TABLE 1. Conditions Included in the Revised 1993 AIDS Surveillance Case Definitions from the Centers for Disease Control³

  Candidiasis of the bronchi, trachea, or lungs
  Candidiasis of the esophagus
  Coiccidioidomycosis, disseminated or extrapulmonary
  Cryptococcosis, extrapulmonary
  Crytptosporidiosis, chronic intestinal (>1 month)
  Cytomegalovirus disease (other than liver, spleen, or lymph nodes)
  Cytomegalovirus retinitis
  Encephalopathy, HIV-related
  Herpes simplex virus, chronic ulcer(s) (>1 month), or bronchitis, pneumonitis, or esophagitis
  Histoplasmosis, disseminated or extrapulmonary
  Isosporiasis, chronic intestinal (>1 month)
  Kaposi's sarcoma
  Lymphoma, Burkitt's (or equivalent term)
  Lymphoma, immunoblastic (or equivalent term)
  Lymphoma, primary central nervous system
  Mycobacterium avium complex or M. kansasii, disseminated or extrapulmonary
  Mycobacterium tuberculosis, any site
  Pneumocystis carinii pneumonia
  Pneumonia, recurrent
  Progressive multifocal leukoencephalopathy
  Salmonella sp. septicemia, recurrent
  Toxoplasmosis of the central nervous system
  Wasting syndrome caused by HIV infection

TABLE 2. Prevalence of Ocular Disorders in Patients Infected with HIV

TABLE 3. Adnexal Manifestations of HIV Infection

  Herpes zoster ophthalmicus
  Kaposi's sarcoma
  Molluscum contagiosum
  Squamous cell carcinoma/conjunctival intraepithelial neoplasia
  Cutaneous lymphoma
  Trichomegaly/Hypertrichosis
  Conjunctival microvasculopathy
  Conjunctivitis
  Preseptal cellulitis

HERPES ZOSTER OPHTHALMICUS

Herpes zoster ophthalmicus refers to a varicella-zoster virus (VZV)-related vesiculobullous dermatitis involving the ophthalmic distribution of the trigeminal nerve.¹¹⁵ Although VZV dermatitis may be observed in otherwise normal elderly patients, its occurrence in someone younger than 50 years of age is uncommon, and should raise the suspicion of systemic immunosuppression due to malignancy, pharmacologic immunosuppression, or HIV infection.^115–117 VZV dermatitis related to HIV infection typically occurs at CD4+ T-lymphocyte counts of less than 200 cells/μL, and is considered disseminated if it involves multiple dermatomes or unrelated organ systems. Herpes zoster ophthalmicus (Fig. 3) affects approximately 5% to 15% of HIV-infected patients (see Table 2), and in these patients keratitis, scleritis, uveitis, retinitis, or central nervous system involvement may develop.^116,117 Treatment involves a 1-week course of intravenous acyclovir (10 mg/kg, three times daily), followed by oral maintenance therapy (800 mg, three to five times daily). Famciclovir (500 mg, three times daily) was approved in 1994 by the US Food and Drug Administration for the treatment of herpes zoster infections offering the advantage of decreased daily dosings. However, the relative efficacy of oral acyclovir versus famciclovir for long-term maintenance therapy in HIV-infected patients is still under study. For patients initially unresponsive to acyclovir, or for those who show reactivation on oral acyclovir or famciclovir, a trial of intravenous foscarnet should be considered.

KAPOSI'S SARCOMA

Kaposi's sarcoma is a highly vascularized mesenchymal tumor of the skin and mucous membranes. It occurs in up to 25% of HIV-infected patients, and it is often the presenting sign of disease.¹¹⁸ Kaposi's sarcoma involving the ocular adnexa will develop in approximately 5% of patients infected with HIV.^119–121 Both the eyelids and the conjunctiva (Fig. 4) may be involved. Lesions may occur on either the upper or lower eyelid and often mimic a chalazion. Conjunctival lesions are most commonly found in the inferior fornix, but may occur on any aspect of the palpebral or bulbar conjunctiva. Conjunctival Kaposi's sarcoma is often mistaken for benign subconjunctival hemorrhage.

Radiation therapy is effective in treating eyelid and conjunctival Kaposi's sarcoma, but it is expensive and can be associated with loss of lashes, skin irritation, and a mild conjunctivitis.^122,123 Alternatively, isolated lesions of the eyelid may be treated by cryotherapy or intralesional chemotherapy. Excision can be performed, but is often difficult and complicated by bleeding. Conjunctival lesions also respond to cryotherapy or intralesional chemotherapy, but unlike eyelid lesions, they can be excised with relative ease. Fluorescein angiography is occasionally helpful for identifying a tumor-free margin of 1 to 2 mm at the time of surgery. Eyelid or conjunctival lesions accompanied by systemic involvement are often best treated with systemic chemotherapy. Interferon α has also been used with success. Recurrences are common.¹²⁴ Recent work has implicated a novel member of the herpes virus family, human herpes virus-8 (HHV-8), in the pathogenesis of Kaposi's sarcoma.¹²⁵

MOLLUSCUM CONTAGIOSUM

Molluscum contagiosum is a highly contagious papulonodular dermatitis caused by a poxvirus. Both the skin and mucous membranes may be affected, typically with multiple, small, umbilicated lesions. Molluscum contagiosum is more common in HIV-infected patients and, when present, tends to be more severe, producing larger, more numerous, and more rapidly growing lesions.¹¹⁸ Molluscum contagiosum occurs on the eyelids (Fig. 5) in less than 5% of patients infected with HIV (see Table 2).^126–129 Although described in the literature, cases of conjunctival molluscum contagiosum are rare. An association with follicular conjunctivitis and superficial keratitis has been described in immunocompetent patients, but appears to be uncommon in HIV-infected persons. Treatment options include cryotherapy, curettage, incision, excision, and topical chemotherapy.

SQUAMOUS CELL CARCINOMA/CONJUNCTIVAL INTRAEPITHELIAL NEOPLASIA

Patients infected with HIV appear to be at increased risk for conjunctival and eyelid squamous cell carcinoma, possibly associated with human papillomavirus (HPV) infection.^130–138 When at the limbus, gonioscopy should be performed to rule out intraocular extension. Treatment consists of wide excision with frozen section monitoring of the margins. A single case of basal cell carcinoma has been reported in a patient with AIDS.⁶⁵

CUTANEOUS LYMPHOMA

Non-Hodgkin's lymphoma is more common and tends to be of higher grade malignancy in patients infected with HIV.¹³⁹ There has been one report of a patient with primary eyelid non-Hodgkin's lymphoma.¹⁴⁰ Treatment included local radiation therapy.

TRICHOMEGALY

Acquired trichomegaly, or hypertrichosis of the eyelashes (Fig. 6), typically occurs in the late stages of HIV infection.^141–147 The cause is unknown, although elevated viral titers, drug toxicity, and poor nutrition have been implicated as contributing factors. Excessively long lashes may be trimmed, as needed, if they interfere with the use of eyeglasses or if the patient finds them cosmetically unacceptable.

CONJUNCTIVAL MICROVASCULOPATHY

Most HIV-infected patients will eventually develop conjunctival microvascular changes, including segmental vascular dilatation and narrowing, microaneurysm formation, the appearance of comma-shaped vascular fragments, and a visible granularity to the flowing blood-column, termed “sludging.”^148,149 These changes are usually most evident near the limbus inferiorly (Fig. 7), and are highly correlated with the occurrence of retinal microvasculopathy. The reason for the occurrence of conjunctival microvascular changes in the setting of HIV infection is unknown. Theories have included an HIV-induced increase in plasma viscosity, HIV-related immune complex deposition, and direct infection of the conjunctival vascular endothelium by HIV. No treatment is indicated.^46,91

CONJUNCTIVITIS

In one of the first clinic-based cohort studies, Holland and associates⁷ reported a nonspecific, culture-negative conjunctivitis in 10% of patients with AIDS. More recent clinic-based studies have, however, reported a prevalence of less than 1%, similar to that of the general population (see Table 2). Uncommon infectious forms of conjunctivitis have been reported in HIV-infected patients, including CMV^150,151 and Cryptococcus.¹⁵² Treatment should be guided by the results of Gram stains and cultures.

PRESEPTAL CELLULITIS

Preseptal cellulitis caused by Staphylococcus aureus has been reported in two HIV-infected patients.^18,65 Staphylococcus aureus is the most common cause of cutaneous and systemic bacterial infections in HIV-infected patients, and these patients infected with Staphylococcus aureus have a nasal carriage that is nearly twice that of normal controls.¹¹⁸ Treatment is the same as that used for preseptal cellulitis in immunocompetent patients.

TABLE 4. Anterior Segment Manifestations of HIV Infection

  Keratoconjunctivitis sicca
  Infectious keratitis

  Viral keratitis—herpes zoster virus, herpes simplex virus, cytomegalovirus
  Bacterial and fungal keratitis
  Microsporidial keratitis

KERATOCONJUNCTIVITIS SICCA

Keratoconjunctivitis sicca, or dry eye, occurs in 10% to 20% of HIV-infected patients, typically at late stages of their illness.^153–157 Abnormal Schirmer's testing and interpalpebral rose bengal staining (Fig. 8) are invariably present. The cause is complex, but is most probably related to combined effects of HIV-mediated inflammation and destruction of the lacrimal and salivary glands ( Sjögren's syndrome) and direct HIV infection of the conjunctiva. Concurrent exposure due to lagophthalmos and decreased blink rate in the setting of encephalopathy can worsen the keratopathy. Treatment consists of artificial tears and long-acting lubricating ointments, which are applied at bedtime.

INFECTIOUS KERATITIS

Infectious keratitis occurs at about the same rate in HIV-infected and HIV-uninfected persons, with most cohorts reporting keratitis in less than 1% of patients (see Table 2). However, when HIV-positive patients do acquire infectious keratitis, the organisms are more likely to be opportunistic, and the course more severe or protracted.^35,46,91

VIRAL KERATITIS

Herpes zoster ophthalmicus is often associated with either a dendritic epithelial (Fig. 9) or disciform stromal keratitis in HIV-infected patients. VZV keratitis can, however, also occur with transient or no skin lesions, a condition termed herpes zoster sine herpete and reported to occur rarely in HIV-positive persons.^158,159 Decreased corneal sensation and elevated intraocular pressure are clues to the diagnosis. Treatment is similar to that for herpes zoster ophthalmicus, as discussed earlier.

Herpes simplex keratitis, in contrast, seems not to be more common in HIV-positive patients.^160–163 HIV-associated herpes simplex keratitis may, however, recur more frequently and in some cases be more resistant to treatment than similarly severe cases occurring in immunocompetent patients. At least one case series has suggested that herpes simplex epithelial keratitis may occur more commonly near the limbus, and with more and larger dendrites in HIV-infected patients.¹⁶⁰ Treatment includes oral acyclovir (400 mg, five times daily) or topical antivirals.

Wilhelmus and associates¹⁶⁴ recently reported an HIV-positive patient with CMV dendritic epithelial keratitis. This patient's disease was resistant to débridement, as well as to standard oral and topical antiviral therapy. The patient died shortly after diagnosis with active keratouveitis.

BACTERIAL AND FUNGAL KERATITIS

Bacterial keratitis and fungal keratitis do not appear to be more common in HIV-positive persons, but when they do occur, they tend to be more severe and have a higher tendency toward perforation.^35,46,91 Various reported organisms have included α-hemolytic streptococci, Staphylococcus aureus, Staphylococcus epidermidis, Pseudomonas aeruginosa, Klebsiella oxytoca, Capnocytophaga sp., and Candida sp.^91,165–171 Treatment should be aggressive, with intensive use of fortified antibiotics.

MICROSPORIDIOSIS

Microsporidia are obligate intracellular parasites known to cause gastroenteritis, sinusitis, pneumonitis, and urogenital infections in HIV-infected patients.¹⁷² In these patients, ocular infection with microsporidia is uncommon, but when present typically produces a punctate epithelial keratopathy (Fig. 10) with a mild papillary conjunctivitis.^173–188 Microsporidia are extremely difficult to culture, but can be readily seen within Geimsa-stained corneal or conjunctival epithelial cells. Treatment options include oral itraconazole, topical propamidine, topical fumagillin, and oral albendazole.

IRIDOCYCLITIS

Mild iridocyclitis is common in HIV-infected patients, and most typically observed in the setting of viral retinitis, including CMV retinitis,^189,190 VZV retinitis,^191–194 and herpes simplex retinitis.^195,196 In contrast, more severe anterior chamber inflammation is relatively uncommon in HIV-positive patients. Here too, however, the iridocyclitis is usually secondary to severe posterior inflammation, including toxoplasmosis retinochoroiditis,^197–201 syphilitic chorioretinitis,^202–217 and bacterial or fungal retinitis or endophthalmitis.^218–225 Infectious causes of isolated iridocyclitis have also been described in HIV-positive patients, including toxoplasmosis,²²⁶ Cryptococcus,²²⁷ syphilis,^214,215 and CMV.²²⁸ Iridocyclitis may be part of Reiter's syndrome, which may be more common and appears to be more severe in HIV-infected patients.^229,230 Lastly, drugs used to treat opportunistic infections in HIV-positive patients, such as rifabutin,^231–233 used for Mycobacterium avium complex, and cidofovir^234,235 given to treat viral retinitis, can cause severe iridocyclitis. Treatment should be directed toward a specific infectious cause; when toxicity is suspected, the offending drug should be discontinued or the dosage decreased.

ANGLE-CLOSURE GLAUCOMA

Acute angle-closure glaucoma has been described in association with uveal effusion syndrome in HIV-infected patients.^236–239 Typically, miotics worsen this condition and peripheral iridotomies have little effect. Anterior choroidal effusions should be either visible or present on ultrasonography. The cause of HIV-associated angle-closure glaucoma is unknown, although uveal effusions can occur in nanophthalmos and ocular axial length should be checked in all patients. Treatment includes cycloplegia, topical corticosteroids, and, when necessary, surgical drainage of suprachoroidal fluid.²⁴⁰

TABLE 5. Posterior segment manifestations of HIV Infection

  Retinal microvasculopathy
  Infectious retinitis

  Cytomegalovirus retinitis
  Varicella-zoster virus retinitis
  Herpes simplex virus retinitis
  Toxoplasmosis retinochoroiditis
  Bacterial and fungal retinitis

RETINAL MICROVASCULOPATHY

Retinal microvasculopathy occurs in more than 50% of HIV-infected patients (see Table 2). The most commonly observed manifestation is cotton-wool spots (Fig. 11), although intraretinal hemorrhages, microaneurysms,^241,242 and, uncommonly, retinal ischemia^12,243 also occur. With the exception of retinal ischemia, these findings are transient. All forms of retinal microvasculopathy increase in frequency in more advanced stages of HIV infection.^241,242 Hypotheses regarding the pathogenesis of retinal microvasculopathy parallel those suggested for conjunctival vascular changes,¹⁴⁹ and include HIVinduced increase in plasma viscosity, HIV-related immune complex deposition, and direct infection of the conjunctival vascular endothelium by HIV. HIV-associated retinal microvasculopathy is typically asymptomatic, but may play a role in the progressive optic nerve atrophy,^244,245 electroretinographic abnormalities,²⁴⁶ and loss of color vision, contrast sensitivity, and visual field observed in HIV-infected patients.^247,248 The role of retinal microvasculopathy in the development of CMV retinitis is controversial, with some investigators finding no relationship²⁴² and others suggesting that retinal vascular damage may provide increased access to circulating CMV-infected lymphocytes.²⁴⁹

INFECTIOUS RETINITIS

Cytomegalovirus Retinitis

CMV retinitis affects 30% to 40% of HIV-infected patients (see Table 2).^33,189,190 Any aspect of the fundus may be involved, including the optic nerve head. Affected patients typically report gradual visual field loss or the onset of floaters. Clinical examination shows geographic retinal thickening and opacification. Associated intraretinal hemorrhages are often present (Fig. 12A). Anterior chamber and vitreous inflammation, although invariably observed, are usually minimal. CMV retinitis typically occurs at CD4⁺ T-lymphocyte counts of less than 50 cells/mm³, and almost always at counts less than 100 cells/mm³. Treatment of CMV retinitis is a complicated, rapidly evolving field.^33,189,190 Current FDA-approved treatments for active retinitis include intravenous ganciclovir, foscarnet, and cidofovir. Any of the same medicines or the recently approved oral formulation of ganciclovir can be used for maintenance therapy. Local therapy with intravitreal injection of ganciclovir, foscarnet, or cidofovir, or via implantation of a slow-release ganciclovir-containing reservoir, is also possible. Choice of an appropriate antiviral and route of delivery needs to be individualized, based on consideration of the location and extent of ocular and systemic disease, understanding of potential drug-related side-effects, and knowledge of viral response to past treatments.^250–253

Varicella-Zoster Virus Retinitis

VZV is the second most common cause of necrotizing retinitis in HIV-infected individuals, affecting approximately 5% of large cohorts with AIDS (see Table 2).^191–194 Like CMV, VZV produces retinal whitening (Fig. 12B), occasionally accompanied by intraretinal hemorrhages. However, VZV retinitis is usually distinguished by its rapid progression, multifocal nature, and initial involvement of deep retinal layers. A concurrent or recent herpes zoster dermatitis provides added circumstantial support for the diagnosis. The risk of retinal detachment is greater than observed with CMV retinitis. Treatment involves the use of intravenous and intravitreal antivirals, typically combination therapy with acyclovir and foscarnet.

Herpes Simplex Virus Retinitis

Herpes simplex virus is a rare cause of retinitis in HIV-infected patients.^195,196 Like VZV retinitis, onset of symptoms and disease progression is rapid. Clinical appearance may mimic VZV retinitis (Fig. 12C). Treatment should include prompt use of intravenous and intravitreal antivirals, again most typically acyclovir and foscarnet.

Toxoplasmosis Retinochoroiditis

Ocular toxoplasmosis affects less than 1% of HIV-infected patients in most countries (see Table 2).^{197–201,254–256} Toxoplasmosis retinochoroiditis in HIV-positive patients is usually distinguished by the occurrence of a moderate to severe anterior chamber and vitreous inflammation, a relative lack of retinal hemorrhage, and the presence of a smooth rather than granular leading edge (Fig. 12D). Moreover, unlike toxoplasmosis retinochoroiditis in immunocompetent patients, HIV-infected patients often have multifocal and bilateral disease, with no evidence of inactive toxoplasmosis scars. Testing should include serology for IgG and IgM toxoplasmosis antibodies, but may be negative in profoundly immunosuppressed patients. Between 30% and 50% of HIV-positive patients with toxoplasmosis retinochoroiditis will have central nervous system involvement.^199,200 Treatment consists of pyrimethamine in combination with a sulfonamide or clindamycin, either alone or in combination. Chronic or repeated therapy is often necessary. Atovaquone has been used successfully in the treatment of toxoplasmosis retinochoroiditis in an HIV-positive patient,²⁵⁷ but it is expensive and has yet to be shown to be superior to more standard combination therapy.

Bacterial and Fungal Retinitis

Ocular syphilis is the most common intraocular bacterial infection in HIV-positive patients, affecting up to 2% of patients (see Table 2). Patients may present with either an iridocyclitis^214,215 or a more diffuse intraocular inflammation, with or without retinal or optic nerve involvement.^202–217 Laboratory testing should include both a rapid plasma reagin (RPR) or Venereal Diseases Research Laboratory (VDRL) test and a specific treponemal antibody (fluorescent treponemal antibody absorption [FTA-ABS] or micro-hemagglutination treponemal pallidum [MHA-TP]) test. Rarely, these test may be negative in HIV-positive patients despite active intraocular disease.²¹⁷ Treatment includes intravenous penicillin G, 24 million units/day for 7 to 10 days. Recurrences can occur even after adequate treatment.

Other bacterial and fungal causes of retinitis or endophthalmitis are rare in HIV-infected patients,^{218–225,253,257} but have included Staphylococcus aureus,^223,225 Histoplasma capsulatum,²¹⁸ Sporothrix schenckii,²¹⁹ Bipolaris hawaiienisis,²²² and Fusarium.²²⁴ Neuroretinitis associated with systemic Bartonella henselae infection has also been described in these patients.^258,259

INFECTIOUS CHOROIDITIS

Infectious choroiditis is uncommon in HIV-infected patients, accounting for less than 1% of all eye findings in most clinic-based series (see Table 2).^27,260–264 Organisms have included Pneumocystis carinii (Fig. 13), Cryptococcus neoformans, M. avium complex, Mycobacterium tuberculosis, H. capsulatum, Candida, and Aspergillus fumigatus. Most of these cases have appeared in autopsy series, reflecting the serious nature of the underlying systemic infections. Up to one third of cases have concurrent CMV retinitis.^27,264

INTRAOCULAR LYMPHOMA

HIV-infected patients are at increased risk for developing non-Hodgkin's lymphoma.¹³⁹ Although uncommon, cases of intraocular lymphoma have been reported in HIV-infected patients, and are composed primarily of B cells.^265–267 Treatment includes radiation and chemotherapy.

RETINAL VEIN OR ARTERY OCCLUSION

Large retinal vessel occlusion occurs in less than 1% of patients with AIDS and appears to be more common in severely immunosuppressed persons.^30,33 Retinal veins are affected more often than retinal arteries.³³ The cause is unknown but might be related to the same rheologic and vascular factors that contribute to small retinal vessel disease.¹⁴⁹

TABLE 6. Orbital and Neuro-ophthalmic Manifestations of HIV Infection

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