for intraocular infection
from Candida septicemia. In the United States, ophthalmologists are consulted in the hospital to screen for
intraocular infection routinely for patients with Candida bloodstream infections. This practice was established in
the era before the use of systemic antifungal medication and the establishment of definitions of ocular disease
with candidemia. A recent systematic review found a rate of less than 1% of routinely screened patients with
endophthalmitis from Candida septicemia. Other studies found higher rates of endophthalmitis but had limitations
in terms of inaccuracies in ocular disease classification, lack of vitreous biopsies, selection biases, and lack of
longer-term visual outcomes. Some studies attributed ocular findings to Candida infections, rather than other
comorbidities. Studies also have not demonstrated differences in medical management that are modified for eye
disease treatment; therefore, therapy should be dictated by the underlying Candida infection, rather than be
tailored on the basis of ocular findings. In summary, the Academy does not recommend a routine ophthalmologic
consultation after laboratory findings of systemic Candida septicemia, which appears to be a low-value practice.
An ophthalmologic consultation is a reasonable practice for a patient with signs or symptoms suggestive of
ocular infection regardless of Candida septicemia. Ophthalmology 2021;-:1e4 ª 2021 by the American Academy
of Ophthalmology

Instituting evidence-based guidelines for patient care helps advises an eye screening examination, “preferably performed
to reduce care practices that are less cost-effective or lack by an ophthalmologist” for all (even asymptomatic) patients
benefit.1,2 Low-value care not only is inefficient but also with candidemia.7 The recommendation is made without
may be unsafe. Low-value care leads to an estimated $67 participation by a body of similar stature representing
billion in unnecessary cost to the healthcare system annually ophthalmologists and is based on the presumption that such
in the United States.1,2 Harm appears to be more challenging screening will prevent vision loss.7 It is extracted from
to quantify, although hospital-acquired complications are studies that are decades old, performed before
reported as high as 15% after procedures considered to be implementing appropriate definitions of ocular disease with
low value.3 For example, when unrecognized, overdiagnosis candidemia and before the era of systemic antifungal
(identifying indolent lesions otherwise not posing risk) leads medication.7e9 The “low-quality evidence” status has been
to overtreatment and harm, a concept that has been used in recognized by the IDSA, whereas the guideline inflates the
reforming various cancer screening paradigms.4 likelihood of sight-threatening disease and the benefits of
We propose exploring the low-value care practice of ophthalmologic evaluation.7e10 Because disagreement exists
routine screening for intraocular infection from Candida between specialists concerning the necessity and utility of
bloodstream infections (candidemia), one of the most these examinations,8e14 the purpose of this position statement
common hospital consultations for American ophthalmolo- is to initiate steps to correct widespread misunderstanding and
gists.5 We advocate to minimize candidemia-related establish new recommendations.
screening examinations and share evidence in the literature Knowledge gaps in overuse and misuse, both within
that is based on numerous studies of endogenous Candida ophthalmology9,15,16 and infectious diseases7,11,17,18
endophthalmitis. Two professional organizations interna- literature, may explain the inconsistency in understanding
tionally, the Royal College of Ophthalmologists and the between screening and vision loss.1 Overuse (increased
Intensive Care Society, have recently implemented guide- intervention with inefficacies and potentially harm) and
lines in collaboration that support these efforts.6 misuse (an effective intervention in an inappropriate context)
The root cause of this practice pattern can be traced to the apply,1 and include using advanced vitreoretinal surgical
Infectious Diseases Society of America (IDSA) Clinical techniques with known risks19 or alterations in systemic
Practice Guideline for the Management of Candidiasis, which antifungal therapy that may be contrary to principles of

ª 2021 by the American Academy of Ophthalmology https://doi.org/10.1016/j.ophtha.2021.07.015 1

Published by Elsevier Inc. ISSN 0161-6420/21

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 Ophthalmology Volume -, Number -, Month 2021

antimicrobial stewardship (i.e., adding, switching, or cohort of patients in a critical care unit regardless of
extending agents with different side effect profiles for a candidemia status, representing a control group, and
theoretical rather than substantiated purpose).20,21 Studies of identified abnormal retinal findings in 19%.31 The IDSA
examined patients have demonstrated the risks without guidelines cite a comparable rate (16%) of associated ocular
demonstrating proven benefit. These risks result from findings in patients with candidemia.7 Given the lack of
intervening upon incidental findings due to the underlying control groups among remaining candidemia studies, there
conditions and comorbidities, yet not specifically from is concern of potential harm from interventions that arises
intraocular infection due to candidemia.9,11,12,22,23 from screening because retinal findings in contemporary
Endophthalmitis from Candida septicemia occurs in less studies are often attributed to candidemia rather than
than 1% of routinely screened patients based on a systematic associated comorbidities.12,22,23 Perhaps, the question is not
review of approximately 7500 examined patients, including if unnecessary intervention and misuse1 are occurring, but
more than 1000 identified prospectively.9 Older definitions how much. Overuse of interventions1 is challenging to
of endophthalmitis differ from current literature. For quantify,3,4 particularly with cases of mild endophthalmitis
example, a study from 1982 in Ophthalmology reports an (e.g., peripheral vitreoretinal lesions) or chorioretinitis that
endophthalmitis incidence of 37%.15 However, at least 1 may resolve without any intervention.25,32 Screening has
photographic example was inconsistent with an not been proven beneficial and may lead to harm, especially
endophthalmitis diagnosis.15 A multicenter, prospective given poor outcomes that have been associated with
investigation in 1994 from the same journal helped clarify invasive intervention.9 Furthermore, mortality rates of
the discrepancy, by using rigorous definitions, with no patients with systemic candidemia approach 30%,33 and
cases of endophthalmitis identified among 3 different adherence to screening is missed beyond 30% without
centers from screening over 2.5 years.16 evidence of unfavorable outcomes.12,22,26
Patients with candidemia generally have comorbidities Optimizing systemic treatment of the underlying condi-
that can explain intraocular findings: anemia, hypertension, tions, the Candida bloodstream infection itself, and related
and thrombocytopenia, among many other conditions comorbidities appear to be most important in successful
simultaneously as critically ill patients.16 Such abnormal, management of incidentally associated ocular disease and the
nonspecific retinal features include Roth spots or other overall survival of the patient.9,19,33 Early suspicion and
hemorrhages, and cotton wool spots, and do not require detection of systemic candidemia are essential, in addition to
ophthalmologic intervention.16 Cotton wool spots can be appropriate systemic antifungal therapy for a minimum of 2
challenging to distinguish clinically from a deeper weeks after negative blood culture growth and clearance of
chorioretinitis, even when using advanced imaging other infectious sources with immediate exchange of
modalities such as OCT.24,25 Histopathologic analysis in indwelling catheters, as advocated by the IDSA.7,18 At least
many of these cases is necessary for distinction but 2 patients from 2 studies developed endophthalmitis after
impractical outside of autopsy. These screening findings failure to exchange indwelling catheters for more than 1
leave ophthalmologists with a diagnostic and therapeutic week,17 or having received systemic antifungal therapy for
dilemma, given the lack of specificity for these lesions just 2 days,18 after detection of systemic candidemia.
without established criteria for intervention in this context. Interestingly, 1 patient had resolution of endophthalmitis
Numerous recent studies perpetuate deficiencies, after removal of an indwelling catheter without any systemic
including selection bias, lack of vitreous biopsies, absent antifungal therapy or invasive ophthalmologic intervention.34
criteria for intervention or change in management based on Experimental evidence suggests that voriconazole has su-
screening, inaccurate or misleading ocular disease classifi- perior vitreous penetration from the bloodstream,35 lending
cation, and exclusion of critical outcomes data.26e30 For potential credence to continuing screening examinations to
example, in 2019, Ueda et al26 reported a retrospective, tailor medical management, even if invasive intervention is
multicenter study from 15 medical centers in Japan with an not performed.17,36 However, these data have not been
incidence of 13% when ophthalmologists examined non- replicated in clinical literature.17,37 One large, prospective
neutropenic patients and 43% of these with endophthalmitis study by Oude Lashof et al17 was unable to demonstrate an
or macular involvement. Although the authors concluded that advantage of systemic voriconazole to amphotericin B
routine screening is warranted, the quality of data is limited followed by fluconazole. Post hoc analysis of another
with a high risk of bias. The weaknesses found in this report prospective, multicenter study of candidemia (CANDIPOP)
include the following: (1) Only 71.7% of the cohort was examined the systemic efficacy of echinocandins (speculated
screened; (2) 0% of the screened cohort had vitreous to have relatively poor vitreous penetration)36 and did not
confirmed biopsy; (3) the positive cases were considered show a difference in associated ocular findings when
“probably or possible ocular candidiasis”; (4) no vitrectomies compared with other drugs.8,37 It is unknown if other organ
were performed; (5) only 2 patients received intravitreal systems are affected by a change in systemic antifungal
therapy; (6) and all positive cultures were exclusively ob- therapy based on ocular findings (including extensions in
tained from the blood.26 Thus, the data from this study are treatment duration). In our experience, many infectious
insufficient to support the authors’ conclusions. diseases physicians feel compelled to adjust systemic
A major shortcoming throughout the literature is the fail- management on the basis of the evidence of retinal findings.
ure of recognizing the prevalence of ocular findings in criti- This practice does not appear substantiated given the lack of
cally ill patients without candidemia. A notable exception is specificity of the lesions and a multitude of potential
the study by Rodríguez-Adrián et al,31 who examined a complications from altering systemic agents.18,21 Thus,

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 Breazzano et al 
Screening for Endogenous Candida Endophthalmitis

systemic management should be tailored to the underlying consultation is reasonable for anyone with a clinical
candidemia, rather than associated ocular findings. rationale including signs or symptoms concerning for an
The pathophysiology of endogenous Candida endoph- ocular infection. However, because current evidence does
thalmitis can largely explain many of these clinical findings not support a routine ophthalmologic consultation after
and outcomes as they relate to bloodstream infections. laboratory findings of systemic Candida septicemia, this
Experimentation, autopsy, and conventional imaging have all low-value practice should be de-adopted. Any future rec-
demonstrated that the origin of typical lesions is localized to the ommendations should be developed through collaborative
inner choroid.25,38,39 The choroid is the most vascular tissue of efforts between specialists represented by ophthalmology
the body,40,41 and therapeutic systemic antifungal drug levels and infectious diseases. Such efforts and any future studies
should be easily achieved without regard to vitreous must eliminate discrepancies regarding the incidence of
penetration. A direct relationship between increased sight-threatening disease and potential benefit of ophthal-
microcirculatory blood flow and greater antibiotic mologic screening for candidemia within the literature
concentration has been supported in a study of human after carefully applying rigorous definitions, reviewing
volunteers.42 Vitreous penetration from systemic therapy associated clinical data, including control groups, and
may be enhanced by the breakdown of the outer blood- including long-term visual outcomes data. These recom-
retinal barrier known to occur with intraocular inflammation.43 mendations are based on, but not limited to, safety, effi-
In conclusion, the American Academy of Ophthal- cacy, epidemiology, and pathophysiology of endogenous
mology recommendations are as follows. Ophthalmologic Candida endophthalmitis.

Footnotes and Disclosures

Originally received: July 8, 2021. HUMAN SUBJECTS: No human subjects were included in this study.
Final revision: July 13, 2021. Institutional Review Board approval was not required. All research adhered
Accepted: July 14, 2021. to the tenets of the Declaration of Helsinki. Individual patient-level consent
Available online: ---. Manuscript no. D-21-01379. was not required.
1
Wilmer Eye Institute, Johns Hopkins Hospital, Johns Hopkins University, No animal subjects were used in this study.
Baltimore, Maryland. Author Contributions:
2
Vanderbilt Eye Institute, Vanderbilt University Medical Center, Nashville, Conception and design: Breazzano, Bond, Bearelly, Lum, Olsen
Tennessee.
Data collection: Breazzano, Bond, Bearelly
3
Edward S. Harkness Eye Institute, New York-Presbyterian Hospital,
Analysis and interpretation: Breazzano, Bond, Bearelly, Kim, Donahue,
Columbia University Medical Center, New York City, New York. Lum, Olsen
4
Casey Eye Institute, Oregon Health and Sciences University, Portland, Obtained funding: N/A; Study was performed as part of the authors’ regular
Oregon. employment duties. No additional funding was provided.
5
American Academy of Ophthalmology, San Francisco, California. Overall responsibility: Breazzano, Bond, Bearelly, Kim, Donahue, Lum,
6
Department of Ophthalmology, Mayo Clinic, Rochester, Minneapolis. Olsen
Disclosure(s):
Abbreviations and Acronyms:
All authors have completed and submitted the ICMJE disclosures form. IDSA ¼ Infectious Diseases Society of America.
The author(s) have made the following disclosure(s): S.B.: New York
Keywords:
Community Trust e Frederick J. and Theresa Dow Wallace Fund, all
outside the submitted work Candida, Policy, Screening.
F.L.: Other e Employee of the American Academy of Ophthalmology. Correspondence:
T.W.O.: Grants e Novartis to May Clinic, NIH/NEI STTR funding; Other e Flora Lum, MD, Quality and Data Science, American Academy of
Founder of IMacular Regeneration, LLC; Secretary Quality of Care, American Ophthalmology, 655 Beach Street, San Francisco, CA 94109-7424. E-mail:
flum@aao.org.
Academy of Ophthalmology, all outside the submitted work.
Approved by the Board of Trustees, June 2021.

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American Academy of Ophthalmology Recommendations on Screening 000
for Endogenous Candida Endophthalmitis
Mark P. Breazzano, MD, John B. Bond, III, MD, Srilaxmi Bearelly, MD, MHS, Donna H. Kim,
MD, Sean P. Donahue, MD, PhD, Flora Lum, MD, Timothy W. Olsen, MD, for the American
Academy of Ophthalmology
The American Academy of Ophthalmology does not recommend a routine ophthalmologic
consultation after laboratory findings of systemic Candida septicemia, although a consultation
is reasonable for a patient with signs or symptoms suggestive of ocular infection.

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