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Show Journal of Clinical Neuro- ophtluJlmology 10( 3): 167- 174, 1990. Neuro- ophthalmic Findings in Acquired Immunodeficiency Syndrome Ahmad M. Mansour, M. D. © 1990 Raven Press, Ltd., New York We reviewed the neuro- ophthalmic findings in 177 subjects with the acquired immunodeficiency syndrome ( AIDS) or AIDS- related complex who underwent an eye examination in one center from January 1984 to May 1989. The findings included ocular motor nerve palsies ( five cases), papilledema ( two cases), cytomegalovirus optic neuritis ( two cases), cortical blindness ( one case), conjugate gaze palsy ( one case), and altitudinal visual field defect ( one case). These findings were attributed to central nervous system toxoplasmosis ( four cases) or lymphoma ( one case), cryptococcal meningitis ( two cases), systemic cytomegalovirus infections ( two cases), and herpes simplex encephalitis ( one case). Of 177 patients, 61 patients were tested for syphilis. Twenty- six patients had positive rapid plasma reagin titers, and 28 had positive fluorescent treponemal antibody- absorbed tests. Human immunodeficiency virus- infected individuals need to be screened routinely for syphilis. Key Words: Acquired immunodeficiency syndromeCortical blindness- Cryptococcal meningitis- Cytomegalovirus optic neuritis- Gaze palsy- Herpes simplex encephalitis- Human immunodeficiency virusLymphoma- Ocular motor nerve palsy- Papilledema- Syphilis- Toxoplasmosis. From the Department of Ophthalmology, University of Texas Medical Branch, Galveston, Texas. Address correspondence and reprint requests to Ahmad Mansour, M. D., Ophthalmology- UTMB, Galveston, IX 77550, U. S. A. 167 The acquired immunodeficiency syndrome ( AIDS) is marked by the occurrence of various opportunistic infections and malignancies in previously healthy individuals. The most common ocular findings in subjects with AIDS include cottonwool spots and cytomegalovirus retinitis. The neuro- ophthalmic findings in one series of patients with AIDS are presented, MATERIALS AND METHODS We reviewed prospectively the ocular findings of patients with AIDS or AIDS- related complex examined by the author from September 1987 to May 1989, together with a retrospective review of subjects seen from January 1984 to August 1987 in the Department of Ophthalmology. The systemic findings of each patient were reviewed, focusing on opportunistic infections, malignancies, lymphocyte marker profile ( T4! f8 or T helperff suppressor ratio), and time interval from the neuro- ophthalmic findings to death. The majority of the patients had serum titers drawn against Toxoplasma gondii, herpes simplex, cytomegalovirus, and EpsteinBarr virus. Several patients were tested for syphilis using the fluorescent treponemal antibody absorbed test ( FTA- ABS), and the rapid plasma reagin ( RPR) test. RESULTS The results are presented in Tables 1 and 2. Of 177 patients, 127 had AIDS and 50 had AIDSrelated complex. None of the 50 patients with AIDS- related complex had neuro- ophthalmic complications. Ten of the 127 patients with AIDS had neuro- ophthalmic findings. These ten patients had a mean age of 34 years ( range 27-- 46), and consisted of nine men and 1 woman, with a racial distribution of six whites, two blacks, and two 168 AHMAD M. MANSOUR TABLE 1. Neuro- ophthalmic findings in 177 patients with AIDS or AIDS- related complex CNS, central nervous system. Cases reported are from the University of Texas Medical Branch, Galveston. Ocular motor nerve palsies Oculomotor nerve Trochlear nerve Abducens nerve Papilledema CNS toxoplasmosis Cryptococcal meningitis Cytomegalovirus optic neuritis Direct spread of cytomegalovirus retinitis Gaze palsy Paramedian pontine reticular formation lesion Cortical blindness Cryptococcal meningitis Visual field defect Inferior altitudinal field defect Multiple scotomas No. cases 1 ( CNS toxoplasmosis) 2 ( CNS toxoplasmosis and CNS lymphoma) 1 ( CNS toxoplasmosis) 2 1 ( CNS toxoplasmosis) 1 ( cryptococcal meningitis) 1 ( toxoplasmic encephalitis) Latin Americans. Neuro- ophthalmic findings included ocular motor nerve palsies ( five cases) ( Figs. 1- 4), papilledema ( two cases), and cytomegalovirus optic neuritis ( two cases) ( Figs. 5 and 6). Less common findings included cortical blindness ( one case), conjugate gaze palsy from a lesion of the paramedian pontine reticular formation ( one case), and an inferior altitudinal visual field defect ( one case) ( Fig. 7). The ocular findings in four cases were attributed to focal midbrain toxoplasmic lesions. The diagnosis of cerebral toxoplasmosis was established by the appearance of the lesions with and without contrast on computed tomography of the head, elevated serum antibody to Toxoplasma, a positive response to Toxoplasma chemotherapy, and finding of tachyzoites or tissue cysts on needle brain biopsy ( case 1) ( Figs. 2 and 3). The ocular findings were attributed to cryptococcal meningitis ( two cases), spread of cytomegalovirus retinitis ( two cases), lymphoma of the frontal lobe ( one case) ( Fig. 4), and herpes encephalitis ( one case). Other systemic findings included oral candidiasis ( six cases), Pneumocystis carinii pneumonia ( three TABLE 2. Clinical profile of 10 AIDS patients with neuro- ophthalmic findings Age ( yr) 1 Risk Systemic Eye Eye exam Patient sex/ race factors findings T4fT8 findings to death 30/ M/ LA Homosexual CNS toxoplasmosis 0.8 Right oculomotor palsy, 15 mo, alive scotomas OU 2 31/ M/ B Lv. drug abuse CNS lymphoma Left trochlear palsy Died (? time) 3 28/ MIW Homosexual CNS toxoplasmosis, 0.3 Left trochlear palsy Alive oral candidiasis, PCP, CMV pneumonitis 4 35/ M/ B Lv. drug abuse CNS toxoplasmosis, 0.4 Bilateral abducens 2 yr miliary tuberculosis, palsies, papilledema oral candidiasis 5 35/ MIW Homosexual, Herpes encephalitis, 0.8 Right abducens 1 mo Lv. drug abuse oral candidiasis, palsy, cotton-candida meningitis, wool spots Kaposi's sarcoma 6 34/ MIW Homosexual CMV pneumonitis, PCP, 0.2 Left CMV optic 10 mo oral candidiasis, neuritis HIV encephalopathy 7 38/ MIW Homosexual, CMV of brain and lung, 0.2 Left CMV optic 4mo Lv. drug abuse oral candidiasis neuritis 8 34/ MIW Homosexual, Cryptococcal Papilledema, 1 mo Lv. drug abuse meningitis cortical blindness, left Bell's palsy 9 46/ M/ LA Homosexual, CNS toxoplasmosis, 0.3 Left gaze paralysis 20 mo Lv. drug abuse oral candidiasis ( PPRF lesion) 10 27/ FIW Heterosexual Cryptococcal 0.3 Left altitudinal 1 yr, alive contacts meningitis, PCP field defect W, white; B, black; LA, Latin American; PCP, pneumocystis pneumonia; CMV, cytomegalovirus; PPRF, paramedian pontine reticular formation; OU, bilateral. '''', V'.'!. 10. ,\'". J. L: J'j1) NEURO- OPHTHALMIC FINDINGS IN AIDS 169 FIG. 1. Case 1. Cardinal gaze positions showing right third nerve palsy. cases), miliary tuberculosis ( one case), Kaposi's sarcoma ( one case), and human immunodeficiency virus ( HIV) encephalopathy ( one case). Accompanying ocular findings included cotton- wool spots in three cases and cytomegalovirus retinitis in two cases. The average T- helper/ T- suppressor ratio was 0.4 ( range 0.2-- 0.8). Six patients died an average of 8 months after the neuro- ophthalmic manifestations. Serological tests for syphilis were done FIG. 2. Case 1. Computed tomography of the brain reveals two ring- enhancing masses in the midbrain ( arrow) and in the frontal lobe with edema of the frontal lobe. Magnetic resonance imaging revealed intense enhancement of eight separate lesions on T2 imaging ( one in caudate, two in frontal region, two in parietal region, two in midbrain, and one in occipital region). " ... f FIG. 3. Case 1. Histopathology of brain biopsy from the occipital lobe demonstrates the presence of tachyzoites ( arrow). Serum toxoplasma titer was 1/ 1,024, and the patient responded to toxoplasma chemotherapy, but with persistence of the third nerve palsy. in the Pathology Department at the University of Texas Medical Branch on 61 of 177 patients. FTAABS testing was negative in eight patients, RPR testing was negative in 20 separate patients, and both FTA- ABS and RPR testing were negative in four additional patients ( Table 3). One patient had FIG. 4. Case 2. Computed tomography showing an enhancing ill- defined mass in the posterior aspect of the frontal lobe ( arrow), and a smaller mass in the thalamus. Histopathologically, the lesion corresponded to a lymphoma. The mass decreased in size and became surrounded by an area of gliosis after radiotherapy. J Clin Neuro- ophthalmol. Vol. 10, No. 3, 1990 170 AHMAD M. MANSOUR FIG. 5. Case 6. Top left: There is early involvement of the inferior sector of the optic disc with 20/ 20 visual acuity. Top right: Five weeks later, there is diffuse optic neuritis. Bottom left: Nine days later. Bottom right: Three months later there is resolution of the optic neuritis and retinitis on gangyclovir therapy. The optic disc appears pale but the visual acuity remained hand motion. Six weeks later there was relapse of the retinitis and optic neuritis. borderline FfA- ABS with 1: 1 RPR titer. Twentyeight patients had positive FfA- ABS with the following RPR titer: nonreactive ( two patients), 1: 1 ( six patients), 1: 2 ( five patients), 1: 4 ( four patients), 1: 8 ( three patients), 1: 16 ( five patients), 1: 256 ( one patient), 1: 512 ( one patient), and unknown ( one FIG. 6. Case 7. Top left: Cytomegalovirus retinitis with involvement of the superior sector of the optic nerve. Top right: Four weeks later the optic neuritis has involved three quadrants of the nerve except the inferotemporal quadrant. Bottom: Two weeks later there is diffuse optic neuritis with surrounding diffuse retinitis. FIG. 7. Case 10. Visual field of the left eye shows an altitudinal defect from presumed perineuritic adhesive cryptococcal arachnoiditis ( outer field and inner field correspond to 1114e and 12e light stimulus). patient). RPR of the cerebrospinal fluid was tested in four patients and found to be negative. DISCUSSION The neuro- ophthalmic findings in the present series parallel the findings reported by other investigators ( 1- 53) ( Table 4). The most common central nervous system lesions included cerebral toxoplasmosis, followed by cryptococcal meningitis and cytomegalovirus infection. This is consistent with the findings of cerebral toxoplasmosis in 10- 15% of AIDS patients, cryptococcal meningitis in 10% of AIDS patients, and cytomegalovirus involvement of the central nervous system in one third of AIDS patients at autopsy ( Table 5) ( 54- 64). Neuro- ophthalmic findings were present in 8% of 127 patients with AIDS in the present series. Similarly, Jabs et al. ( 11), Palestine et al. ( 29), and Freeman et al. ( 3) found 8% occurrence of neuroophthalmic signs among 200, 40, and 26 patients with AIDS, respectively. Neurological complications occurred in 40% of AIDS patients in various clinical studies ( 40,41,44). Neuropathologic changes in AIDS were detected in 73% in an autopsy study ( 61). Subclinical involvement of the ocular motility apparatus by HIV appears to be common and the analysis of ocular motility may detect early neurologic dysfunction in HIVinfected subjects. Peak saccadic velocities were abnormal in AIDS patients with or without dementia ( 14,16), and in asymptomatic HIV- infected subjects ( 4). The neuroanatomic substrate for horizontal saccades seems to be affected early in HIV infection because the neuropathologic changes in ~" •••• 1 (' vi 10. Nu. J. 1~ 90 NEURO- OPHTHALMIC FINDINGS IN AIDS 171 TABLE 3. Syphilis serology results in 61 patients tested among 177 patients with AIDS or AIDS- related complex RPR RPR RPR RPR RPR RPR RPR RPR RPR not done nonreactive 1: 1 1: 2 1: 4 1: 8 1: 16 1: 256 1: 512 Positive FTA- ABS Borderline FTA- ABS Negative FTA- ABS FTA- ABS not done 8 2 4 20 6 1 5 4 3 5 mv infection are concentrated in the subcortical structures. Ocular motor nerve palsy may be the presenting central nervous system manifestation in AIDS ( 1,32,49). Palsy of the third ( 3,11,29,32,39,44), TABLE 4. Neuro- ophthalmic findings in AIDS- literature review Cranial nerve palsies CNS infections [ toxoplasmosis ( 3,39,40), cryptococcosis ( 3), varicella zoster ( 29), PML ( 47), CMV ( 42) 1 CNS lymphoma ( primary or metastatic) ( 44,48) Orbital lymphoma ( 49) Cavernous and orbital apex eosinophilic granuloma ( 10) Optic neuropathy Papilledema [ cryptococcal meningitis, CNS toxoplasmosis, CNS lymphoma ( 29)) Optic neuritis [ CMV ( 9,20,22,28,35), syphilitic ( 17,18,37), varicella zoster ( 2,5), hepatitis B ( 19), toxoplasmic ( 38)) Retrobulbar optic neuritis [ syphilitic ( 30,31), CMV ( 9), cryptococcal ( 2)) Optic nerve perineuritis [ syphilitic ( 2), cryptococcal ( 15)) Anterior ischemic optic neuropathy ( 33) Toxic optic neuropathy [ e. g., ethambutol toxicity ( 11)) Optic atrophy as a sequelae of the neuropathy Eye movement disorders Slowed saccades and abnormal oculokinetic response [ HIV encephalopathy ( 4,14,16,24,26), CMV encephalitis ( 42)) Progressive convergence insufficiency ( 24) Reverse ocular dipping [ cryptococcal meningitis ( 25)) Parinaud's syndrome [ herpes encephalitis ( 23), HIV encephalopathy ( 24)) Internuclear ophthalmoplegia [ CMV encephalitis ( 6,27), cerebral mucormycosis ( 43)) PPRF lesions [ HIV encephalopathy ( 24)] Blepharospam [ HIV encephalopathy ( 24)) Opsiclonus ( 11) Skew deviation ( 11) Visual field defects Homonymous hemianopsia [ PML ( 13,44,47,52), cryptococcal meningitis ( 25), internal carotid occlusion from meningovascular syphilis ( 50)] Homonymous quadranopsia [ CNS astrocytoma ( 45)) Enlarged blind spot [ PML: ( 12)) Pericentral scotoma [ PML ( 12)) Miscellaneous Cortical blindness [ cryptococcal meningitis ( 5), CNS tuberculosis ( 46)) Visual allesthesia ( 44) Visual hallucination ( 1,8) Photophobia ( cryptococcal meningitis) ( 53) PML, progressive multifocal leukoencephalopathy. fourth ( 29), and sixth ( 3,42,44,49) cranial nerves have occurred in AIDS, and may be bilateral ( 44) or combined ( 3,29). The majority of these cranial nerve palsies were due to focal brainstem toxoplasmic lesions around the area of the cranial nerve nuclei ( 1) as in cases 1, 3, and 4. By computed tomography, toxoplasmic encephalitis gave the appearance of rounded, single or multiple, isodense or hypodense lesions. These lesions revealed ring or nodular enhancement by contrast studies ( 65). Increased intracranial pressure and mass effects ( lymphoma of the frontal lobe as in case 2), as well as constrictive arachnoiditis from cryptococcal meningitis, can affect the ocular motor nerves at the base of the skull. Varicella zoster involvement of the trochlear nerve have been reported by Palestine et al. ( 29), and abducens palsy from herpetic encephalitis was encountered in case 5. Gaze paresis from nuclear and supranuclear lesions ( includ- TABLE 5. Central nervous system complications in AIDS- literature review ( 54) HIV infection ( 56) Asymptomatic encephalomeningitis ( abnormal CSF) Aseptic meningitis ( headache) HIV encephalopathy- dementia complex ( subcortical dementia with disturbance in cognition, motor skills, and behavior; cerebral atrophy by CT scan and white matter pallor histopathologically) ( 4) Opportunistic infections Cerebral toxoplasmosis ( 13% of AIDS patients) ( 39,44,55,57) Cryptococcal meningitis ( 10% of AIDS patients) ( 44) Progressive multifocal leukoencephalopathy ( 3% of AIDS patients) ( 12,44,58,59) CMV encephalitis ( 42,60) Varicella zoster and herpes simplex encephalitis or cerebral vasculitis ( 56,62) Tuberculosis and atypical mycobacteria ( 2% of AIDS patients) ( 46) Mucormycosis ( 43) Bacterial abscess ( 63) Tumors Primary and metastatic CNS lymphomas ( 9% of AIDS patients) ( 54,57) Astrocytoma ( 45) Metastatic Kaposi's sarcoma ( rare) Other complications Intracerebral hemorrhage ( 2% of AIDS patients) ( 44,63) Cerebrovascular accidents ( 63) CSF, cerebrospinal fluid. J elin Neuro- ophthalmol, Vol. 10, No. 3, 1990 172 AHMAD M. MANSOUR ing lesions of the paramedian pontine reticular formation and the medial longitudinal fasciculus) were noted in toxoplasmic encephalitis ( 1), cytomegalovirus encephalitis ( 6,23,27), cerebral mucormycosis ( 43), and HIV encephalopathy ( 24). Optic nerve involvement in HIV infection commonly includes papilledema and papillitis. Papilledema is a frequent manifestation of intracranial diseases in AIDS patients, occurring in as many as 14% of these patients ( 36). Papilledema results from cryptococcal meningitis, cerebral toxoplasmosis, and central nervous system lymphoma. Papillitis commonly complicates cytomegalovirus retinitis. Optic neuritis was detected in seven of 22 patients with cytomegalovirus retinitis ( 9). Cytomegalovirus papillitis starts initially in the sector adjacent to the cytomegalovirus retinitis and spreads gradually to involve the whole optic nerve, with severe loss of vision. Cytomegalovirus papillitis may respond early in its course to gancyclovir therapy with preservation of vision ( 20), but most cases suffer irreversible visual loss ( 28,34). Histopathologically, the optic nerve in cytomegalovirus infection displays necrosis and replacement of nerve tissue by fibrous tissue and inflammatory cells ( 22,35). Less common forms of optic nerve disease in HIV- infected individuals include papillitis ( syphilitic, varicella zoster, toxoplasmic, and hepatitis B), retrobulbar optic neuritis ( syphilitic, cryptococcal, and cytomegalovirus), optic nerve perineuritis ( syphilitic and cryptococcal), and anterior ischemic optic neuropathy ( Table 4). Patient 10 had an inferior altitudinal field defect ( Fig. 7), normal- looking optic discs, and presumed retrobulbar neuropathy from cryptococcal perineuritic adhesive arachnoiditis as described by Lipson et al. ( 15), and by Okun and Butler ( 64). Patients with cryptococcal meningitis, with ( 11) or without AIDS ( 64), should be screened thoroughly for neuro- ophthalmic disorders because more than a third of these subjects have neuro- ophthalmic findings in the form of papilledema, optic neuropathy, and extraocular muscle palsies. Anterior ischemic optic neuropathy in AIDS may be related to an optic nerve microvasculopathy similar to the HIV microvasculopathy of the retina ( 36), or may be precipitated by severe anemia. Papillitis in asymptomatic HIV- infected individuals may result from ocular syphilis because patients at risk for contracting the HIV virus are at high risk for concomitant infection with syphilis ( 17). The majority of HIV- infected individuals with ocular syphilis also have neurosyphilis and should be treated accordingly ( 50,51). Patients with AIDS receive a variety of chemo- I elin Neuro- ophtlullmol. Vol. 10, N~ 1. 199/ 1 therapeutic medications, some of which are known to cause toxic optic neuropathy, as in the case of ethambutol optic neuropathy reported by Jabs et al. ( 11). Various visual field defects have been reported secondary to lesions of the visual pathways from cryptococcal meningitis ( 25), cerebral astrocytoma ( 45), and progressive multifocalleukoencephalopathy ( 47), or occlusion of the internal carotid from meningovascular syphilis ( 50). Progressive multifocal leukoencephalopathy is characterized by progressive demyelinating disorder caused by papova JC virus. This leukoencephalopathy occurs in about 4% of AIDS patients ( 63) and manifests as insidious onset of extremity weakness, memory disturbance, and aphasia. Visual field defects, especially homonymous hemianopsia ( 13,52), occur in one fourth of patients with progressive multifocal leukoencephalopathy ( 47). Computed tomography of the brain frequently shows hypodense, nonenhancing white matter lesions ( Fig. 8), whereas histopathologically intranuclear inclusions in the oligodendroglial cells are characteristic FIG. 8. Magnetic resonance imaging demonstrates multiple discrete lesions involving the white matter of the brain ( arrows) in a 36- year- old white man with positive HIV testing, cotton- wool spots, and multiple sclerosis- like symptoms ( transient episodes of diplopia, and increasing fatigue. vertigo. gait imbalance. and numbness of the distal extremities). The clinical and MAl findings were consistent with progressive multifocal leukoencephalopathy. The present case is outside the present study population. NEURO- OPHTHALMIC FINDINGS IN AIDS 173 of progressive multifocal leukoencephalopathy ( 59). Other manifestations in AIDS include cortical blindness ( case 8) ( 5,46), visual hallucinations ( 1,8), and visual allesthesias ( 44). Photophobia is experienced by one fourth of patients with cryptococcal meningitis ( 53). AIDS patients at risk for neuro- ophthalmic manifestations include patients with cryptococcal meningitis, central nervous system toxoplasmosis, extensive cytomegalovirus retinitis, progressive multifocal leukoencephalopathy, neurosyphilis, and HIV encephalopathy. These patients should undergo thorough neuro- ophthalmic examination. The author examined a patient in December 1989 with the AIDS- related complex syndrome who had unilateral ocular involvement in the form of severe visual loss, peripheral choroidal infiltrates with normal optic disc appearance and no vitritis, and loss of central visual field. Workup revealed neurosyphilis in that patient. The author became aware of a patient with diffuse central nervous system toxoplasmosis who was found to have bilateral papillitis. That patient had a whitish fungating mass emanating from the optic disc ( patient of Kevin Harmon, M. 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