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    9 Uveitis and Ocular Inflammation

    Chapter 12: Endophthalmitis

    Endogenous Endophthalmitis

    Endogenous Fungal Endophthalmitis

    Endogenous fungal endophthalmitis develops slowly as focal or multifocal areas of chorioretinitis. Granulomatous or nongranulomatous inflammation is observed with keratic precipitates, hypopyon, and vitritis with cellular aggregates. The infection usually begins in the choroid, appearing as yellow-white lesions with indistinct borders that range in size from small cotton-wool spots to several disc diameters. It can subsequently break through into the vitreous, producing localized cellular and fungal aggregates overlying the original site(s). Iris nodules and rubeosis may also be observed in cases of severe fungal endophthalmitis.

    Endogenous fungal endophthalmitis due to Candida (the most common cause; Fig 12-2), and Coccidioides species can be mistaken for noninfectious uveitis and treated with corticosteroids alone. This treatment usually worsens the clinical course of the disease, necessitating further investigation to establish the correct diagnosis. There is often a history of indwelling line or intravenous drug abuse. The condition often requires aggressive systemic and local antifungal therapy as well as surgical intervention.

    Endogenous fungal endophthalmitis caused by Histoplasma capsulatum, Cryptococcus neoformans, Sporothrix schenckii, and Blastomyces dermatitidis is less common than that caused by Candida and Aspergillus species.

    Figure 12-2. Endogenous endophthalmitis. A, “String of pearls” seen in the vitreous of a 36-year-old male with endogenous Candida endophthalmitis. B, Fundus photograph of endogenous endophthalmitis.

    (Part A courtesy of H. Nida Sen, MD, and Henry Wiley, MD/National Eye Institute; part B courtesy of Debra A. Goldstein, MD.)

    • Sridhar J, Flynn HW Jr, Kuriyan AE, Miller D, Albini T. Endogenous fungal endophthalmitis: risk factors, clinical features, and treatment outcomes in mold and yeast infections. J Ophthalmic Inflamm Infect. 2013;3(1):60.

    Candida endophthalmitis

    Candida species are an important cause of nosocomial infections and are the most common fungal organisms, causing endogenous endophthalmitis in both pediatric and adult populations. Although Candida albicans remains the most common pathogen, non-albicans species (eg, Candida glabrata) have also been identified in patients developing ocular disease. In patients with candidemia, the reported prevalence rates of intraocular candidiasis vary widely, ranging between 9% and 78%. However, when strict criteria are applied for the classification of chorioretinitis and endophthalmitis, these numbers drop precipitously. In 1 series, when patients were examined within 72 hours of a positive blood culture result, only 9% had chorioretinitis and none had endophthalmitis. Endogenous Candida endophthalmitis occurs in up to 37% of patients with candidemia if they are not receiving antifungal therapy. Ocular involvement drops to 3% in patients who are receiving treatment.

    Predisposing conditions associated with candidemia and the development of intraocular infection include

    • hospitalization with a history of recent major gastrointestinal surgery

    • bacterial sepsis

    • systemic antibiotic use

    • use of indwelling catheters

    • hyperalimentation

    • debilitating diseases (eg, diabetes mellitus)

    • immunomodulatory therapy

    • prolonged neutropenia

    • organ transplantation

    • a combination of these conditions

    Hospitalized neonates and intravenous drug users are also at risk. Immunodeficiency per se does not appear to be a prominent predisposing factor, attested to by the paucity of reported cases of Candida chorioretinitis or endophthalmitis among patients with HIV infection or AIDS.

    • Shah CP, McKey J, Spirn MJ, Maguire J. Ocular candidiasis: a review. Br J Ophthalmol. 2008;92(4):466–468.

    Manifestations Patients may present with blurred or decreased vision resulting from macular chorioretinal involvement or pain arising from anterior uveitis, which may be severe. Typically, Candida chorioretinitis is characterized by multiple, bilateral, white, well-circumscribed lesions less than 1 mm in diameter. These lesions are distributed throughout the postequatorial fundus and associated with overlying vitreous cellular inflammation (Fig 12-3). The chorioretinal lesions may be associated with vascular sheathing and intraretinal hemorrhages. The vitreous exudates may assume a string-of-pearls appearance.

    Histologically, Candida species are recognized as budding yeast with a characteristic pseudohyphate appearance (Fig 12-4). The organisms reach the eye hematogenously through metastasis to the choroid. Fungi may then break through the Bruch membrane, form subretinal abscesses, and secondarily involve the retina and vitreous.

    • Rao NA, Hidayat AA. Endogenous mycotic endophthalmitis: variations in clinical and histopathologic changes in candidiasis compared with aspergillosis. Am J Ophthalmol. 2001;132(2):244–251.

    Diagnosis The diagnosis of ocular candidiasis is suggested by the presence of chorioretinitis or endophthalmitis in the appropriate clinical context and confirmed by positive results on either blood or vitreous cultures. It has been suggested that all patients with candidemia undergo baseline dilated funduscopic examinations and receive monitoring for the development of metastatic ocular candidiasis for at least 2 weeks after an initial eye examination. The reasoning is that earlier treatment of Candida endophthalmitis has been associated with better visual outcomes, and patients with ocular lesions are more likely to have infection involving a greater number of organ systems than are patients without eye lesions. The presence of vitreous snowballs and endophthalmitis requires diagnostic and therapeutic vitrectomy. Fungal stains and cultures, and PCR for Candida species, should be obtained on undiluted vitreous fluid samples.

    The differential diagnosis of Candida endophthalmitis includes toxoplasmic retinochoroiditis, which exhibits posterior pole lesions that can appear yellow-white with fluffy borders and range in size from small cotton-wool spots to several disc diameters wide. Candida vitreous snowball lesions may also resemble pars planitis.

    • Hidalgo JA, Alangaden GJ, Eliott D, et al. Fungal endophthalmitis diagnosis by detection of Candida albicans DNA in intraocular fluid by use of a species-specific polymerase chain reaction assay. J Infect Dis. 2000;181(3):1198–1201.

    • Krishna R, Amuh D, Lowder CY, Gordon SM, Adal KA, Hall G. Should all patients with candidemia have an ophthalmic examination to rule out ocular candidiasis? Eye (Lond). 2000;14(Pt 1):30–34.

    Figure 12-3 Fundus photograph of Candida retinitis.

    Figure 12-4 Pathology of Candida retinitis. Fungi (black) are revealed in a Gomori methenamine silver stain of the retina taken from a patient diagnosed with fungal endophthalmitis.

    Treatment The treatment of intraocular candidiasis includes systemic and intravitreal administration of antifungal drugs. Consultation with a specialist in infectious diseases is essential. Chorioretinal lesions not yet involving the vitreous body may be treated effectively with the oral triazole antifungal drugs fluconazole or voriconazole (200 mg, twice daily, for 2–4 weeks), with vigilant monitoring for evidence of progression. Voriconazole has good oral bioavailability, achieving therapeutic intravitreal levels with a broad spectrum of antifungal activity. When the vitreous body is involved, intravitreal injection of antifungal drugs (amphotericin B, 5–10 μg/0.1 mL, or voriconazole, 100 μg/0.1 mL) should be considered, usually in conjunction with pars plana vitrectomy. Long-acting corticosteroid injections should be avoided. Vitrectomy may be useful diagnostically by allowing for the analysis of intraocular fluid by microbiologic and molecular techniques, and therapeutically by debulking the pathogen load.

    More severe infections may require intravenous amphotericin B with or without flucytosine. Significant dose-limiting toxicities (renal, cardiac, and neurologic) associated with conventional amphotericin B therapy were greatly reduced by the development of liposomal lipid complex formulations. Finally, intravenously administered caspofungin, an antifungal drug in the echinocandin class (drugs that inhibit synthesis of glucan in the cell wall) with activity against Candida and Aspergillus species, has been successfully employed in a small number of patients with Candida endophthalmitis; some treatment failures have also been reported with this drug, however. Another echinocandin, intravenous micafungin, is also available in the United States and Europe for treatment of candidiasis. Oral voriconazole, flucytosine, fluconazole, or rifampin may be administered in addition to intravenous amphotericin B or caspofungin.

    • Breit SM, Hariprasad SM, Mieler WF, Shah GK, Mills MD, Grand MG. Management of endogenous fungal endophthalmitis with voriconazole and caspofungin. Am J Ophthalmol. 2005;139(1):135–140.

    • Paulus YM, Cheng S, Karth PA, Leng T. Prospective trial of endogenous fungal endophthalmitis and chorioretinitis rates, clinical course, and outcomes in patients with fungemia. Retina. 2016;36(7):1357–1363.

    Cryptococcosis

    Cryptococcus neoformans is a yeast found in high concentrations worldwide in contaminated soil and pigeon feces. Infection is acquired through inhalation of the aerosolized fungus. It has a predilection for the central nervous system and may produce severe disseminated disease among immunocompromised or debilitated patients. Although overall it remains an uncommon disease, cryptococcosis is the most common cause of fungal meningitis, as well as the most frequent fungal eye infection in patients with HIV infection or AIDS. The fungus probably reaches the eye hematogenously; however, the frequent association of ocular cryptococcosis with meningitis suggests that ocular infection may result from direct extension from the optic nerve. Ocular infections may occur months after the onset of meningitis or, in rare instances, before the onset of clinically apparent central nervous system disease.

    Manifestations Ocular findings associated with cryptococcal meningitis include mainly papilledema followed by optic atrophy and cranial nerve palsies. Other manifestations include diplopia, nystagmus, ptosis, and ophthalmoplegia. The most frequent presentation of ocular cryptococcosis that is not directly related to meningoencephalitis is multifocal chorioretinitis. Associated findings include variable degrees of vitritis, vascular sheathing, exudative retinal detachment, papilledema, and granulomatous anterior chamber inflammation. It has been hypothesized that the infection begins as a focus in the choroid, with subsequent extension and secondary involvement of overlying tissues. Severe intraocular infection progressing to endophthalmitis may be observed in the absence of meningitis or clinically apparent systemic disease.

    Diagnosis and treatment The clinical diagnosis requires a high degree of suspicion and is supported by demonstration of the organism with India ink stains or by culture of the fungus from cerebrospinal fluid. Intravenous amphotericin B and oral flucytosine are required to halt disease progression. With optic nerve or macular involvement, the prognosis is poor for recovery of vision.

    • Kestelyn P, Taelman H, Bogaerts J, et al. Ophthalmic manifestations of infections with Cryptococcus neoformans in patients with the acquired immunodeficiency syndrome. Am J Ophthalmol. 1993;116(6):721–727.

    • Sheu SJ, Chen YC, Kuo NW, Wang JH, Chen CJ. Endogenous cryptococcal endophthalmitis. Ophthalmology. 1998;105(2):377–381.

    • Wykoff CC, Albini TA, Couvillion SS, Dubovy SR, Davis JL. Intraocular cryptococcoma. Arch Ophthalmol. 2009;127(5):700–702.

    Aspergillus endophthalmitis

    Endogenous Aspergillus endophthalmitis is a rare disorder associated with disseminated aspergillosis among patients with severe chronic pulmonary diseases, cancer, endocarditis, severe immunocompromise, or intravenous drug abuse. In rare instances, Aspergillus endophthalmitis may occur in immunocompetent patients with no apparent predisposing factors. Disseminated infection most commonly involves the lung, with the eye as the second most common site of infection. Aspergillus fumigatus and A flavus are the species most frequently isolated from patients with intraocular infection.

    Aspergillus species are found in soils and decaying vegetation. The spores of these ubiquitous saprophytic molds become airborne and seed the lungs and paranasal sinuses of humans. Human exposure is very common, but infection is rare and depends on the virulence of the fungal pathogen and immunocompetence of the host. Ocular disease occurs via hematogenous dissemination of Aspergillus organisms to the choroid.

    Manifestations Endogenous Aspergillus endophthalmitis results in rapid onset of pain and loss of vision. A confluent yellowish infiltrate is often present in the macula, beginning in the choroid and subretinal space. A hypopyon can develop in the subretinal or subhyaloidal space (Fig 12-5A). Retinal hemorrhages, retinal vascular occlusions, and full-thickness retinal necrosis may occur. The infection can spread to produce a dense vitritis and variable degrees of cells, flare, and hypopyon in the anterior chamber. The macular lesions form a central atrophic scar when healed. In contrast to the lesions associated with Candida chorioretinitis and endophthalmitis, lesions produced by Aspergillus species are larger and more likely to be hemorrhagic, and they commonly invade the retinal and choroidal vessels, which may result in broad areas of ischemic infarction.

    Figure 12-5 Coccidioidal iris granuloma in the pupil. A, Fundus photograph. B, This granuloma was biopsied and a peripheral iridectomy was performed because it was causing pupillary block and angle-closure glaucoma.

    (Courtesy of Ramana S. Moorthy, MD.)

    Diagnosis The diagnosis of endogenous Aspergillus endophthalmitis is based on clinical findings combined with positive results from pars plana vitreous biopsy and cultures as well as results from Gram and fungal stains. Coexisting systemic aspergillosis can be a strong clue, especially among high-risk patients. The diagnosis requires a high degree of suspicion within the correct clinical context and is confirmed by the demonstration of septate, dichotomously branching hyphae on analysis of vitreous fluid specimens. Aspergillus organisms may be difficult to culture from the blood.

    The differential diagnosis of endogenous Aspergillus endophthalmitis includes Candida endophthalmitis, cytomegalovirus retinitis, Toxoplasma retinochoroiditis, coccidioidomycotic choroiditis or endophthalmitis, and bacterial endophthalmitis.

    In Candida endophthalmitis, the vitreous is the prominent focus of infection, but in Aspergillus endophthalmitis, the principal foci are retinal and choroidal vessels and the subretinal or subretinal pigment epithelial space.

    Treatment Endogenous Aspergillus endophthalmitis usually requires aggressive treatment with diagnostic and therapeutic pars plana vitrectomy combined with intravitreal injection of amphotericin B or voriconazole; intravitreal corticosteroids may be used in conjunction with these drugs. Because most patients with this condition have disseminated aspergillosis, systemic treatment with oral voriconazole, intravenous amphotericin B, or caspofungin is often required. Other systemic antifungal drugs, such as itraconazole, miconazole, fluconazole, and ketoconazole, may also be used. Systemic aspergillosis is best managed by an infectious diseases specialist.

    Despite aggressive treatment, the visual prognosis is poor because of frequent macular involvement. Final visual acuity is usually less than 20/200.

    • Hariprasad SM, Mieler WF, Holz ER, et al. Determination of vitreous, aqueous, and plasma concentration of orally administered voriconazole in humans. Arch Ophthalmol. 2004;122(1):42–47.

    Coccidioidomycosis

    Coccidioidomycosis is a disease produced by the dimorphic soil fungus Coccidioides immitis, which is endemic to the San Joaquin Valley of central California, certain parts of the southwestern United States, and parts of Central and South America. Infection follows inhalation of dust-borne arthrospores, most commonly resulting in pulmonary infection and secondary dissemination to the central nervous system, skin, skeleton, and eyes. Approximately 40% of infected patients are symptomatic; the vast majority present with a mild upper respiratory tract infection or pneumonitis approximately 3 weeks after exposure to the organism. Erythema nodosum or multiforme may appear from 3 days to 3 weeks after the onset of symptoms. Disseminated infection is rare, occurring in less than 1% of patients with pulmonary coccidioidomycosis.

    Manifestations Ocular coccidioidomycosis is likewise uncommon, even with disseminated disease. Disseminated disease usually causes blepharitis, keratoconjunctivitis, phlyctenular and granulomatous conjunctivitis, episcleritis and scleritis, and extraocular nerve palsies and orbital infection. Uveal involvement is still rarer: fewer than 20 pathologically verified cases have been reported. The anterior and posterior segments are equally involved. Intraocular manifestations include unilateral or bilateral granulomatous anterior uveitis, iris granulomas (Fig 12-5), and a multifocal chorioretinitis characterized by multiple, discrete, yellow-white lesions usually less than 1 disc diameter in size located in the postequatorial fundus. These choroidal granulomas may resolve, leaving punched-out chorioretinal scars. Vitreous cellular infiltration, vascular sheathing, retinal hemorrhage, serous retinal detachment, and involvement of the optic nerve have also been reported.

    Diagnosis Positive results of serologic testing for anticoccidioidal antibodies in the serum, cerebrospinal fluid, vitreous, and aqueous, as well as of skin testing for exposure to coccidioidin establish the diagnosis in the correct clinical context.

    Treatment The Infectious Diseases Society of America recommends initiating treatment with an oral azole antifungal drug such as fluconazole or itraconazole. Surgical debulking of anterior chamber granulomas, pars plana vitrectomy, and intraocular injections of amphotericin and voriconazole may be required. With systemic disease, much higher doses and a longer duration of intravenous amphotericin therapy or oral voriconazole therapy may be needed. An infectious diseases specialist is essential in the management of coccidioidomycosis.

    Despite aggressive treatment, ocular coccidioidomycosis carries a poor visual prognosis, and most eyes require enucleation because of pain and blindness.

    • Glasgow BJ, Brown HH, Foos RY. Miliary retinitis in coccidioidomycosis. Am J Ophthalmol. 1987;104(1):24–27.

    • Moorthy RS, Rao NA, Sidikaro Y, Foos RY. Coccidioidomycosis iridocyclitis. Ophthalmology. 1994;101(12):1923–1928.

    • Vasconcelos-Santos DV, Lim JI, Rao NA. Chronic coccidioidomycosis endophthalmitis without concomitant systemic involvement: a clinicopathological case report. Ophthalmology. 2010;117(9):1839–1842.

    Excerpted from BCSC 2020-2021 series: Section 9 - Uveitis and Ocular Inflammation. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.

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