Korean J Ophthalmol.  2015 Aug;29(4):241-248. 10.3341/kjo.2015.29.4.241.

Ocular Manifestations of Acquired Immunodeficiency Syndrome

• Kim YS
• Sun HJ
• Kim TH
• Kang KD
• Lee SJ

• KMID: 2363768
• DOI: http://doi.org/10.3341/kjo.2015.29.4.241

Abstract

PURPOSE
To investigate the patterns and risk factors of the ocular manifestations of acquired immunodeficiency syndrome (AIDS) and their correlation with CD4+ count in the era of highly active antiretroviral therapy (HAART).
METHODS
This retrospective study examined 127 AIDS patients who presented to Soonchunhyang University Hospital. Data were collected from patient interviews, clinical examinations, and laboratory investigations. Ophthalmologic examinations included the best-corrected visual acuity, intraocular pressure, anterior segment and adnexal examination, and dilated fundus examination.
RESULTS
Of the 127 patients with AIDS, 118 were on HAART and 9 were not. The mean CD4+ count was 266.7 +/- 209.1 cells/microL. There were ocular manifestations in 61 patients (48.0%). The incidence of anterior segment manifestations was higher than posterior segment manifestations at 28.3% and 19.7%, respectively. The mean CD4+ count was significantly (p < 0.05) lower in the patients with posterior versus anterior segment ocular manifestations. The most common ocular manifestation was retinal microvasculopathy (15.0%), followed by keratoconjunctivitis sicca (14.2%), conjunctival microvasculopathy (9.4%), cytomegalovirus retinitis (3.1%), herpes zoster ophthalmicus (2.4%), and blepharitis (1.6%). Retinal microvasculopathy and cytomegalovirus retinitis were common in patients with CD4+ counts <200 cells/microL, while keratoconjunctivitis sicca and conjunctival microvasculopathy were common in patients with CD4+ counts of 200 to 499 cells/microL. There was a significant (p < 0.05) association between ocular manifestation and CD4+ count or age.
CONCLUSIONS
The introduction of HAART has changed the landscape of ocular presentations in patients with AIDS. In this study, anterior segment and external ocular manifestations occurred more frequently than posterior segment manifestations. Also, the mean CD4+ count was significantly lower in patients with posterior segment ocular manifestations versus anterior segment ocular manifestations. We found that CD4+ count and age >35 years were independent risk factors for developing ocular manifestations.

Keyword

Acquired immunodeficiency syndrome; CD4-positive T-lymphocytes; Eye manifestations; Highly active antiretroviral therapy

MeSH Terms

Acquired Immunodeficiency Syndrome/*complications
Adult
Aged
Eye Diseases/diagnosis/epidemiology/*etiology
Female
Humans
Incidence
Male
Middle Aged
Republic of Korea/epidemiology
Retrospective Studies
Risk Factors
Visual Acuity
Young Adult

Figure

• 

  Fig. 1 (A) Fundus photograph showing retinal microvasculopathy with numerous cotton-wool spots and retinal hemorrhages. (B) Fundus photograph showing characteristic findings of cytomegalovirus retinitis, including prominent perivascular sheating and retinal necrosis with irregular granular borders.

• 

  Fig. 2 Relative frequencies (percentages) of ocular manifestations in patients grouped according to the CD4+ counts. *p < 0.05; †p < 0.01, chi-square test.

Reference

1. Gottlieb MS, Schroff R, Schanker HM, et al. Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men: evidence of a new acquired cellular immunodeficiency. N Engl J Med. 1981; 305:1425–1431.

2. Jeng BH, Holland GN, Lowder CY, et al. Anterior segment and external ocular disorders associated with human immunodeficiency virus disease. Surv Ophthalmol. 2007; 52:329–368.

3. Moraes HV Jr. Ocular manifestations of HIV/AIDS. Curr Opin Ophthalmol. 2002; 13:397–403.

4. Vrabec TR. Posterior segment manifestations of HIV/AIDS. Surv Ophthalmol. 2004; 49:131–157.

5. 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.

6. Hodge WG, Seiff SR, Margolis TP. Ocular opportunistic infection incidences among patients who are HIV positive compared to patients who are HIV negative. Ophthalmology. 1998; 105:895–900.

7. Kestelyn PG, Cunningham ET Jr. HIV/AIDS and blindness. Bull World Health Organ. 2001; 79:208–213.

8. Lai TY, Wong RL, Luk FO, et al. Ophthalmic manifestations and risk factors for mortality of HIV patients in the post-highly active anti-retroviral therapy era. Clin Experiment Ophthalmol. 2011; 39:99–104.

9. Shuler JD, Engstrom RE Jr, Holland GN. External ocular disease and anterior segment disorders associated with AIDS. Int Ophthalmol Clin. 1989; 29:98–104.

10. Rodrigues ML, Rodrigues Mde L, Figueiredo JF, de Freitas JA. Ocular problems in Brazilian patients with AIDS before and in highly active antiretroviral therapy (HAART) era. Braz J Infect Dis. 2007; 11:199–202.

11. Goldberg DE, Smithen LM, Angelilli A, Freeman WR. HIV-associated retinopathy in the HAART era. Retina. 2005; 25:633–649.

12. Hogg RS, O'Shaughnessy MV, Gataric N, et al. Decline in deaths from AIDS due to new antiretrovirals. Lancet. 1997; 349:1294.

13. Schiffman RM, Christianson MD, Jacobsen G, et al. Reliability and validity of the Ocular Surface Disease Index. Arch Ophthalmol. 2000; 118:615–621.

14. Miller KL, Walt JG, Mink DR, et al. Minimal clinically important difference for the ocular surface disease index. Arch Ophthalmol. 2010; 128:94–101.

15. Acharya NR, Cunningham ET Jr. Corneal, anterior segment, and adnexal manifestations of human immunodeficiency virus. Int Ophthalmol Clin. 1998; 38:161–177.

16. Biswas J, Fogla R, Gopal L, et al. Current approaches to diagnosis and management of ocular lesions in human immunodeficiency virus positive patients. Indian J Ophthalmol. 2002; 50:83–96.

17. Freeman WR, Lerner CW, Mines JA, et al. A prospective study of the ophthalmologic findings in the acquired immune deficiency syndrome. Am J Ophthalmol. 1984; 97:133–142.

18. Henderly DE, Freeman WR, Smith RE, et al. Cytomegalovirus retinitis as the initial manifestation of the acquired immune deficiency syndrome. Am J Ophthalmol. 1987; 103(3 Pt 1):316–320.

19. Holland GN, Gottlieb MS, Yee RD, et al. Ocular disorders associated with a new severe acquired cellular immunodeficiency syndrome. Am J Ophthalmol. 1982; 93:393–402.

20. Jabs DA. Ocular manifestations of HIV infection. Trans Am Ophthalmol Soc. 1995; 93:623–683.

21. Ausayakhun S, Watananikorn S, Ittipunkul N, et al. Epidemiology of the ocular complications of HIV infection in Chiang Mai. J Med Assoc Thai. 2003; 86:399–406.

22. Chiou SH, Liu CY, Hsu WM, et al. Ophthalmic findings in patients with acquired immunodeficiency syndrome. J Microbiol Immunol Infect. 2000; 33:45–48.

23. Gharai S, Venkatesh P, Garg S, et al. Ophthalmic manifestations of HIV infections in India in the era of HAART: analysis of 100 consecutive patients evaluated at a tertiary eye care center in India. Ophthalmic Epidemiol. 2008; 15:264–271.

24. Kim SJ, Park SJ, Yu HG, et al. Ocular manifestations of acquired immunodeficiency syndrome in Korea. J Korean Med Sci. 2012; 27:542–546.

25. Lin YC, Yang CH, Lin CP, et al. Cytomegalovirus retinitis and immune recovery uveitis in AIDS patients treated with highly active antiretroviral therapy in Taiwanese. Ocul Immunol Inflamm. 2008; 16:83–87.

26. Miyamoto C, Yashiro S, Nagata Y, Nagataki S. Ocular complications in patients infected with human immunodeficiency virus seen at the Acquired Immunodeficiency Syndrome Clinical Center. Nihon Ganka Gakkai Zasshi. 2001; 105:483–487.

27. Pathai S, Deshpande A, Gilbert C, Lawn SD. Prevalence of HIV-associated ophthalmic disease among patients enrolling for antiretroviral treatment in India: a cross-sectional study. BMC Infect Dis. 2009; 9:158.

28. Uemura A, Yashiro S, Takeda N, Oka S. Ocular complications in patients with human immunodeficiency virus infection. Nihon Ganka Gakkai Zasshi. 2006; 110:698–702.

29. Wang J, You Q, Yang H, et al. Retinal findings in Chinese patients with HIV infection. Ophthalmic Res. 2008; 40:98–100.

30. DeCarlo DK, Penner SL, Schamerloh RJ, Fullard RJ. Dry eye among males infected with the human immunodeficiency virus. J Am Optom Assoc. 1995; 66:533–538.

31. Lucca JA, Farris RL, Bielory L, Caputo AR. Keratoconjunctivitis sicca in male patients infected with human immunodeficiency virus type 1. Ophthalmology. 1990; 97:1008–1010.

32. Lucca JA, Kung JS, Farris RL. Keratoconjunctivitis sicca in female patients infected with human immunodeficiency virus. CLAO J. 1994; 20:49–51.

33. Biswas J, Madhavan HN, Kumarasamy N, Solomon S. Blepharitis and lid ulcer as initial ocular manifestation in acquired immunodeficiency syndrome patients. Indian J Ophthalmol. 1997; 45:233–234.

34. Friedlaender MH, Masi RJ, Osumoto M, et al. Ocular microbial flora in immunodeficient patients. Arch Ophthalmol. 1980; 98:1211–1213.

35. Kahraman G, Krepler K, Franz C, et al. Seven years of HAART impact on ophthalmic management of HIV-infected patients. Ocul Immunol Inflamm. 2005; 13:213–218.

36. Teich SA. Conjunctival vascular changes in AIDS and AIDS-related complex. Am J Ophthalmol. 1987; 103(3 Pt 1):332–333.

37. Engstrom RE Jr, Holland GN, Hardy WD, Meiselman HJ. Hemorheologic abnormalities in patients with human immunodeficiency virus infection and ophthalmic microvasculopathy. Am J Ophthalmol. 1990; 109:153–161.

38. Geier SA, Klauss V, Goebel FD. Ocular microangiopathic syndrome in patients with acquired immunodeficiency syndrome and its relationship to alterations in cell adhesion and in blood flow. Ger J Ophthalmol. 1994; 3:414–421.

39. Ali R, Kim JY, Henderson BA. Adnexal and anterior segment manifestations of HIV/AIDS. Int Ophthalmol Clin. 2007; 47:15–32.

40. d'Arminio Monforte A, Mainini F, Testa L, et al. Predictors of cytomegalovirus disease, natural history and autopsy findings in a cohort of patients with AIDS. AIDS. 1997; 11:517–524.

41. Drew WL. Cytomegalovirus infection in patients with AIDS. Clin Infect Dis. 1992; 14:608–615.

42. Gallant JE, Moore RD, Richman DD, et al. Incidence and natural history of cytomegalovirus disease in patients with advanced human immunodeficiency virus disease treated with zidovudine. The Zidovudine Epidemiology Study Group. J Infect Dis. 1992; 166:1223–1227.

43. Hoover DR, Saah AJ, Bacellar H, et al. Clinical manifestations of AIDS in the era of pneumocystis prophylaxis. Multicenter AIDS Cohort Study. N Engl J Med. 1993; 329:1922–1926.

44. Palella FJ Jr, Delaney KM, Moorman AC, et al. HIV Outpatient Study Investigators. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N Engl J Med. 1998; 338:853–860.

45. Collier AC, Coombs RW, Schoenfeld DA, et al. AIDS Clinical Trials Group. Treatment of human immunodeficiency virus infection with saquinavir, zidovudine, and zalcitabine. N Engl J Med. 1996; 334:1011–1017.

46. Hammer SM, Squires KE, Hughes MD, et al. AIDS Clinical Trials Group 320 Study Team. A controlled trial of two nucleoside analogues plus indinavir in persons with human immunodeficiency virus infection and CD4 cell counts of 200 per cubic millimeter or less. N Engl J Med. 1997; 337:725–733.

47. Robinson MR, Reed G, Csaky KG, et al. Immune-recovery uveitis in patients with cytomegalovirus retinitis taking highly active antiretroviral therapy. Am J Ophthalmol. 2000; 130:49–56.

48. Karavellas MP, Lowder CY, Macdonald C, et al. Immune recovery vitritis associated with inactive cytomegalovirus retinitis: a new syndrome. Arch Ophthalmol. 1998; 116:169–175.

49. Kuppermann BD, Petty JG, Richman DD, et al. Correlation between CD4+ counts and prevalence of cytomegalovirus retinitis and human immunodeficiency virus-related noninfectious retinal vasculopathy in patients with acquired immunodeficiency syndrome. Am J Ophthalmol. 1993; 115:575–582.

50. Geier SA, Libera S, Klauss V, Goebel FD. Sicca syndrome in patients infected with the human immunodeficiency virus. Ophthalmology. 1995; 102:1319–1324.

51. Turner BJ, Hecht FM, Ismail RB. CD4+ T-lymphocyte measures in the treatment of individuals infected with human immunodeficiency virus type 1: a review for clinical practitioners. Arch Intern Med. 1994; 154:1561–1573.

52. Ambiya V, Sagar A, Patyal S, Mohanty AP. Ocular manifestations in 321 male consecutive cases of human immunodeficiency virus infection/acquired immunodeficiency syndrome at an HIV-referral centre. Med J Armed Forces India. 2012; 68:214–221.

53. Ndoye NB, Sow PS, Ba EA, et al. Ocular manifestations of AIDS in Dakar. Dakar Med. 1993; 38:97–100.

54. Bekele S, Gelaw Y, Tessema F. Ocular manifestation of HIV/AIDS and correlation with CD4+ cells count among adult HIV/AIDS patients in Jimma town, Ethiopia: a cross sectional study. BMC Ophthalmol. 2013; 13:20.

55. Bron AJ, Evans VE, Smith JA. Grading of corneal and conjunctival staining in the context of other dry eye tests. Cornea. 2003; 22:640–650.