Optometry & Vision Science:
Ocular Problems in HIV and AIDS Patients in Nigeria
Emina, Michael Osita*; Odjimogho, Stella E.†
†OD, MBA, FAAO
Department of Optometry, University of Benin, Benin City, Nigeria.
Received February 18, 2010; accepted August 23, 2010.
Purpose. To investigate ocular disease and visual acuity defects in patients with HIV/AIDS according to CD4+T-cells counts.
Methods. The CD4+T lymphocyte counts of all the volunteers were obtained. Visual acuity, refraction, ophthalmoscope, and slitlamp examinations were performed on each patient after the CD4+T-cell count result was obtained.
Results. Young adults aged between 21 and 30 years were mostly affected, 39 (97.5%) of the HIV patients had refractive errors, and 10 (25%) had reduced vision. Seven (17.5%) moderate and one (2.5%) severe low vision patients were found between 499 to 0 and 299 to 200 CD4+T-cell counts, respectively. Ocular diseases found in various CD4+T-cells counts were proptosis (2.5%), orbital cellulitis (2.5%), and cytomegalovirus retinitis (2.5%) in 99 to 0, keratoconjunctivitis sicca (2.5%) and corneal keratitis (2.5%) in 499 to 400, molluscum contagiosum (2.5%) in 299 to 200, iridocyclitis (2.5%) in 199 to 100, cloudy media (22.5%), red eyes (30%), poor pupillary reflexes (17.5%), and painful eye (30%) in 499 to 0, retinal exudates (15%), disc edema (30%), and choroidoretinitis (15%) in 399 to 0, ocular toxoplasmosis (5%) and herpes zoster (7.5%) in 299 to 100, Kaposi sarcoma (12.5%) in 199 to 0, conjunctivitis (7.5%) in 499 to 300, and uveitis (7.5%) in 399 to 200. There were significant differences between visual acuity of the control and the HIV/AIDS patients, p < 0.05.
Conclusions. Ocular impairments increased with decrease in CD4+T-cells counts. Additional studies are required in predicting the CD4+T-cells counts that will serve as a marker for specific ocular disease manifestation in HIV/AIDS.
Ocular problems in patients with human immunodeficiency virus (HIV) and acquired immunodeficiency syndrome (AIDS) may be aggravated by the presence of diseases that placed burden on the structure of the eye in the sub-Saharan Africa.1–3 Several literatures on the ocular lesions found in HIV and AIDS are focused on the developed industrialized nations of the world.4,5 There may be differences in the presentation of signs and symptoms in HIV and AIDS between the developing countries and the industrialized nations. Some of the differences in the presentation of the disease in the developing countries could be as a result of the presence of more opportunistic infections, higher mortality, and morbidity rates in the course of HIV disease. The presentations of the HIV disease differ from one region to the other. It has been reported that there were different types of virus strains and opportunistic infections in HIV and AIDS across the regions and across countries within the region.6,7 Therefore, there may be also variations in the ocular manifestations of the disease. This study is an attempt to associate the ocular problems with the CD4+T lymphocyte counts in cells per cubic millimeter (CD4+T-cells count) and to highlight the ocular manifestations of HIV and AIDS for inclusion in the baseline data in Nigeria.
At the time of this study, most HIV and AIDS patients were not on the antiretroviral drugs either as a result of availability or cost. For the fortunate few persons, treatments were often commenced at a desperate stage in the progress of the disease. Therefore, the totality of the ocular manifestations of the diseases might not have been observed either as a result of short life span or the patient was too ill to present for eye examination or the fear of disclosure. However, with the advent of new antiretroviral drugs and the assistance of the Federal government of Nigeria in making the drugs available, patients living with HIV and AIDS may live longer with better quality of life.8
This prospective study, performed in November 2004 at the University of Lagos teaching hospital, was conducted in accordance with the tenants of the Declaration of Helsinki. The written consents of the hospital management and of the 80 individuals to be examined were obtained. The participants examined were 40 HIV/AIDS positive patients and the control (40 HIV/AIDS negative) patients in the hospital medical unit. The control patients were matched by sex and age (ages matched were approximated to ±1 year) with the patients living with HIV and AIDS. The control was patients in the hospital for other systemic problems. The hospital certified the control patients HIV free status at the time of this study. The age of the control group was determined after the HIV/AIDS patients indicated interest as volunteers in the study. All the patients were identified with numbers assigned for the purpose of the study. The HIV/AIDS positive volunteers were on highly active antiretroviral therapy (HAART) drugs regimen before being enrolled in this study. The CD4+T lymphocyte counts (in cells per cubic millimeter) of all the participants were obtained with the assistance of health workers in the Department of Hematology, University of Lagos teaching hospital, Nigeria. The patients ordered and offered voluntarily for their CD4+T-cell counts and eye examinations. The ocular examination of each patient was performed after the CD4+T lymphocyte count (CD4+T-cells count) result was obtained. Ocular examinations were performed with pen-torch, ophthalmoscope, and slitlamp. Visual acuity (VA), ophthalmoscope, and slitlamp examinations were performed on the HIV/AIDS and control patients. The volunteers were all refracted, using the standard refraction procedures to prescribe free glasses to them and to identify peculiar VA defects associated with HIV/AIDS.
VA was measured with a Snellen illiterate “E” chat for distance (at 6 m). The VA for distance were classified and recorded as normal, reduced, and low vision with their best optical correction in place. The VA classification is based on WHO recommendations that present normal vision as when the VA in the best eye is between 6/5 and 6/6 and reduced VA between 6/9 and 6/18 with the best optical correction. Low vision was presented as moderate visual impairment when the VA is <6/18 but equal to or better than 6/60 and severe visual impairment as VA < 6/60 but equal to or better than 3/60 in the best eye with the best spectacle correction.9
Statistical significance between the VA of the control and trials were estimated by Pearson χ2, and p < 0.05 was considered statistically significant. Analysis of variance (ANOVA) statistical test was also used in determining the groups of age that had more HIV/AIDS patients. The frequency of ocular problems was also determined.
The age range of the individuals examined was between 21 and 50 years. The HIV/AIDS patients were put in groups of age as shown in Table 1. In the age group of 21 to 30 years, a female patient whose CD4+T-cells count was within 899 to 800 showed no ocular sign of the disease. However, many of the patients with HIV/AIDS were between 21 and 40 years. Young females in the age group 21 to 30 years were more affected than the males, and there were more affected males than females in the 41 to 50 years age groups (Table 2).
It was observed that more males than female patients had their CD4+T-cells counts between 899 and 500 and more females (12, 30%) than males (11, 27.5%) were found to have the CD4+ T-cells counts between 499 to 0 (Table 3). Thirty-nine (97.5%) of the HIV patients had refractive errors; 22 (55%) patients had normal VA with their spectacle correction in place, and 10 persons had reduced vision (Table 4). Seven (17.5%) moderate low vision, and one person with severely impaired vision were found among the HIV/AIDS patients. Low vision manifested in the patients with 499 to 0 CD4+T-cells counts.
Ocular defects of the disease began to manifest from 499 to 0 CD4+T-cells counts. However, one patient with 499 to 400 CD4+T-cells counts did not manifest any ocular problems. We observed few cases of proptosis (2.5%), cytomegalovirus retinitis (2.5%), chalazion (2.5%), infected canaliculi in keratoconjunctivitis sicca (2.5%), molluscum contagiosum (2.5%), corneal keratitis (2.5%), orbital cellulitis (2.5%), and iridocyclitis (2.5%), and many patients had cloudy media (22.5%), retinal exudates (15%), Kaposi sarcoma (12.5%), poor papillary light reflexes (17.5%), conjunctivitis (17.5%), choroidoretinitis (15%), disc edema (30%), red eyes (30%), and burning painful eye (30%). Twenty-two (55%) patients with CD4+T-cells counts <500 cells/mm3 presented more than one sign of the disease (Table 5). Patients with low CD4+T-cells counts (99 to 0 cells/mm3) were very weak and emaciated and often on bed. They were encouraged to keep up with the hope of living a better life again. The ocular problems observed in the control were on four patients; one patient had binocular choroidoretinitis and moderate low vision in the CD4+T-cells count range of 899 to 800.
Statistical results revealed significant differences between the VA of the control and the HIV/AIDS patients (calculated χ2 = 12.712, p < 0.05). There were no statistical significant differences between the three groups of age of infected persons with CD4+ T-cells count values from 499 to 0 (critical F = 1.075; calculated values = 0.257, 0.188, and 0.188, respectively, p > 0.05), using ANOVA at 95% confidence interval. The statistical power to find the differences between the ocular problems was not there because of the low incidence of the ocular manifestations. Many of the ocular problems manifested in the CD4+T-cells counts below 500 cells/mm3 (Table 5). The cumulative percentages revealed that the ocular problems increased with decrease in CD4+T-cells counts (CD4+T-cells counts 499 to 400, 399 to 4300, 299 to 4200, 199 to 4100, and 99 to 40 and cumulative percentages 13.9, 35.7, 49.6, 66.1, and 100%, respectively).
Posterior segment structures involved in HIV-positive patients were the retina, choroid, and optic nerve head. Disorders of these structures occurred in 22 (55%) of the patients who were HIV positive. Common complaints of the HIV patients included floaters, flashing lights, and decreased VA. The presence of an afferent pupillary defect strongly suggested significant retinal or optic nerve involvement. The diagnoses were based on clinical evidences observed during funduscopic examinations.
HIV sufferers gradually degenerate over time with signs of AIDS, a blood-borne infectious disease that results in the gradual decrease in CD4+T lymphocytes counts, allowing opportunistic infections and neoplasia to develop, if unchecked. There were many reports that described the spectrum and nature of HIV associated eye problems, which affected 70 to 80% of all patients at some point during the illness.10–13 CD4+T-cells counts <500 cells/mm3 were associated with Kaposi sarcoma and lymphoma. CD4+T-cell counts <250 cells/mm3 were also associated with pneumocystosis and toxoplasmosis and CD4+T-cell counts <100 cells/mm3 was associated with retinal or conjunctival microvasculopathy and cytomegalovirus (CMV) retinitis.14–16 The CMV retinitis in this study was observed in a patient with CD4+T-cells count 99 to 0 cells/mm3.
In the developing world, the prevalence of CMV retinitis was observed to be lower than that in the developed nations. A comparison of various reports from different regions in Africa indicated that the overall prevalence of CMV retinitis in African patients with AIDS varied from 0 to 8.5%; a recent study on the incidence of CMV retinitis corresponded to a point prevalence of 1.5%.17 With the use of HAART, the pattern and prevalence of the ocular manifestations of the disease were expected to be different.18
CD4+T lymphocyte counts (CD4+T-cells counts) had been used to predict the onset of certain ocular infections in HIV-positive patients. The predictive values of CD4+T-cells counts for ocular manifestations in HIV infection had been queried particularly in patients with CMV retinitis when CD4+T-cell counts were above 200 cells/mm3. These patients were placed on HAART. These observations may argue against the protective effect of an increased CD4+T-cells counts, and it may not rule out the possibility that CMV retinitis precedes the recovery of CD4+T-cells counts. Therefore, whether the reconstituted CD4+T-cells count will serve as a better predictor of specific ocular infection should be investigated. However, as a result of these uncertainties, the use of CD4+T-cells count as the parameter for predicting the occurrence of specific ocular infection in HIV-positive patients may remain, until antigen-specific tests of recovered CD4+T lymphocytes become available, at the face of already damaged ocular tissues.7,16,19
There were many HIV-infected individuals in the developing countries, particularly in the sub-Saharan Africa, but the prevalence of CMV retinitis among HIV-infected persons in the developing Africans countries was reported to be lower than that in the developed countries.20 On the contrary, ocular complications of toxoplasmosis, herpes zoster ophthalmicus (HZO), and papillomavirus-associated conjunctival squamous cell tumor were prevalent in HIV infected persons in developing countries, with slight differences from region to region. The reasons for the differences were attributed to the frequency of the causative agents, morbidity, and poor control of HIV infection in the developing countries.21–23
It was observed that 21 (52.5%) of HIV-positive patients manifested anterior segment complications, including dry eyes (keratoconjunctivitis sicca), infectious keratitis, uveitis, and anterior chamber inflammation (iridocyclitis). Keratitis was found in seven (17.5%) patients. It had been reported that herpes zoster and herpes simplex virus were most commonly implicated in infectious keratitis in HIV-positive patients. Other common symptoms observed were irritation, pain, photophobia, and reduced vision (Table 5). The observations in this study agreed with the report that the prevalence of infectious keratitis was higher in patients who were infected with HIV. 24–26 Keratitis was often associated with HZO, which was also used as a marker in early stages of HIV in young Africans.4,27
A total of 39 (97.5%) of the HIV patients had refractive errors and 10 (25%) patients had reduced vision. It was also found that three (7.5%) volunteers in the control had reduced vision, which was less than that found in the HIV patients. One HIV patient (2.5%) had severely impaired vision. Moderate visual impairment was found in seven (17.5%) patients, which differed from the control that had one patient with moderate visual impairment. Moderate low vision manifested in the HIV patients with 499 to 0 CD4+T-cells counts. Severe low vision was found in a patient with 299 to 200 CD4+T-cells count. The observations in this study were similar to the report of Otiti-Sengeri et al.28 who found VA of 6/18 or worse in at least one eye (low vision) and reduced vision associated with ocular diseases such as optic nerve disease and uveitis, but differed from that of Shah et al.18 who found in India that 6% of 112 HIV patients had visual impairment and one patient was blind with CD4+T-cells count of 0 to 100 cells/μl. The differences in the report of Shah et al.18 and this study could be attributed to the regional presentation of the disease and late recognition of uncorrected refractive errors. Various factors are responsible for the refractive errors remaining uncorrected in Africa: the lack of awareness and recognition of the problem at personal and family levels, community and public health levels, non-availability or inability to afford refractive services, and cultural disincentives to compliance were common factors.29
There were significant differences between the VA of the control and the HIV/AIDS patients (calculated χ2 = 12.712, p < 0.05). There were no statistical significant differences between the three groups of age of infected persons with CD4+T-cells counts from 499 to 0. The frequency of ocular manifestations of the disease increased with decrease in CD4+T-cells counts, but the statistical power to find the significant differences between HIV ocular manifestations was not there because of the low incidence in the number of each ocular problem. Young adults (40%) in the group of age 21 to 30 years were found with signs and symptoms of HIV/AIDS infection in different stages of CD+T-cell counts (Table 2). A patient (2.5%) with infected canaliculi and keratoconjunctivitis sicca was found in 499 to 400 cells/mm3 CD4+T-cells counts (Table 5). CMV retinitis in this study was observed in a patient (2.5%) with CD4+T-cell counts 99 to 0 cells/mm3, an ocular manifestation at a later stage of the disease.14
Many signs and symptoms of HIV/AIDS infection manifested between 499 and 0 CD4+T-cells/mm3 counts. HZO (7.5%), conjunctivitis (7.5%), ocular toxoplasmosis (5%), uveitis (7.5%), Kaposi sarcoma (12.5%), disc edema (30%), retinal exudates (15%), choroidoretinitis (15%), cloudy media (22.5%), and poor pupillary light reflexes (17.5%) were found to be more than the other ocular manifestations among the HIV/AIDS patients (Table 5). These could serve as good predictors of ocular manifestations in HIV/AIDS, because of the range of CD4+T-cells counts in which they appeared. However, additional studies may be required in predicting the CD4+T-cell counts that will serve as a predictor of specific ocular manifestation in HIV/AIDS patients.
Michael O. Emina
Department of Optometry
University of Benin
Benin City PMB1154, Nigeria
2. Bhatia RS. Tuberculosis and acquired immunodeficiency syndrome. J Assoc Physicians India 2000;48:613–6.
3. Biswas J. Acquired immunodeficiency syndrome and the eye. J Assoc Physicians India 2001;49:551–7.
4. Lewallen S. HIV/AIDS: what is the impact on prevention of blindness programmes? Community Eye Health 2003;16:33–4.
5. Moore PS, Chang Y. Detection of herpesvirus-like DNA sequences in Kaposi's sarcoma in patients with and without HIV infection. N Engl J Med 1995;332:1181–5.
6. Jabs DA, Quinn TC. Acquired immunodeficiency syndrome. In: Pepose JS, Holland GN, Wilhelmus KR, eds. Ocular Infection and Immunity. St. Louis, MO: Mosby; 1995:289–310.
7. Ragupathy V, Zhao J, Wang X, Wood O, Lee S, Burda S, Nyambi P, Hewlett I. Comparative analysis of cell culture and prediction algorithms for phenotyping of genetically diverse HIV-1 strains from Cameroon. AIDS Res Ther 2009;27:6405–27. Available at: http://www.aidsrestherapy.com/content/pdf/1742-6405-6-27.pdf
. Accessed September 24, 2010.
8. Moraes HV Jr. Ocular manifestations of HIV/AIDS. Curr Opin Ophthalmol 2002;13:397–403.
9. World Health Organization. Prevention of Blindness and Deafness. Consultation on Development of Standards for Characterization of Vision Loss and Visual Functioning: WHO/PBL/03.91. Geneva, Switzerland: World Health Organization; 2003.
10. Nasoodi A, Lim LT, Al-Ani A, Quah S, Dinsmore WW. What you can see in your patient's eyes? Review of ocular manifestations of HIV in HAART era. Int J STD AIDS 2008;19:4–11.
11. Congdon NG, Friedman DS, Lietman T. Important causes of visual impairment in the world today. JAMA 2003;290:2057–60.
12. Dix RD, Podack ER, Cousins SW. Loss of the perforin cytotoxic pathway predisposes mice to experimental cytomegalovirus retinitis. J Virol 2003;77:3402–8.
13. Nau JA, Shields CL, Shields JA, Eagle RC, Rice E. Clinicopathologic reports, case reports, and small case series: acute myeloid leukemia manifesting initially as a conjunctival mass in a patient with acquired immunodeficiency syndrome. Arch Ophthalmol 2002;120:1741–2.
14. Dunn JP, Jabs DA. Cytomegalovirus retinitis in AIDS: natural history, diagnosis, and treatment. AIDS Clin Rev 1995;99–129.
15. Cheung TW, Teich SA. Cytomegalovirus infection in patients with HIV infection. Mt Sinai J Med 1999;66:113–24.
16. Faber DW, Wiley CA, Lynn GB, Gross JG, Freeman WR. Role of HIV and CMV in the pathogenesis of retinitis and retinal vasculopathy in AIDS patients. Invest Ophthalmol Vis Sci 1992;33:2345–53.
17. Kestelyn P. The epidemiology of CMV retinitis in Africa. Ocul Immunol Inflamm 1999;7:173–7.
18. Shah SU, Kerkar SP, Pazare AR. Evaluation of ocular manifestations and blindness in HIV/AIDS patients on HAART in a tertiary care hospital in western India. Br J Ophthalmol 2009;93:88–90.
19. Connors M, Kovacs JA, Krevat S, Gea-Banacloche JC, Sneller MC, Flanigan M, Metcalf JA, Walker RE, Falloon J, Baseler M, Feuerstein I, Masur H, Lane HC. HIV infection induces changes in CD4+ T-cell phenotype and depletions within the CD4+ T-cell repertoire that are not immediately restored by antiviral or immune-based therapies. Nat Med 1997;3:533–40.
20. Kozak I, Bartsch DU, Cheng L, Kosobucki BR, Freeman WR. Objective analysis of retinal damage in HIV-positive patients in the HAART era using OCT. Am J Ophthalmol 2005;139:295–301.
21. Ng WT, Versace P. Ocular association of HIV infection in the era of highly active antiretroviral therapy and the global perspective. Clin Experiment Ophthalmol 2005;33:317–29.
22. Margolis TP, Milner MS, Shama A, Hodge W, Seiff S. Herpes zoster ophthalmicus in patients with human immunodeficiency virus infection. Am J Ophthalmol 1998;125:285–91.
23. Lucca JA, Farris RL, Bielory L, Caputo AR. Keratoconjunctivitis sicca in male patients infected with human immunodeficiency virus type 1. Ophthalmology 1990;97:1008–10.
24. Cunningham ET Jr, Margolis TP. Ocular manifestations of HIV infection. N Engl J Med 1998;339:236–44.
25. Jeng BH, Holland GN, Lowder CY, Deegan WF III, Raizman MB, Meisler DM. Anterior segment and external ocular disorders associated with human immunodeficiency virus disease. Surv Ophthalmol 2007;52:329–68.
26. Hodge WG, Margolis TP. Herpes simplex virus keratitis among patients who are positive or negative for human immunodeficiency virus: an epidemiologic study. Ophthalmology 1997;104:120–4.
27. Karbassi M, Raizman MB, Schuman JS. Herpes zoster ophthalmicus. Surv Ophthalmol 1992;36:395–410.
28. Otiti-Sengeri J, Colebunders R, Kempen JH, Ronald A, Sande M, Katabira E. The prevalence and causes of visual loss among HIV-infected individuals in Uganda. J AIDS 2010;53:95–101.
29. Resnikoff S, Pascolini D, Mariotti SP, Pokharel GP. Global magnitude of visual impairment caused by uncorrected refractive errors in 2004. Bull World Health Organ 2008;86:63–70.
visual acuity; refractive errors; CD4+ T-cells lymphocyte counts; ocular impairments; ocular disease
© 2010 American Academy of Optometry
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Highlight selected keywords in the article text.
Data is temporarily unavailable. Please try again soon.
Readers Of this Article Also Read