Methods

This prospective survey was carried out from August 1, 2009 to July 31, 2010. China initiated a comprehensive program to promote free HAART in 2003. The subjects of our study were HIV/AIDS patients diagnosed at the Shanghai Public Health Clinical Center at Fudan University, the HIV/AIDS diagnosis and treatment institution in eastern China, and offered free regular HAART treatment. Patients were diagnosed with HIV/AIDS according to the 1993 Centers for Disease Control and Prevention case surveillance definition of AIDS. We obtained detailed medical histories for all of the patients, including HIV/AIDS-related diseases and antiviral treatment history. We then performed a range of ophthalmologic examinations including best-corrected visual acuity (VA), ocular adnexal examination, anterior segment slit-lamp microscopy, examination of the posterior segment with an indirect ophthalmoscope, and slit-lamp examination with pupillary dilation and fundus photography. Some of the suspected cases were examined with fundus fluorescence angiography (FFA) and optical coherence tomography.

In this study, we were looking for all of the ocular complications of these HIV/AIDS patients. CMVR is clinically diagnosed by the characteristic appearance of a necrotizing retinitis with either edematous white borders or a granular white border with or without hemorrhage. HIV vasculopathy included HIV microangiopathy and large vessel disease. HIV microangiopathy is diagnosed when the patient presents with cotton-wool spots, microaneurysms, retinal hemorrhages, telangiectatic vessels, and ischemic maculopathy. HIV large-vessel disease included branch retinal artery occlusion and central and branch retinal vein occlusions. In patients whose CD4+ T-lymphocyte counts have increased after receiving HAART, immune recovery uveitis (IRU) was clinically diagnosed by a decrease in vision caused by moderate or severe vitritis, macular edema, epiretinal membranes, keratic precipitate, neovascularization of the optic disc or retina, posterior synechia, and cataract. The absence of other inflammatory conditions such as syphilis, herpetic retinitis, drug toxicity, trauma, and so on confirmed the diagnosis.

The diagnosis of acute retinal necrosis (ARN) followed the standard diagnostic criteria developed by the Executive Committee of the American Uveitis Society, including the triad of vitreous inflammation, peripheral retinitis, and retinal arteritis. Complicated cataract referred to the characteristic opacity of anterior and posterior lens capsules. Other ocular complications, such as retinal detachment (RD), optic neuropathy, disc edema, ptosis, keratitis, and Kaposi sarcoma, were diagnosed according to the Studies of Ocular Complications of AIDS by certified ophthalmologists using standardized descriptions and characteristic clinical features. Other complications of AIDS were diagnosed according to the AIDS Clinical Trials Group guidelines for evaluation and diagnosis of these disorders.

The HAART regime that the patients received included lamivudine (300 mg, twice daily), zidovudine (300 mg, twice daily), or stavudine (30 mg, twice daily); and nevirapine (200 mg, every night) or efavirenz (600 mg, every night).

In this study, the HIV/AIDS patients were assigned to 2 groups: 1 with ocular complications and the other without ocular complications. All data were statistically analyzed using SPSS version 17.0 (SPSS, Inc, Chicago, Illinois, USA). The categorical variables of sex, age, race/ethnicity, history of HIV exposure, educational degree, visual acuity, and CD4 levels were analyzed by χ ² or Fisher exact tests and Student or nonparametric tests to obtain P values. P < .05 is considered significant.

Results

There were 1132 outpatients or inpatients enrolled at the Shanghai Public Health Clinical Center at Fudan University from January 2003 to July 2010 who were still eligible for our study. From that group, 69.5% (787/1132) of the patients agreed to be recruited and enrolled in the study. All of them had a history of HAART and 87.5% of these patients (689/787) were receiving HAART. Of the 787 participants, 226 (28.72%; 95% confidence interval [CI] = 0.26−0.32) had a systemic disease. The prevalence of ocular complications was 26.3% (95% CI = 0.23−0.29; 207/787). Patient sex, age, race/ethnicity, history of HIV exposure, and education level are listed in Table 1 . All 787 patients were Chinese and 83.5% of the participants (657/787) were male. There were no significant differences in the morbidity of the patients with ocular complications between sexes (χ ² test, P > .05) and ages ( t test, P > .05). The patient group was mostly of Han ethnicity (779/787, 99.0%), with the remaining patients of other race/ethnicity (8/787, 1.0%). There is a significant difference in education level between the group with ocular complications and the group without ocular complications (χ ² test, P < .05); the group with ocular complications had more individuals with an education level of high school or college (98/207, 47.3%) compared to the group without ocular complications (341/580, 58.8%). Of all the 787 enrolled HIV/AIDS patients, 73.58% (579/787) had sex contact history, which included homosexual (30.40%, 176/579), heterosexual (66.10%, 383/579), and homosexual and heterosexual (3.50%, 20/579). There was no significant difference in the history of HIV exposure between the group with ocular complications and the group without ocular complications (χ ² test, P > .05).

The VA and ocular complications for all 787 patients (1574 eyes) are listed in Table 2 . The VA of the group with ocular complications was significantly poorer than that of the group without ocular complications ( t test, P < .01). CMVR is the most common ocular complication (10.5%, 83/787), with 44.5% of these patients (37/83) demonstrating binocular involvement and 10.8% of them (9/83) blind (RD, 5 patients; IRU, 4 patients). Among all 83 CMVR patients, only 28 (33.7%) were treated with ganciclovir (5 mg/kg is administered twice a day by intravenous injection for 2 to 3 weeks during the inductive phase and the same dose is given once a day intravenously or 1000 mg 3 times a day orally during the maintenance phase). Fourteen patients (22 eyes) who had received or were receiving HAART had the complication of IRU (16.9%, 14/83). Ocular drops of corticosteroids were used in all of the 14 IRU patients during the active and maintenance phase, and there was no history of sub-Tenon’s or systemic injections of repository corticosteroids and vitrectomy. Also, 5 of the IRU patients had a history of ganciclovir treatment. There were 9 patients (12 eyes) with RD, among which 9 eyes were secondary to atrophic hole with 4 eyes treated by pars plana vitrectomy. Of these 9 eyes, the 5 that were left untreated became blind. Three eyes with exudative RD secondary to CMVR were treated with intravenous ganciclovir and local or systemic steroid injection but vision remained poor. Microangiopathy (9.4%, 74/787) was the second most common complication, with 45.9% (34/74) demonstrating binocular involvement. Twenty-seven of the 787 HIV/AIDS patients (3.4%) suffered from neuro-ophthalmologic disorders, in which optic disc edema had the highest prevalence (63.0%, 17/27), followed by optic neuritis (29.6%, 8/27), abducent paralysis (3.7%, 1/27), and ptosis of herpes zoster ophthalmoplegia (3.7%, 1/27).

Most of the patients with HIV/AIDS had a history of severe immunodeficiency. After the HAART, patient immune functions reformed and the CD4 T-cell counts were improved or maintained at a steady level. The levels of CD4 T cells were monitored every 2 to 3 months in all patients, so the patient’s CD4 T-cell count was known at the time of the ocular examination. For the patients with newly diagnosed or active stage of ocular complications, we selected the CD4 T-cell count at the time of diagnosis during several 1-year visits. Even with treatment of HAART, the median CD4 T-cell count of the group with ocular complications was 43 cells/μL, which is significantly lower (nonparametric test, P < .01) than that in the group without ocular complications (116.5 cells/μL). The median CD4 nadir of IRU was 21 cells/μL. Apart from those with IRU, more than half of the patients with main complications, such as CMVR and HIV microangiopathy, had a CD4 T-cell count of <100 cells/μL. CD4 T-cell count data for all 787 patients are listed in Table 3 .

TABLE 3

Number of HIV/AIDS Patients With or Without Ocular Complications in Eastern China, by CD4 T-Cell Level

	CD4 T-Cell Level (Cells/μL)				Total	Median	Mean ± SD	95% CI
	<50	50-<100	100-<200	≥200
Total patients	305	111	145	226	787	89	137.03 ± 134.35	127.63–146.44
No ocular complication	194	86	115	185	580	116.5	149.39 ± 135.28	138.36–160.43
Ocular complication	111 a	25 a	30 a	41 a	207 a	43	102.40 ± 125.69	85.18–119.62
CMVR	51	9	11	12	83	35	83.71 ± 117.47	58.06–109.36
IRU	2	2	5	5	14	170	222.78 ± 213.34	11.45–301.98
RD	4	1	3	1	9	86	223.33 ± 212.71	59.83–386.84
ARN	0	1	2	0	3	101	123.33 ± 40.43	22.91–223.76
HIVM	37	9	12	16	74	49	106.51 ± 117.84	79.21–133.82
CRVO	5	2	0	0	7	25	36.29 ± 34.05	4.79–67.78
Optic neuropathy	14	1	4	6	25	40	118.68 ± 153.24	55.43–118.93
Cataract	3	1	0	3	7	73.5	127.71 ± 179.63	26.00–233.43
Keratitis	4	1	2	4	11	130	135.36 ± 144.64	38.19–232.53

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